Introduction
Antibiotic resistance is a great threat to patient care. This antibiotic resistance
not only increases the total cost of effective treatment but also is associated with
a substantial increase in morbidity and mortality in hospitalized patients.[1]
[2]
[3]
[4] Nosocomial infections are one of the main causes of death in trauma patients, and
bacteria belonging to family Enterobacteriaceae are the most prominent causative agents of these nosocomial infections.[2]
[5] Beta lactam antibiotics are usually the first line of treatment used against the
infections caused by Enterobacteriaceae, however, with time these bugs have evolved by producing extended spectrum of β lactamases
(ESBL). The first ESBL producing Enterobacteriaceae reported from Germany in 1983 and since then, their incidence has been reported to
be increasing rapidly worldwide.[6] In 1994, the first KPC-producing Klebsiella pneumoniae isolate was reported in Japan, which conferred resistance to carbapenems.[7] In 1999, Martínez-Martínez et al found that the combination of porin loss and the
presence of plasmid-mediated β lactamases resulted in carbapenem resistance.[8] New Delhi metallo-β-lactamase (NDM-1) producing Enterobacteriaceae are resistant to all β-lactams and carbapenemens.[9] Unfortunately, today these bugs have started to confer resistance against colistin,
which is the last resort against these highly resistant gram-negative pathogens.[10]
[11]
[12]
This study is unique because of its large sample size, different source of samples,
patients admitted to different settings (intensive care unit [ICU], ward, and outpatient
department [OPD]) and use of wide range of antimicrobial agents. Very few authors
have reported the study with such a large sample size. The present study would help
in understanding the antimicrobial resistance pattern in Enterobacteriaceae pathogens isolated from different settings of level-1 trauma center over a period
of 5 years.
Materials and Methods
Study Period and Place
Retrospective 5 years data (January 2012 to December 2016) was collected from laboratory
information system software of microbiology laboratory of 186 bedded tertiary apex
trauma center, New Delhi. A total of 6,061 isolates belonging to family Enterobacteriaceae were recovered from 5,067 nonrepeated clinical samples. These clinical isolates were
recovered from patients’ clinical samples received during this study period, namely,
blood, urine, body fluid, bone and tissue, tip culture, pus/wound and swab, and respiratory
samples. Duplicate samples were excluded from the study. All organisms were not subjected
to antimicrobial susceptibility testing (AST) by both methods. Therefore, for accuracy,
only those isolates which were subjected to AST by both methods constituted the analysis.
Intermediate sensitive isolates were not included in the study. [Fig. 1] shows the exclusion and inclusion criteria.
Fig. 1 Exclusion and inclusion criteria included in the study.
Bacterial Identification
All the samples were processed as per standard microbiological methods. Bacterial
isolates were identified to species level by the Vitek2 compact identification system
(Biomeriux, France).
Antimicrobial Susceptibility Testing
The antimicrobial susceptibility testing of all isolates was done by the disk diffusion
method on Mueller-Hinton agar. Apart from this, the minimum inhibitory concentrations
(MICs) were also determined by the Vitek2 compact system (using AST GN cards; Biomeriux,
France). The interpretation of zone diameters and MICs was done according to each
year’s CLSI guidelines.
Escherichia coli ATCC 25922 was taken as the control strains. The following antimicrobials (Himedia,
India) were tested: ceftazidime (30 μg), cefotaxime (30 μg), ceftriaxone (30 μg),
cefoxitin (30 μg), cefepime (30 μg), piperacillin (100 µg), piperacillin-tazobactam
(100/10 μg), ticarcillin-clavulanate (75/10 μg), cefoperazone-sulbactam (75/30 μg),
cefepime-tazobactam (30/10 µg), ceftriaxone- sulbactam (30/15 µg), imipenem (10 μg),
meropenem (10 μg), ertapenem (10 μg), amikacin (30 μg), gentamicin (10 μg), netilmicin
(30 μg), tobramycin (10 μg), tetracycline (30 µg), Trimethoprim-sulfamethoxazole (1.25/24
µg), ciprofloxacin (5 μg), levofloxacin (5 μg), tigecycline (15 μg), nitrofurantoin
(300 μg), and chloramphenicol (30 μg).
We interpreted the zone diameters and MICs of the isolates as per CLSI recommendations,
2018.[13]
Statistical Analyses
Statistical analyses were performed using the SPSS software for Windows (SPSS Inc.,
Chicago, Illinois, United States, version 15.0). The decreased resistance percentage
was reported as the resistance percentage difference between the first year (2012)
and the last year (2016) of the study.
Results
During the study, a total of 5,067 positive samples were included. The mean age of
the patients from whom the samples were received was 32 years (range ± standard deviation
[SD]: 1 to 87 ± 15.1 years). In male patients, the mean age was 46 years (range ±
SD: 1 to 112 ± 27.11 years) whereas, in female patients, the mean age was found to
be 44.5 years with a range of 2 to 96 ± 26.84 years). The difference of the means
of the age in male and female patients was found to be statistically significant (p = 0.002, 95% confidence interval [CI] = 0.9481–4.2187).
Samples received from ICU (1,472, 29%), wards (2,714, 53.6%), and OPD (881, 17.4%)
admitted patients were included in this study. Maximum number of Enterobacteriaceae isolates were obtained from patients admitted to general surgical ward (1,254, 25%)
followed by neurosurgical ward (1,242, 25%), neurosurgical ICU (739, 15%), polytrauma
ICU (733, 14%), and orthopaedics ward (218, 4%). The outpatients contributed about
(881) 17% of the samples.
The samples included in our study were blood, urine, body fluid, respiratory samples,
bone and tissue, pus/wound and swab, and tip culture. [Table 1] shows the distribution of clinical samples included in this study. Blood culture
yielded the maximum number of isolates (1,663, 33%), followed by pus/wound and swab
(1,317, 26%), urine (849, 17%), respiratory samples (761, 15%), body fluid (268, 5%),
bone and tissue (135, 3%), and tip culture samples (74, 1%).
Table 1
Percentage distribution of Enterobacteriaceae isolates in different samples during
2012–2016
|
Samples (N = 5,067)
|
|
N (%)
|
|
a
N, total number of isolates.
|
|
Blood
|
1,663 (33%)
|
|
Pus/wound + swab
|
1,317 (30%)
|
|
Urine
|
849 (17%)
|
|
Respiratory
|
761 (15%)
|
|
Body fluid
|
268 (5%)
|
|
Bone + tissue
|
135 (3%)
|
|
Tip culture
|
74 (1%)
|
The maximum number of Enterobacteriaceae isolates recovered are from wards (3,535, 58.3%), followed by ICUs (1,626, 26.8%),
and OPDs (900, 14.8%). In ICUs, Klebsiella spp. (815, 50.1%) was found to be the most predominant Enterobacteriaceae followed by E. coli (371, 22.8%) and Enterobacter spp. (135, 8.3%) throughout the study period (
[Fig. 2A]
). In wards also, we found the same pattern except in 2014 and 2015 where E. coli was the most prominent (
[Fig. 2B]
). In OPD, E. coli was the most predominant Enterobacteriaceae (476, 52.8%), followed by Klebsiella spp. (166, 18.4%) and Enterobacter spp. (77, 8.6%) (
[Fig. 2C]
). For the purpose of conciseness, we concentrate on only predominant Enterobacteriaceae isolates, i.e., Klebsiella spp. and E. coli.
Fig. 2 Yearly distribution of Enterobacteriaceae isolates in (A) ICUs, (B) wards, and (C) OPDs. ICU, intensive care unit; OPD, outpatient department.
In ICU settings, both E. coli and Klebsiella spp. isolates showed more than 80% resistance against cephalosporins and quinolones.
E. coli isolates showed maximum resistance to ciprofloxacin (94.6%), followed by ceftazidime
and piperacillin (92%), ticarcillin-clavulanate (84.6%), and levofloxacin (84%). Among
carbapenems, E. coli isolates showed more resistance against ertapenem (56%), followed by meropenem (36.3%)
and imipenem (19.4%). The resistance against amikacin and chloramphenicol in E. coli isolates was observed in 38 and 29%, respectively. Among quinolones, Klebsiella spp. isolates showed maximum resistance to ciprofloxacin (85%), followed by levofloxacin
(77.8%). These isolates also showed resistance against carbapenems; the resistance
pattern was the same as observed in E. coli isolates, i.e., ertapenem (69%) > meropenem (67.3%) > imipenem (59%). Both E. coli and Klebsiella spp. isolates showed least resistance to tigecycline; Klebsiella spp. isolates showed 16% resistance, while E. coli isolated showed less than 1% resistance. All the urine isolates were resistant (98–100%)
to nitrofurantoin. The year-wise resistance pattern against different antibiotics
of Enterobacteriaceae in ICU settings is given in [Table 2]. In wards, E. coli showed 90% resistance to cephalosporins, 84% resistance to ceftazidime, and 81% resistance
to levofloxacin. Among aminoglycosides, highest resistance was observed against gentamycin
(55%), followed by tobramycin (41%) and amikacin (27%). Among carbapenems, maximum
resistance was observed against ertapenem (46.8%), followed by meropenem (31.8%) and
imipenem (16.1%). Klebsiella spp. isolates showed 92% resistance to ceftazidime, 89% to ciprofloxacin, and 79%
to levofloxacin. Among aminoglycosides, Klebsiella spp. showed highest resistance against gentamycin (80%), followed by amikacin (73%).
Among carbapenems, resistance against both ertapenem and meropenem was 67% and against
imipenem was 53%. The year-wise resistance pattern against different antibiotics of
Enterobacteriaceae in wards settings is given in [Table 3].
