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Research
(Published
online: 30-11-2014)
23.
Detection of extended-spectrum β-lactamases
(blaCTX-M-1
and
blaTEM)
in Escherichia coli, Salmonella spp., and
Klebsiella pneumoniae isolated from poultry in North Eastern
India -
H. Lalzampuia, T. K.
Dutta, Iadarilin Warjri and Rajesh Chandra
Veterinary World, 7(11): 1026-1031
doi:
10.14202/vetworld.2014.1026-1031
H. Lalzampuia:
Department of Veterinary Microbiology, Central Agricultural
University, Selesih, Aizawl, Mizoram, India;
ateahlawndo@gmail.com
T. K.
Dutta:
Department of Veterinary Microbiology, Central Agricultural
University, Selesih, Aizawl, Mizoram, India;
tapandutta@rediffmail.com
Iadarilin Warjri:
Department of Veterinary Microbiology, Central Agricultural
University, Selesih, Aizawl, Mizoram, India;
iadawarjri@gmail.com
Rajesh
Chandra: Department of Veterinary Microbiology, Central
Agricultural University, Selesih, Aizawl, Mizoram, India;
rajeshchandra2k@rediffmail.com
Received:
05-08-2014, Revised: 19-10-2014, Accepted: 27-10-2014, Published
online: 30-11-2014
Corresponding author:
T. K. Dutta, e-mail: tapandutta@rediffmail.com
Abstract
Aim:
The present study was conducted to record the association of
extended spectrum β-lactamases (ESBLs) producing enteric bacteria
with diarrhea of poultry birds in Mizoram, India.
Materials and Methods: Fecal samples were collected from
poultry birds with the history of diarrhea from different parts of
Mizoram. Samples were processed for isolation and identification
of Escherichia coli, Salmonella, and Klebsiella
pneumoniae. All the isolates were subjected to antibiotic
sensitivity assays. Phenotypically, ESBLs production ability was
determined by double discs synergy test (DDST) method. ESBLs
producing isolates were subjected to polymerase chain reaction (PCR)
for detection of ESBLs genes. Plasmids were cured by acridine
orange. Transfer of resistance from donor to recipient strains was
done by in vitro horizontal method.
Results: A total of 134 enteric bacteria was isolated, of
which 102 (76.12%), 21 (15.67%) and 11 (8.21%) were E. coli,
Salmonella spp. and K. pneumoniae, respectively. By
DDST 7 (5.22%) isolates (6 E. coli and 1 K. pneumoniae)
were ESBLs producer. PCR analysis confirmed 5 (3.73%) (4 E.
coli and 1 K. pneumoniae) isolates harboured
blaCTX-M-1
gene
and/or blaTEM
gene. All the isolates were carrying plasmids
ranging between 0.9 kb and ~30 kb. Of the 4 isolates positive for
blaCTX-M-1 and/or
blaTEM,
2 (1.84%) were confirmed for blaCTX-M-1
gene in their plasmid. No
blaTEM
gene was detected from plasmid. The resistance
plasmid could not be transferred to the recipient by in vitro
horizontal gene transfer method.
Conclusion: ESBLs producing enteric bacteria are circulating
in poultry in North Eastern Region of India. As poultry is one of
the most common food animals in this region, these organisms may
enter in human population through them.
Keywords: blaCTX-M-1,
blaTEM,
extended spectrum β-Lactamases,
North East India, poultry.
