Abstract

Objectives

To document resistance patterns of three important nosocomial pathogens, Pseudomonas aeruginosa, Acinetobacter baumannii and Klebsiella pneumoniae, present in hospitals in Brooklyn, NY.

Methods

Susceptibility profiles of pathogens gathered during a surveillance study in 2006 were analysed and compared with similar surveys performed in 1999 and 2001. MICs were determined according to CLSI standards, and selected isolates were screened by PCR for the presence of VIM, IMP and KPC β-lactamases.

Results

For P. aeruginosa, susceptibility to most antimicrobials fell in 2001 and then reached a plateau. However, there was a progressive decrease in the number of patients with P. aeruginosa during the three surveys. While the total number of isolates of A. baumannii remained steady, there was a progressive decrease in susceptibility to most classes of antimicrobial agents, and approximately one-third had combined resistance to carbapenems, fluoroquinolones and aminoglycosides. There was a noticeable rise in the number of isolates of K. pneumoniae over the surveillance periods, suggesting that this has become the predominant pathogen in many medical centres. Over one-third of K. pneumoniae collected in 2006 carried the carbapenemase KPC, and 22% were resistant to all three classes of antimicrobial agents.

Conclusions

Hospitals in our region have been beset with antimicrobial-resistant Gram-negative bacteria. K. pneumoniae has rapidly emerged as the most common multidrug-resistant pathogen. Improved therapeutic agents and methods of detection are needed to reduce transmission of these bacteria.

Introduction

Nosocomial infections due to multidrug-resistant bacterial pathogens have been associated with increased hospital expenditures and poorer clinical outcomes. Three multidrug-resistant Gram-negative bacteria have emerged in many medical centres as particularly troublesome pathogens. First, Pseudomonas aeruginosa is a frequent cause of respiratory, surgical site and urinary tract infections in patients from intensive care areas.1 Several studies have documented increasing resistance rates in P. aeruginosa to fluoroquinolones, cephalosporins and carbapenems, particularly among ICU isolates.2–4 In these reports, carbapenem and ciprofloxacin resistance has been noted in ∼20% and ∼30% of the isolates, respectively.

Second, Acinetobacter baumannii is being recognized as an emerging pathogen in many medical facilities. According to NNIS data, the proportion of infections due to Acinetobacter spp. has increased, and accounts for ∼7% of ICU-related pneumonias.1 In several wide-scale surveillance studies, carbapenem, cephalosporin and ciprofloxacin resistance rates have approached ∼20%, ∼50% and ∼50%, respectively.1,3,4 Infections due to multidrug-resistant Acinetobacter baumannii have been associated with increased length of hospital and ICU stays, and a polymyxin is often the antimicrobial agent of last resort.

Third, Klebsiella pneumoniae is also a well-recognized nosocomial pathogen, and an important cause of pneumonia and urinary tract infections in the ICU setting. Since the early 1990s, extended-spectrum β-lactamase (ESBL)-possessing K. pneumoniae have rapidly emerged.1,2 In surveillance studies, resistance to third-generation cephalosporins has reached ∼15–20%, and ciprofloxacin resistance has ranged from ∼10–50%.1,3–7 Outbreaks of carbapenemase-producing K. pneumoniae have been reported,8 threatening this class of antimicrobial agents.

Our group has performed periodic citywide surveillance studies in Brooklyn, NY, the most populous borough of New York City. In this report we document the susceptibility results of the most recent surveillance study, performed in 2006, and note trends involving P. aeruginosa, A. baumannii and K. pneumoniae.

Materials and methods

The surveillance studies involved the collection of all single-patient isolates of bacteria over a 3 month period from the microbiology laboratories in Brooklyn, NY. Investigations in 1999,6,9 200110 and 2006 involved 15 hospitals in the city; 14 hospitals participated in all three surveillances. Isolates were identified by the participating laboratories according to standard techniques. Susceptibility testing and interpretation was performed in the central research laboratory according to CLSI standards.11 Isolates with MICs ≤2 mg/L were considered susceptible to polymyxin B and tigecycline. Isolates of K. pneumoniae with either ceftazidime or ceftriaxone MICs >1 mg/L were considered to possess ESBLs. In this report, multidrug-resistant bacteria are defined as those isolates non-susceptible to amikacin, ciprofloxacin and imipenem and/or meropenem. χ2 analysis was used to compare susceptibility rates between the surveillance periods; a P value of ≤0.05 was considered significant.

