See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/377159950

Interpretative reading of antimicrobial susceptibility testing of gram-negative

bacteria from clinical isolates

Article in Journal of Dr NTR University of Health Sciences · December 2023

DOI: 10.4103/jdrysruhs.jdrysruhs_64_23

CITATIONS READS

0 96

3 authors:

Yazhini Karuppiah Sulakshana Sony Cheemala

Apollo Institute of Medical Sciences and Research Government Medical College, Ongole, India
10 PUBLICATIONS 1 CITATION 7 PUBLICATIONS 12 CITATIONS

SEE PROFILE SEE PROFILE

Swarajya Lakshmi

7 PUBLICATIONS 5 CITATIONS

SEE PROFILE

All content following this page was uploaded by Yazhini Karuppiah on 05 January 2024.

The user has requested enhancement of the downloaded file.

 Original Article

Interpretative reading of antimicrobial susceptibility

testing of gram‑negative bacteria from clinical isolates
Downloaded from http://journals.lww.com/jdyu by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XMi0hCywCX1AW

Yazhini Karuppiah, Sulakshana S. Cheemala1, Swarajya Lakshmi1

Department of Microbiology, Apollo Institute of Medical Sciences and Research (AIMSR), Hyderabad, Telengana,
1
Department of Microbiology, Mamata Academy of Medical Sciences, Hyderabad, Telengana, India
nYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC4/OAVpDDa8KKGKV0Ymy+78= on 01/05/2024

ABSTRACT
Introduction: The reading of antibiotic sensitivity testing goes beyond the determination of the bacterial sensitivity profile. The
interpretive reading of antibiotic susceptibility tests based on different patterns observed with beta-lactam agents is proposed in this
article, which will provide an understanding of the identification of unusual patterns, interpretation of possible resistance phenotypes
based on existing knowledge in antibiotic resistance mechanisms.
Methods: Antimicrobial susceptibility testing of 320 isolates of gram‑negative bacterial pathogens isolated from clinical samples were
performed using various phenotypic methods for the detection of resistance mechanisms. Interpretive reading of the antibiogram
data was performed to investigate the unusual resistance mechanisms from resistance phenotype.
Results: Out of 249 isolates 128 isolates (59%) were positive for cefoxitin screen. Out of these 128 isolates, 86 (67%) were
extended spectrum beta-lactamase (ESBL) co‑producers. Distorted patterns of antibiotic inhibition zones in the presence of
beta‑lactamase‑inducing agent provide information which is not otherwise evident from conventional methods.
Discussion: Distorted morphology of antibiotic inhibition zones in the presence of beta‑lactamase‑inducing agent provides
information which is not otherwise evident from routine testing by conventional methods.
Conclusion: The antibiotic susceptibility patterns observed on antimicrobial susceptibility testing (AST) plate for isolates harboring
multiple resistance can be obscure. Hence, it is important to practice mindfulness while reporting in microbiology laboratories in this
era of increased antimicrobial resistance; to promptly identify the resistant pathogens, to prevent its spread and for better patient
outcomes by selecting the most suitable drug even in resource‑limited settings.

Key words: AmpC beta‑lactamase, distorted patterns, imipenem induction, interpretative reading

INTRODUCTION intermediate, or resistant, and are analyzed taking into

account the cohort points established by the different
Antibiotic sensitivity testing evaluates the committees. However, the reading of antibiotic
susceptibility of a pathogen to an antibiotic. The sensitivity testing goes beyond the determination of
results are expressed in the categories: sensitive, the bacterial sensitivity profile. [1] The interpretive
reading of antibiotic susceptibility tests is proposed
Address for correspondence: in this article, which will provide an understanding
Dr. Yazhini Karuppiah,
Department of Microbiology, Apollo Institute of Medical Sciences of the identification of unusual patterns, interpretation
and Research (AIMSR), Hyderabad, Telengana, India. of possible resistance phenotypes based on existing
E‑mail: kyazh2306@gmail.com
This is an open access journal, and articles are distributed under the
Submitted: 31-Mar-2023 Accepted: 05-May-2023 terms of the Creative Commons Attribution‑NonCommercial‑ShareAlike
Published: 30-Dec-2023 4.0 License, which allows others to remix, tweak, and build upon the
work non‑commercially, as long as appropriate credit is given and
Access this article online
the new creations are licensed under the identical terms.
Quick Response Code:
Website:
For reprints contact: WKHLRPMedknow_reprints@wolterskluwer.com
https://journals.lww.com/jdyu
How to cite this article: Karuppiah Y, Cheemala SS,
DOI: Lakshmi S. Interpretative reading of Antimicrobial susceptibility testing
of gram‑negative bacteria from clinical isolates. J YSR Univ Health Sci
10.4103/jdrysruhs.jdrysruhs_64_23
2023;12:360-5.