Table 2
Antimicrobial resistance pattern of Enterobacteriaceae pathogens isolated from ICUs
against different antibiotics
|
Organism name
|
Year
|
AMK, N (%)
|
CEFEP, N (%)
|
CEFEPTAZ, N (%)
|
CEFOSUL, N (%)
|
CEFOT, N (%)
|
CEFOX, N (%)
|
CEFTAZ, N (%)
|
CEFTRX, N (%)
|
CEFTRXSUL, N (%)
|
CHL, N (%)
|
CIPRO, N (%)
|
ERTA, N (%)
|
GENTA, N (%)
|
IMI, N (%)
|
LEVO, N (%)
|
MERO, N (%)
|
NETIL, N (%)
|
PIP, N (%)
|
PIPTAZ,N (%)
|
TETRA, N (%)
|
TIC, N (%)
|
TICLAV,N (%)
|
TIG, N (%)
|
TOBRA, N (%)
|
TMZ, N (%)
|
|
Abbreviations: AMK, amikacin; CEFEP, cefepime; CEFEPTAZ, cefepime-tazobactam; CEFOSUL,
cefoperazone-sulbactam; CEFOT, cefotaxime; CEFOX, cefoxitin; CEFTAZ, ceftazidime;
CEFTRX, ceftriaxone; CEFTRXSUL, ceftriaxone-sulbactam; CHL, chloramphenicol; CIPRO,
ciprofloxacin; ERTA, ertapenem; GENTA, gentamicin; IMI, imipenem; IR, intrinsic resistance;
LEVO, levofloxacin; MERO, meropenem; NA, not applicable; NETIL, netilmicin; PIP, piperacillin;
PIPTAZ, piperacillin-tazobactam; TETRA, tetracycline; TIC, ticarcillin-clavulanate;
TIG, tigecycline; TOBRA, tobramycin; TMZ, Trimethoprim/sulfamethoxazole.
Note: N denotes the number of isolates.
|
|
Citrobacter spp.
|
2012 (8)
|
8 (100)
|
8 (100)
|
NA
|
8 (100)
|
NA
|
8 (100)
|
8 (100)
|
8 (100)
|
NA
|
2 (25)
|
8 (100)
|
1 (14)
|
8 (100)
|
2 (25)
|
2 (25)
|
2 (25)
|
8 (100)
|
8 (100)
|
8 (100)
|
0
|
8 (100)
|
8 (100)
|
0
|
8 (100)
|
NA
|
|
2013 (1)
|
0 (0)
|
0 (0)
|
NA
|
0
|
NA
|
0
|
0
|
0
|
NA
|
NA
|
0
|
NA
|
0
|
0
|
0
|
0
|
0
|
1 (100)
|
0
|
0
|
1 (100)
|
0
|
0
|
NA
|
NA
|
|
2014 (0)
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
|
2015 (1)
|
0 (0)
|
0 (0)
|
0 (0)
|
0
|
0
|
0
|
0
|
0
|
0
|
1 (100)
|
0
|
1 (100)
|
0
|
0
|
0
|
0
|
0
|
0
|
0
|
0
|
0
|
0
|
0
|
NA
|
1 (100)
|
|
2016 (0)
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
|
Enterobacter spp.
|
2012 (44)
|
39 (88)
|
39 (88)
|
NA
|
38 (86)
|
NA
|
IR
|
40 (91)
|
40 (91)
|
NA
|
30 (69)
|
38 (86)
|
40 (92)
|
39 (89)
|
33 (75)
|
37 (84)
|
37 (82)
|
38 (86)
|
40 (91)
|
38 (86)
|
20 (45)
|
43 (97)
|
38 (87)
|
4 (9)
|
43 (97)
|
NA
|
|
2013 (28)
|
13 (46)
|
19 (67)
|
13 (46)
|
18 (64)
|
15 (53)
|
IR
|
24 (86)
|
19 (68)
|
13 (46)
|
10 (35)
|
19 (68)
|
12 (43)
|
17 (61)
|
15 (54)
|
13 (46)
|
17 (61)
|
16 (57)
|
24 (86)
|
15 (52)
|
14 (50)
|
28 (100)
|
20 (70)
|
4 (13)
|
28 (100)
|
0 (0)
|
|
2014 (31)
|
20 (65)
|
22 (71)
|
20 (63)
|
21 (67)
|
23 (74)
|
IR
|
23 (74)
|
24 (77)
|
23 (74)
|
10 (31)
|
21 (68)
|
22 (71)
|
23 (74)
|
17 (55)
|
21 (68)
|
18 (58)
|
21 (69)
|
24 (77)
|
19 (61)
|
0 (0)
|
NA
|
26 (84)
|
5 (17)
|
NA
|
24 (77.4)
|
|
2015 (21)
|
8 (40)
|
13 (63)
|
6 (29)
|
6 (29)
|
14 (67)
|
IR
|
15 (70)
|
18 (88)
|
8 (40)
|
11 (50)
|
11 (50)
|
10 (46)
|
13 (60)
|
3 (16)
|
11 (50)
|
3 (15)
|
13 (60)
|
14 (65)
|
5 (26)
|
21 (100)
|
0 (0)
|
13 (61)
|
2 (11)
|
NA
|
10 (50)
|
|
2016 (11)
|
5 (46)
|
4 (36)
|
6 (55)
|
6 (55)
|
11 (100)
|
IR
|
6 (55)
|
6 (55)
|
6 (55)
|
4 (36)
|
6 (55)
|
0 (0)
|
6 (55)
|
4 (36)
|
6 (50)
|
6 (55)
|
5 (46)
|
6 (55)
|
6 (55)
|
NA
|
NA
|
6 (50)
|
0 (0)
|
0 (0)
|
0 (0)
|
|
Escherichia coli
|
2012 (52)
|
17 (33)
|
39 (75)
|
NA
|
32 (62)
|
NA
|
35 (67)
|
46 (88)
|
47 (90)
|
NA
|
10 (20)
|
49 (94)
|
9 (17)
|
27 (52)
|
11 (21)
|
44 (85)
|
29 (56)
|
16 (30)
|
51 (98)
|
39 (75)
|
44 (85)
|
50 (96)
|
35 (67)
|
0
|
52 (100)
|
NA
|
|
2013 (80)
|
26 (33)
|
66 (82)
|
22 (28)
|
37 (46)
|
77 (96)
|
48 (60)
|
76 (95)
|
73 (91)
|
37 (46)
|
20 (25)
|
72 (90)
|
21 (26)
|
51 (64)
|
11 (14)
|
67 (84)
|
41 (51)
|
26 (33)
|
65 (81)
|
51 (64)
|
70 (88)
|
78 (97)
|
75 (94)
|
1 (1)
|
80 (100)
|
0 (0)
|
|
2014 (100)
|
33 (33)
|
77 (77)
|
34 (34)
|
43 (43)
|
94 (94)
|
67 (67)
|
85 (85)
|
94 (94)
|
48 (48)
|
22 (22)
|
94 (94)
|
62 (62)
|
62 (62)
|
27 (27)
|
70 (70)
|
41 (41)
|
33 (33)
|
87 (87)
|
55 (55)
|
NA
|
NA
|
84 (84)
|
1 (1)
|
NA
|
83 (83.8)
|
|
2015 (65)
|
32 (49)
|
57 (88)
|
33 (51)
|
28 (43)
|
65 (100)
|
NA
|
63 (97)
|
65 (100)
|
46 (70)
|
23 (36)
|
65 (100)
|
49 (76)
|
50 (77)
|
6 (9)
|
64 (99)
|
9 (14)
|
34 (53)
|
64 (99)
|
34 (53)
|
NA
|
NA
|
59 (91)
|
0 (0)
|
NA
|
47 (72.3)
|
|
2016 (74)
|
34 (46)
|
69 (93)
|
26 (35)
|
30 (40)
|
71 (96)
|
NA
|
71 (96)
|
71 (96)
|
44 (60)
|
33 (44)
|
71 (96)
|
66 (89)
|
60 (81)
|
17 (23)
|
66 (89)
|
18 (24)
|
36 (48)
|
73 (99)
|
37 (50)
|
NA
|
NA
|
61 (83)
|
0 (0)
|
NA
|
56 (75)
|
|
Klebsiella pneumoniae
|
2012 (176)
|
148 (84)
|
162 (92)
|
NA
|
162 (92)
|
176 (100)
|
165 (94)
|
169 (96)
|
171 (97)
|
NA
|
116 (66)
|
171 (97)
|
128 (73)
|
158 (90)
|
121 (69)
|
162 (92)
|
144 (82)
|
160 (91)
|
169 (96)
|
153 (87)
|
118 (67)
|
IR
|
172 (98)
|
42 (24)
|
174 (99)
|
NA
|
|
2013 (199)
|
167 (84)
|
187 (94)
|
151 (76)
|
177 (89)
|
195 (98)
|
171 (86)
|
187 (94)
|
189 (95)
|
159 (80)
|
111 (56)
|
185 (93)
|
109 (55)
|
169 (85)
|
123 (62)
|
169 (85)
|
161 (81)
|
165 (83)
|
191 (96)
|
153 (77)
|
107 (54)
|
IR
|
189 (94)
|
34 (17)
|
199 (100)
|
0 (0)
|
|
2014 (119)
|
88 (74)
|
104 (87)
|
87 (73)
|
94 (79)
|
106 (89)
|
95 (80)
|
104 (87)
|
112 (94)
|
88 (74)
|
48 (40)
|
95 (80)
|
83 (70)
|
94 (79)
|
71 (60)
|
75 (63)
|
90 (76)
|
83 (70)
|
105 (88)
|
91 (76)
|
0 (0)
|
IR
|
106 (89)
|
19 (16)
|
NA
|
94 (79.6)
|
|
2015 (184)
|
96 (52)
|
166 (90)
|
94 (51)
|
131 (71)
|
177 (96)
|
NA
|
158 (86)
|
166 (90)
|
132 (72)
|
101 (55)
|
145 (79)
|
118 (64)
|
134 (73)
|
75 (41)
|
138 (75)
|
88 (48)
|
107 (58)
|
169 (92)
|
132 (71)
|
NA
|
IR
|
160 (87)
|
21 (12)
|
NA
|
145 (80.1)
|
|
2016 (137)
|
122 (89)
|
126 (92)
|
104 (76)
|
96 (70)
|
137 (100)
|
NA
|
132 (96)
|
123 (90)
|
119 (87)
|
92 (67)
|
104 (76)
|
121 (88)
|
100 (73)
|
90 (66)
|
90 (66)
|
66 (48)
|
127 (93)
|
136 (99)
|
89 (65)
|
NA
|
IR
|
117 (86)
|
19 (14)
|
0 (0)
|
112 (82)
|
|
Morganella spp.
|
2012 (0)
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
IR
|
NA
|
NA
|
|
2013 (0)
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
IR
|
NA
|
NA
|
|
2014 (0)
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
IR
|
NA
|
NA
|
|
2015 (2)
|
2 (100)
|
0
|
0
|
2 (100)
|
2 (100)
|
0
|
2 (100)
|
0
|
2 (100)
|
0
|
2 (100)
|
0
|
2 (100)
|
0
|
2 (100)
|
0
|
2 (100)
|
2 (100)
|
2 (100)
|
0
|
NA
|
2 (100)
|
IR
|
NA
|
2 (100)
|
|
2016 (0)
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
IR
|
NA
|
NA
|
|
Proteus spp.