References
1. Schmid, A., Hörmansdorfer, S., Messelhäusser, U., Käsbohrer,
A., Sauter-Louis, C. and Mansfeld, R. (2013) Prevalence of
extended-spectrum β-lactamase-producing Escherichia coli on
Bavarian dairy and beef cattle farms. Appl. Environ. Microbiol.,
79(9): 3027-3032.
http://dx.doi.org/10.1128/AEM.00204-13
PMid:23455336 PMCid:PMC3623142 |
|
2. Moodley, A. and Guardabassi, L. (2009) Transmission of IncN
plasmids carrying blaCTX-M-1 between commensal Escherichia
coli in pigs and farm workers. Antimicrob. Agents Chemother.,
53: 1709-1711.
http://dx.doi.org/10.1128/AAC.01014-08
PMid:19188380 PMCid:PMC2663060 |
|
3. Horton, R.A., Randall, L.P., Snary, E.L., Cockrem, H., Lotz,
S., Wearing, H., Duncan, D., Rabie, A., McLaren, I., Watson,
E., La Ragione, R.M. and Coldham, N.G. (2011) Fecal carriage
and shedding density of CTX-M extended-spectrum-β-lactamase-producing
Escherichia coli in cattle, chickens, and pigs: Implications
for environmental contamination and food production. Appl.
Environ. Microbiol., 77: 3715-3719.
http://dx.doi.org/10.1128/AEM.02831-10
PMid:21478314 PMCid:PMC3127594 |
|
4. Hiroi, M., Harada, T., Kawamori, F., Takahashi, N., Kanda,
T., Sugiyama, K., Masuda, T., Yoshikawa, Y. and Ohashi, N.
(2011) A survey of β-lactamase-producing Escherichia coli in
farm animals and raw retail meat in Shizuoka prefecture,
Japan. Jpn. J. Infect. Dis., 64: 153-155.
PMid:21519132 |
|
5. Yuan, L., Liu, JH., Hu, GZ., Pan, YS., Liu, ZM., Mo, J. and
Wei, YJ. (2009) Molecular characterization of
extended-spectrum β-lactamase-producing Escherichia coli
isolates from chickens in Henan province, China. J. Med.
Microbiol., 58: 1449-1453.
http://dx.doi.org/10.1099/jmm.0.012229-0
PMid:19574412 |
|
6. Ewers, C., Bethe, A., Semmler, T., Guenther, S. and Wieler,
L.H. (2012) Extended-spectrum b-lactamase-producing and AmpC-producing
Escherichia coli from livestock and companion animals, and
their putative impact on public health: A global perspective.
Clin. Microbiol. Infect., 18: 646-655.
http://dx.doi.org/10.1111/j.1469-0691.2012.03850.x
PMid:22519858 |
|
7. Nóbrega, D.B., Guiduce, M.V.S, Guimarães, F.F., Riboli, D.F.,
Cunha, M.L.R.S, Langoni, H., Pantoja, J.C.F. and Lucheis, S.B.
(2013) Molecular epidemiology and extended-spectrum β-lactamases
production of Klebsiella pneumoniae isolated from three dairy
herds. Pesqui. Vet. Bras., 33(7): 855-859.
http://dx.doi.org/10.1590/S0100-736X2013000700005 |
|
8. Geser, N., Stephan, R. and Hächler, H. (2012) Occurrence
and characteristics of extended spectrum β-lactamase (ESBL)
producing Enterobacteriaceae in food producing animals, minced
meat and raw milk. BMC Vet. Res., 8(21): 1746-6148. |
|
9. Perez, F., Endimiani, A., Hujer, K.M. and Bonomo, R.A.
(2007) The continuing challenge of ESBLs. Curr. Opin.
Pharmacol., 7(5): 459-469.
http://dx.doi.org/10.1016/j.coph.2007.08.003
PMid:17875405 PMCid:PMC2235939 |
|
10. Hartmann, A., Locatelli, A., Amoureux, L., Depret, G.,
Jolivet, C., Gueneau, E. and Neuwirth, C. (2012) Occurrence of
CTX-M producing Escherichia coli in soils, cattle, and farm
environment in France (Burgundy region). Front. Microbiol., 3:
83.
http://dx.doi.org/10.3389/fmicb.2012.00083
PMid:22408639 PMCid:PMC3297819 |
|
11. Willis, C. (2000) Antibiotics in the food chain: Their
impact on the consumer. Rev. Med. Microbiol., 11: 153-160.
http://dx.doi.org/10.1097/00013542-200011030-00005 |
|
12. Aarestrup, F.M. (2006) Antimicrobial Resistance in
Bacteria of Animal Origin. ASM Press, Washington, DC, USA. |
|
13. dos Santos, L., Moura, R.A., Ramires, P.A., Pestana de
Castro, A. and Lincopan, N. (2013) Current status of
extended-spectrum β-lactamase (ESBL)-producing
Enterobacteriaceae in animals. In: Méndez-Vilas, A., editor.