360 © 2023 Journal of Dr. YSR University of Health Sciences | Published by Wolters Kluwer - Medknow
 Karuppiah, et al.: Interpretative reading of antimicrobial susceptibility testing
knowledge in antibiotic resistance mechanisms, and
finally, a change in the therapeutic management.
Multidrug resistant (MDR) organisms constitute
a major threat, [2] especially in hospital‑acquired
infections and intensive care units. Some resistance
Downloaded from http://journals.lww.com/jdyu by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XMi0hCywCX1AW
mechanisms may not be identified [3] or may be
missed in routine testing because they may appear
falsely susceptible; leading to patients receiving
ineffective antibiotics and hence, contribute to the
nYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC4/OAVpDDa8KKGKV0Ymy+78= on 01/05/2024
spread of MDR pathogens in hospital settings.
Thus, microbiology laboratory and the clinical
microbiologists play a very important role in
preventing this disaster from happening by promptly
identifying the resistant pathogens and guiding
the treating physician to ensure proper and timely
treatment of the patient and thereby prevent the
spread of resistance.
“Interpretative reading” requires that the isolates are
identified properly and tested with a complete set of
antibiotics for it predicts unusual patterns.[4,5] This
study aims to (i) analyze the susceptibility pattern for
individual antibiotics and to predict the underlying
resistance mechanisms; (ii) augment targeted treatment
with appropriate antibiotic based on interpretative
susceptibility results; (iii) make existing methods
more user‑friendly to detect complex mechanisms of
antibiotic resistance by interpretative reading for use
in routine diagnostic laboratories; and (iv) pass on the
benefit to the ultimate beneficiary, the patient.
MATERIALS AND METHODS
Institutional Ethics Committee clearance was
obtained. EC letter no. IEC/MAMS/2022/012; Dated
09/06/2022.
Antimicrobial susceptibility testing of 320 isolates
of gram‑negative bacterial pathogens isolated
from clinical samples was performed using
various phenotypic methods for the detection of
TABLE 1: FREQUENCIES OF ORGANISMS
Organisms Counts % Total Cumulative %
Citrobacter spp. 3 0.9 %
E. coli 142 44.4 %
Klebsiella spp. 87 27.2 %
Morganella spp. 1 0.3 %
Proteus spp. 16 5.0 %
Pseudomonas aeruginosa 71 22.2 %
Journal of Dr. YSR University of Health Sciences | Volume 12 | Issue 4 | October-December 2023
resistance mechanisms described below, and studied
to understand the different resistance patterns
exhibited by these pathogens. Arrangement of
antibiotic discs of all beta‑lactam agents in one
AST plate with imipenem (IMP) in the center and
co‑amoxiclav (CAC) adjacent to the third‑generation
cephalosporins (CTX/CTR and CAZ) to test for
induction of AmpC and ESBL; and all other classes
of drugs in another plate was designed as shown in
Figures 1 and 2, respectively.
The susceptibility of the isolates to were determined
by the standard disk diffusion method as per CLSI
M100‑Ed 32, 2022 guidelines. [6] E. coli (ATCC
25922) and K. pneumoniae (ATCC 700603) were
used as controls for quality. Interpretive reading of
the antibiogram data was performed to investigate the
unusual resistance mechanisms from the resistance
phenotype.
The susceptibility to cefoxitin disk (30 μg) was used
as a primary screening for AmpC beta‑lactamase
detection and the isolate with zone inhibition
diameter <18 mm was selected and then tested for
AmpC beta‑lactamase inhibition by cloxacillin.
The test for inducibility of AmpC beta‑lactamase by
cefoxitin, and imipenem; and inducible resistance
to third‑generation cephalosporins (cefotaxime and
ceftazidime (CAZ)) were performed by Kirby‑Bauer
disk approximation (KBDA) method.[7,8] Ceftazidime
resistance is the best indicator for TEM and
SHV‑derived ESBL; whereas cefotaxime resistance is
a better indicator for CTX‑M.[9–11] And so, resistance
CAC
CTX/C CAZ
TR
IMP
CFS AT
0.9 %
45.3 %
72.5 % CPM PIT
72.8 %
77.8 %
Figure 1: Arrangement of discs of all beta-lactam agents in one
100.0 % AST plate
361
