Indian Journal of Animal Research

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Detection and Characterization of b-lactamases and Biofilm-producing Escherichia coli and Klebsiella pneumoniae from Ducks and Duck Environments in West Bengal

Tousif Mondal1, Kunal Batabyal1,*, Samir Dey1, Siddhartha Narayan Joardar1, Indranil Samanta1, Devi Prasad Isore1, Soumen Samanta1, Aditya Paul1
1Department of Veterinary Microbiology, Faculty of Veterinary and Animal Sciences, West Bengal University of Animal and Fishery Sciences, Kolkata-700 037, West Bengal, India.

ABSTRACT

Background: Escherichia coli and Klebsiella pneumoniae are two important commensals with pathogenic potentiality in animals and birds, causing intestinal and extra-intestinal infections. These are somewhat zoonotic too via different routes. So, the present study was undertaken to investigate the prevalence of these two bacteria from cloaca and environment of ducks from different districts of West Bengal, followed by detailed characterization and antibiogram.

Methods: Around 197 duck and environmental samples were collected from different districts of West Bengal. E. coli and K. pneumoniae were isolated from collected samples as per standard methods followed by serotyping of the E. coli isolates. The detection of ESBL/ACBL producing isolates was done both phenotypically and genotypically by detecting the presence of antibiotic-resistant genes. Virulence property and biofilm-producing ability of these isolates were also studied. Antibiogram of the ESBL and biofilm positive isolates were done using common 12 antibiotics by disc diffusion method.   

Result: A total of 134(68.02%) Escherichia coli and 33(16.75%) Klebsiella pneumoniae isolates were recovered and confirmed by PCR. The prevalence of E. coli and K. pneumoniae in cloacal swabs were less in comparison to the environmental samples (72.09% and 20.93%). Approx. 79.85% E. coli and 72.73% K. pneumoniae isolates were found to be the ESBL/ACBL producers in vitro. E. coli and K. pneumoniae isolates possessed all major antibiotic-resistant genes with the blaAmpC (64.18% & 48.48%) being the most prevalent one. Twenty three (17.16%) E. coli isolates were found positive for the virulence genes, of which stx1 (39.13%) was the most common one as detected by multiplex PCR. No virulence gene was found in K. pneumoniae isolates. Ninety one (67.91%) E. coli and 26(78.79%) K. pneumoniae isolates possessed the biofilm-producing genes. All the ESBL and biofilms producing E. coli and K. pneumoniae isolates showed 100% - 95.24% resistance to ampicillin. A high percentage of resistances were also seen against cefotaxime, ticarcillin/ clavulanic acid, ertapenem, ceftazidime, norfloxacin and ciprofloxacin, which may be due to several reasons. Maximum overall sensitivity was detected against chloramphenicol, co-trimoxazole and gentamicin.

INTRODUCTION

Rearing ducks is a source of income to the poor marginal farmers in India. Ducks grow faster, need less attention, simple housing and are resistant to common diseases (Rajput et al., 2014). The agricultural economy gets boosted up by the eggs and meat production in Indian scenario.

Ducks may get affected by a few pathogens like Escherichia coli, Salmonella spp., Klebsiella pneumoniae, Pasteurella multocida, Reimerella anatipestifer and Streptococcus spp., etc. Among these, E. coli and K. pneumoniae have virulence properties, biofilm production and antimicrobial resistance properties, which are a matter of concern. These can infect humans too via contaminated water and food. These gram-negative bacteria can produce β-lactamases (Wickens and Wade, 2005) which creates antimicrobial resistance in them. Most of them are biofilm producers too (Melo et al., 2012). Both can cause a wide variety of diseases causing up to 20-30% of mortality (Khelfa and Morsy, 2015). In this background, samples were collected from ducks and duck environments from different districts of West Bengal, to detect the prevalence of antibiotic-resistant and biofilm-producing E. coli and K. pneumoniae isolates to insight into the depth of the problem.

MATERIALS AND METHODS

Sample background
 
A total of 197 samples (154 cloacal swabs and 43 environmental samples [soil 19, water collected from duck environment/sheds 13, duck feed 11]) were collected aseptically with sterilized cotton swabs (HiMedia, India) from ducks and their environments during the year 2020-21. The swab samples were transported under ice cover to the Department of Veterinary Microbiology laboratory, F/VAS, WBUAFS, Kolkata via the shortest route.
 
