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A decade of change in susceptibility patterns of Gram-negative blood culture isolates: a single center study.

Background

Bloodstream infections caused by multidrug-resistant Gram-negative organisms continue to be leading causes of morbidity and mortality in hospitalized patients. (1-3) Knowledge of longitudinal trends in antimicrobial susceptibility patterns will help both clinicians and infection control practitioners. Unlike many developed countries, India does not have a nationwide antimicrobial resistance monitoring network and therefore long term longitudinal single center studies can give important information regarding emerging resistance patterns. Most studies from India have been performed over 1 to 4 years; (4-11) only one has analyzed data over an 8 year period. (12) We herewith describe antibiotic susceptibility patterns of important Gram-negative blood culture isolates at a single center over 10 years.

Methods

A retrospective observational study was carried out at a 550-bed tertiary care referral center in South India. We studied the antimicrobial susceptibility patterns of 4128 non-repetitive blood culture isolates of Escherichia coli, Klebsiella pneumoniae and Pseudomonas aeruginosa from 2003-2013. Acinetobacter baumannii was included from 2009-2013 as blood culture isolates were uncommon prior to 2009. We collected the susceptibility patterns of all the four organisms both together and separately based upon whether collected from ward inpatients (IP), outpatients (OP) and patients in the critical care unit (CCU). Subsequent cultures of the same organism from the same patient were not included.

Isolation and identification was done with BacT/ALERT (bioMerieux, Marcy-l'Etoile, France) and VITEK 2 (bioMerieux, Marcy-l'Etoile, France) and also through standard microbiological tests. Susceptibility testing was done with the disc diffusion method (modified Kirby-Bauer method) using Mueller-Hinton agar and VITEK 2 antimicrobial susceptibility testing (AST) cards. The results were interpreted as per CLSI (Clinical and Laboratory Standards Institute) guidelines corresponding to that period. (13) All antibiotic discs were obtained from OXOID (Oxoid Ltd, Altrincham, Cheshire, United Kingdom) and BD BBL (Becton, Dickinson and Company Ltd, Franklin Lakes, New Jersey, USA). Extended-spectrum beta-lactamase (ESBL) production and carbapenem resistance was interpreted based on Kirby-Bauer disc susceptibility testing and the minimum inhibitory concentration (MIC) criteria by the VITEK COMPACT 2 as per CLSI guidelines. Tigecycline susceptibility was not performed for P. aeruginosa as it is inherently resistant. Meropenem was taken as a representative of the Group 2 carbapenems (meropenem, imipenem, doripenem).

Data was entered in Microsoft Excel worksheet and susceptibility percentages were calculated. Comparison of resistance of 2003 and 2013 was done with Z test for 2 population proportions.

We obtained institutional ethics committee clearance for the study.

Results

During the study period, susceptibility patterns of 4128 blood culture isolates of E. coli, K. pneumoniae, P. aeruginosa and A. baumannii were analysed. E. coli predominated in outpatient isolates whereas K. pneumoniae and P. aeruginosa predominated in CCU isolates. All A. baumannii isolates were from the CCU. Details of isolates are in Table 1. The overall susceptibility pattern of all blood isolates is depicted in Figure 1.

Outpatient isolates (Tables 2 and 5): Amikacin susceptibilities fell between 2003 (85%) and 2013 (74%), not statistically significant (p = .136). ESBL production rates increased from 45% to 67%. Susceptibility to ciprofloxacin was low throughout the study period (37%-40%). There was a significant drop in susceptibility to beta-lactam--beta-lactamase inhibitor (BL-BLIs) from 80% to 60% (p = .006 for cefoperazone-sulbactam and p = .0003 for piperacillin-tazobactam).

Meropenem susceptibility dropped from 96% to 79% (p = .005). Most isolates were susceptible to polymyxin E and tigecycline (97% and 89% respectively).

Inpatient isolates (Table 2): Susceptibility to amikacin was maintained throughout this period (77% to 76%). A drop in the susceptibility to ciprofloxacin was noted (40% to 29%) but it was not statistically significant (p = .082). There was a statistically significant drop in the susceptibility to ceftazidime and cefepime (p = .038 and .044). The drop in BL-BLIs (statistically significant - p = .005 and .003) and meropenem (not statistically significant, p = .327) susceptibilities was similar to outpatient isolates.