 Karuppiah, et al.: Interpretative reading of antimicrobial susceptibility testing
CX
G CO
Downloaded from http://journals.lww.com/jdyu by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XMi0hCywCX1AW
MRP
TOB NIT
nYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC4/OAVpDDa8KKGKV0Ymy+78= on 01/05/2024
AK
CIP
Figure 2: Classes of drugs other than beta-lactams (in no particular
fashion) in another AST plate
to cefotaxime/ceftriaxone (30 μg) and/or CAZ were
taken as indicators for ESBL production as per CLSI
M100‑Ed 32, 2022 breakpoints.[6]
Statistical analysis was done using JAMOVI
software (version 2.3).[12]
RESULTS
Frequency of organisms isolated and studied is shown
in Table 1. Out of 249 isolates, 128 isolates (59%)
were positive for cefoxitin screen as shown in
Table 2. The frequency of organisms positive for
cefoxitin screen agar include E. coli 49%; Klebsiella
spp. 46%; and Proteus spp. 7.8%. Among these 128
isolates, 86 (67%) were ESBL co‑producers; 35%
of them were ESBL ceftazidimase, and 65% ESBL
broad enzyme producers. Klebsiella spp. showed
a high percentage of ESBL‑producing isolates and
30% of them produced both ESBL and acquired
AmpC enzyme. Upon the induction test, 39% of
the isolates showed a positive result by flattening
the inhibition zones of various beta‑lactam agents
adjacent to the imipenem or cefoxitin disk. The
different patterns observed on AST plate and their
interpretation are decribed in Table 3 and Figures 3-6.
The interpretative reading remarks for the different
isolates based on the patterns observed on antibiogram
is described in Tables 4-7.
DISCUSSION
Of the cephamycins, cefoxitin is used as a screening
agent for AmpC beta‑lactamse because this is stable
362 Journal of Dr. YSR University of Health Sciences | Volume 12 | Issue 4 | October-December 2023
TABLE 2: CEFOXITIN SCREEN OF THE
GRAM‑NEGATIVE ISOLATES
Cefoxitin screen CX N
Organisms R 128
(excluding Pseudomonas aeruginosa) S 121
against the activity of multiple like TEM‑1,2, SHV‑1,
and ESBLs but hydrolyzed by AmpC enzyme. [13]
Similarly, cefepime is not hydrolyzed by AmpC, but
is a substrate for ESBL. So, cefepime resistance,
irrespective of CTX/CTR breakpoints can be taken
as an indicator of ESBL production. Pseudomonas
aeruginosa isolates were excluded from the cefoxitin
screen because identification of P.aeruginosa by
default implies AmpC production.
In this study, out of 249 isolates (excluding
P.aeruginosa) 128 isolates (59%) were positive for
cefoxitin screen, which correlated with Handa D
et al.[14] Among these isolates, 42 (33%) were reported
susceptible (S) to cefotaxime and ceftazidime by
conventional KBDD testing but in KBDA method,
74% of them have shown inducible resistance, which
correlated with Xuan Qin et al.[15] who had reported
80% of inducible resistance. 39% of the isolates
showed a positive result upon induction, by flattening
the inhibition zones of various beta‑lactam agents
adjacent to the imipenem or cefoxitin disk; while the
remaining isolates could be considered as derepressed
mutant or ESBL co‑producers.
For all P.aeruginosa isolates, irrespective of the
susceptibility patterns, mutational resistance is possible
for any anti‑pseudomonal agent upon initiation of
treatment with the exception of colistin and possibly
meropenem. In addition, P. aeruginosa may also harbor
additional resistance mechanisms like impermeability and
efflux pumps wherein they show reduced susceptibility
to different classes of antibiotics including any one of
the carbapenems (either imipenem or meropenem) that
often also affects quinolones [Table 3].
Out of these 128 isolates, 86 (67%) were ESBL
co‑producers. 35% of them were ESBL Ceftazidimase
and 65% ESBL broad enzyme producers which
correlated with Lafi et al.[16] Klebsiella spp. showed a
high percentage of ESBL‑producing isolates and 30%
of them produced both ESBL and acquired AmpC
enzyme. Plasmid‑mediated AmpC enzymes present
the greatest threat clinically by seriously limiting
therapeutic doses, even more so than ESBLs.[17]
 Karuppiah, et al.: Interpretative reading of antimicrobial susceptibility testing

