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Original research

Prevalence of meropenem susceptibility

among Gram-negative pathogens
isolated from intensive care units in
Jordan
Jamal Wadi1*, Naheel Haloub2, Mais Al Ahmad1,
Amani Samara2 and Amani Romman1

1 Al Khalidi Medical Center , Amman, Jordan

2 The Specialty Hospital, Amman, Jordan
*Corresponding author:
jamalwadimd@yahoo.com

Abstract
Background. Meropenem is a relatively new carbapenem in some Middle East
countries; our aim is to evaluate its susceptibility in gram-negative pathogens isolated from ICU patients and to identifythe prevalence of ICU bacterial isolates identified
as pathogens based on CDC-NHSN definition for pathogens in the affected organs.
Methods. Pathogens as identified by CDC-NHNS were studied for prevalence and
antibiotic susceptibility. Patients and charts were prospectively reviewed; attending
physician diagnosis was considered after being reviewed by two qualified infection
control nurses and infectious diseases physician.
Results. One-hundred and seventy-three gram-negative pathogen were reviewed
for susceptibilities and ESBL production. E. coli was a dominant pathogen followed
by Klebsiella, and Pseudomonas. ESBL-production was in E. coli (62.7%) and Klebsiella (58.6%), considering all gram-negative bacilli studied; ESBL rates were 30.7%.
Both Carbapenems showed superior activity against gram-negative pathogens. Meropenem did better than imipenem against pseudomonas species, but PIP/TAZ did
better than both carbapenems (p = 0.02). The difference in susceptibility patterns
among ESBL-producing pathogens compared with same non-ESBL producers species showed that carbapenems were superior to other classes of antibacterials tested
in this regard, and rates of resistant ESBL to both carbapenems were 5.6%; trustworthy in the initial empiric therapy in ICUs and hospitals that suffer from high rates of
ESBL-producers. While PIP/TAZ showed highly significant difference (p < 0.0001) in
activity against ESBL and non-ESBL producers.
Conclusion. Meropenem and imipenem are trustworthy in the initial empiric
therapy. Gram-negative pathogens are highly susceptibility to both carbapenems,
and benefit extends to ICUs with high rates of ESBL-producers.
Keywords: Meropenem, Imipenem, Gram-negative pathogens susceptibility,
ESBL-producer, ICU-Jordan

Introduction
Intensive care units beds occupy about 10% of hospital beds
meanwhile representing the hospital epidemiology in as much
as 80%, where most of infections take place in ICU. (1, 2) Furthermore, the amount of antibacterial drugs used is enormous
in this part of the hospital, especially wide-spectrum antibacterials as mono-therapy or in combination. Among antibacterials, carbapenems are widely used, and meropenem is a relatively new antimicrobial agent in our part of the world. Some
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studies state that it is different from imipenem in its potency

and target attainment, especially against Pseudomonas species.(3) The major concern of infectious disease has been in
the last decades the problem of combating resistance. Many
antimicrobial agents became less useful as resistance evolve.
(4) Resistance trends among bacteria are on the rise in hospitals, especially in ICUs where highly morbid patients are residing, with multiple interventions, and the use of wide-spectrum
antimicrobials, among other risk factors.(5, 6) Gram-negative
bacteria contribute to a large fraction of ICU nosocomial infec-

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tions, mostly contributing to a big part of ventilator-associated

pneumonia (VAP), catheter-associated urinary tract infections
(CAUTI) and central line associated infections (CLABSI) as identified by CDC-NHNS.(4, 7) Vigilance is highly needed in this
regard and adjusting antimicrobials use in ICUs has to cope
with the evolving changes in prevalence and susceptibility.
The invaluable continued ICU surveillance for prevalence of
pathogens and their antimicrobial susceptibility shed light on
empiric treatment; here, using meropenem as a model to compare with.(7) The ultimate goal is that antimicrobial prescription would be more educated, based on proper suspicion of
the likely pathogen (not simply isolate) and their antimicrobial
susceptibility results.