The detailed antibiotic susceptibility patterns are in Table 3 a, 3b, 4, 5 and 6.

CCU isolates (Tables 3 and 5): Amikacin susceptibility fell from 93% to 52% (p = .000). ESBL production rates increased from 60% to 80%, higher than among outpatient and inpatient isolates. There was a drop in meropenem susceptibility (from 99% to 77%). The drop in susceptibility to all antibiotics except for ciprofloxacin was statistically significant. The only antibiotics with susceptibilities greater than 80% were polymyxin E and tigecycline.

E. coli (Figure 2, Tables 3a and 3b): Amikacin susceptibility was maintained for OP/IP/CCU isolates at 90%. ESBL rates increased from 56% in 2003 to 71% in 2013. The increase was more important in CCU isolates. There was a significant drop in ceftazidime susceptibility in CCU isolates (p = .037). Among the BL-BLIs, cefoperazone-sulbactam susceptibility was about 10% higher overall than that to piperacillin-tazobactam, although susceptibility to both fell by about 10% between 2003 and 2013. The statistically significant drop in cefoperazone-sulbactam (p = .024) susceptibility was more contributed by the inpatient isolates (p = .046). For piperacillin-tazobactam, the drop in susceptibility was significant (p = .012), more from the outpatient isolates (p = .038). There was a reduction in susceptibility to meropenem from 2003 to 2013 (100% to 95%), falling to as low as 91% among CCU isolates but this was not statistically significant.

Susceptibility to polymyxin E and tigecycline was high (100% to 95%).

K pneumoniae (Figure 3, Tables 3a and 3b): There was a significant drop in the susceptibility to amikacin in CCU isolates from 94% in 2003 to 44% in 2013 (p = .000). ESBL production rates were 75% in outpatient isolates and 81% in CCU isolates. The susceptibility rates to BL-BLIs were as low as 40% in both outpatient and inpatient isolates and just 30-35% in CCU isolates. The drops in the susceptibility to BLBLIs of all isolates (outpatient, inpatient and CCU) were statistically significant. Meropenem susceptibility fell from 100% in outpatient isolates in 2003 to 60% in 2013 (p = .019). A similar trend was seen in CCU isolates (p = .000). Even though there was a drop for inpatient isolates, it was not statistically significant. In 2013, only 59% of inpatient isolates and 43% CCU isolates were susceptible to meropenem. Susceptibility to tigecycline (76%) was lower than that to polymyxin E (100%) in CCU isolates (Table 5).

P. aeruginosa (Figure 4, Tables 3a and 3b): Amikacin susceptibility was maintained throughout the study period in inpatient isolates whereas there was a 20% reduction in CCU isolates (87% to 66%). The number of isolates susceptible to piperacillin-tazobactam was higher than that for ceftazidime and cefoperazone-sulbactam and the susceptibility to piperacillin-tazobactam was maintained throughout the study period. In 2003 strains were more susceptible to meropenem compared to BL-BLIs but from 2009, the trend got reversed. Even though there was a drop in the susceptibility to all antibiotics, the only statistically significant drop was for meropenem from CCU isolates (p = .0006). More than 90% of isolates were susceptible to polymyxin E (Table 5).

A. baumannii (Figure 5): We analyzed data from 2009 to 2013 only, all from the CCU. Susceptibility to amikacin was low but steady (35% to 25%) between 2009 and 2013. Susceptibility to third generation cephalosporins/ BL-BLIs was low at 33% to 23%. Meropenem susceptibility was low throughout the study period (33% to 26%). Polymyxin E and tigecycline susceptibility fell from 100% to 95% and 80% respectively, both not statistically significant.

Discussion

The rapid emergence of multidrug-resistant Gram-negative bacteria is an enormous problem not only in India but also globally. (14-17) We hereby demonstrate steadily increasing resistance rates among Gram-negative blood culture isolates with the greatest rise among CCU isolates, compared to outpatient and inpatient isolates.

