Journal of Medical Microbiology (2014), 63, 962–967
DOI 10.1099/jmm.0.068486-0
Detection of TEM-, SHV- and CTX-M-type
b-lactamase production among clinical isolates
of Salmonella species
Sathishkumar Elumalai,1 G. Muthu,2 R. Esther Mary Selvam3
and Srivani Ramesh1
Correspondence
Srivani Ramesh
srivani.ramesh@gmail.com
1
Department of Microbiology, Dr ALM Post Graduate Institute of Basic Medical Sciences,
University of Madras, Taramani, Chennai 600 113, Tamil Nadu, India
2
Central Research Laboratory, Sri Manakula Vinayagar Medical College and Hospital, Madagadipet,
Pondicherry 605 107, India
3
Department of Microbiology, ESIC Hospital, K. K. Nagar, Chennai 600078, Tamil Nadu, India
Received 19 September 2013
Accepted 10 May 2014
Enteric fever is a major public health problem in developing countries. Due to the problem of
resistance to first-line drugs and fluoroquinolone, cephalosporins are currently used for treatment
of enteric fever. Cephalosporin resistance in Salmonella spp. is mainly due to production of
extended-spectrum b-lactamases (ESBLs). The majority of ESBLs in Salmonella are derivatives of
the TEM and SHV b-lactamase families. The objectives of this study were to detect antibiotic
susceptibility patterns, ESBL production and TEM-, SHV- and CTX-M-encoding genes (blaTEM,
blaSHV and blaCTX-M) among clinical isolates of Salmonella spp. A total of 134 Salmonella isolates
[Salmonella Typhi (n5101), Salmonella Paratyphi A (n531), Salmonella Paratyphi B (n51) and
Salmonella Typhimurium (n51)] were included in this study. Multidrug resistance was seen in 5/
134 (3.73 %) isolates, all of which belonged to serotype S. Typhi. A better susceptibility profile
was observed for first-line drugs (ampicillin, chloramphenicol, co-trimoxazole and tetracycline) and
cephalosporins (cefotaxime, ceftazidime, ceftriaxone, cefixime and cefepime). However, 131
(97.76 %) of the 134 isolates were resistant to nalidixic acid and one (0.75 %) was resistant to
ciprofloxacin. TEM-1-type b-lactamase (blaTEM-1) was detected in six (4.47 %) of the 134
isolates, which belonged to the serotype S. Typhi. All six TEM-positive isolates were negative for
the blaSHV gene and none of the isolates was positive for the blaCTX-M gene. The presence of the
blaTEM gene encoding TEM-1 b-lactamase is believed to confer resistance only to penicillins and
early cephalosporins; however, the resistance spectrum of TEM-1 descendants may extend to
second-, third- and fourth-generation cephalosporins. The ESBLs derived from TEM-1 differ from
their progenitors by as few as 1 aa, and have the ability to hydrolyse third-generation
cephalosporins. Therefore, appropriate selection and rotation of antibiotics as well as continuous
monitoring of antibiotic susceptibility profiles could help to control the emergence and spread of
resistant strains.
INTRODUCTION
Enteric fever includes typhoid and paratyphoid fever. It is
an important public health problem caused by Salmonella
enterica serovar Typhi and S. enterica serovars Paratyphi A,
B and C respectively. Both serotypes are solely human
pathogens. Infection occurs mainly due to ingestion of
food or water contaminated with human waste (Scherer &
Abbreviations: ESBL, extended-spectrum b-lactamase; MDR, multidrug
resistant.
The GenBank/EMBL/DDBJ accession number for the Salmonella
enterica serovar Typhi strain determined in this study is KF551994.
962
Miller, 2001). Typhoid fever is a major cause of morbidity
and mortality, estimated to cause 21.7 million illnesses and
217 000 deaths per year, whereas paratyphoid fever causes
illness in an estimated 5.4 million people per year worldwide
(Crump et al., 2004). Appropriate treatment reduces the
mortality rate as low as 0.5 % (Cooke & Wain, 2004).
Multidrug-resistant (MDR) S. enterica (resistant to chloramphenicol, ampicillin and trimethoprim-sulfamethoxazole) has emerged worldwide in the last two decades
(Madhulika et al., 2004). Invasive Salmonella infections can
be treated with fluoroquinolones and b-lactam (cephalosporins) antibiotics (Rotimi et al., 2008). However, S.