Materials and Methods

Settings and Microbiology
The study was conducted in Amman-Jordan in two private
hospitals with a total bed occupancy of 370 and total ICU
beds of 45 (The Specialty Hospital and Al Khalidi Hospital).The
study period was from September 2009 February 2011. Isolates were processed for susceptibility by Viteck II ( BioMrieux
SA. F-69280 Marcy lEtoile, France) few isolates were processed
by E-test (AB BIODISK Dalvgen 10, S - 169 56 Solna, Sweden).
Antimicrobials used for susceptibilities including meropenem,
imipenem, ertapenem, PIP/TAZ, tigecycline, cefepime, ceftazidime, ceftriaxone,, ciprofloxacin, levofloxacin and aztreonam.
Gram-negative pathogens tested were those isolated fromall
sources (table 1); Escherichiacoli,Klebsiella pneumonia, Pseudomonasaeruginosa, Pseudomonas species, Acinetobactercomplex, Enterobacter spp.Serratia marscesenece and others bacteria spp. like (Proteus mirabilis, Morganella morgani, Providentia
stuarti, Chrysomonas luteola, Flavimonoas arrhyzohabitans).

2011
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Definitions and Methodology

F our major indicators are utilized in both hospitals (quality
performance indicators)were considered for obtaining isolates
(VAP, CLABSI, CAUTI and SSI), an isolate isconsidered a pathogen and included in the study when causing infection in the
organ as it followed thedefinition for hospital-acquired infections described by CDC-NHSN. (7) Qualified infection control
nurses (M.A and A.S) collect cultures results from the microbiology laboratory. The methodologies of pathogenssampling
were monitored, especially in VAP, whether samples were taken
from tracheal aspiration or BAL or other methods, abiding by
CDC-NHSN definition.Daily collected cultures were discussed
on case-by-case basis, with patientschart review, radiological
review, urine analysis and blood cultureswith an infectious diseases physician, before enrolling the suspect pathogen in the
study. In the other hospital, a qualified experienced infection
control nurse did the review and strictly applied same CDCNHNS definitions,keeping incontact withthe same infectious
diseases physician (J.W).
Microbiological Methodology
Microbiological procedures to identify the target microorganisms: specimens from the target sources are cultured on bloodagar, chocolate-agar, MacConkeysagar & SAB agar plates Pus
was cultured on two plates of blood agar (aerobic and anaerobic incubation) andon chocolate agar, MacConkeys agar & SAB
agar plates. Pus is also incubated in thioglycolate for growth
augmentation, subsequently cultured on plates as above in
twenty-four, forty-eight hours and at the end of incubation i.e.
five days. Chocolate agar plates were incubated in CO2 environment for twenty-four hours. Microorganisms were identified
from growth plate by colony morphology (shape, color, size)
and gram stain; Gram-negative bacteria grew on selective Mac-

TABLE 1. Gram-negative Pathogens isolated in ICU Setting, and their Distribution according to Source.
Pathogens

CLABSI

CAUTI

VAP

SSI

Total No. of Pathogens

E.coli

17

32

56

K. pneumonia

14

29

P. aeruginosa

10

26

Acinetobacter spp.

28

Enterobacter spp.

Pseudomonas spp.

Other GNB

22

Total

57

71

16

29

173

CLA-BSI: Central line associated blood stream infection. CA-UTI: Catheter associated urinary tract infection. VAP: ventilator associated pneumonia. SSI: Surgical
site infection.
Others GNB: Serratia marscesence, Flavimonas arryzohabitanz, Hemophilus influenzae, Proteus mirabilis, Morganella spp., Providentia spp., Chrysomonas luteola,
Achromobacter sppecies.

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Conkeys agar plate, and then identified as lactose fermenter

(LF) or non-fermenter (NLF) and processed by theautomated
Viteck II. Microorganism susceptibility is processed by isolating
colonies in one of sterile solutions (saline solution for use in
Viteck II); suspension density is checked by the digital density
check (0.5-0.63) densitocheck(add the name of company and
country).The results are reported as minimum inhibitory concentration(MIC) according tothe published document byclinical and laboratory standards institute (CLSI) break points( 8).E.
coli ATCC 25922 and P. aeruginosa ATCC 25423 were used as
Controls.

Results

Statistical analysis

One-hundred seventy-three gram-negative pathogens (table

1) were isolated from CLABSI, CAUTI, VAP and SSI. E. coli was
dominant (N = 56) pathogen, mostly was isolated from urinary
source (n = 32) followed by CLABSI (n = 17). K. pneumonia (N
= 29) was isolated from CATUI (n = 14), followed by CLABSI (n
= 9) and VAP (n = 4). P. aeruginosa (N = 26) from CAUTI (n=
10), from CLABSI (n = 7), and from VAP (n = 4) and SSI (n = 5)
pathogens. Acinetobacter species were more-or-less uniformly
isolated from all sources (N = 28). Enterobacter species and
Pseudomonas species were minor in numbers; the other gramnegatives were heterogenous and came from SSI, CLABSI and
CAUTI.