ESBL production in Enterobacteriaceae in India has been increasing steadily in various studies. In our study ESBL production rate in E. coli increased from 56% in 2003 to 71% in 2013 and was as high as 80% in the CCU, which is higher than previous studies where it was between 45-70%.5-8 Our ESBL rate in E. coli was similar to the rates in the study by Rajeevan et al. (9) ESBL production in K. pneumoniae similarly increased from 50% in 2003 to 73% in 2013. A worrying trend in our study was the increasing ESBL production rate even in outpatient isolates (from 45% in 2003 to 67% in 2013). This increase in rates unfortunately may require clinicians to use high end antibiotics such as carbapenems even for community-acquired bacteremias.

The increase in ESBL rates may have resulted in widespread carbapenem usage in many Indian hospitals during the first decade of this century, which in turn probably fuelled emergence of carbapenem resistance. Carbapenem resistance in Enterobacteriaceae increased over this period in our study: E. coli isolates were fully susceptible to carbapenems in 2003 but not in 2013, when 4% of isolates were resistant. K. pneumoniae showed an even greater increase in carbapenem resistance (1% in 2003 to 46% in 2013--Table 3b). The changes in carbapenem resistance were statistically significant in isolates from outpatient and CCU. This was similar to two other studies that showed that carbapenem resistance increased from 10% to 40% over a two year period. (6,16) A similar increase in carbapenem resistance from 2008 was reported in another study done in South India. (12) This probably reflects the emergence and subsequent dissemination of New Delhi metallo-betalactamase (NDM-1)-producing Enterobacteriaceae in multiple Indian hospitals in this period. (17)

A similar rise in carbapenem resistance was noted in P. aeruginosa and A. baumannii. Carbapenem resistance in P. aeruginosa was not seen in 2003 but in 2013, 52% of CCU isolates were resistant, the difference being statistically significant. The drop in susceptibility in other isolates was not statistically significant. In another study done in India, 30-37% of P. aeruginosa isolates were resistant to carbapenem. (18) P. aeruginosa isolates were more susceptible to piperacillin-tazobactam (70% to 80%) than cefoperazone-sulbactam (50%) or carbapenems (65%). Again, the widespread use of carbapenems instead of BL-BLIs to treat ESBL Enterobacteriaceae may have contributed.

In our study A. baumannii isolates were all from the CCU. Susceptibility to meropenem was just 33% and decreased further to 26% in 2013 similar to another study which analyzed isolates between 2011 and 2012 and showed 20% susceptibility to carbapenems. (19) Carbapenem-resistant A. baumannii is a common cause of hospital-acquired bacteremia and pneumonia at our center. Carbapenems are therefore currently inappropriate as empiric therapy for hospital-acquired infections where A. baumannii may be a pathogen.

Beta-lactam/ beta-lactam inhibitors have been used as carbapenem-sparers for nosocomial infections, but susceptibility rates declined over time in our study (Table 4). Cefoperazone-sulbactam susceptibility of outpatient isolates declined from around 83% in 2003 to 60% in 2013 (p = .005). Susceptibility to piperacillin-tazobactam also declined from 87% in 2003 to 57% in 2013 for outpatient isolates (p = .0003)--Table 2. Although the drop in the susceptibility to BL-BLIs was statistically significant in all isolates (p [less than or equal to].005), it was more pronounced in CCU isolates (40%) than in outpatient (60%) and inpatient isolates (60%). These findings have important implications for therapy: these drugs are no longer reliable as empiric choices for hospital-acquired infections and may not be effective as empiric choices for severe community-acquired bacteremias.

Polymyxin E and tigecycline were the most effective antibiotics for E. coli and K. pneumoniae (susceptibility ranged between 90-100%). However resistance to these antibiotics of last resort is clearly emerging at our center. Although there was a drop in overall susceptibility to polymyxin E and tigecycline in 2013, this was statistically significant (p = .0001) only for polymyxin E from CCU isolates (Table 6). In 2013, 3-5% of P. aeruginosa and A. baumannii isolates were resistant to polymyxin E and there was a fall in tigecycline susceptibility from 100% in 2011 to 70%-80% in 2013 among K. pneumoniae and A. baumannii isolates from CCU (Table 5). This highlights the need for careful antimicrobial stewardship to preserve polymyxin E and tigecycline as the drugs of last resort.