Selected isolates gathered in 2006 were screened for the presence of class A and B carbapenem-hydrolysing β-lactamases. All cephalosporin- and/or carbapenem-resistant P. aeruginosa, and all isolates of A. baumannii, were screened by PCR for the presence of VIM, IMP and KPC β-lactamases using previously defined primers and amplification conditions.8,12 All cephalosporin-resistant isolates of K. pneumoniae and Enterobacter spp. were screened for the presence of blaKPC. Positive control isolates included strains of Escherichia coli with IMP-4 and P. aeruginosa with VIM-2 (kindly provided by bioMerieux, Inc., Hazelwood, MO, USA) and an isolate of K. pneumoniae with KPC-2 (previously characterized in our laboratory). Selected resistant isolates also underwent genetic fingerprinting by ribotyping using the Riboprinter Microbial Characterization System (Qualicon, Wilmington, DE, USA), according to the manufacturer's recommendations.

Results

During the 2006 survey, a total of 597 unique-patient isolates of P. aeruginosa were collected (Table 1). A modest but significant reduction in susceptibility to most agents (particularly ciprofloxacin, the cephalosporins and the two carbapenems) was seen between 1999 and 2001. Virtually all of the isolates gathered in 2006 were susceptible to polymyxin B. It is noteworthy that there was a progressive decrease in the number of isolates of P. aeruginosa collected during the surveys; whether this reflects effective infection control practices or simply their replacement by other nosocomial Gram-negative bacteria (see below) is unknown. None of the screened isolates were found to possess VIM, IMP or KPC enzymes. Fifteen carbapenem-resistant isolates underwent ribotyping, and most belonged to previously identified ribotypes predominant in our region.9

Table 1.

Susceptibility data for P. aeruginosa collected during the three surveillance studies

Antibiotic 1999 (n = 823)a 2001 (n = 691) 2006 (n = 597) 
number susceptible (%) MIC50 (mg/L) number susceptible (%) MIC50 (mg/L) number susceptible (%) MIC50 (mg/L) 
Piperacillin/tazobactam 701 (85) 575 (83) 499 (84) 
Ceftazidime 680 (82) 531 (77)c 489 (82)c 
Cefepime 625 (76) 491 (71)c 435 (73) 
Imipenem 629 (76) 482 (70)c 412 (69) 
Meropenem 687 (83) 0.5 531 (77)c 458 (77) 
Amikacin 786 (95) 652 (94) 575 (96) 
Ciprofloxacin 588 (71) 0.25 385 (56)c 0.5 355 (59) 0.5 
Polymyxin B NTb  690 (99.9)  596 (99.8) 
Multidrug-resistant (%) 21 (2.6)  24 (3.5)  18 (3.0)  
Antibiotic 1999 (n = 823)a 2001 (n = 691) 2006 (n = 597) 
number susceptible (%) MIC50 (mg/L) number susceptible (%) MIC50 (mg/L) number susceptible (%) MIC50 (mg/L) 
Piperacillin/tazobactam 701 (85) 575 (83) 499 (84) 
Ceftazidime 680 (82) 531 (77)c 489 (82)c 
Cefepime 625 (76) 491 (71)c 435 (73) 
Imipenem 629 (76) 482 (70)c 412 (69) 
Meropenem 687 (83) 0.5 531 (77)c 458 (77) 
Amikacin 786 (95) 652 (94) 575 (96) 
Ciprofloxacin 588 (71) 0.25 385 (56)c 0.5 355 (59) 0.5 
Polymyxin B NTb  690 (99.9)  596 (99.8) 
Multidrug-resistant (%) 21 (2.6)  24 (3.5)  18 (3.0)  

aData from reference 9.

bNT, not tested.

cP < 0.05 compared with the previous surveillance data.

There was a relentless decline in susceptibility to most antimicrobial agents when tested against A. baumannii (Table 2). By 2006, only ∼10% of isolates remained susceptible to cephalosporins or ciprofloxacin, and only 37% were susceptible to imipenem. Polymyxin B remained the most consistently active agent. The number of isolates gathered during each surveillance period remained remarkably stable, and in 2006 approached the number of isolates of P. aeruginosa. None of the isolates of A. baumannii was found to harbour VIM, IMP or KPC β-lactamases.