All results were uploaded into statistical software (SPSS version 15). Data generation for tables, numbers, ratios as well as
raters were measured. Where appropriate, the differences in
susceptibility among gram-negative pathogens were calculated using 95% confidence intervals and P-value (p-value to
be < 0.05). The hypothesis was that meropenem is different
from other antimicrobials especially imipenem, in its activity
against major ICU gram-negative pathogens. Susceptibility of
pseudomonas to meropenem and imipenem were specifically
measured for the claim that meropenem is more of anti-pseudomonal than imipenem. Furthermore, p-value was calculated
based on meropenem as a reference for other selected antipseudomonal antimicrobials, representing different antimicrobials classes (Figure 1).

100
80
60

66.6

58.6

78.7
51.5

42.4

40

58.3

Two-hundred
twenty pathogen were isolated; 39 gram-positive, 173 gram-negative (54 ESBL; 30.7%), and 8 Candida species. Eight were duplicate isolates considered all as pathogens;
it was not certain which one was the pathogen in the absence
of lung biopsy for gram staining, to correlate with culture
(however, 6 Candida were isolated with gram-negative bacilli,
and 2 S. fecalis with gram negative-bacilli), gram-negative bacilli were considered the pathogens for they were treated by
the attending physician.

Carbapenems (meropenem, imipenem and ertapenem)

showed superior activity over other tested antimicrobial classes against E. coli, K. pneumonia and Enterobacter spp. (Table 2),

66.6
48.1

FIGURE 1. Susceptibility of Pseudomonas aeruginosa including Pseudomonas species

to selected antimicrobial
agents expressed in percentages.

20

26/33
17/33
14/24
22/33
P = 0.02 P = 0.43 P = 0.97 P = 0.35
Z = 2.34 Z = -0.77 Z = -0.03 Z = 0.99

Aztreonam

Cefepime

Levofloxacin

22/33
P = 0.35
Z = 0.99

Ciprofloxacin

14/33
P = 0.07
Z = -1.88

PIP/TAZ

Amikacin

17/29

Imipenem

Meropenem

13/27
P = 0.25
Z = -1.15

Numbers below antimicrobials denote the total pathogens susceptible over total tested for that
antimicrobial. P-values are for comparing meropenem with the respected antimicrobial. Z: the
standard normal variant for same comparison.

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TABLE 2. Antimicrobial Susceptibility of all Gram-negative pathogen isolates in ICUs.

Antibiotic

Meropenem Imipenem
S/R
S/R

Amikacin
S/R

PIP/TAZ
S/R

Tigecycline Ciprofloxacin Levofloxacin Ertapenem Ceftraixone Cefepime Aztreonam

S/R
S/R
S/R
S/R
S/R
S/R
S/R

E. col n=56

49 / 1

54 / 1

54 / 1

29 / 24

11 / 4

18 / 38

17 / 33

50 / 1

19 / 13

18 /12

13 / 13

K.pneumoniae
n= 29

27 / 2

27 / 2

28 / 1

17 / 11

8/3

12 / 15

12 / 13

24 / 1

13 / 4

11 / 6

10 / 3

P. aeruginosa
n = 26

13 / 10

14 / 12

21 / 5

18 / 7

0/3

15 / 11

12 / 9

0/1

0/6

18 / 8

10 / 11

Acinetobacter
n = 28

2 / 26

2 / 26

10 / 17

2 / 26

14 / 8

1 / 24

1 / 21

0 / 11

1 / 19

2 / 23

1 / 20

Enterobacter
n=6

6/0

6/0

4/1

4/1

1/0

3/2

3/4

2/1

3/2

3/1

2/1

Pseudomonas
spp. n = 7

4/2

0/7

1/6

7/0

0/1

2/5

2/1

--------

0/4

4/3

3/3

PIP/TAZ: pipracillin-tazobactam.
S; Susceptible, R: resistant, n: total number of pathogens tested to various antimicrobials.

TABLE 3. Antimicrobial susceptibility of all Gram-negative bacilli isolated from all sources

Antibiotics

Susceptible

Intermediate

Resistant

% Susceptible

The Percent difference of each

antimicrobial vs. Meropenem
and (95% C.I.)