In 2013, 67% of the isolates were susceptible to amikacin, with a minimal fall in susceptibilities over a 10 year period. This could be due to the fact that aminoglycosides are rarely used as empiric or definitive therapy for Gram-negative sepsis at our center due to concern about toxicity: perhaps it is time to reconsider the use of aminoglycosides as empiric agents in Gram-negative sepsis, probably in combination with beta-lactam antibiotics.

We acknowledge some limitations in our study. The increase in carbapenem resistance in 2012 and 2013 may have been because of lowered MIC breakpoints by CLSI in 2012. (13) We also did not test for molecular mechanisms of resistance, which might have yielded valuable insight into reasons behind emergence of resistance. For instance, we do not know whether carbapenem resistance was due to the production of NDM-1, other carbapenemases or still other mechanisms such as porin channel mutations or efflux pumps. We also did not test for clonality among isolates which might give useful information regarding the role of infection control efforts versus antimicrobial stewardship.

Conclusion

We hereby demonstrate significant increases in resistance in blood culture isolates of Gram-negative bacteria to all major classes of antibiotics. Inclusion of blood culture isolates alone, as opposed to cultures from non-sterile sites, increases the applicability of our findings to clinical practice. The majority of Enterobacteriaceae at our center are ESBL producers and this was true even for outpatient isolates. There was a drop in susceptibility to beta-lactam/beta-lactamase inhibitors, which are potential carbapenem-sparers. Carbapenem-resistant A. baumannii has established itself as a nosocomial pathogen, and almost half of P. aeruginosa isolates were also resistant. Rising carbapenem resistance was also noted with K. pneumoniae, especially for isolates from the CCU, where carbapenems can no longer be used as reliable empiric therapy. Resistance to polymyxin E and tigecycline, considered drugs of last resort, has begun to emerge in K. pneumoniae. Antimicrobial stewardship and other measures, such as those suggested by the Chennai Declaration, (20) are urgently needed to tackle the problem of Gram-negative resistance.

Authors' contribution statement

MA contributed to study concept, design, data collection, data analysis, and manuscript preparation. RG contributed to study concept, data analysis, and manuscript preparation. SNP contributed to study concept, data collection, data analysis, and manuscript preparation. SD contributed to study concept and manuscript editing. TMA contributed to study concept, data collection, and manuscript editing. VR contributed to study concept and manuscript editing. All authors read and approved the final version of the manuscript.

Conflicts of interest

All authors--none to declare

References

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(8.) Kaul S, Brahmadathan KN, Jagannati M, et al. One year trends in the gram-negative bacterial antibiotic susceptibility patterns in a medical intensive care unit in South India. Indian J Med Microbiol 2007;25:230-5. [PubMed]

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(16.) Mohamudha Parveen R, Harish BN, Parija SC. Emerging carbapenem resistance among nosocomial isolates of Klebsiella pneumoniae in South India. Int J Pharma Biosci 2010;1:1-11.

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doi: 10.11599/germs.2015.1073

Murali Alagesan [1], *, Ram Gopalakrishnan [2], Senthur Nambi Panchatcharam [3], Sureshkumar Dorairajan [4], Thirunarayan Mandayam Ananth [5], Ramasubramanian Venkatasubramanian [6]

Received: 27 February 2015; revised 28 April 2015 and 12 June 2015; accepted: 13 August 2015

[1] MD, Fellowship in Infectious Diseases, Professor of Medicine, PSG Institute of Medical Sciences & Research, Coimbatore, Tamilnadu, India; [2] MD, MRCP (UK), AB (Internal Medicine), AB (Infectious Diseases), FIDSA, Senior Consultant, Institute of Infectious Diseases, Apollo Hospitals, Chennai, Tamilnadu, India; [3] MD, FNB (Infectious Diseases), Consultant, Institute of Infectious Diseases, Apollo Hospitals, Chennai, Tamilnadu, India; [4] MD, FNB (Infectious Diseases), Consultant, Institute of Infectious Diseases, Apollo Hospitals, Chennai, Tamilnadu, India; [5] MD, Department of Microbiology, Apollo Hospitals, Chennai, Tamilnadu, India; [6] MD, MRCP, DGUM, DTMH, Senior Consultant, Institute of Infectious Diseases, Apollo Hospitals, Chennai, Tamilnadu, India.