|
2012 (17)
|
11 (63)
|
17 (100)
|
NA
|
0 (0)
|
NA
|
2 (14)
|
15 (88)
|
17 (100)
|
NA
|
11 (67)
|
17 (100)
|
NA
|
9 (50)
|
0 (0)
|
13 (77)
|
9 (53)
|
17 (100)
|
5 (31)
|
0 (0)
|
IR
|
14 (82)
|
6 (36)
|
IR
|
17 (100)
|
NA
|
|
2013 (33)
|
13 (38)
|
29 (89)
|
4 (13)
|
3 (9)
|
24 (73)
|
9 (26)
|
26 (79)
|
20 (61)
|
4 (13)
|
24 (74)
|
15 (46)
|
33 (100)
|
18 (55)
|
2 (6)
|
18 (55)
|
21 (64)
|
28 (85)
|
7 (21)
|
1 (3)
|
IR
|
33 (100)
|
14 (43)
|
IR
|
33 (100)
|
0 (0)
|
|
2014 (15)
|
11 (73)
|
12 (80)
|
1 (7)
|
6 (40)
|
9 (63)
|
5 (36)
|
12 (80)
|
8 (53)
|
2 (13)
|
12 (80)
|
13 (87)
|
0 (0)
|
12 (80)
|
6 (39)
|
12 (80)
|
6 (40)
|
14 (93)
|
6 (40)
|
0 (0)
|
IR
|
NA
|
8 (53)
|
IR
|
NA
|
14 (93.3)
|
|
2015 (10)
|
0 (0)
|
3 (30)
|
0
|
0
|
2 (22)
|
0
|
3 (30)
|
0
|
0
|
8 (80)
|
3 (30)
|
0
|
2 (20)
|
0
|
3 (30)
|
0
|
3 (30)
|
0
|
6 (60)
|
IR
|
NA
|
0
|
IR
|
NA
|
4 (40)
|
|
2016 (16)
|
5 (31)
|
3 (19)
|
1 (6)
|
1 (6)
|
10 (60)
|
NA
|
6 (38)
|
7 (44)
|
2 (13)
|
2 (15)
|
9 (56)
|
0 (0)
|
6 (38)
|
3 (19)
|
10 (60)
|
1 (6)
|
6 (38)
|
1 (6)
|
1 (6)
|
IR
|
0 (0)
|
1 (6)
|
IR
|
0 (0)
|
6 (35.7)
|
|
Providencia spp.
|
2012 (8)
|
7 (88)
|
5 (57)
|
NA
|
7 (88)
|
NA
|
7 (86)
|
7 (88)
|
7 (88)
|
NA
|
8 (100)
|
4 (50)
|
NA
|
7 (88)
|
6 (75)
|
4 (50)
|
1 (13)
|
7 (88)
|
7 (88)
|
6 (7.5)
|
IR
|
6 (80)
|
8 (100)
|
IR
|
8 (100)
|
NA
|
|
2013 (34)
|
23 (68)
|
23 (67)
|
28 (83)
|
26 (77)
|
31 (92)
|
20 (60)
|
26 (76)
|
26 (76)
|
28 (83)
|
23 (69)
|
28 (82)
|
0 (0)
|
28 (82)
|
9 (27)
|
29 (85)
|
21 (62)
|
25 (74)
|
22 (65)
|
13 (38)
|
IR
|
13 (38)
|
27 (79)
|
IR
|
34 (100)
|
0 (0)
|
|
2014 (18)
|
17 (94)
|
17 (94)
|
13 (72)
|
17 (92)
|
17 (94)
|
14 (78)
|
18 (100)
|
17 (94)
|
15 (83)
|
13 (71)
|
17 (94)
|
18 (100)
|
18 (100)
|
17 (94)
|
17 (94)
|
13 (72)
|
18 (100)
|
17 (94)
|
17 (94)
|
IR
|
NA
|
18 (100)
|
IR
|
NA
|
7 (41.2)
|
|
2015 (1)
|
1 (100)
|
1 (100)
|
0
|
0
|
1 (100)
|
0
|
1 (100)
|
0
|
0
|
1 (100)
|
1 (100)
|
0
|
1 (100)
|
0
|
1 (100)
|
0
|
1 (100)
|
0
|
0
|
IR
|
NA
|
1 (100)
|
IR
|
NA
|
NA
|
|
2016 (4)
|
1 (33)
|
1 (33)
|
1 (33)
|
1 (33)
|
0 (0)
|
NA
|
1 (33)
|
1 (33)
|
1 (33)
|
0 (0)
|
1 (33)
|
0 (0)
|
1 (33)
|
0 (0)
|
1 (33)
|
1 (33)
|
1 (33)
|
1 (33)
|
1 (33)
|
IR
|
0 (0)
|
1 (33)
|
IR
|
0 (0)
|
1 (25)
|
|
Salmonella spp.
|
2012 (0)
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
|
2013 (0)
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
|
2014 (1)
|
1 (100)
|
1 (100)
|
0
|
0
|
1 (100)
|
0
|
1 (100)
|
1 (100)
|
0
|
0
|
0
|
0
|
1 (100)
|
0
|
0
|
0
|
0
|
0
|
0
|
0
|
NA
|
0
|
0
|
0
|
0
|
|
2015 (4)
|
1 (25)
|
0
|
0
|
0
|
0
|
0
|
0
|
0
|
0
|
0
|
1 (25)
|
0
|
1 (25)
|
0
|
1 (25)
|
0
|
0
|
1 (25)
|
0
|
0
|
NA
|
0
|
0
|
NA
|
0
|
|
2016 (0)
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
|
Serratia spp.
|
2012 (21)
|
17 (81)
|
14 (65)
|
NA
|
15 (71)
|
NA
|
IR
|
18 (86)
|
18 (86)
|
NA
|
6 (30)
|
14 (67)
|
NA
|
8 (38)
|
5 (25)
|
13 (62)
|
9 (45)
|
14 (67)
|
21 (100)
|
18 (86)
|
7 (35)
|
18 (86)
|
21 (100)
|
11 (50)
|
18 (86)
|
NA
|
|
2013 (20)
|
11 (55)
|
12 (62)
|
6 (29)
|
9 (47)
|
10 (50)
|
IR
|
17 (85)
|
15 (75)
|
6 (29)
|
2 (10)
|
7 (37)
|
0 (0)
|
6 (30)
|
4 (21)
|
3 (15)
|
7 (35)
|
15 (75)
|
15 (75)
|
2 (11)
|
0 (0)
|
19 (93)
|
15 (74)
|
2 (11)
|
18 (92)
|
0 (0)
|
|
2014 (36)
|
28 (78)
|
29 (81)
|
1 (4)
|
5 (14)
|
33 (91)
|
IR
|
32 (89)
|
30 (83)
|
4 (11)
|
9 (25)
|
15 (42)
|
12 (33)
|
5 (14)
|
13 (37)
|
8 (22)
|
9 (25)
|
27 (74)
|
28 (78)
|
0 (0)
|
0 (0)
|
NA
|
24 (67)
|
8 (23)
|
NA
|
15 (41.7)
|
|
2015 (25)
|
2 (8)
|
8 (32)
|
4 (17)
|
5 (20)
|
25 (100)
|
IR
|
12 (48)
|
20 (80)
|
3 (12)
|
4 (16)
|
8 (32)
|
25 (100)
|
1 (4)
|
6 (22)
|
3 (13)
|
4 (16)
|
21 (83)
|
8 (32)
|
7 (28)
|
0 (0)
|
NA
|
8 (32)
|
4 (17)
|
NA
|
1 (4)
|
|
2016 (30)
|
26 (85)
|
26 (85)
|
3 (11)
|
6 (19)
|
27 (90)
|
IR
|
29 (96)
|
29 (96)
|
19 (63)
|
9 (29)
|
12 (40)
|
0 (0)
|
8 (26)
|
0 (0)
|
23 (75)
|
0 (0)
|
29 (96)
|
29 (96)
|
2 (8)
|
0 (0)
|
0 (0)
|
29 (96)
|
2 (7)
|
0 (0)
|
0 (0)
|
Table 3
Antimicrobial resistance pattern of Enterobacteriaceae pathogens isolated from wards
against different antibiotics
|
Organism name
|
Year
|
AMK, N (%)
|
CEFEP, N (%)
|
CEFEPTAZ, N (%)
|
CEFOSUL, N (%)
|
CEFOT, N (%)
|
CEFOX, N (%)
|
CEFTAZ, N (%)
|
CEFTRX, N (%)
|
CEFTRXSUL, N (%)
|
CHL, N (%)
|
CIPRO, N (%)
|
ERTA, N (%)
|
GENTA, N (%)
|
IMI, N (%)
|
LEVO, N (%)
|
MERO, N (%)
|
NETIL, N (%)
|
PIP, N (%)
|
PIPTAZ, N (%)
|
TETRA, N (%)
|
TIC, N (%)
|
TICLAV, N (%)
|
TIG, N (%)
|
TOBRA, N (%)
|
TMZ, N (%)
|
|
Abbreviations: AMK, amikacin; CEFEP, cefepime; CEFEPTAZ, cefepime-tazobactam; CEFOSUL,
cefoperazone-sulbactam; CEFOT, cefotaxime; CEFOX, cefoxitin; CEFTAZ, ceftazidime;
CEFTRX, ceftriaxone; CEFTRXSUL, ceftriaxone-sulbactam; CHL, chloramphenicol; CIPRO,
ciprofloxacin; ERTA, ertapenem; GENTA, gentamicin; IMI, imipenem; IR, intrinsic resistance;
LEVO, levofloxacin; MERO, meropenem; NETIL, netilmicin; PIP, piperacillin; PIPTAZ,
piperacillin-tazobactam; TETRA, tetracycline; TIC, ticarcillin-clavulanate; TIG, tigecycline;
TOBRA, tobramycin; TMZ, trimethoprim/sulfamethoxazole.