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TEM-, SHV- and CTX-M-type ESBLs in Salmonella spp.
enterica isolates have developed resistance to fluoroquinolones in the Indian subcontinent and other regions (Effa &
Bukirwa, 2008).
In Salmonella, resistance to cephalosporins is largely due to
the production of extended-spectrum b-lactamases (ESBLs)
and is often plasmid mediated (Rotimi et al., 2008). The
majority of ESBLs in Salmonella are derivatives of the TEM
and SHV b-lactamase families. Other b-lactamases like
CTX-M have also been described in Salmonella (Bradford,
2001; Bonnet, 2004). CTX-M-type ESBLs or cefotaximases
are encoded by blaCTX-M genes located on a plasmid or on
the chromosome (Rodriguez et al., 2004). Studies on ESBLproducing Salmonella strains have revealed the presence of
insertion sequence ISEcp1 upstream of the blaCTX-M gene,
which may contribute to the mobility and dissemination of
these genes to other bacteria in the environment (Sjölund
et al., 2008; Tamang et al., 2011).
In this background, the present study was carried out to
document recent antibiotic susceptibility profiles of ESBL
production and to screen for the presence of TEM-, SHVand CTX-M-encoding genes (blaTEM, blaSHV and blaCTX-M)
among clinical isolates of Salmonella spp.
METHODS
Bacterial isolates and serotyping. A total of 134 Salmonella
isolates (98 isolates were collected in 2007–2009 and the remaining 36
were collected in 2011–2012) from blood samples of patients attending
tertiary-care hospitals and other diagnostic laboratories in Chennai,
India, were included in this study. Characterization and identification
of the isolates were performed using a battery of biochemical tests
(Old, 1996). Serotyping of the Salmonella isolates was performed using
specific antisera procured from the King Institute of Preventive
Medicine and Research, Chennai, India. Institutional ethical clearance
was obtained to conduct this study.
boiled suspension of bacterial cells as DNA template (Lim et al.,
2009). The primers used were blaTEM: TEM-F, 59-ATGAGTATTCAACATTTCCG-39, and TEM-R, 59-CTGACAGTTACCAATGCTTA39; blaSHV: SHV-F, 59-GGTTATGCGTTATATTCGCC-39, and SHVR, 59- TTAGCGTTGCCAGTGCTC-39; and blaCTX-M: CTX-MU1, 59ATGTGCAGYACCAGTAARGT-39, and CTX-MU2, 59-TGGGTRAARTARGTSACCAGA-39. Reaction mixtures of 25 ml containing
1.5 U Taq DNA polymerase (New England BioLabs) in the reaction
buffer provided by the manufacturer containing 1.5 mM MgCl2,
200 mM dNTPs, 0.2 mM selected primer and 2 ml DNA template were
prepared in a thermal cycler (Eppendorf). The cycling parameters
employed comprised one cycle of 5 min at 96 uC, followed by 35
cycles of 1 min at 96 uC, 1 min at 58 uC for blaTEM or at 60 uC for
blaSHV and 1 min at 72 uC, with a final extension of 10 min at 72 uC.
The thermal cycling conditions for the CTX-M gene were one cycle of
7 min at 94 uC, followed by 35 cycles of 50 s at 94 uC, 40 s at 50 uC
and 1 min at 72 uC, with a final extension of 5 min at 72 uC. The
amplicon size for blaTEM and blaSHV was 867 bp, and for blaCTX-M
was 593 bp. Aliquots (10 ml) of each PCR product were subjected to
electrophoresis on a 1.5 % agarose gel. The amplified product was
sequenced using an ABI 3730XL DNA Analyser (Applied Biosystems).
Nucleotide sequences were analysed by searching GenBank using
BLAST (http://www.ncbi.nlm.nih.gov/blast/).
RESULTS
Of the 134 isolates recovered from blood cultures of suspected cases of enteric fever, Salmonella Typhi was the
predominant serotype (n5101, 75.4 %), followed by Salmonella Paratyphi A (n531, 23.12 %), Salmonella Paratyphi B
(n51, 0.74 %) and Salmonella Typhimurium (n51, 0.74 %).
Tables 1 and 2 show the antibiotic susceptibility pattern
and resistance pattern for all the Salmonella isolates. Table
3 depicts the MICs of various antimicrobials for S. Typhi
and S. Paratyphi A.