* Corresponding author: Alagesan Murali, MD, Fellowship in Infectious Diseases, Professor of Medicine, PSG Institute of Medical Sciences & Research, Coimbatore, Tamilnadu, 641004, India. muralimd2000@yahoo.com

Caption: Figure 1. Susceptibility patterns of all blood isolates

Caption: Figure 2. Susceptibility patterns of E. coli

Caption: Figure 3. Susceptibility patterns of K pneumoniae

Caption: Figure 4. Susceptibility patterns of P. aeruginosa

Caption: Figure 5. Susceptibility patterns of A. baumannii
Table 1. Details of number of isolates included
in the study

                Outpatient   Inpatient   CCU    Total

All isolates       1111        1365      1652   4128
E. coli             687         774       457   1918
K. pneumoniae       286         396       568   1250
P. aeruginosa       138         195       295    628
A. baumannii        --           --       332    332

CCU critical care unit.

Table 2. Comparison of resistance of all blood
culture isolates in 2003 vs. 2013
                                             Resistance
                                             comparison
                                             2003 vs. 2013
                          2003   2013
OUTPATIENT                 %      %      Z score    p value

Amikacin                   85     74     1.4888     .13622
Ceftazidime                55     35     2.3068     .02088
Cefepime                   58     37     2.4384     .01468
Ciprofloxacin              40     43    -0.4112     .6818
Cefoperazone-sulbactam     83     60     2.7667     .0056
Piperacillin-tazobactam    87     57     3.6607     .00026
Meropenem                  96     79     2.7931     .00528

INPATIENT

Amikacin                   77     76     0.128      .89656
Ceftazidime                46     32     2.0772     .03752
Cefepime                   51     37     2.014      .0444
Ciprofloxacin              40     29     1.7445     .08186
Cefoperazone-sulbactam     83     65     2.7752     .00544
Piperacillin-tazobactam    80     61     2.2309     .00338
Meropenem                  88     83     0.9845     .32708

CCU

Amikacin                   93     52     6.6121       0
Ceftazidime                41     25     2.838      .00452
Cefepime                   58     31     4.4315       0
Ciprofloxacin              40     29     1.8114     .0703
Cefoperazone-sulbactam     78     43     5.5771       0
Piperacillin-tazobactam    73     40     5.3191       0
Meropenem                  99     50     7.9709       0

TOTAL

Amikacin                   86     66     5.2925       0
Ceftazidime                46     30     4.3462       0
Cefepime                   56     34     5.335        0
Ciprofloxacin              40     31     2.3333     .0198
Cefoperazone-sulbactam     81     56     6.4772       0
Piperacillin-tazobactam    79     52     6.8697       0
Meropenem                  95     69     7.3563       0

CCU critical care unit.

Table 3a. Antibiotic susceptibility patterns of Gram-negative
isolates in 2003 and 2013 (in percentage, rounded to the nearest full
number) and comparison of resistance in 2003 vs. 2013

                      Ceftazidime

                                Resistance
                                comparison
                               2003 vs. 2013
               2003   2013
                %      %     Z score   p value
E. coli
Total           44     29     3.466    .00058
Outpatient      53     41    1.0466    .29372
Inpatient       40     24    1.7747    .07672
CCU             41     21    2.0918    .03662
K. pneumoniae
Total           50     27    3.2198    .00128
Outpatient      57     25    2.1543    .03156
Inpatient       55     36    1.5663    .11642
CCU             39     19    2.2114     .0217
P. aeruginosa
Total           51     57    -1.0625   .28914
Outpatient      60     50    0.3519    .72634
Inpatient       46     67    -1.2635   .20766
CCU             47     55    -0.5354    .5892