Note: N denotes the number of isolates.
|
|
Citrobacter spp.
|
2012 (25)
|
18 (73)
|
14(57)
|
0 (0)
|
17 (69)
|
0 (0)
|
18 (73)
|
18 (73)
|
19 (76)
|
0 (0)
|
15 (60)
|
15 (58)
|
16 (63)
|
18 (73)
|
13 (50)
|
7 (28)
|
10 (39)
|
17 (67)
|
19 (76)
|
15 (60)
|
4 (17)
|
23 (92)
|
21 (85)
|
0 (0)
|
25 (100)
|
0 (0)
|
|
2013 (9)
|
5 (55)
|
5 (55)
|
6 (71)
|
5 (55)
|
9 (100)
|
7 (82)
|
6 (64)
|
7 (82)
|
6 (71)
|
6 (71)
|
5 (55)
|
7 (75)
|
5 (55)
|
2 (27)
|
2 (27)
|
4 (46)
|
5 (55)
|
5 (60)
|
5 (55)
|
5 (50)
|
6 (67)
|
7 (73)
|
0 (0)
|
9 (100)
|
0 (0)
|
|
2014 (10)
|
3 (31)
|
3 (31)
|
3 (31)
|
4 (38)
|
4 (36)
|
6 (62)
|
5 (50)
|
4 (38)
|
4 (36)
|
2 (23)
|
2 (19)
|
6 (56)
|
4 (38)
|
1 (14)
|
1 (13)
|
1 (6)
|
2 (23)
|
4 (44)
|
4 (38)
|
0 (0)
|
0 (0)
|
5 (50)
|
0 (0)
|
0 (0)
|
0 (0)
|
|
2015 (3)
|
2 (50)
|
1 (33)
|
0 (0)
|
1 (40)
|
1 (40)
|
0 (0)
|
1 (33)
|
2 (67)
|
0 (0)
|
1 (25)
|
2 (60)
|
1 (25)
|
2 (50)
|
1 (33)
|
2 (50)
|
1 (33)
|
2 (50)
|
1 (17)
|
0 (0)
|
0 (0)
|
0 (0)
|
2 (50)
|
0 (0)
|
0 (0)
|
0 (0)
|
|
2016 (18)
|
5 (30)
|
10 (55)
|
5 (25)
|
11 (60)
|
18 (100)
|
0 (0)
|
12 (68)
|
12 (68)
|
12 (65)
|
12 (68)
|
12 (65)
|
10 (55)
|
7 (39)
|
3 (15)
|
5 (28)
|
3 (17)
|
7 (40)
|
13 (70)
|
8 (44)
|
0 (0)
|
0 (0)
|
13 (70)
|
0 (0)
|
0 (0)
|
3 (17)
|
|
Enterobacter spp.
|
2012 (89)
|
57 (64)
|
59 (66)
|
0 (0)
|
61 (68)
|
0 (0)
|
IR
|
68 (76)
|
69 (77)
|
0 (0)
|
36 (41)
|
60 (67)
|
39(44)
|
61(68)
|
46 (52)
|
53 (60)
|
54 (61)
|
58 (65)
|
73 (82)
|
55 (62)
|
40 (45)
|
75 (84)
|
76 (85)
|
7 (8)
|
89 (100)
|
0 (0)
|
|
2013 (99)
|
51 (52)
|
57(58)
|
44 (44)
|
60 (61)
|
70 (71)
|
IR
|
73 (74)
|
68 (69)
|
58 (59)
|
58 (59)
|
53 (54)
|
41 (41)
|
58 (59)
|
41 (41)
|
47 (47)
|
40 (40)
|
59 (60)
|
77 (78)
|
55 (56)
|
32 (32)
|
84 (85)
|
76 (77)
|
4 (4)
|
95 (96)
|
0 (0)
|
|
2014 (56)
|
27 (48)
|
36 (64)
|
29 (51)
|
30 (54)
|
38 (68)
|
IR
|
42 (75)
|
30 (54)
|
38 (68)
|
25 (45)
|
28 (50)
|
31 (55)
|
35 (63)
|
24 (42)
|
17 (31)
|
23 (41)
|
30 (54)
|
39 (69)
|
31 (55)
|
0 (0)
|
0 (0)
|
41 (74)
|
1 (2)
|
0 (0)
|
0 (0)
|
|
2015 (58)
|
31 (54)
|
32 (56)
|
6 (11)
|
24 (41)
|
36 (62)
|
IR
|
43 (74)
|
41 (71)
|
26 (44)
|
27 (47)
|
30 (52)
|
24 (41)
|
39 (68)
|
15 (25)
|
27 (46)
|
15 (25)
|
26 (45)
|
38 (65)
|
26 (44)
|
0 (0)
|
0 (0)
|
41 (70)
|
0 (0)
|
0 (0)
|
0 (0)
|
|
2016 (49)
|
24 (48)
|
20 (41)
|
18 (37)
|
21 (42)
|
20 (41)
|
IR
|
22 (45)
|
21 (42)
|
22 (44)
|
15 (30)
|
19 (39)
|
30 (61)
|
24 (48)
|
13 (26)
|
20 (40)
|
15 (30)
|
20 (41)
|
22 (44)
|
21 (42)
|
0 (0)
|
0 (0)
|
24 (48)
|
5 (10)
|
0 (0)
|
17 (35)
|
|
Escherichia coli
|
2012 (180)
|
50 (28)
|
124 (69)
|
0 (0)
|
86 (48)
|
4 (2)
|
85 (47)
|
153 (85)
|
160 (89)
|
0 (0)
|
34 (19)
|
166 (92)
|
47 (26)
|
118 (66)
|
32 (18)
|
149 (83)
|
83 (46)
|
40 (22)
|
164 (91)
|
76 (42)
|
157 (87)
|
171 (95)
|
169 (94)
|
9 (5)
|
178 (99)
|
0 (0)
|
|
2013 (264)
|
58 (22)
|
219 (83)
|
71 (27)
|
121 (46)
|
216 (82)
|
153 (58)
|
232 (88)
|
230 (87)
|
116 (44)
|
116 (44)
|
243 (92)
|
69 (26)
|
161 (61)
|
48 (18)
|
206 (78)
|
121 (46)
|
74 (28)
|
246 (93)
|
116 (44)
|
214 (81)
|
259 (98)
|
253 (96)
|
1 (0.3)
|
264 (100)
|
0 (0)
|
|
2014 (248)
|
62 (25)
|
174 (70)
|
62 (25)
|
82 (33)
|
208 (84)
|
149 (60)
|
193(78)
|
82 (33)
|
208 (84)
|
42 (17)
|
218 (88)
|
117 (47)
|
124 (50)
|
42 (17)
|
188 (76)
|
64 (26)
|
87 (35)
|
181 (73)
|
107 (43)
|
0 (0)
|
0 (0)
|
181 (73)
|
2 (1)
|
0 (0)
|
0 (0)
|
|
2015 (172)
|
53 (31)
|
136 (79)
|
52 (30)
|
83 (48)
|
151 (88)
|
0 (0)
|
146 (85)
|
139 (81)
|
96 (56)
|
60 (35)
|
151 (88)
|
120 (70)
|
86 (50)
|
26 (15)
|
146 (85)
|
34 (20)
|
50 (29)
|
151 (88)
|
101 (59)
|
0 (0)
|
0 (0)
|
139 (81)
|
7 (4)
|
0 (0)
|
0 (0)
|
|
2016 (216)
|
69 (32)
|
179 (83)
|
71 (33)
|
102 (47)
|
192 (89)
|
0 (0)
|
179 (83)
|
192 (89)
|
117 (54)
|
63 (29)
|
197 (91)
|
153 (71)
|
104 (48)
|
26 (12)
|
188 (87)
|
41 (19)
|
63 (29)
|
194 (90)
|
106 (49)
|
0 (0)
|
0 (0)
|
166 (77)
|
89 (41)
|
0 (0)
|
147 (68)
|
|
Klebsiella pneumoniae
|
2012 (371)
|
301 (81)
|
341 (92)
|
0 (0)
|
308 (83)
|
0 (0)
|
289 (78)
|
352 (95)
|
349 (94)
|
0 (0)
|
193 (52)
|
341 (92)
|
223 (60)
|
338 (91)
|
237 (64)
|
312 (84)
|
286 (77)
|
289 (78)
|
356 (96)
|
293 (79)
|
249 (67)
|
IR
|
371 (100)
|
111 (30)
|
371 (100)
|
0 (0)
|
|
2013 (290)
|
206 (71)
|
267 (92)
|
168 (58)
|
229(79)
|
247 (85)
|
238 (82)
|
273 (94)
|
273 (94)
|
186 (64)
|
186 (64)
|
261 (90)
|
171 (59)
|
229 (79)
|
165 (57)
|
200 (69)
|
215 (74)
|
223 (77)
|
273 (94)
|
220 (76)
|
136 (47)
|
IR
|
281 (97)
|
78 (27)
|
290 (100)
|
0 (0)
|
|
2014 (206)
|
122 (59)
|
167 (81)
|
136 (66)
|
148 (72)
|
187 (91)
|
161 (78)
|
173 (84)
|
148 (72)
|
187 (91)
|
97 (47)
|
183 (89)
|
146 (71)
|
157 (76)
|
103 (50)
|
150 (73)
|
138 (67)
|
161 (78)
|
173 (84)
|
150 (73)
|
0 (0)
|
IR
|
177 (86)
|
29 (14)
|
0 (0)
|
0 (0)
|
|
2015 (162)
|
115 (71)
|
149 (92)
|
78 (48)
|
125 (77)
|
147 (91)
|
0 (0)
|
152 (94)
|
152 (94)
|
117 (72)
|
91 (56)
|
144 (89)
|
118 (73)
|
122 (75)
|
73 (45)
|
138 (85)
|
84 (52)
|
118 (73)
|
156 (96)
|
120 (74)
|
0 (0)
|
IR
|
152 (94)
|
8 (5)
|
0 (0)
|
0 (0)
|
|
2016 (313)
|
238 (76)
|
269 (86)
|
200 (64)
|
257 (82)
|
297 (95)
|
0 (0)
|
285 (91)
|
285 (91)
|
238 (76)
|
160 (51)
|
269 (86)
|
247 (79)
|
231 (74)
|
135 (43)
|
254 (81)
|
182 (58)
|
257 (82)
|
297 (95)
|
222 (71)
|
0 (0)
|
IR
|
282 (90)
|
16 (5)
|
0 (0)
|
194 (62)
|
|
Morganella spp.