Meropenem

125

54

67.4

---

Imipenem

134

68

64.7

-2.7 (-6 to 12)

PIP/TAZ

106

85

54.4

-13 (-3 to -23)

Ertapenem

86

15

84.3

16.9 (7- 27)

Levofloxacin

69

99

39.9

-27.5 (-17 to -37)

Ciprofloxacin

71

127

35.3

-32.1 (-22 to -41)

Ceftriaxone

45

64

40.9

-26.5 (-15 to - 38)

Amikacin

135

35

78.5

11.1 (2 - 20)

Tigecycline

70

18

74.5

7.1 (-4 to 18)

Cefepime

66

52

53.6

-13.8 (-3 to -25)

but within the same class; meropenem did better than imipenem against pseudomonas species, However both carbapenems have 5.6% resistance rates among the fifty-four tested
ESBL producing gram-negative bacilli. PIP/TAZ did better than
both carbapenems (p = 0.02) against Pseudomonas aeruginosa
and species (Figure 1). Lumping gram-negative pathogens
susceptibility together, as what actually occur in clinical initial empiric therapy; carbapenems, tigecycline, and amikacin were better in activity than other tested antimicrobials
(Table 3 and Figure 2).

ESBL was detected by Viteck II employing Ceftazidime, ceftriaxone and aztreonam plus clavulonic acid (in combination
with amoxicillin), subtypes were CTX-M 31%, SHV 10.3%, AmpC
19%, others 5.2% and untypable 34.5%. ESBLs distribution
among each gram-negative were; E. coli (62.7%), K. pneumonia
(58.6%) and Enterobacter (100%). ESBL rates were 30.7% of all
gram-negatives, and 44.5% of ESBL-producing gram-negative
pathogens.

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PIP/TAZ: pipracillin-tazobactam
FIGURE 2. Forest representation of the 95% confidence interval comparing meropenem activity against Gram-negative pathogens
with other antimicrobials (data from table 3).

Discussion
In our current study as well as in others, Enterobacteriaceae
dominated the isolates, thus, being frequent candidate pathogens causing sepsis in ICUs. (8) E. coli was the prevalent pathogen 56 (32.4%), followed by K. pneumonia, Pseudomonas aeruginosa and Acinetobacter species. This is divergent from some
prevalence studies of isolates where it showed dominance
of Pseudomonas aeruginosa in a US study.(9) While in Europe
Enterobacteriaceae lead by E. coli was dominant.(8) However
both studies show that Acinetobacter and Serratia marscesence
defined as pathogens are less than what physicians use to diagnose and treat in ICUs.(8, 9)
Meropenem is a carbapenem belongs to the same family of
antimicrobials with imipenem and ertapenem as well as others not yet available in our part of the world e.g. Doripenem,
Faropenem, Panipenem, and the investigational agents; Tomopenem, Tebinepem, Razupenem.(10) Meropenem mechanism
of action against pseudomonas is exerted through binding to
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PBP2 and PBP3, while in E. coli it binds to PBP2, much similar

to the recently released doripenem, while imipenem binds to
PBP1a and PBP1b in Pseudomonas.(11) This may reflect on meropenem in being a marginally better anti-pseudomonal and
antigram-negative agent.(12)
In our study meropenem showed tendency towards being
better anti-pseudomonal than imipenem (p = 0.07), while it
showed no significant difference against the other tested
gram-negative pathogens (p > 0.05). PIP/TAZ showed a significant but marginal better anti-pseudomonal activity than
meropenem, p = 0.02 (Fig 1). Both carbapenems harbor 5.6%
resistance rates among the fifty-four tested ESBL producing
gram-negative bacilli.
However, considering all gram-negative pathogens together
for susceptibility, as actually what happens in the clinical approach for initial empiric therapy, Imipenem is the only antimicrobial that is comparable with meropenem. While other
antimicrobials like Amikacin (95% C.I, 0.02 - 0.27), ertapenem
(95% C.I, 0.07-0.27) show tendency towards a better suscep-

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TABLE 4. Gram-negative bacilli showing ESBL production andESBL-producers distribution according to their source.
Source

Gram-negative pathogens

CLA-BSI

CA-UTI

VAP

SSI

Total (%)