                  Cefepime

                                Resistance
                               comparison
                              2003 vs. 2013
               2003  2013
                %     %     Z score   p value
E. coli
Total          47     35    2.4535    .01428
Outpatient     56     41    1.2927    .19706
Inpatient      40     32    0.8882    .37346
CCU            46     34    1.1173    .26272
K. pneumoniae
Total          62     30    4.7265       0
Outpatient     57     33     1.543    .12356
Inpatient      68     37    2.5915     .0096
CCU            61     23    3.8936     .0001
P. aeruginosa
Total          57     55    0.6747    .50286
Outpatient     80     38    1.4954    .13362
Inpatient      46     67    -1.2635   .20766
CCU            80     59    1.4181     .1556

                   Cefoperazone-sulbactam

                                Resistance
                              comparison
                             2003 vs. 2013
               2003   2013
                %      %     Z score   p value
E. coli
Total           87     76    2.2 53    .02444
Outpatient      85     81    0.4732    .63836
Inpatient       93     77    1.9972     .0455
CCU             84     71    1.4529    1.14706
K. pneumoniae
Total           78     41    4.9607       0
Outpatient      79     42    2.3453    .01878
Inpatient       77     46    2.6293    .00854
CCU             77     34    3.5991    .00032
P. aeruginosa
Total           82     52    2.2574    .02382
Outpatient      98     50    1.0817    .28014
Inpatient       69     53    0.9705    .33204
CCU             80     52    1.8259    .06724

                     Piperacillin-tazobactam

                                Resistance
                               comparison
                              2003 vs. 2013
               2003   2013
                %      %      Z score   p value
E. coli
Total          78      65     2.5117    .01174
Outpatient     88      68     2.8022    .03752
Inpatient      83      68     1.9536     .5118
CCU            65      60     0.4428    .65994
K. pneumoniae
Total          77      38     5.9395       0
Outpatient     79      39     2.5198    .01174
Inpatient      82      47     2.9157     .0035
CCU            71      29      4.784       0
P. aeruginosa
Total          85      77     0.9561    .33706
Outpatient     100     88     0.8229    .41222
Inpatient      69      73     0.2755    .77948
CCU            87      69     1.2853    .19706

CCU critical care unit.

Table 3b. Antibiotic susceptibility patterns of Gram-negative
isolates in 2003 and 2013 (in percentage, rounded to the nearest full
number) and comparison of resistance in 2003 vs. 2013

                       Amikacin

                                      Resistance
                                      comparison
                                    2003 vs. 2013
                2003     2013
                 %        %       Z score   p value
E. coli

Total            90       89       0.147    .88076
Outpatient       88       89      -0.127    .89656
Inpatient        87       90      -0.481    .63122
CCU              95       90      0.8454    .39532

K. pneumoniae

Total            88       53      4.9262       0
Outpatient       79       58      1.3386    .18024
Inpatient        77       57      0.7648     .0784
CCU              94       44       4.567       0

P. aeruginosa

Total            74       66      0.9967    .31732
Outpatient       80       75      0.2082    .83366
Inpatient        54       57      -0.171    .86502
CCU              87       66      1.4932    .31732

                       Ciprofloxacin

                                  Resistance
                                  comparison
                                2003 vs. 2013
                2003   2013
                 %      %     Z score   p value
E. coli

Total            31     31    0.8808    .37886
Outpatient       32     57    -2.0645    .0394
Inpatient        30     21    0.1237    .26272
CCU              32     26    0.6924     .4902

K. pneumoniae

Total            46     32    1.9986     .0455
Outpatient       43     31    0.8245    .41222
Inpatient        55     39    1.3516    .17702
CCU              39     26    1.4054    .15854

P. aeruginosa

Total            59     47    0.4977    .61708
Outpatient       80     38    1.4954    .13362
Inpatient        38     47    0.4976    .61708
CCU              60     55    0.3064    .75656

                    Meropenem

                                 Resistance
                                 comparison
                                2003 vs. 2013
                2003   2013
                 %      %     Z score   p value
E. coli

Total           100     95    1.1698     .242
Outpatient      100    100    1.0596    .29372
Inpatient       100     96    0.2368    .81034
CCU             100     91    1.8349    .06724

K. pneumoniae

Total            99     54    5.5334       0
Outpatient      100     60    2.3496    .01878
Inpatient        99     59    1.6498    .09894
CCU              99     43     5.274       0

P. aeruginosa

Total           100     65    3.4913    .00048
Outpatient      100     75    1.2154    .22246
Inpatient       100     50    1.1662     .242
CCU             100     48     3.431     .0006

CCU critical care unit.