TABLE 3: PATTERNS OBSERVED ON AST PLATE

Observation Interpretation Remarks
Flattening of Aztreonam zone adjacent to Imipenem Imipenem induction Mutational resistance is possible for
in P.aeruginosa isolate that is otherwise susceptible any anti‑pseudomonal drug upon
to Ceftazidime, Aztreonam, and Cefepime initiation of treatment. (except
Colistin and possibly Meropenem)
Flattening of Aztreonam and Piperacillin‑Tazobactam Imipenem induction. AmpC and ESBL co‑producer.
zones adjacent to Imipenem in an isolate that is otherwise Phantom phenomenon
Downloaded from http://journals.lww.com/jdyu by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XMi0hCywCX1AW

susceptible to Piperacillin‑Tazobactam and resistant (Clavulanic acid

to Cefoxitin, Aztreonam, and Ceftriaxone. induction of ESBL).
Spur/Phantom zone at the intersection of Co‑amoxiclav and Ceftriaxone.
Flattening of Cefepime zone at the intersection of Ceftazidime and ESBL Cefipime is not hydrolyzed by
nYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC4/OAVpDDa8KKGKV0Ymy+78= on 01/05/2024

Cefoxitin zones in an isolate that is otherwise susceptible to Ceftazidime AmpC AmpC, but is a substrate for ESBL.
and Aztreonam and resistant to Cefoxitin, Cefotaxime/Ceftriaxone. Possible therapeutic
Phantom zone at the intersection of failure with Cefepime.
Piperacillin‑Tazobactam and Aztreonam.
Spur/Phantom zone adjacent to Co‑amoxiclav for Ceftriaxone and Phantom phenomenon
Cefepime in an isolate that is otherwise resistant to Cefepime and (Clavulanic acid
Ceftriaxone. induction of ESBL).

Figure 3: Imipenem induction in P.aeruginosa Figure 4: Imipenem induction and Phantom phenomenon

Figure 5: Cefoxitin induction Figure 6: Phantom phenomenon

Though from the past decade, many individual Distorted morphology of antibiotic inhibition zones
hospital antibiograms have reported only 30–40% in the presence of beta‑lactamase‑inducing agent
ESBL rates, many a times, there were cases of provides information which is not otherwise evident
treatment failure and relapse of the infection. from routine testing by conventional methods. The

Journal of Dr. YSR University of Health Sciences | Volume 12 | Issue 4 | October-December 2023 363
 Karuppiah, et al.: Interpretative reading of antimicrobial susceptibility testing

distorted zone morphologies observed may be due to CONCLUSION

the action of auxillary regulatory genes, rather than
mutations in AmpC regulators or promotors.[18‑21] The antibiotic susceptibility patterns observed on the
AST plate for isolates harboring multiple resistance
For organisms known to produce an inducible can be obscure. For instance, reduced susceptibility
chromosomal AmpC beta‑lactamase[3] (Enterobacter to any of the carbapenems could be either due
Downloaded from http://journals.lww.com/jdyu by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XMi0hCywCX1AW

spp., Citrobacter freundii, Pseudomonas aeruginosa, to increased efflux or impermeability rather than
Serratia marcescens, Providencia spp., Morganella carbapenemase production. Hence, it is important to
morganii, etc.,), it is not necessary to perform further practice mindfulness while reporting in microbiology
testing to identify AmpC production; and by default,
nYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC4/OAVpDDa8KKGKV0Ymy+78= on 01/05/2024

laboratory in this era of increased antimicrobial

these isolates can be assumed to be AmpC producers resistance; to promptly identify the resistant
upon identification. pathogens, to prevent its spread, and for better