|
2012 (8)
|
3 (33)
|
4 (44)
|
0 (0)
|
6 (78)
|
0 (0)
|
6 (78)
|
4 (56)
|
4 (56)
|
0 (0)
|
3 (38)
|
6 (78)
|
0 (0)
|
5(67)
|
3(33)
|
5 (67)
|
4 (56)
|
3 (33)
|
5 (63)
|
2 (25)
|
6 (71)
|
7 (88)
|
6 (75)
|
IR
|
6 (75)
|
0 (0)
|
|
2013 (13)
|
5 (38)
|
5 (40)
|
4 (30)
|
7 (56)
|
0 (0)
|
11 (88)
|
8 (63)
|
8 (64)
|
4 (30)
|
4 (30)
|
11 (81)
|
13 (100)
|
7 (50)
|
4 (31)
|
10 (75)
|
7 (50)
|
6 (44)
|
8 (63)
|
4 (27)
|
13 (100)
|
11 (83)
|
10 (75)
|
IR
|
13 (100)
|
0 (0)
|
|
2014 (18)
|
10 (53)
|
6 (35)
|
1 (7)
|
10 (53)
|
12 (64)
|
18 (100)
|
13 (71)
|
10 (53)
|
12 (64)
|
12 (67)
|
14 (77)
|
9 (50)
|
13 (71)
|
1 (7)
|
13 (71)
|
2 (12)
|
12 (64)
|
5 (29)
|
4 (24)
|
0 (0)
|
0 (0)
|
10 (53)
|
IR
|
0 (0)
|
0 (0)
|
|
2015 (5)
|
1 (25)
|
1 (13)
|
1 (17)
|
1 (14)
|
2 (33)
|
0 (0)
|
1 (25)
|
1 (17)
|
1 (13)
|
0 (0)
|
2 (38)
|
0 (0)
|
2 (38)
|
1 (25)
|
2 (38)
|
1 (13)
|
2 (33)
|
1 (25)
|
1 (25)
|
0 (0)
|
0 (0)
|
1 (25)
|
IR
|
0 (0)
|
0 (0)
|
|
2016 (7)
|
4 (50)
|
5 (75)
|
4 (50)
|
5 (75)
|
4 (50)
|
0 (0)
|
5 (75)
|
5 (75)
|
5 (75)
|
2 (33)
|
5 (75)
|
0 (0)
|
5 (75)
|
4 (50)
|
5 (75)
|
2 (25)
|
5 (75)
|
5 (75)
|
4 (50)
|
0 (0)
|
0 (0)
|
5 (75)
|
IR
|
0 (0)
|
7 (100)
|
|
Proteus spp.
|
2012 (104)
|
66 (63)
|
62 (60)
|
0 (0)
|
22 (21)
|
0 (0)
|
27 (26)
|
74 (71)
|
76 (73)
|
0 (0)
|
70 (67)
|
79 (76)
|
26 (25)
|
56 (54)
|
17 (16)
|
72 (69)
|
49 (47)
|
87 (84)
|
35 (34)
|
8 (8)
|
IR
|
61 (59)
|
56 (54)
|
IR
|
104 (100)
|
0 (0)
|
|
2013 (106)
|
42 (40)
|
86(81)
|
39 (37)
|
37 (35)
|
57 (54)
|
27 (25)
|
88 (83)
|
76 (72)
|
35 (33)
|
35 (33)
|
75 (71)
|
0 (0)
|
71 (67)
|
18 (17)
|
78 (74)
|
41 (39)
|
88 (83)
|
29 (27)
|
11 (10)
|
IR
|
61 (58)
|
34 (32)
|
IR
|
106 (100)
|
0 (0)
|
|
2014 (46)
|
20 (43)
|
31 (68)
|
15 (32)
|
19 (41)
|
21 (46)
|
16 (35)
|
38 (82)
|
19 (41)
|
21 (46)
|
23 (51)
|
34 (73)
|
0 (0)
|
35 (75)
|
13 (29)
|
29 (62)
|
14 (30)
|
38 (82)
|
10 (21)
|
3 (7)
|
IR
|
0 (0)
|
15 (33)
|
IR
|
0 (0)
|
0 (0)
|
|
2015 (36)
|
16 (45)
|
26 (71)
|
2 (6)
|
1 (4)
|
24 (67)
|
0 (0)
|
25 (70)
|
26 (72)
|
0 (0)
|
26 (71)
|
31 (86)
|
0 (0)
|
23 (64)
|
0 (0)
|
26 (72)
|
0 (0)
|
31 (86)
|
4 (11)
|
4 (11)
|
IR
|
0 (0)
|
7 (20)
|
IR
|
0 (0)
|
0 (0)
|
|
2016 (41)
|
22 (54)
|
25 (60)
|
1 (3)
|
2 (6)
|
23 (55)
|
0 (0)
|
29 (71)
|
27 (67)
|
2 (6)
|
29 (71)
|
18 (44)
|
0 (0)
|
28 (69)
|
7 (18)
|
29 (71)
|
1 (3)
|
29 (71)
|
9 (23)
|
1 (3)
|
IR
|
0 (0)
|
2 (6)
|
IR
|
0 (0)
|
30 (73)
|
|
Providencia spp.
|
2012 (42)
|
31 (73)
|
27 (64)
|
0 (0)
|
28 (67)
|
0 (0)
|
22 (53)
|
31 (73)
|
34 (80)
|
0 (0)
|
15 (36)
|
38 (90)
|
0 (0)
|
37 (87)
|
8 (18)
|
34 (82)
|
26 (63)
|
35 (84)
|
29 (68)
|
6 (15)
|
IR
|
32 (77)
|
32 (75)
|
IR
|
42 (100)
|
0 (0)
|
|
2013 (39)
|
26 (67)
|
26 (66)
|
28 (73)
|
31 (79)
|
35 (90)
|
31 (79)
|
35 (91)
|
36 (93)
|
23 (59)
|
23 (59)
|
32 (81)
|
9 (22)
|
32 (81)
|
18 (47)
|
33(84)
|
29 (75)
|
31 (79)
|
27 (70)
|
24 (61)
|
IR
|
39 (100)
|
32 (83)
|
IR
|
39 (100)
|
0 (0)
|
|
2014 (22)
|
17 (77)
|
14 (62)
|
11 (50)
|
17 (77)
|
20 (89)
|
20 (89)
|
17 (77)
|
17 (77)
|
20 (89)
|
15 (67)
|
18 (83)
|
0 (0)
|
17 (77)
|
10 (44)
|
12 (54)
|
12 (54)
|
17 (78)
|
17 (77)
|
17 (77)
|
IR
|
0 (0)
|
15 (70)
|
IR
|
0 (0)
|
0 (0)
|
|
2015 (1)
|
1 (50)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
1 (50)
|
0 (0)
|
0 (0)
|
1 (50)
|
1 (100)
|
0 (0)
|
1 (50)
|
0 (0)
|
1 (50)
|
0 (0)
|
1 (50)
|
0 (0)
|
1 (50)
|
IR
|
0 (0)
|
0 (0)
|
IR
|
0 (0)
|
0 (0)
|
|
2016 (5)
|
2 (40)
|
0 (0)
|
0 (0)
|
4 (80)
|
0 (0)
|
0 (0)
|
2 (40)
|
2 (40)
|
0 (0)
|
0 (0)
|
4 (80)
|
0 (0)
|
4 (80)
|
2 (40)
|
4 (80)
|
2 (40)
|
2 (40)
|
2 (40)
|
2 (40)
|
IR
|
0 (0)
|
2 (40)
|
IR
|
0 (0)
|
0 (0)
|
|
Salmonella spp.
|
2012 (0)
|
0 (43)
|
0 (0)
|
0 (0)
|
0 (6)
|
0 (0)
|
0 (13)
|
0 (6)
|
0 (7)
|
0 (0)
|
0 (8)
|
0 (21)
|
0 (50)
|
0 (25)
|
0 (7)
|
0 (7)
|
0 (7)
|
0 (20)
|
0 (27)
|
0 (10)
|
0 (0)
|
0 (21)
|
0 (38)
|
0 (8)
|
0 (0)
|
0 (0)
|
|
2013 (4)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
3 (67)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
1 (17)
|
0 (0)
|
0 (0)
|
0 (0)
|
1 (17)
|
3 (83)
|
0 (0)
|
0 (0)
|
0 (0)
|
|
2014 (1)
|
0 (0)
|
0 (0)
|
0 (0)
|
0(0)
|
0 (0)
|
0 (33)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (17)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (17)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (17)
|
0 (0)
|
0 (0)
|
0 (0)
|
|
2015 (1)
|
0 (20)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (40)
|
0 (40)
|
0 (0)
|
0 (0)
|
1 (60)
|
0 (0)
|
1 (60)
|
0 (0)
|
0 (20)
|
0 (0)
|
0 (0)
|
0 (40)
|
0 (40)
|
0 (0)
|
0 (0)
|
0 (40)
|
0 (0)
|
0 (0)
|
0 (0)
|
|
2016 (2)
|
0 (15)
|
0 (8)
|
0 (0)
|
0 (15)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (8)
|
0 (15)
|
0 (0)
|
1 (46)
|
0 (0)
|
0 (8)
|
0 (0)
|
0 (0)
|
0 (15)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (8)
|
0 (0)
|
0 (0)
|
0 (0)
|
|
Serratia spp.
|
2012 (54)
|
49 (91)
|
44 (82)
|
0 (0)
|
46 (86)
|
0 (0)
|
IR
|
40 (74)
|
51 (94)
|
0 (0)
|
14 (26)
|
46 (85)
|
0 (0)
|
21 (38)
|
8 (15)
|
26 (49)
|
12 (23)
|
46 (85)
|
39 (73)
|
8 (15)
|
15 (27)
|
32 (59)
|
42 (78)
|
0 (0)
|
52 (97)
|
0 (0)
|
|
2013 (56)
|
18 (32)
|
31 (55)
|
13 (23)
|
21 (37)
|
44 (79)
|
IR
|
42 (75)
|
38 (68)
|
21 (38)
|
21 (38)
|
18 (32)
|
22 (40)
|
12 (21)
|
14 (25)
|
17 (30)
|
20 (35)
|
29 (51)
|
41 (74)
|
7 (13)
|
18 (33)
|
31 (56)
|
39 (70)
|
0 (0)
|
46 (83)
|
56 (100)
|
|
2014 (35)
|
14 (41)
|
17 (48)
|
2 (5)
|
7 (21)
|
16 (47)
|
IR
|
18 (50)
|
7 (21)
|
16 (47)
|
8 (24)
|
14 (41)
|
12 (33)
|
3 (8)
|
3 (8)
|
9 (25)
|
4 (10)
|
18 (50)
|
14 (40)
|
4 (10)
|
0 (0)
|
0 (0)
|
16 (45)
|
1 (3)
|
0 (0)
|
0 (0)
|
|
2015 (9)
|
1 (11)
|
4 (44)
|
0 (0)
|
2 (25)
|
3 (33)
|
IR
|
4 (44)
|
0 (0)
|
3 (38)
|
4 (43)
|
4 (44)
|
0 (0)
|
0 (0)
|
0 (0)
|
2 (22)
|
0 (0)
|
5 (50)
|
8 (88)
|
5 (50)
|
0 (0)
|
0 (0)
|
6 (67)
|
0 (0)
|
0 (0)
|
0 (0)
|
|
2016 (42)
|
23 (54)
|
28 (67)
|
7 (17)
|
14 (33)
|
32 (77)
|
IR
|
28 (67)
|
28 (67)
|
21 (50)
|
16 (38)
|
24 (57)
|
0 (0)
|
11 (27)
|
1 (3)
|
24 (58)
|
0 (0)
|
28 (67)
|
25 (60)
|
13 (31)
|
0 (0)
|
0 (0)
|
25 (60)
|
10 (23)
|
0 (0)
|
0 (0)
|
In OPD, E. coli showed less than 70% resistance to cephalosporins, resistance against ciprofloxacin
and levofloxacin was 79.4 and 69%, respectively. Among aminoglycosides, maximum resistance
was seen against gentamycin (44%), followed by tobramycin (31.5%) and amikacin (18.3%).