Table 2.

Susceptibility results for A. baumannii gathered during the three citywide surveys

Antibiotic 1999 (n = 419)a 2001 (n = 436)b 2006 (n = 431) 
number susceptible (%) MIC50 (mg/L) number susceptible (%) MIC50 (mg/L) number susceptible (%) MIC50 (mg/L) 
Ampicillin/sulbactam 276 (66) 234 (54)d 240 (56) 
Piperacillin/tazobactam 138 (33) 128 82 (19)d 128 85 (20) 128 
Ceftazidime 132 (31) >32 78 (18)d >32 66 (15) >32 
Cefepime 147 (35) 16 59 (14)d 32 48 (11) >32 
Imipenem 282 (67) 274 (63) 160 (37)d 
Meropenem 196 (47) 139 (32)d 111 (26)d 
Amikacin 288 (69) 245 (56)d 272 (63)d 
Ciprofloxacin 115 (27) >4 54 (12)d >4 38 (9) >4 
Polymyxin B 409 (98) 0.5 410 (94)d 418 (97)d 
Tigecycline NTc  NT  396 (92) 
Multidrug-resistant (%) 103 (25)  160 (37)d  134 (31)  
Antibiotic 1999 (n = 419)a 2001 (n = 436)b 2006 (n = 431) 
number susceptible (%) MIC50 (mg/L) number susceptible (%) MIC50 (mg/L) number susceptible (%) MIC50 (mg/L) 
Ampicillin/sulbactam 276 (66) 234 (54)d 240 (56) 
Piperacillin/tazobactam 138 (33) 128 82 (19)d 128 85 (20) 128 
Ceftazidime 132 (31) >32 78 (18)d >32 66 (15) >32 
Cefepime 147 (35) 16 59 (14)d 32 48 (11) >32 
Imipenem 282 (67) 274 (63) 160 (37)d 
Meropenem 196 (47) 139 (32)d 111 (26)d 
Amikacin 288 (69) 245 (56)d 272 (63)d 
Ciprofloxacin 115 (27) >4 54 (12)d >4 38 (9) >4 
Polymyxin B 409 (98) 0.5 410 (94)d 418 (97)d 
Tigecycline NTc  NT  396 (92) 
Multidrug-resistant (%) 103 (25)  160 (37)d  134 (31)  

aData from reference 9.

bData from reference 10.

cNT, not tested.

dP < 0.05 compared with the previous surveillance data.

An unequivocal decline in antimicrobial susceptibility has occurred among isolates of K. pneumoniae (Table 3). Persistent declines in susceptibility to all β-lactams, amikacin, ciprofloxacin and trimethoprim/sulfamethoxazole were noted. Remarkably, approximately one-fourth of the isolates were resistant to carbapenems, and the β-lactamase KPC was detected in 38% of all isolates. Eight isolates possessing blaKPC underwent ribotyping, and all belonged to one of two previously identified strains.13 Virtually all isolates gathered in the 2006 study were susceptible to polymyxin B and tigecycline. There was also a noticeable increase in the total number of isolates of K. pneumoniae gathered during the surveillance in 2006, suggesting this has become the predominant nosocomial pathogen in most medical centres.

Table 3.

Antimicrobial susceptibility of isolates of K. pneumoniae collected during the three surveillance investigations