TABLE 4: ESCHERICHIA COLI: PATTERNS OBSERVED ON ANTIBIOGRAM

AMP CZ CX CAZ AT CPM CAC CFS PIT IMP MRP Interpretation
R S S S S S S S S S S Classical penicillinase
R R R S S S S S S S S ESBL; Chromosomal AmpC
R R S R R R S S S S ESBL ‑ broad
R R S R R R S S S S S ESBL ‑ broad
R R R R R R R R S S S ESBL ‑ broad; Chromosomal AmpC
R R R S S S R S S S S Penicillinase; Chromosomal AmpC
R R R S R S R R R R S Plasmid acquired AmpC
R R S R R R R S S S S ESBL ‑ broad
R R S S S S S S S S S Penicillinase
R S S S S S S S S S S Classical penicillinase
R‑ Resistant, S‑ Susceptible

TABLE 5: KLEBSIELLA SPP.: PATTERNS OBSERVED ON ANTIBIOGRAM

CZ CX
R R
R S
R S
R R
R S
R R
R S
R‑ Resistant, S‑ Susceptible
CTX CAZ AT CPM CFS PIT IMP MRP Interpretation
R R R R R R S S ESBL; Plasmid acquired AmpC
S S S S S R S S K1 ‑ high
R R R S S S S S ESBL
R S S S S S S S Plasmid acquired AmpC
S S S S S S S S Classical low SHV‑1/K1
S S S S S S R S ? Porin deficient
R R R R S S S S ESBL – broad

TABLE 6: PROTEUS SPP.: PATTERNS OBSERVED ON ANTIBIOGRAM

CZ CX CTX CAZ AT CPM CFS PIT IMP MRP Interpretation
R S R R R R S S S S ESBL – broad (P. vulgaris)
R R R R R R R R S S ESBL ‑ broad;
Inducible chromosomal AmpC – derepressed (P. vulgaris)
R R S S S S S S S S AmpC ‑ plasmid acquired (P. mirabilis)
R‑ Resistant, S‑ Susceptible

TABLE 7: PSEUDOMONAS AERUGINOSA: PATTERNS OBSERVED ON ANTIBIOGRAM

CAZ CPM AT PIT IMP MRP CIP LE Interpretation
R R R R S S R S AmpC ‑ fully derepressed
R R R R R S R R AmpC ‑ fully derepressed; loss of Opr D porin
R R R S R S S S loss of Opr D porin
R R R I S R R R Increased efflux/impermeability
R R S S S I R R increased efflux/impermeability
I S R S S S S S AmpC partly derepressed
R‑ Resistant, S‑ Susceptible, I‑ Intermediate