Among carbapenems, maximum resistance was observed against ertapenem (24.5%), followed
by meropenem (18.9%) and imipenem (5.3%). E. coli showed 17% resistance to chloramphenicol. Klebsiella spp. showed 77% resistance to ceftazidime, 70.5% resistance to cefepime, and 65%
resistance to levofloxacin. Among carbapenems, maximum resistance was observed against
meropenem (59%), followed by imipenem (46.3%) and ertapenem (34%). Among aminoglycosides,
maximum resistance seen in Klebsiella spp. isolates was against gentamycin (70%), followed by tobramycin (62.6%) and amikacin
(64%). [Table 4] shows the year-wise resistance pattern against different antibiotics of Enterobacteriaceae of OPD patients. We observed least resistance against tigecycline among both E. coli and Klebsiella spp. (1.5 and 12.6%, respectively).
Table 4
Antimicrobial resistance pattern of Enterobacteriaceae pathogens isolated from OPD
patients against different antibiotics
|
Organism name
|
Year
|
AMK, N (%)
|
CEFEP, N (%)
|
CEFEPTAZ, N (%)
|
CEFOSUL, N (%)
|
CEFOT, N (%)
|
CEFOX, N (%)
|
CEFTAZ, N (%)
|
CEFTRX, N (%)
|
CEFTRXSUL, N (%)
|
CHL, N (%)
|
CIPRO, N (%)
|
ERTA, N (%)
|
GENTA, N (%)
|
IMI, N (%)
|
LEVO, N (%)
|
MERO, N (%)
|
NETIL, N (%)
|
PIP, N (%)
|
PIPTAZ, N (%)
|
TETRA, N (%)
|
TIC, N (%)
|
TICLAV, N (%)
|
TIG, N (%)
|
TOBRA, N (%)
|
TMZ, N (%)
|
|
Abbreviations: AMK, amikacin; CEFEP, cefepime; CEFEPTAZ, cefepime-tazobactam; CEFOSUL,
cefoperazone-sulbactam; CEFOT, cefotaxime; CEFOX, cefoxitin; CEFTAZ, ceftazidime;
CEFTRX, ceftriaxone; CEFTRXSUL, ceftriaxone-sulbactam; CHL, chloramphenicol; CIPRO,
ciprofloxacin; ERTA, ertapenem; GENTA, gentamicin; IMI, imipenem; IR, intrinsic resistance;
LEVO, levofloxacin; MERO, meropenem; NA, not applicable; NETIL, netilmicin; PIP, piperacillin;
PIPTAZ, piperacillin-tazobactam; TETRA, tetracycline; TIC, ticarcillin-clavulanate;
TIG, tigecycline; OPD, outpatient department; TOBRA, tobramycin; TMZ, Trimethoprim/sulfamethoxazole.
Note: N denotes the number of isolates.
|
|
Citrobacter spp.
|
2012 (5)
|
3 (60)
|
2 (40)
|
NA
|
2 (40)
|
NA
|
2 (100)
|
3 (60)
|
3 (75)
|
NA
|
2 (40)
|
1 (25)
|
1 (100)
|
NA
|
2 (40)
|
0 (0)
|
0 (0)
|
2 (50)
|
2 (0)
|
1 (25)
|
1 (25)
|
3 (60)
|
2 (50)
|
0 (0)
|
3 (100)
|
NA
|
|
2013 (2)
|
1 (50)
|
1 (50)
|
NA
|
1 (50)
|
NA
|
1 (50)
|
2 (100)
|
2 (100)
|
NA
|
1 (100)
|
1 (50)
|
2 (100)
|
3 (60)
|
1 (50)
|
1 (50)
|
1 (50)
|
1 (50)
|
1 (50)
|
1 (50)
|
2 (100)
|
2 (100)
|
2 (100)
|
0 (0)
|
1 (100)
|
NA
|
|
2014 (6)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
1 (16.7)
|
1 (16.7)
|
1 (16.7)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
1 (50)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (100)
|
0 (0)
|
NA
|
NA
|
0 (0)
|
0 (0)
|
4 (100)
|
1 (16.7)
|
|
2015 (3)
|
1 (33.3)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
NA
|
0 (0)
|
0 (0)
|
0 (0)
|
1 (50)
|
1 (50)
|
1 (50)
|
0 (0)
|
0 (0)
|
1 (33.3)
|
0 (0)
|
1 (33.3)
|
1 (0)
|
0 (0)
|
NA
|
NA
|
1 (33.3)
|
0 (0)
|
NA
|
1 (33.3)
|
|
2016 (3)
|
0 (0)
|
0 (0)
|
0 (0)
|
2 (66.)
|
NA
|
NA
|
2 (66.)
|
2 (66.7)
|
3 (100)
|
1 (33.)
|
2 (66.7)
|
0 (0)
|
1 (33.3)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
2 (33.3)
|
0 (0)
|
NA
|
NA
|
2 (66.7)
|
0 (0)
|
NA
|
0 (0)
|
|
Enterobacter spp.
|
2012 (11)
|
5 (50)
|
6 (54.6)
|
NA
|
6 (60)
|
NA
|
IR
|
6 (60)
|
7 (63.6)
|
NA
|
4 (44.)
|
6 (54.6)
|
1 (100)
|
5 (45.5)
|
4 (36.4)
|
4 (36.4)
|
4 (36.4)
|
4 (57.1)
|
4 (50)
|
4 (50)
|
4 (40)
|
6 (60)
|
3 (50)
|
2 (25)
|
6 (100)
|
NA
|
|
2013 (31)
|
6 (19.4)
|
5 (16.1)
|
4 (16)
|
4 (13.3)
|
4 (30.8)
|
IR
|
15 (48.4)
|
4 (12.9)
|
5 (20)
|
3 (10.)
|
4 (13.3)
|
0 (0)
|
4 (12.9)
|
0 (0)
|
4 (12.9)
|
4 (12.9)
|
2 (7.1)
|
11 (35.5)
|
4 (13.8)
|
1 (16.7)
|
1 (14.3)
|
11 (35.5)
|
1 (3.5)
|
1 (100)
|
NA
|
|
2014 (10)
|
3 (33.3)
|
6 (60)
|
2 (22.2)
|
3 (33.3)
|
5 (83.3)
|
IR
|
6 (60)
|
7 (70)
|
4 (40)
|
2 (25)
|
5 (50)
|
1 (50)
|
6 (60)
|
2 (20)
|
3 (30)
|
2 (20)
|
3 (60)
|
6 (60)
|
3 (30)
|
NA
|
NA
|
7 (70)
|
0 (0)
|
7 (100)
|
7 (70)
|
|
2015 (10)
|
5 (50)
|
5 (50)
|
2 (20)
|
3 (30)
|
6 (66.7)
|
IR
|
7 (70)
|
5 (71.4)
|
3 (30)
|
2 (22.)
|
5 (50)
|
2 (66.)