Escherichia coli ESB

yes
No
Total

9
8
17

21
11
32

0
0
0

7
0
7

37 (62.7)
19
59

Klebsiella pneumonia ESB

yes
No
Total

3
6
9

10
4
14

2
2
4

2
0
2

17 (58.6)
12
29

Enterobacter spp. ESBL

yes
No
Total

2
0
2

2
0
2

0
0
0

2
0
2

6 (100)
0
6

14 (50%)

33 (68.7%)

2 (50%)

11 100%

Total ESBL-Producing bacteria and rates per source

Total ESBL rates from E.coli, K. pneumonia and Enterobacter spp. from all sources were = 44.5%. Total ESBL rates from all gram-negative pathogens isolated from
all sources were 30.7%. CLA-BSI: Central line associated blood stream infection. CA-UTI: Catheter associated urinary tract infection. VAP: ventilator associated
pneumonia. SSI: Surgical site infection.
ESBL-GNB: Extended spectrum beta lactamase- producing gram-negative bacilli.

TABLE 6. Susceptibility of ESBL-producing and-nonproducing Gram-negative bacilli to meropenem and to other tested comparator antimicrobials
Susceptible
ESBL
Yes No

Intermediate
ESBL
Yes
No

Resistant
ESBL
Yes
No

(%) Susceptible
ESBL
Yes
No

Difference in percent
Susceptibility and
(95% C.I)

Meropenem

46

27

94

96

(-8 - 12)

Imipenem

50

28

94

90

(-8 - 16)

PIP/TAZ

18

25

30

36

89

Tigecycline

13

76

73

(-30 - 36)

Ertapenem

46

25

96

93

(-8 - 14)

Levofloxacin

20

37

15

74

-59 (-39 to -78)*

Ciprofloxacin

23

44

14

77

63 (-45 to -81) *

Ceftriaxone

26

16

16

93

77 (-58 to -96) *

Amikacin

51

28

98

100

Aztreonam

19

16

00

95

-53 ( -35 to- 70)*

-2

(-2 - 6)

-95 (-85 to -100)*

*Starred antimicrobials show significant difference in activity against ESBL and non-ESBL producing gram-negative bacilli.
ESBL-GNB: Extended spectrum beta lactamase- producing gram-negative bacilli.

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tibility patterns in vitro, and tigecycline show no significant

difference (95% C.I, -0.04 to 0.18) in susceptibility patterns in
comparison with meropenem. Nevertheless, the later three
agents are not approved and should not be used in sever sepsis syndrome or bacteremia.(13, 14, 15, 16) Moreover, PIP/TAZ
showed tendency towards less activity than meropenem when
gram-negative pathogens were considered together (95%C.I,
-0.023 to 0.030).
ESBL- producers were found among E. coli, K. pneumonia, and
Enterobacter species. The prevalence of ESBL-producers was
30.7% of all gram-negative pathogens, and 44.5% among the
aforementioned ESBL-producers. E. coli lead the three pathogens in ESBL production (Table 4) contrary to other previous
studies that showed K. pneumonia was the leader.(17) The difference in susceptibility among ESBL-producing pathogens
compared with same non-ESBL producers show that meropenem (difference = 4, 95% C.I -8 to 12) and imipenem (difference = 4, 95% C.I -8 to 16) are again trust worthy in the initial
empiric therapy in ICUs and hospitals that suffer from high
rates of ESBL-producers, and both were comparable. PIP/TAZ,
an agent that is frequently used in ICU for sever sepsis of different sources, showed highly significant difference in activity

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against ESBL-producers and non-producers (difference = -53,

95% C.I, -35 to -70, p < 0.0001). The finding in these pathogens
point that IDSA recommendations in using PIP/TAZ in ESBLproducers in complicated intra-abdominal infections is to be
employed in community-acquired infections or health careassociate intra-abdominal infections if their total rates of ESBL
are less than 20%, or ESBL-subtypes are known, e.g. SHV and
Toho-2 were not prevalent. (17, 18) ESBL sub-typing is not available in a good number of laboratories.
This study utilizing pathogens showed that meropenem and
imipenem are trustworthy in the initial empiric therapy before the the documented pathogen is known, since the rates
of gram-negative pathogens susceptibilities are the highest
among tested agents potentially used in ICU sepsis. Looking
for antimicrobials susceptibility among pathogens is not common in literature for being tedious, though this approach may
be more accurate in clinical management of patients, especially
bacteria of the same species may be different in genotypes or
serotypes, which translate to pathogenesis potentials.(19, 20)

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