Table 4. Antibiotic susceptibility of Gram-negative isolates from
2003 to 2013 (in percentage, rounded to the nearest full number)

                                            Cefoperazone-
          Amikacin           Ceftazidime      sulbactam

       OP    IP    CCU   OP    IP    CCU   OP    IP    CCU

2003   85    77    93    55    46    41    83    83    78
2004   85    64    84    54    35    36    81    69    77
2005   88    81    78    72    59    47    91    87    82
2006   67    71    65    41    34    29    91    77    70
2007   62    52    64    47    39    38    77    80    69
2008   79    63    65    56    46    37    82    81    67
2009   67    66    56    49    44    31    84    81    52
2010   61    63    52    34    31    39    82    72    56
2011   72    60    47    37    29    32    72    67    48
2012   81    74    60    38    26    38    70    65    52
2013   74    76    52    35    32    25    60    65    43

       Piperacillin-
        tazobactam          Meropenem

       OP    IP    CCU   OP    IP    CCU

2003   87    80    73    99    98    99
2004   81    73    65    96    95    98
2005   91    85    83    98    97    95
2006   81    66    72    95    98    97
2007   61    58    62    100   96    95
2008   71    65    61    98    97    94
2009   69    60    44    94    95    71
2010   49    48    50    99    94    66
2011   61    60    42    92    86    57
2012   67    53    48    92    84    58
2013   57    61    40    79    83    50

CCU critical care unit; IP inpatient; OP outpatient.

Table 5. Susceptibility to polymyxin E and tigecycline of
Gram-negative isolates (in percentage, rounded to the
nearest full number.
CCU--critical care unit)

                    Total                E. coli

              2011   2012   2013   2011   2012   2013

OUTPATIENT

Polymyxin E    97     93     99     98     98    100
Tigecycline    89     87     89     98    100    100

INPATIENT

Polymyxin E    98    100    100    100    100    100
Tigecycline    90     84     87    100    100     99

CCU
Polymyxin E    91     90     99    100     95    100
Tigecycline    77     79     73    100     95     98

                  Klebsiella

              2011   2012   2013

OUTPATIENT

Polymyxin E   100     96    100
Tigecycline    96     98     97

INPATIENT

Polymyxin E    88    100    100
Tigecycline    89    100     94

CCU
Polymyxin E   100    100    100
Tigecycline   100     89     76

                  Pseudomonas          Acinetobacter

              2011   2012   2013   2011   2012   2013
OUTPATIENT

Polymyxin E    94     96     97
Tigecycline

INPATIENT

Polymyxin E    96    100     99
Tigecycline

CCU

Polymyxin E    98     87     97    100     98     95
Tigecycline                        100     98     80

Table 6. Comparison of susceptibility to polymyxin E and tigecycline
in 2011 vs. 2013 (in percentage, rounded to the nearest full number.
CCU--critical care unit)

                               Comparison of
                            resistance 2011 vs. 2013
              2011   2013
               %      %     Z score   p value
OUTPATIENT

Polymyxin E    97     98    -0.7752    .4354
Tigecycline    89     88    0.1196    .90448

INPATIENT

Polymyxin E    97     99    -1.866    .06148
Tigecycline    89     86    0.9364    .34722

CCU
Polymyxin E    91     98    -3.8051   .00014
Tigecycline    77     73    0.9889    .32218

TOTAL BLOOD
ISOLATES

Polymyxin E    95     99    -4.1913      0
Tigecycline    83     81    1.0556    .28914
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Title Annotation:Original article
Author:Alagesan, Murali; Gopalakrishnan, Ram; Panchatcharam, Senthur Nambi; Dorairajan, Sureshkumar; Ananth
Publication:GERMS
Article Type:Report
Date:Sep 1, 2015
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