Antibiotic 1999 (n = 824)a 2001 (n = 874) 2006 (n = 997) 
number susceptible (%) MIC50 (mg/L) number susceptible (%) MIC50 (mg/L) number susceptible (%) MIC50 (mg/L) 
Piperacillin/tazobactam 695 (84) 654 (75)c 487 (49)c 32 
Ceftriaxone 683 (83) 0.06 619 (71)c 0.12 434 (44)c 32 
Ceftazidime 594 (72) 0.25 565 (65)c 0.25 411 (41)c >32 
Cefepime 784 (95) 0.06 797 (91)c 0.06 588 (59)c 
Ertapenem 793 (96) 0.015 838 (96) 0.03 605 (61)c 0.25 
Imipenem 821 (99.6) 0.25 849 (97)c 0.25 758 (76)c 0.25 
Meropenem 823 (99.9) 0.03 849 (97)c 0.03 762 (76)c ≤0.12 
Amikacin 705 (86) 734 (84) 537 (54)c 16 
Gentamicin 606 (74) 0.5 575 (66)c 648 (65) 
Ciprofloxacin 610 (74) 0.03 606 (69)c 0.06 406 (41)c >4 
Co-trimoxazole 585 (71) ≤0.25 498 (57)c 465 (47)c >4 
Polymyxin B NTb  NT  952 (95) 
Tigecycline NT  NT  937 (94) 0.5 
ESBL-positive (%) 281 (34)  332 (38)  608 (61)c  
Multidrug-resistant (%) 1 (0.1)  22 (2.5)c  219 (22)c  
Antibiotic 1999 (n = 824)a 2001 (n = 874) 2006 (n = 997) 
number susceptible (%) MIC50 (mg/L) number susceptible (%) MIC50 (mg/L) number susceptible (%) MIC50 (mg/L) 
Piperacillin/tazobactam 695 (84) 654 (75)c 487 (49)c 32 
Ceftriaxone 683 (83) 0.06 619 (71)c 0.12 434 (44)c 32 
Ceftazidime 594 (72) 0.25 565 (65)c 0.25 411 (41)c >32 
Cefepime 784 (95) 0.06 797 (91)c 0.06 588 (59)c 
Ertapenem 793 (96) 0.015 838 (96) 0.03 605 (61)c 0.25 
Imipenem 821 (99.6) 0.25 849 (97)c 0.25 758 (76)c 0.25 
Meropenem 823 (99.9) 0.03 849 (97)c 0.03 762 (76)c ≤0.12 
Amikacin 705 (86) 734 (84) 537 (54)c 16 
Gentamicin 606 (74) 0.5 575 (66)c 648 (65) 
Ciprofloxacin 610 (74) 0.03 606 (69)c 0.06 406 (41)c >4 
Co-trimoxazole 585 (71) ≤0.25 498 (57)c 465 (47)c >4 
Polymyxin B NTb  NT  952 (95) 
Tigecycline NT  NT  937 (94) 0.5 
ESBL-positive (%) 281 (34)  332 (38)  608 (61)c  
Multidrug-resistant (%) 1 (0.1)  22 (2.5)c  219 (22)c  

aData from reference 6.

bNT, not tested.

cP < 0.05 compared with the previous surveillance data.

The total number of patients with multidrug-resistant Gram-negative isolates rose from 125 to 206 to 371 over the three surveys. The percentage of multidrug-resistant isolates that were P. aeruginosa fell from 17% to 5%, and A. baumannii fell from 82% to 36%. In contrast, the percentage of multidrug-resistant isolates that were K. pneumoniae increased from 1% to 59%. K. pneumoniae has clearly become the most common multidrug-resistant pathogen in this region. During the time period of the surveys, there was a modest increase in the number of patients discharged from all Brooklyn hospitals. Collectively, there were 328 579 discharges in the year 1999, 344 861 in 2001 and 365 367 in 2006, which may account for a small portion of the increase in the number of isolates of multidrug-resistant K. pneumoniae (data obtained from Infoshare Community Data System, Community Studies of New York, Inc.).

The presence of the carbapenem-hydrolysing β-lactamase KPC is certainly not limited to K. pneumoniae. While the great majority of isolates of Enterobacter spp. remained susceptible to most antimicrobial agents (Table 4), 6% of the isolates collected in 2006 were found to harbour blaKPC.

Table 4.

Susceptibility information involving 220 Enterobacter spp. gathered in 2006

Antibiotic Number susceptible (%) MIC50 (mg/L) 
Piperacillin/tazobactam 172 (78) 
Ceftriaxone 159 (72) 0.5 
Ceftazidime 163 (74) 0.25 
Cefepime 191 (87) ≤0.12 
Ertapenem 213 (97) 0.25 
Imipenem 216 (98) 0.25 
Meropenem 216 (98) ≤0.12 
Amikacin 214 (97) 
Gentamicin 191 (87) 0.5 
Ciprofloxacin 190 (86) ≤0.12 
Co-trimoxazole 176 (80) ≤0.5 
Polymyxin B 207 (94) 0.5 
Tigecycline 213 (97) 0.25 
Antibiotic Number susceptible (%) MIC50 (mg/L) 
Piperacillin/tazobactam 172 (78) 
Ceftriaxone 159 (72) 0.5 
Ceftazidime 163 (74) 0.25 
Cefepime 191 (87) ≤0.12 
Ertapenem 213 (97) 0.25 
Imipenem 216 (98) 0.25 
Meropenem 216 (98) ≤0.12 
Amikacin 214 (97) 
Gentamicin 191 (87) 0.5 
Ciprofloxacin 190 (86) ≤0.12 
Co-trimoxazole 176 (80) ≤0.5 
Polymyxin B 207 (94) 0.5 
Tigecycline 213 (97) 0.25 