364 Journal of Dr. YSR University of Health Sciences | Volume 12 | Issue 4 | October-December 2023
 Karuppiah, et al.: Interpretative reading of antimicrobial susceptibility testing
patient outcomes by selecting the most suitable drug
even in resource‑limited settings where automation
and molecular testing are either unavailable or not
feasible.
Limitations of the study
Downloaded from http://journals.lww.com/jdyu by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XMi0hCywCX1AW
Interpretative reading is not a substitute for identifying
resistance mechanisms by molecular methods and
cannot identify new resistance mechanisms, but just
an improved method of identifying known resistance
nYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC4/OAVpDDa8KKGKV0Ymy+78= on 01/05/2024
mechanisms based on different patterns observed rather
than just measuring zone diameters and following
breakpoints in day‑to‑day practice where identifying
genes coding for resistance may not be possible for
all isolates in a resource‑limited setting.
Acknowledgments
I sincerely acknowledge the support of the laboratory
technicians of Mamata Academy of Medical Sciences
in complying with the instructions for the smooth
conduct of this study.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
REFERENCES
1. Castell CD, Pájaro LQ, Marzola ID, Campo IG, Villegas YR,
Carvajal AM, et al. Lectura interpretada de antibiograma: Un enfoque
basado en preguntas. Acta Colombiana de Cuidado Intensivo
2021;21:252‑62.
2. Cantón R. [Interpretive reading of the antibiogram: A clinical
necessity]. Enferm Infecc Microbiol Clin 2010;28375‑85.
3. Thomson KS. Extended‑spectrum‑β‑lactamase, AmpC, and
carbapenemase issues. J Clin Microbiol 2010;48:1019‑25.
4. Courvalin P. Interpretive reading of antimicrobial susceptibility tests.
ASM News 1992;58:368‑75.
5. Vedel G, Peyret M, Gayral JP, Millot P. Evaluation of an expert
system linked to a rapid antibiotic susceptibility testing system
for the detection of β‑lactam resistance phenotypes. Res Microbiol
Journal of Dr. YSR University of Health Sciences | Volume 12 | Issue 4 | October-December 2023
View publication stats
1996;147:297‑309.
6. National Committee for Clinical Laboratory Standards. Performance
Standards for Antimicrobial Disk Susceptibility tests. Approved
Standard M2‑A7. 7th ed. Wayne, PA: National Committee for Clinical
Laboratory Standards; 2000.
7. Miles RS, Amyes SGB. Laboratory control of antimicrobial therapy.
In: Colle JG, Barrie PM, Fraser AG, Simmons A, editors. Mackie
and McCartney Practical Medical Microbiology. 14th ed. Singapore:
Churchill Livingston; 1996. p. 173‑7.
8. Eliopoulos GM, Moellering RC Jr. Antimicrobial combinations. In
Antibiotics in Laboratory Medicine. Edited by: Victor Lorian. 4th ed.
Williams & Wilkins; 1996. p. 330‑96.
9. Jacoby GA, Carreras I. Activities of β‑lactam antibiotics against E. coli
strains producing extended spectrum β‑lactamases. Antimicrob
Agents Chemother 1990;34:858‑62.
10. Bradford PA, Yang Y, Sahm D, Grope I, Gardovska D, Storch G.
CTX‑M‑5, a novel cefotaxime‑hydrolyzing ‑lactamase from an
outbreak of Salmonella typhimurium in Latvia. Antimicrob Agents
Chemother 1998;42:1980‑4.
11. Nordmann P. Trends in ‑lactam resistance among Enterobacteriaceae.
Clin Infect Dis 1998;27(Suppl. 1):S100‑6.
12. The jamovi project (2022). jamovi (Version 2.3) [Computer Software].
Available from: https://www.jamovi.org.
13. Livermore DM. β‑lactamase‑mediated resistance and opportunities
for its control. J Antimicrob Chemother 1998;41:25‑41.
14. Handa D, Pandey A, Asthana AK, Rawat A, Handa S, Thakuria B.
Evaluation of phenotypic tests for the detection of AmpC
beta‑lactamase in clinical isolates of Escherichia coli. Indian J Pathol
Microbiol 2013;56:135‑8.
15. Qin X, Weissman SJ, Chesnut MF, Zhang B, Shen L. Kirby‑Bauer disc
approximation to detect inducible third‑generation cephalosporin
resistance in Enterobacteriaceae. Ann Clin Microbiol Antimicrob
2004;3:13. doi: 10.1186/1476‑0711‑3‑13.
16. Lafi MAK, Mohammed SF, Al‑Hadithi HA. Novel β‑Lactamases in
the clinical isolates of enterobacter spp. and Klebsiella pneumoniae
in Ramadi General Hospital: A pharmacodynamics study. Iraqi J
Comm Med 2012:124‑9. Available from: https://www.iasj.net/iasj/
download/261d914c49b1fa42.
17. Thomson KS, Moland ES, Sanders CC. Use of microdilution panels
with and without βlactamase inhibitors as a phenotypic test for
βlactamase production among Eschericia coli, Klebsiella spp.,
Enterobacter spp., Citrobacter freundii, and Serratia marcescens.
Antimicrob Agents Chemother 1999;43:1393‑400.
18. Bartowsky E, Normark S. Purification and mutant analysis of
Citrobacter freundii AmpR, the regulator for chromosomal AmpC
beta‑lactamase. Mol Microbiol 1991;5:1715‑25.
19. Lindquist S, Galleni M, Lindberg F, Normark S. Signalling proteins
in enterobacterial AmpC beta‑lactamase regulation. Mol Microbiol
1989;3:1091‑102.
20. Mahlen SD, Morrow SS, Abdalhamid B, Hanson ND. Analyses of
ampC gene expression in Serratia marcescens reveal new regulatory
properties. J Antimicrob Chemother 2003;51:791‑802.
21. Poirel L, Guibert M, Girlich D, Naas T, Nordmann P. Cloning,
sequence analyses, expression, and distribution of ampC‑ampR from
Morganella morganii clinical isolates. Antimicrob Agents Chemother
1999;43:769‑76.
365