Antibiotic susceptibility testing. Antibiotic susceptibility testing of
the isolates was carried out by a standard Kirby–Bauer disk-diffusion
method using Clinical and Laboratory Standards Institute guidelines
(CLSI, 2011). The following antibiotics were tested: ampicillin (10 mg),
chloramphenicol (30 mg), co-trimoxazole (1.25/23.75 mg), tetracycline
(30 mg), cefotaxime (30 mg), ceftazidime (30 mg), ceftriaxone (30 mg),
cefixime (5 mg), cefepime (30 mg), nalidixic acid (30 mg), ciprofloxacin
(5 mg), ofloxacin (5 mg), levofloxacin (5 mg) and imipenem (10 mg).
Antibiotic discs were obtained from HiMedia Laboratories.
The MICs of ampicillin, cefotaxime and ceftazidime (HiMedia
Laboratories) were determined by an agar dilution method (CLSI,
2011). Escherichia coli ATCC 25922 was used as the control strain.
Detection of b-lactamase production. Isolates were screened for
ESBL production by a combination disc method using cefotaxime
(30 mg) and ceftazidime (30 mg) and a disc of cefotaxime+clavulanate
(30+10 mg) and ceftazidime+clavulanate (30+10 mg) (HiMedia
Laboratories). A ¢5 mm increase in diameter of the inhibition zone
of the cefotaxime+clavulanate and ceftazidime+clavulanate disc
compared with the cefotaxime and ceftazidime disc alone was
interpreted as phenotypic evidence of ESBL production (CLSI, 2011).
PCR for b-lactamase-encoding genes and nucleotide sequencing analysis. The b-lactamase genes blaTEM, blaSHV and blaCTX-M
Table 1. Antibiotic susceptibility pattern of Salmonella isolates
(n5134) to various antibiotics
Results are shown as number of isolates (%).
Antibiotics
Ampicillin
Chloramphenicol
Co-trimoxazole
Tetracycline
Cefotaxime
Ceftazidime
Ceftriaxone
Cefixime
Cefepime
Nalidixic acid
Ciprofloxacin
Ofloxacin
Levofloxacin
Imipenem
Sensitive
(%)
127
128
130
127
123
134
132
133
134
2
126
134
134
134
(94.78)
(95.52)
(97.10)
(94.78)
(91.8)
(100)
(98.5)
(99.25)
(100)
(1.49)
(94.03)
(100)
(100)
(100)
Intermediate
(%)
Resistant
(%)
1 (0.75)
1 (0.75)
0 (0)
2 (1.49)
11 (8.2)
0 (0)
0 (0)
1 (0.75)
0 (0)
1 (0.75)
7 (5.22)
0 (0)
0 (0)
0 (0)
6 (4.47)
5 (3.73)
4 (2.9)
5 (3.73)
0 (0)
0 (0)
2 (1.5)
0 (0)
0 (0)
131 (97.76)
1 (0.75)
0 (0)
0 (0)
0 (0)
were detected by PCR using forward and reverse primer pairs with a
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S. Elumalai and others
Table 2. Resistance pattern of the S. Typhi and S. Paratyphi A isolates to various antibiotics
Results are shown as number of isolates (%). The S. Paratyphi B (n51) and S. Typhimurium (n51) isolates were susceptible to all the antibiotics
tested.
Antibiotics
S. Typhi (%) (n5101)
Ampicillin
Chloramphenicol
Co-trimoxazole
Tetracycline
Cefotaxime
Ceftazidime
Ceftriaxone
Cefixime
Cefepime
Nalidixic acid
Ciprofloxacin
Ofloxacin
Levofloxacin
Imipenem
5
5
4
5
0
0
2
0
0
100
1
0
0
0
S. Paratyphi A (%) (n531)
(4.95)
(4.95)
(3.96)
(4.95)
(0)
(0)
(1.98)
(0)
(0)
(99)
(0.99)
(0)
(0)
(0)
1
0
0
0
0
0
0
0
0
31
0
0
0
0
Of the 134 Salmonella isolates studied, 127 (94.78 %) were
sensitive to ampicillin and tetracycline, 128 (95.52 %) were
sensitive to chloramphenicol, 130 (97.10 %) were sensitive
to co-trimoxazole, 123 (91.8 %) were sensitive to cefotaxime, 132 (98.5 %) were sensitive to ceftriaxone, 133
(99.25 %) were sensitive to cefixime and 126 (94.03 %)
were sensitive to ciprofloxacin.
Table 3. MICs of various antibiotics for the S. Typhi and S.