|
6 (60)
|
0 (0)
|
4 (40)
|
1 (10)
|
4 (40)
|
7 (70)
|
3 (30)
|
NA
|
NA
|
8 (80)
|
0 (0)
|
NA
|
6 (66.7)
|
|
2016 (15)
|
8 (53.3)
|
6 (40)
|
4 (26.7)
|
5 (33.3)
|
1 (50)
|
IR
|
5 (33.3)
|
5 (33.3)
|
6 (40)
|
4 (30.8)
|
3 (20)
|
4 (57.1)
|
5 (33.3)
|
3 (20)
|
4 (28.6)
|
3 (20)
|
6 (40)
|
6 (40)
|
5 (33.3)
|
NA
|
NA
|
6 (42.9)
|
1 (7.1)
|
NA
|
3 (37.5)
|
|
Escherichia coli
|
2012 (77)
|
15 (19.5)
|
36 (61)
|
NA
|
31 (41.9)
|
3 (100)
|
33 (50.8)
|
57 (79.2)
|
62 (81.6)
|
NA
|
18 (23.3)
|
61 (82.4)
|
6 (15.8)
|
42 (55)
|
6 (8)
|
58 (77.3)
|
27 (35)
|
10 (16.7)
|
49 (80.3)
|
13 (28.3)
|
54 (80.6)
|
60 (89.6)
|
72 (93)
|
1 (2)
|
50 (100)
|
NA
|
|
2013 (113)
|
16 (14.2)
|
68 (72.3)
|
8 (11.8)
|
42 (37.5)
|
21 (63.6)
|
48 (45.7)
|
87 (77)
|
82 (72.6)
|
18 (26.9)
|
5 (10.4)
|
94 (83.2)
|
12 (16)
|
62 (54.9)
|
7 (6.2)
|
77 (68.8)
|
27 (24)
|
20 (18)
|
97 (85.8)
|
37 (33)
|
39 (84.8)
|
48 (96)
|
99 (88)
|
1 (1)
|
25 (100)
|
NA
|
|
2014 (83)
|
7 (8.4)
|
44 (53.7)
|
7 (9.2)
|
29 (35)
|
32 (62.8)
|
24 (43.6)
|
48 (60.8)
|
50 (63.3)
|
11 (13.4)
|
2 (7.1)
|
59 (74.7)
|
15 (33.3)
|
31 (37.8)
|
4 (4.9)
|
45 (54.9)
|
11 (13.8)
|
13 (20)
|
43 (52.4)
|
16 (19.5)
|
NA
|
NA
|
53 (64)
|
1 (0.9)
|
75 (100)
|
52 (65)
|
|
2015 (70)
|
15 (21.4)
|
51 (75)
|
17 (28.8)
|
22 (34.9)
|
46 (79.3)
|
NA
|
41 (58)
|
28 (65.1)
|
28 (41.8)
|
5 (7)
|
57 (81.4)
|
23 (48.9)
|
26 (37)
|
3(4)
|
52 (77.6)
|
9 (12.9)
|
16 (27.6)
|
52 (75.4)
|
26 (37.1)
|
NA
|
NA
|
39 (56)
|
0 (0)
|
NA
|
47 (69.1)
|
|
2016 (133)
|
34 (26)
|
86 (67.7)
|
28 (21.7)
|
45 (34)
|
47 (88.7)
|
NA
|
67 (50)
|
103 (82.4)
|
53 (41.7)
|
8(6)
|
107 (82.3)
|
61 (70.9)
|
47 (35)
|
5 (3.8)
|
96 (75.6)
|
16 (12)
|
30 (23.3)
|
112 (87.5)
|
46 (35.9)
|
NA
|
NA
|
69 (52)
|
0 (0)
|
NA
|
65 (60.8)
|
|
Klebsiella pneumoniae
|
2012 (47)
|
40 (87)
|
42 (89.3)
|
NA
|
39 (83)
|
NA
|
40 (93)
|
42 (89.1)
|
40 (88.9)
|
NA
|
26 (72.2)
|
42 (91.3)
|
14 (70)
|
42 (91.3)
|
33 (69.6)
|
42 (89)
|
33 (75)
|
32 (88.9)
|
35 (97.2)
|
20 (80)
|
21 (56.8)
|
IR
|
31 (96.9)
|
7 (26.9)
|
42 (100)
|
NA
|
|
2013 (33)
|
14 (42.4)
|
24 (72.7)
|
5 (23.8)
|
13 (41.9)
|
2 (16.7)
|
18 (56.3)
|
26 (79)
|
18 (54.6)
|
6 (28.6)
|
8 (32)
|
18 (56.3)
|
9 (39.1)
|
12 (37.5)
|
15 (46)
|
25 (76)
|
16 (51.6)
|
14 (42.4)
|
26 (78.8)
|
13 (40.6)
|
3 (30)
|
IR
|
27 (81.8)
|
6 (21.4)
|
10 (100)
|
NA
|
|
2014 (26)
|
13 (50)
|
18 (69.2)
|
11 (45.8)
|
12 (48)
|
11 (61.1)
|
11 (55)
|
20 (76)
|
16 (61.5)
|
13 (50)
|
6 (46.2)
|
12 (46.2)
|
5 (33.3)
|
14 (53.9)
|
11 (42)
|
16 (61.6)
|
12 (46.2)
|
11 (55)
|
15 (57.7)
|
14 (53.9)
|
NA
|
IR
|
17 (65.4)
|
4 (18.2)
|
52 (100)
|
13 (54.2)
|
|
2015 (13)
|
7 (53.9)
|
8 (61.52)
|
5 (50)
|
7 (53.9)
|
7 (77.8)
|
NA
|
9 (67)
|
4 (66.7)
|
8 (61.5)
|
4 (57.1)
|
9 (69.2)
|
4 (44.4)
|
9 (69.2)
|
4(30.8)
|
6 (46.1)
|
5 (38.5)
|
6 (60)
|
11 (84.6)
|
8 (66.7)
|
NA
|
IR
|
9 (75)
|
1 (8.3)
|
NA
|
6 (50)
|
|
2016 (47)
|
32 (71.1)
|
25 (53.2)
|
29 (61.7)
|
35 (74.5)
|
24 (88.9)
|
NA
|
31 (65.4)
|
38 (82.6)
|
36 (76.6)
|
25 (69.4)
|
39 (83)
|
25 (80.7)
|
39 (83)
|
14 (30)
|
19 (40)
|
32 (68.1)
|
37 (78.7)
|
41 (87.2)
|
31 (72.1)
|
NA
|
IR
|
42 (91.3)
|
3 (7)
|
NA
|
26 (63.4)
|
|
Morganella spp.
|
2012 (4)
|
1 (25)
|
1 (25)
|
NA
|
3 (75)
|
NA
|
3 (100)
|
2 (50)
|
2 (50)
|
NA
|
1 (33.3)
|
2 (50)
|
NA
|
2 (50)
|
2 (50)
|
2 (50)
|
2 (50)
|
1 (25)
|
2 (50)
|
1 (25)
|
2 (66.7)
|
3 (75)
|
2 (66.7)
|
IR
|
1 (100)
|
NA
|
|
2013 (3)
|
1 (33.3)
|
1 (33.3)
|
0 (0)
|
1 (33.3)
|
NA
|
3 (100)
|
2 (66.7)
|
1 (33.3)
|
0 (0)
|
1 (50)
|
3 (100)
|
NA
|
1 (33.3)
|
1 (33.3)
|
2 (66.7)
|
2 (66.7)
|
0 (0)
|
2 (66.7)
|
1 (33.3)
|
1 (100)
|
1 (100)
|
2 (66.7)
|
IR
|
1 (100)
|
NA
|
|
2014 (5)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
1 (100)
|
2 (40)
|
2 (40)
|
0 (0)
|
0 (0)
|
2 (40)
|
1 (100)
|
2 (40)
|
0 (0)
|
2 (40)
|
1 (20)
|
0 (0)
|
0 (0)
|
0 (0)
|
NA
|
NA
|
2 (40)
|
IR
|
NA
|
2 (50)
|
|
2015 (3)
|
2 (66.7)
|
1 (33.3)
|
1 (50)
|
1 (50)
|
2 (100)
|
NA
|
2 (66.7)
|
1 (50)
|
1 (33.3)
|
0 (0)
|
2 (66.7)
|
NA
|
3 (100)
|
1 (33.3)
|
2 (66.7)
|
1 (33.3)
|
2 (100)
|
2 (66.7)
|
2 (66.7)
|
NA
|
NA
|
2 (66.7)
|
IR
|
NA
|
3 (100)
|
|
2016 (3)
|
2 (66.7)
|
3 (100)
|
2 (66.7)
|
3 (100)
|
1 (100)
|
NA
|
3 (100)
|
3 (100)
|
3 (100)
|
1 (50)
|
3 (100)
|
NA
|
3 (100)
|
2 (66.7)
|
3 (100)
|
1 (33.3)
|
3 (100)
|
3 (100)
|
2 (66.7)
|
NA
|
NA
|
3 (100)
|
IR
|
NA
|
1 (100)
|
|
Proteus spp.
|
2012 (22)
|
10 (45.5)
|
7 (36.8)
|
NA
|
3 (13.6)
|
NA
|
6 (31.6)
|
13 (59.1)
|
13 (61.9)
|
NA
|
12 (66.7)
|
NA
|
0 (0)
|
8 (36.4)
|
3 (13.6)
|
11 (50)
|
6 (28.6)
|
11 (61.1)
|
6 (31.6)
|
2 (12.5)
|
IR
|
6 (46.2)
|
11 (61.1)
|
IR
|
12 (100)
|
NA
|
|
2013 (20)
|
4 (20)
|
6 (50)
|
0 (0)
|
2 (10)
|
3 (50)
|
3 (15)
|
13 (65)
|
11 (55)
|
0 (0)
|
10 (52.6)
|
NA
|
NA
|
9 (45)
|
0 (0)
|
12 (60)
|
5 (26.3)
|
14 (70)
|
3 (15.8)
|
1 (5.6)
|
IR
|
5 (83.3)
|
9 (52.9)
|
IR
|
12 (100)
|
NA
|
|
2014 (11)
|
3 (27.3)
|
5 (45.5)
|
0 (0)
|
1 (9.1)
|
5 (45.5)
|
1 (10)
|
7 (63.6)
|
7 (63.6)
|
0 (0)
|
2 (28.6)
|
6 (54.55)
|
0 (0)
|
5 (45.5)
|
3 (27.3)
|
3 (27.3)
|
3 (27.3)
|
7 (63.6)
|
2 (18.2)
|
0 (0)
|
IR
|
NA
|
2 (18.2)
|
IR
|
24 (100)
|
8 (80)
|
|
2015 (11)
|
5 (45.5)
|
4 (50)
|
1 (14.3)
|
0 (0)
|
4 (57.1)
|
NA
|
6 (54.6)
|
2 (66.7)
|
0 (0)
|
6 (66.7)
|
4 (54.55)
|
NA
|
6 (54.6)
|
0 (0)
|
4 (40)
|
0 (0)
|
4 (57.1)
|
0 (0)
|
0 (0)
|
IR
|
NA
|
1 (10)
|
IR
|
NA
|
7 (63.6)
|
|
2016 (9)
|
7 (77.8)
|
5 (55.6)
|
1 (11.1)
|
2 (22.2)
|
4 (66.7)
|
NA
|
7 (77.8)
|
5 (71.4)
|
1 (11.1)
|
7 (87.5)
|
5 (50)
|
NA
|
6 (85.7)
|
3 (42.9)
|
7 (87.5)
|
1 (12.5)
|
7 (77.8)
|
3 (33.3)
|
1 (12.5)
|
IR
|
NA
|
1 (11.1)
|
IR
|
NA
|
5 (83.3)
|
|
Providencia spp.