Isolation and characterization of E. coli and Klebsiella pneumoniae isolates
 
The enriched samples were streaked on sterilized MacConkey’s agar plates (HiMedia, India) and overnight incubated at 37°C for the isolation of E. coli. The rose-pink colonies were selected and sub-cultured and incubated on EMB agar plates (HiMedia, India) for detection of E. coli isolates with metallic sheen’. All isolates were preserved in nutrient agar slants for further study.

The Klebsiella selective agar (HiMedia, India) plates were used for Klebsiella pneumoniae isolation. The characteristic magenta-coloured colonies were selected and subsequently preserved on nutrient agar (HiMedia, India) slants. Morphological and biochemical characterizations were performed as per Quinn et al., (1994) and Edward and Ewing (1972).
 
Molecular characterization of E. coli and Klebsiella pneumoniae isolates
 
The tentatively confirmed E. coli and Klebsiella spp. isolates were processed for molecular confirmation by PCR as per the methods described by Wang et al., (1996) and Brisse and Verhoef (2001) with some modifications. Then the positive Klebsiella spp. isolates were tested for species-specific PCR for the detection of Klebsiella pneumoniae (Liu et al., 2008).
 
Serogrouping of E. coli isolates
 
The positive E. coli samples from ducks were sent to National Salmonella and Escherichia Centre, Central Research Institute, Kasauli, Himachal Pradesh, India for serotyping.
 
Phenotypic detection of ESBL/ACBL production in E. coli and K. pneumoniae isolates
 
Antibiotic discs containing cefotaxime (30 µg, Hi-Media) and ceftazidime (30 µg, Hi-Media) with and without clavulanate (10 µg, Hi-Media) were used in double-disc diffusion assay (DDSA) for phenotypic confirmation of the presence of ESBLs in all E. coli and Klebsiella pneumoniae isolates. A difference of ³ 5 mm between the zone of inhibition in the presence and absence of clavulanate was considered for phenotypic confirmation of ESBL production (CLSI, 2012). All the E. coli and Klebsiellae spp. isolates were subjected to cefoxitin-cloxacillin double disc synergy (CC-DDS) test for phenotypic confirmation of AmpC β-lactamase production (Tan et al., 2009).

Detection of ESBL and ACBL genes in E. coli and K. pneumoniae isolates
 
All the positive E. coli and Klebsiella pneumoniae isolates including negative control were subjected to PCR for detection of major antibiotic-resistant genes such as blaTEM, blaSHV, blaCTX-M and blaAmpC (Bert et al., 2002; Colom et al., 2003; Weill et al., 2004 and Féria et al., 2002).
 
Detection of Virulence genes in E. coli and K. pneumoniae isolates
 
All positive E. coli isolates were further subjected to multiplex PCR for detection of the Shiga-toxin gene (stx1, stx2) and eaeA, hlyA genes as described by Paton and Paton (1998) with some modifications. Likewise, in K. pneumoniae isolates, PCR detection of the rmpA gene was done (Nahavandinejad and Asadpour, 2017).
 
Molecular detection of biofilm-producing genes among E. coli and K. pneumoniae isolates
 
Detection of biofilm genes like csgA, rpoS, rcsA and sdiA was performed in isolated positive E. coli and K. pneumoniae isolates by PCR (Silva et al., 2013; Adamus-bialek et al., 2015).
 
Antibiotic sensitivity assay
 
All the ESBL and biofilm-producing E. coli and K. pneumoniae isolates were tested for their sensitivity and resistance pattern to 12 different antibiotics by the disc diffusion method (CLSI, 2012). The antibiotics used were ampicillin (10 µg), chloramphenicol (30 µg), co-trimoxazole (25 µg), tetracycline (30 µg), gentamicin (10 µg), amikacin (30 µg), norfloxacin (5 µg), ciprofloxacin (5 µg), cefotaxime (30 µg), ceftazidime (30 µg), ticarcillin/clavulanic acid (30/10 µg) and ertapenem (30 µg).