Microbial Pathogens and Strategies for Combating Them:
Science, Technology and Education. Formatex Research Center,
Badajoz. |
|
14. Quinn, P.J., Carter, M.E., Markey, B. and Carter, G.R.
(1994) Clinical Veterinary Microbiology. Wolfe Publishing,
Grafos, S. A. Arte Sobre Papel, Spain. |
|
15. CLSI. (2010) Performance Standards for Antimicrobial
Susceptibility Testing, Twentieth Informational Supplement,
CLSI Document M100-S20. Clinical and Laboratory Standards
Institute, Wayne, PA. |
|
16. Sambrook, J. and Russel, D.W. (2001) Plasmid and their
usefulness in molecular cloning. Molecular Cloning A
Laboratory Manual. 3rd ed. Cold Spring Harbour Laboratory
Press, New York. p1.32. |
|
17. Nazik, H., Öngen, B., and Kuvat, N. (2008) Investigation
of plasmid-mediated quinolone resistance among isolates
obtained in a Turkish intensive care unit. Jpn. J. Infect.
Dis., 61(4): 310-312.
PMid:18653977 |
|
18. Silhavy, T.J., Berman, M.L. and Enquist, L.W. (1984)
Experiments with Gene Fusions. Cold Spring Harbor Laboratory
Press. Cold Spring Harbor, NY. |
|
19. Schmitt, J., Jacobs, E. and Schmidt, H. (2007) Molecular
characterization of extended-spectrum β-lactamases in
Enterobacteriaceae from patients of two hospitals in Saxony,
Germany. J. Med. Microbiol., 56: 241-249.
http://dx.doi.org/10.1099/jmm.0.46670-0
PMid:17244807 |
|
20. Sun, Y., Zeng, Z., Chen, S., Ma, J., He, L., Liu, Y.,
Deng, Y., Lei, T., Zhao, J., and Liu, J.H. (2010) High
prevalence of blaCTX-M extended spectrum β-lactamase genes in
Escherichia coli isolates from pets and emergence of CTX-M-64
in china. Clin. Microbiol. Infect., 16(9): 1475-1481.
http://dx.doi.org/10.1111/j.1469-0691.2010.03127.x
PMid:21681998 |
|
21. Gniadkowski, M. (2001) Evolution and epidemiology of
extended spectrum ß-lactamases (ESBLs) and ESBL-producing
microorganisms. Clin. Microbiol. Infect., 7(11): 597-608.
http://dx.doi.org/10.1046/j.1198-743x.2001.00330.x
PMid:11737084 |
|
22. Weill, F.X., Demartin, M., Lae¨titia Fabre, L. and Grimont
Patrick, A.D. (2004) Extended-Spectrum-β-lactamase
(TEM-52)-producing strains of Salmonella enterica of various
serotypes isolated in France. J. Clin. Microbiol., 42(7):
3359-3362.
http://dx.doi.org/10.1128/JCM.42.7.3359-3362.2004
PMid:15243117 PMCid:PMC446253 |
|
23. Meunier, D., Jouy, E., Lazizzera, C., Kobisch, M. and
Madec, J.Y. (2006) CTX-M-1- and CTX-M-15-type β-lactamases in
clinical Escherichia coli isolates recovered from
food-producing animals in France. Int. J. Antimicrob. Agents.,
28: 402-407.
http://dx.doi.org/10.1016/j.ijantimicag.2006.08.016
PMid:17027237 |
|
24. Carattoli, A. (2008) Animal reservoirs for extended
spectrum β-lactamase producers. Clin. Microbiol. Infect., 14:
117-123.