|
2012 (3)
|
1 (33.3)
|
1 (33.3)
|
NA
|
0 (0)
|
NA
|
1 (100)
|
1 (33.3)
|
0 (0)
|
NA
|
NA
|
2 (66.7)
|
NA
|
1 (33.3)
|
1 (33.3)
|
0 (0)
|
1 (33.3)
|
1 (50)
|
0 (0)
|
0 (0)
|
IR
|
1 (33.3)
|
1 (50)
|
IR
|
1 (100)
|
NA
|
|
2013 (5)
|
3 (60)
|
3 (60)
|
0 (0)
|
3 (60)
|
0 (0)
|
2 (100)
|
4 (80)
|
4 (80)
|
0 (0)
|
0 (0)
|
4 (80)
|
(0)
|
4 (80)
|
1 (20)
|
4 (80)
|
4 (80)
|
3 (60)
|
3 (60)
|
1 (20)
|
IR
|
3 (100)
|
3 (60)
|
IR
|
3 (100)
|
NA
|
|
2014 (2)
|
1 (50)
|
1 (50)
|
1 (50)
|
1 (50)
|
0 (0)
|
2 (100)
|
1 (50)
|
1 (50)
|
1 (50)
|
0 (0)
|
1 (50)
|
NA
|
1 (50)
|
0 (0)
|
1 (50)
|
0 (0)
|
1 (50)
|
1 (50)
|
1 (50)
|
IR
|
NA
|
1 (50)
|
IR
|
4 (100)
|
1 (50)
|
|
2015 (1)
|
0 (0)
|
0 (0)
|
NA
|
0 (0)
|
NA
|
NA
|
0 (0)
|
NA
|
0 (0)
|
NA
|
1 (100)
|
NA
|
0 (0)
|
NA
|
1 (100)
|
0 (0)
|
NA
|
0 (0)
|
0 (0)
|
IR
|
NA
|
0 (0)
|
IR
|
NA
|
0 (0)
|
|
2016 (2)
|
0 (0)
|
0 (0)
|
1 (20)
|
2 (100)
|
NA
|
NA
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
2 (100)
|
NA
|
2 (100)
|
0 (0)
|
2 (100)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
IR
|
NA
|
0 (0)
|
IR
|
NA
|
0 (0)
|
|
Salmonella spp.
|
2012 (16)
|
6 (42.9)
|
0 (0)
|
NA
|
1 (8.3)
|
NA
|
2 (18.2)
|
1 (7.1)
|
1 (7.1)
|
NA
|
1 (0)
|
3 (21.4)
|
1 (50)
|
3 (25)
|
1 (7.1)
|
1 (7.1)
|
1 (7.1)
|
2 (20)
|
3 (27.3)
|
1 (10)
|
0 (0)
|
3 (21.4)
|
3 (37.5)
|
1 (7.7)
|
NA
|
NA
|
|
2013 (2)
|
0 (0)
|
0 (0)
|
NA
|
0 (0)
|
NA
|
0 (0)
|
0 (0)
|
0 (0)
|
NA
|
0 (0)
|
0 (0)
|
NA
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
1 (50)
|
0 (0)
|
0 (0)
|
0 (0)
|
1 (50)
|
1 (50)
|
0 (0)
|
NA
|
NA
|
|
2014 (5)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
1 (33.3)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
1 (20)
|
0 (0)
|
0 (0)
|
0 (0)
|
1 (20)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
NA
|
NA
|
1 (20)
|
0 (0)
|
NA
|
1 (20)
|
|
2015 (4)
|
1 (25)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
NA
|
2 (50)
|
2 (66.7)
|
0 (0)
|
0 (0)
|
2 (50)
|
NA
|
3 (75)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
2 (50)
|
2 (50)
|
NA
|
NA
|
2 (50)
|
0 (0)
|
NA
|
0 (0)
|
|
2016 (11)
|
0 (0)
|
1 (9.1)
|
0 (0)
|
2 (18.2)
|
0 (0)
|
NA
|
0 (0)
|
0 (0)
|
0 (0)
|
1 (0)
|
2 (18.2)
|
NA
|
3 (33.3)
|
0 (0)
|
1 (9.1)
|
0 (0)
|
0 (0)
|
2 (18.2)
|
0 (0)
|
NA
|
NA
|
1 (10)
|
0 (0)
|
NA
|
2 (20)
|
|
Serratia spp.
|
2012 (2)
|
1 (50)
|
1 (50)
|
NA
|
1 (50)
|
NA
|
IR
|
1 (50)
|
1 (50)
|
NA
|
0 (0)
|
1 (50)
|
NA
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
1 (50)
|
1 (50)
|
NA
|
1 (100)
|
NA
|
1 (50)
|
0 (0)
|
1 (100)
|
NA
|
|
2013 (1)
|
0 (0)
|
0 (0)
|
NA
|
0 (0)
|
NA
|
IR
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
NA
|
NA
|
NA
|
0 (0)
|
0 (0)
|
1 (100)
|
NA
|
|
2014 (16)
|
0 (0)
|
0 (0)
|
NA
|
0 (0)
|
0 (0)
|
IR
|
0 (0)
|
1 (6.3)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
0 (0)
|
1 (6.3)
|
NA
|
NA
|
NA
|
1 (6.3)
|
0 (0)
|
NA
|
NA
|
|
2015 (0)
|
1 (100)
|
1 (100)
|
NA
|
NA
|
NA
|
IR
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
NA
|
|
2016 (1)
|
2 (10)
|
2 (10)
|
NA
|
0 (0)
|
NA
|
IR
|
1 (100)
|
1 (100)
|
0 (0)
|
0 (0)
|
0 (0)
|
NA
|
0 (0)
|
0 (0)
|
NA
|
0 (0)
|
1 (100)
|
1 (100)
|
NA
|
NA
|
NA
|
1 (100)
|
0 (0)
|
NA
|
NA
|
From 5-years resistance pattern in ICUs, we observed that E. coli and Klebsiella spp. isolates showed some decrease in resistance percentage against some antimicrobials.
About 32% decreased resistance was observed in E. coli against meropenem, while against Klebsiella spp. isolates it was 34%. Against piperacillin-tazobactam, E. coli showed 25% decreased resistance, while Klebsiella spp. showed 22%. Both E. coli and Klebsiella spp. isolates showed 22% decreased resistance against cefoperazone-sulbactam. In
addition to these, Klebsiella spp. isolates also showed decreased resistance against ceftriaxone (7%), 21% against
ciprofloxacin, 12% against ticarcillin-clavulanate, 17% against gentamycin, 3% decreased
resistance against imipenem, and 26% against levofloxacin.
In wards also, both E. coli and Klebsiella spp. isolates showed decreased resistance across the study period. In E. coli, maximum decreased resistance was observed against meropenem (27%), followed by gentamicin
(18%) and imipenem (6%). In Klebsiella spp. maximum decreased resistance was observed against tigecycline (25%), followed
by imipenem (21%), meropenem (19%), gentamicin (17%), piperacillin-tazobactam (8%),
and ciprofloxacin (6%).
In OPD patients, E. coli showed maximum decreased resistance against ticarcillin-clavulanate (41%), followed
by ceftazidime (29%), meropenem (23%), gentamycin (20%), chloramphenicol (17.7%),
cefoperazone-sulbactam (8%), imipenem (4.2%), and tigecycline (1%). Klebsiella spp. isolates showed maximum decreased resistance against levofloxacin (49%), followed
by imipenem (39.6%), cefepime (36.1%), and ceftazidime (23.7%).
Discussion
In this study, we evaluated the antimicrobial resistance pattern of Enterobacteriaceae in trauma patients. We found that in ICUs and wards, the most common gram-negative
pathogens responsible for nosocomial infections were Klebsiella spp., followed by E. coli and Enterobacter spp. These findings are in concordant with other published studies.[14]
[15] In OPD patients, the most common gram-negative pathogens responsible for nosocomial
infections were E. coli, followed by Klebsiella spp. and Enterobacter spp.
Our study showed Enterobacteriaceae isolates from ICUs, wards, and OPD showed high level of resistant to all classes
of cephalosporins. In addition, β lactam and β-lactamase inhibitor combination remained
less effective. This encouraged therapy with quinolones, aminoglycosides, or carbapenems.
However, among quinolones, aminoglycosides, and carbapenems we found least resistance
to carbapenems followed by aminoglycosides and quinolones in all settings; this result
is in concordant with another study.[16] This shows that the resistance is increasing to currently used antibiotics, and
the older drugs may prove as an effective option. Both imipenem and meropenem showed
good activity against Enterobacteriaceae even when they are producing either ESBLs or Amp C. It was found that meropenem showed
≥ 97.3% sensitivity among Enterobacteriaceae isolates while imipenem showed 87.5% sensitivity, showing that meropenem is 4 to
16 times more active than imipenem against Enterobacteriaceae.[17]
[18] In contrast, we found imipenem more effective than meropenem in all settings. Among
aminoglycosides group of antimicrobial agents, less resistance was shown against amikacin
than gentamycin; similar results were observed in other published studies.[19]
[20] The least resistant was observed against tigecycline (1–15%) among all isolates
in all settings. A similar result was found in another study where tigecycline was
active against multidrug-resistant E. coli and Klebsiella spp. isolates.[21]
[22]
From 5-year resistance pattern of antimicrobials ([Tables 2]
[3]
[4]), we found that Enterobacteriaceae isolates showed increased sensitivity against some antimicrobials in all settings.
In ICU settings, both E. coli and Klebsiella spp. isolates showed significant increased sensitivity percentage against β-lactamase
inhibitors and carbapenem. Klebsiella spp. isolates also showed increased sensitivity against quinolones and aminoglycosides
(gentamycin). These results suggest the substantial use of these antibiotics against
these pathogens. In wards and OPDs, increased sensitivity was observed across the
study period; both pathogens showed increased sensitivity against carbapenems (meropenem,
imipenem) and aminoglycosides (gentamycin). Klebsiella spp. isolates also showed increased sensitivity against piperacillin-tazobactam,
ciprofloxacin, and tigecycline in wards settings. In OPD patients, increased sensitivity
against ceftazidime and cefepime was also observed in both pathogens, showing primitive
antibiotics like ceftazidime and cefepime can be used as choice of antibiotic against
these pathogens in OPD patients, although it is administered intravenously.
Among different classes of antimicrobials, tigecycline proved most effective in all
settings. Tigecycline is a potent therapeutic option for multidrug resistance enterobacterial
infections. Although tigecycline resistance has been observed, it is still active
among Enterobacteriaceae. However, increased resistance was observed than other studies which is < 10%.[23]
[24]
[25]
[26]
This study is among the very few studies done in the Indian setting. The large sample
size of this study makes its results more reliable. Isolates of Enterobacteriaceae included in this study were collected from multiple sources in terms of location
of the patients and types of samples. Therefore, the findings can be generalized to
a variety of location of patients and samples. However, all the samples were collected
from the apex trauma center of a tertiary care center. This limits the generalizability
of the study in terms of study settings. The burden, profile, and AST of Enterobacteriaceae bacteria isolated from a secondary or primary care setting or from community settings
are expected to be different from this study. Hence the interpretation with reference
to study setting should be cautiously done.
No intermediate isolate was reported in the study results. This study includes the
results based on automated system (Vitek2 compact system). These need to be validated
by molecular methods or by sequencing.