Paratyphi A isolates
The number of strains for each MIC is shown, –, No growth. The
CLSI (2011) interpretive criteria for sensitive, intermediate and
resistant strains, respectively, are (mg ml21): ampicillin (Amp), ¡8,
16, ¢32; cefotaxime (Ctx), ¡1, 2, ¢4; ceftazidime (Caz), ¡4, 8,
¢16.
MIC (mg ml”1)
¡0.032
0.064
0.125
0.25
0.5
1
2
4
8
16
¢32
Total
*MIC90 values.
964
S. Typhi (n5101)
S. Paratyphi A
(n531)
Amp
Ctx
Caz
Amp
Ctx
Caz
–
–
–
–
–
24
55
15*
1
1
5
101
–
4
24
51
22*
–
–
–
–
–
–
101
–
–
7
8
84*
2
–
–
–
–
–
101
–
–
–
–
–
6
22
2*
–
–
1
31
3
3
9
14*
2
–
–
–
–
–
–
31
–
–
–
1
30*
–
–
–
–
–
–
31
(3.22)
(0)
(0)
(0)
(0)
(0)
(0)
(0)
(0)
(100)
(0)
(0)
(0)
(0)
Total no. isolates (n5132)
6 (4.54)
5 (3.78)
4 (3.03)
5 (3.78)
0 (0)
0 (0)
2 (1.5)
0 (0)
0 (0)
131 (99.24)
1 (0.75)
0 (0)
0 (0)
0 (0)
All 134 isolates were susceptible to ceftazidime, cefepime,
ofloxacin, levofloxacin and imipenem. Multidrug resistance was seen in 5/134 (3.73 %) isolates, all of which
belong to serotype S. Typhi.
A better pattern of sensitivity was observed for first-line
drugs (ampicillin, chloramphenicol, co-trimoxazole and
tetracycline) and cephalosporins (cefotaxime, ceftazidime,
ceftriaxone, cefixime and cefepime). However, 97.76 %
(131/134) of isolates were resistant to nalidixic acid and
0.75 % (1/134) were resistant to ciprofloxacin. All the
isolates were negative for ESBL production by the
combination disc method.
TEM-type b-lactamase (blaTEM) was detected in six
(4.47 %) of the 134 isolates, which belonged to the serotype
S. Typhi (Fig. 1), and nucleotide sequencing analysis
revealed that the six isolates carried the blaTEM gene (TEM1-type b-lactamase). All the six TEM-positive isolates were
negative for the blaSHV gene and showed resistance to
ampicillin (MIC .32 mg ml21) but were sensitive to thirdand fourth-generation cephalosporins. None of the 134
isolates was positive for the blaCTX-M gene.
DISCUSSION
Enteric fever is a major systemic health problem in
developing countries, including India. Various studies
document S. Typhi as the predominant serotype and S.
Paratyphi A as the second most common serotype (Hirose
et al., 2001; Manchanda et al., 2006; Choudhary et al.,
2013), which correlates well with our study result.
The Salmonella Paratyphi A isolates showed a better
susceptibility to routinely used antibiotics than S. Typhi.
In comparison with previous studies, which reported 11–
13 % multidrug-resistant Salmonella (Dutta et al., 2005;
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Journal of Medical Microbiology 63
TEM-, SHV- and CTX-M-type ESBLs in Salmonella spp.
M
1
2
3
4
5
1000 bp
800 bp
6
876 bp
500 bp
100 bp
Fig. 1. PCR detection of blaTEM gene. Lanes: M, 100 bp ladder; 1–6, 876 bp PCR product from the six S. Typhi isolates
carrying the blaTEM gene.
Verma et al., 2010; Bhattacharya et al., 2011), we observed
a significant decrease in MDR (3.73 %) among our study
isolates. The majority of the isolates were resistant to
nalidixic acid, whereas only one isolate showed resistance
to ciprofloxacin. Several studies have shown that Salmonella spp. resistant to nalidixic acid may show reduced
fluoroquinolone susceptibility in vivo, resulting in treatment failure (Crump et al., 2003; Kownhar et al., 2007;
Choudhary et al., 2013).
In our study, none of the isolates was found to be positive
for ESBLs by a combination disc method. A possible reason
for this result is that TEM-1 b-lactamase has the ability to
hydrolyse only penicillins/early cephalosporins but not
third- or fourth-generation cephalosporins, which could
not be detected by the ESBL combination disc method.