http://dx.doi.org/10.1111/j.1469-0691.2007.01851.x
PMid:18154535 |
|
25. Kiratisin, P., Apisarnthanarak, A., Laesripa, C. and
Saifon, P. (2008) Molecular characterization and epidemiology
of extended-spectrum-β-lactamase-producing Escherichia coli
and Klebsiella pneumoniae isolates causing health
care-associated infection in Thailand, where the CTX-M family
is endemic. Antimicrob. Agents Chemother., 52(8): 2818-2824.
http://dx.doi.org/10.1128/AAC.00171-08
PMid:18505851 PMCid:PMC2493136 |
|
26. Paterson, D.L. and Bonomo, R.A. (2005) Extended-spectrum
ß-lactamases: A clinical update. Clin. Microbiol. Rev., 18:
657-686.
http://dx.doi.org/10.1128/CMR.18.4.657-686.2005
PMid:16223952 PMCid:PMC1265908 |
|
27. Tamang, M.D., Nam, H.M., Gurung, M., Kim, S.R., Jang, G.C.,
Jung, S.C., Park, Y.H. and Lim, S.K. (2013) Molecular
characterization of CTX-M β-lactamase and associated addiction
systems in Escherichia coli circulating among cattle, farm
workers, and the farm environment. Appl. Environ. Microbiol.,
79(13): 3898-3905.
http://dx.doi.org/10.1128/AEM.00522-13
PMid:23584784 PMCid:PMC3697548 |
|
28. Alexandra, O.K., Tabitha, A.H., Dieter, M.S. and Shelley,
C.R. (2010) First detection of CTX-M and SHV extended-spectrum
β-lactamases in Escherichia coli urinary tract isolates from
dogs and cats in the United States. Antimicrob. Agents
Chemother., 54(8): 3489-3492.
http://dx.doi.org/10.1128/AAC.01701-09
PMid:20479196 PMCid:PMC2916344 |
|
29. Barguigua, A., El Otmani, F., Talmi, M., Bourjilat, F.,
Haouzane, F., Zerouali, K. and Timinouni, M. (2011)
Characterization of ESBL-producing Escherichia coli and
Klebsiella pneumoniae isolates from community in Morocco. J.
Med. Microbiol., 60: 1344-52.
http://dx.doi.org/10.1099/jmm.0.032482-0
PMid:21546559 |
|
30. Barlow, M., Reik, R.A., Jacobs, S.D., Medina, M. & Meyer,
M.P. (2008) High rate of mobilization for blaCTX-M. Emerg.
Infect. Dis., 14: 423-428.
http://dx.doi.org/10.3201/eid1403.070405
PMid:18325257 PMCid:PMC2570810 |
|
31. Muzaheed, Doi Y, Adams-Haduch, J.M., Shivannavar, C.T.,
Paterson, D.L. and Gaddad, S.M. (2009) Faecal carriage of
CTX-M-15 producing Klebsiella pneumoniae in patients with
acute gastroenteritis. Indian J. Med. Res., 129(5): 599-602. |
|
32. Denholm, J.T., Huysmans, M. and Spelman, D. (2009)
Community acquisition of ESBL-producing Escherichia coli: A
growing concern. Med. J. Aust., 190(1): 45-46.
PMid:19120010 |
|
33. Randall, L.P., Clouting, C., Horton, R.A., Coldham, N.G.,
Wu, G., Clifton-Hadley, F.A., Davies, R. H. & Teale, C.J.
(2010) Prevalence of Escherichia coli carrying
extended-spectrum beta-lactamases (CTX-M and TEM-52) from
broiler chickens and turkeys in Great Britain between 2006 and
2009. J. Antimicrob. Chemother., 66(1): 86-95.
http://dx.doi.org/10.1093/jac/dkq396
PMid:21098542 |
|
34. DeFlaun, M.F. & Levy, S.B. (1989) In: Levy, S.D. and
Miller, R.V., editors. Gene Transfer in the Environment,
McGraw-Hill Publishing Company, New York. p1-32. |
|
35. Shoemaker, N.B., Wang, G.R. and Salyers, A.A. (1992)
Evidence for natural transfer of a tetracycline resistance
gene between bacteria from the human colon and bacteria from
the bovine lumen. Appl. Environ. Microbiol., 58(4): 1313-1320.