Discussion

The evolution involving antimicrobial resistance in three important nosocomial Gram-negative bacilli in New York City has been rapid and relentless. With ∼25% of P. aeruginosa resistant to both carbapenems and fluoroquinolones, there is increasing reliance on aminoglycosides and polymyxins for effective therapy. A. baumannii is an unusually frequent pathogen in our region, with the number of patient isolates approaching that of P. aeruginosa in our most recent survey. Since approximately 30% of A. baumannii are multidrug-resistant (resistant to carbapenems, fluoroquinolones and aminoglycosides), therapeutic options are limited. Also, both the resistance profile and the sheer number of unique-patient isolates of K. pneumoniae make this an especially troublesome pathogen. In some ICUs, this has become the predominant cause of nosocomial infection. Given that 20% are resistant to all β-lactams, fluoroquinolones and amikacin, therapy is also exceedingly difficult.

Our susceptibility trends for these three pathogens are comparable or considerably worse than those found in other surveillance studies that involve the collection of only ICU-associated pathogens. Compared with the latest NNIS system report (for the year 2003),2 the isolates from Brooklyn hospitals had appreciably greater rates of fluoroquinolone resistance (for P. aeruginosa) and cephalosporin resistance (for K. pneumoniae). Although isolates of P. aeruginosa gathered from ICUs in Europe and North America had similar susceptibility rates, higher susceptibility rates for fluoroquinolones, cephalosporins and carbapenems were noted for A. baumannii and K. pneumoniae, when compared with the Brooklyn isolates.3,4

Our increasing reliance on the polymyxins is fraught with trepidation. Renal and neurological toxicities remain a concern, and clinical outcome in the therapy of respiratory tract infections has been poor in some studies.14 Although our most recent survey demonstrated continued activity of these agents, resistance has been noted,8 and the emergence of pathogens (e.g. Serratia marcescens) with intrinsic resistance to the polymyxins has been sporadically noted. Whether the addition of other antimicrobial agents (e.g. rifampicin) that enhance the in vitro activity of polymyxin can result in improved clinical outcome remains unknown.15,16 It is evident that new effective agents are acutely needed. Tigecycline has demonstrated in vitro activity against most of the multidrug-resistant isolates of A. baumannii and K. pneumoniae. However the utility of tigecycline for the treatment of multidrug-resistant Gram-negative infections is unknown, and in vivo data are needed.

With the continued emergence of multidrug-resistant A. baumannii and K. pneumoniae, it is apparent that reducing transmission in healthcare centres has been difficult. Effective infection control measures will likely require a multifaceted programme. At the forefront of such a programme will be accurate identification of the multidrug-resistant pathogens, and of patients with asymptomatic colonization. It is evident that carbapenem susceptibility testing may not readily identify KPC-possessing K. pneumoniae.13 Indeed, 38% of our recent isolates of K. pneumoniae carried blaKPC, but only 24% were non-susceptible to imipenem and meropenem. Clearly, more accurate methods of detection are required. Also, no prepared commercial medium exists that is suited for screening faecal samples for carbapenem-resistant Gram-negative pathogens. While novel microbiological techniques have been identified for screening for these multidrug-resistant pathogens,17 standardized methods are lacking. Until solutions to the therapeutic and infection control hurdles are realized, our region will undoubtedly continue to struggle with these pathogens.

Acknowledgements

Financial support: research funding from AstraZeneca Pharmaceuticals, Elan Pharmaceuticals, Merck & Co., Inc. and Wyeth Pharmaceuticals (D. L., S. B. and J. Q.).

Transparency declarations

None to declare.

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