In Gram-negative pathogens, b-lactamase production
remains the most important contributing factor to blactam resistance (Medeiros, 1997). The persistent exposure of bacterial strains to a multitude of b-lactams has led
to overproduction and mutation of b-lactamases leading to
their ability to hydrolyse penicillins and broad-spectrum
cephalosporins (Bush, 2001).
In addition to bacteria that have long been known to
produce b-lactamase (such as Staphylococcus aureus and
Enterobacteriaceae), these enzymes have spread to pathogens such as Haemophilus influenzae and Neisseria gonorrhoeae that previously lacked b-lactamase (Jacoby &
Munoz-Price, 2005). Additionally, there are a few reports
of ESBL production in pathogens such as Shigella flexneri,
Shigella dysenteriae, Shigella sonnei and Vibrio cholerae
(Ahamed & Kundu, 1999; Fortineau et al., 2001; Pai et al.,
2001; Petroni et al., 2002).
TEM-type b-lactamases are found mainly in Escherichia
coli, Klebsiella pneumoniae and Proteus mirabilis. The first
TEM variant with increased activity against extendedspectrum cephalosporins was TEM-3. In 1983, SHV-2
isolated from K. pneumoniae showed transferable resistance
to cefotaxime as well as to other cephalosporins (Gupta,
http://jmm.sgmjournals.org
2007). The ESBLs derived from TEM-1, TEM-2 and SHV-1
differ from their progenitors by as few as 1 aa, which
results in the ability to hydrolyse third-generation cephalosporins (Paterson & Bonomo, 2005). The CTX-M-type
b-lactamases, which differ from TEM- and SHV-type
ESBLs, were initially reported in 1980s and are closely
related to the b-lactamases of Kluyvera spp. (Bonnet 2004).
Salmonella strains may acquire the gene encoding CTX-Mtype ESBLs from E. coli and Klebsiella spp. in the
community and then spread it among the various serotypes
of Salmonella (Rotimi et al., 2008).
Although we found the blaTEM gene encoding TEM-1 blactamase in our isolates, which was shown to confer
resistance only to penicillins and early cephalosporins,
the resistance spectrum of its descendants may extend
to second-, third- and fourth-generation cephalosporins
(Salverda et al., 2010). This was supported by an outbreak
of TEM-1-producing Klebsiella oxytoca in a neonatal unit,
which was reported in Liverpool, UK, in 1982. Initially, the
isolate was sensitive to ceftazidime, and infected patients
were treated with this drug, but subsequent isolation of K.
oxytoca from the same unit found that they harboured the
TEM-type ESBL (TEM-12) and showed resistance to
ceftazidime (Du Bois et al., 1995). It was demonstrated
that the ceftazidime resistance gene was transferrable and
carried on a plasmid (Payne et al., 1990).
ESBL production in Salmonella spp. was first identified in
1988 and is increasing in prevalence worldwide; it has been
detected in Salmonella enterica strains of different serovars
in a number of countries including Italy, France, Ireland
and the Philippines (Morris et al., 2006; Al Naiemi et al.,
2008). S. Paratyphi A and S. Typhi with high rates of MDR
and ESBL production (SHV-12 and TEM-1) were reported
in a study conducted in Nepal (Pokharel et al., 2006).
Salmonella spp. co-producing CTX-M- and TEM-type blactamases have been documented in a few case reports
from Bangladesh (Ahmed et al., 2012) and India
(Karthikeyan et al., 2011). Plasmid analysis of the resistant
isolate revealed that the blaCTX-M and blaTEM genes were
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965
S. Elumalai and others
located in the same plasmid, which carried the ISEcp1
element upstream of the blaCTX-M gene to facilitate mobilization and expression (Karthikeyan et al., 2011). The
present study is important in understanding the mechanism of resistance operating in these common pathogens,
which are also endemic in India.
Crump, J. A., Luby, S. P. & Mintz, E. D. (2004). The global burden of
Extended-spectrum cephalosporins are the drugs of choice
for the treatment of infections due to fluoroquinoloneresistant Salmonella spp. The emergence of ESBLs in
Salmonella constitutes a new challenge. ESBLs are the most
evolving mechanism of antibiotic resistance among the
family of Enterobacteriaceae due to the selective pressure
imposed by inappropriate use of third-generation cephalosporins. This emergence may be due to the exchange of
mobile genetic elements, such as plasmids and transposons,
between enteric bacteria. Therefore, appropriate selection
and rotation of antibiotics, as well as continuous monitoring of antibiotic susceptibility profiles, could help to
control the emergence and spread of resistance strains.
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