PMid:1599250 PMCid:PMC195592 |
|
36. Jenks, P.J., Hu, Y.M., Danel, F., Mehtar, S. and
Livermore, D.M. (1995) Plasmid mediated production of class I
(AmpC) β-lactamase by two Klebsiella pneumoniae. J. Antimicrob.
Chemother., 35(1): 235-236.
http://dx.doi.org/10.1093/jac/35.1.235
PMid:7768779 |
|
37. Nuesch-Inderbinen, M., Hachler, H. & Kayser, F.H. (1996)
Detection of genes coding for extended-spectrum SHV beta-lactamases
in clinical isolates by a molecular genetic method, and
comparison with the E test. Eur. J. Clin. Microbiol. Infect.
Dis., 15(5): 398-402.
http://dx.doi.org/10.1007/BF01690097
PMid:8793399 |
|
38. Franiczek, R., Dolna, I., Krzyzanowska, B., Szufnarowski,
K. and Krochmal, B.K. (2007) Conjugative transfer of multi
resistance plasmids from ESBL-positive Escherichia coli and
Klebsiella spp. clinical isolates to Escherichia coli strain
K12 C600. Adv. Clin. Exp. Med., 16(2): 239-247. |
|
39. Yuan, M., Hall, L.M.C., Savelkoul, P.H.M.,
Vandenbroucke-Grauls, C.M.J.E. and Livermore, D.M. (2000)
SHV-13, a novel extended-spectrum β-lactamase, in Klebsiella
pneumoniae isolates from patients in an intensive care unit in
Amsterdam. Antimicrob. Agents Chemother., 44(4): 1081-1084.
http://dx.doi.org/10.1128/AAC.44.4.1081-1084.2000
PMid:10722518 PMCid:PMC89819 |
|
40. Tamang, M.D., Nam, H.M., Kim, S.R., Chae, M.H., Jang, G.C.,
Jung, S.C. and Lim, S.K. (2013) Prevalence and molecular
characterization of CTX-M b-lactamase - producing Escherichia
coli isolated from healthy swine and cattle. Foodborne Pathog.
Dis., 10(1): 13-20.
http://dx.doi.org/10.1089/fpd.2012.1245
PMid:23210923 |
|
41. Rotimi, V.O., Jamal, W., Pal, T., Sovenned, A. and Albert,
M.J. (2008) Emergence of CTX-M-15 type extended-spectrum β-lactamase-producing
Salmonella spp. in Kuwait and the United Arab emirates. J.
Med. Microbiol., 57: 881-886.
http://dx.doi.org/10.1099/jmm.0.47509-0
PMid:18566147 |
|
42. Cloeckaert, A., Praud, K., Lefevre, M., Doublet, B.,
Pardos, M., Granier, S.A., Brisabois, A., Weill, F.X. (2010)
IncI1 plasmid carrying extended-spectrum-β-lactamase gene
blaCTX-M-1 in Salmonella enterica isolates from poultry and
humans in France, 2003 to 2008. Antimicrob. Agents Chemother.,
54(10): 4484-4486.
http://dx.doi.org/10.1128/AAC.00460-10
PMid:20643895 PMCid:PMC2944622 |
|
43. Girlich, D., Poirel, L., Carattoli, A., Kempf, I.,
Lartigue, M.F., Bertini, A. and Nordmann, P. (2007)
Extended-spectrum β-lactamase CTX-M-1 in Escherichia coli
isolates from healthy poultry in France. Appl. Environ.
Microbiol., 73(14): 4681-4685.
http://dx.doi.org/10.1128/AEM.02491-06
PMid:17513592 PMCid:PMC1932829 |
|