RESULTS AND DISCUSSION

Out of 197 samples, a total of 134(68.02%) Escherichia coli and 33(16.75%) Klebsiella pneumoniae were detected from the cloacal and environmental samples of the duck. The study showed a higher prevalence of E. coli (72.09%) and Klebsiella pneumoniae (20.93%) in environmental samples (Nnachi et al., 2015). In Nigeria, a similar investigation by Adzitey et al., (2012) revealed 70.83% E. coli isolates from soil, confirming the present findings. Bariha et al., (2019) from India, reported 55% positivity of E. coli from different duck samples from ducks. Again Banerjee et al., (2019) found 53.96% E. coli and 14.80% K. pneumoniae from faecal samples of ducks in West Bengal, which were lower than the current findings. Both were gram-negative bacilli and typical in biochemical characterization (Quinn et al., 1994).

All 134 nos. tentatively positive E. coli isolates were having the 16S rRNA gene (585 bp) specific for E. coli (Fig 1). Around 33 isolates were confirmed to be Klebsiella pneumoniae with 130 bp amplified product in PCR (Fig 2). A total of 12 different serogroups were found such as O98, O157, O135, O120, O63, O26, O121, O101, O8, O118, O119 and O22 among which, O120 was the most prevalent one, in serogrouping of E. coli isolates (Banerjee et al., 2019; Wang et al., 2010).

Fig 1: Confirmation of Escherichia coli strains by detection of 16S rRNA gene (585 bp). [L1: 100 bp DNA Ladder, L2: Positive control, L3-L7: Test samples, L8: Negative control].



Fig 2: Confirmation of Klebsiella pneumoniae strains with the detection of the specific gene (130 bp). [L1: 50 bp DNA Ladder, L2: Positive control, L3-L6: Test samples, L7: Negative control].



Out of 134, 107 (79.85%) Escherichia coli isolates (Fig 3) and out of 33, 24 (72.73%) Klebsiella pneumoniae isolates (Fig 4) were detected as phenotypical ESBL/ACBL producers based on double-disc synergy assays. During molecular detection of the resistance genes, a total of 36(26.86%) E. coli and 6(18.18%) K. pneumoniae isolates were found to possess the blaCTX-M gene (540bp) with other genes (blaTEM and blaSHV) too (Table 1). The presence of the blaAmpC gene (634 bp) was quite high in both bacteria. Nalband et al., (2020), Ma et al., (2012) also reported much higher prevalence of ESBL genes in E. coli which is almost similar to the present study. The findings of Banerjee et al., (2019), Raza et al., (2017) also match this report and thus stand confirmed.

Fig 3: Phenotypic assay showing ESBL and ACBL production by Escherichia coli isolates.



Fig 4: Phenotypic assay showing ESBL and ACBL production by K. pneumoniae isolates.



Table 1: Distribution of the ESBLs and ACBL genes in different isolates.



A total of 23 (17.16%) Escherichia coli isolates were found to be positive for different virulence genes viz. stx1 (180bp), stx2 (255bp), eaeA (384bp) and hlyA (534bp) in the multiplex PCR assay (Table 2, Fig 5). Majumder et al., (2017) and Banerjee and Acharyya (2020) reported approx. 20-24% STEC producing E. coli from cloacal samples of duck which was higher than the present findings.

Table 2: Distribution of virulence genes in Escherichia coli isolates.



Fig 5: mPCR showing different STEC genes in E. coli isolates. [L1: 100 bp Ladder, L2-L6: Test samples, L7: Positive control, L8: Negative control].



No Klebsiella pneumoniae isolate was found positive for the rmpA gene (535bp) in this study. Yang et al., (2019) reported a very less (10.6%) prevalence of the rmpA gene in human origin Klebsiella pneumoniae. Animal origin Klebsiella spp. may possess this gene (Younis et al., 2016) but the present variation might be due to variation in geographical variances.

Around 67.91% Escherichia coli and 78.79% Klebsiella pneumoniae isolates were found to possess at least one of these biofilm-producing genes viz. rpoS (120 bp), csgA (178 bp), sdiA (239 bp) and rcsA (306 bp) (Table 3). Approx. 27 E. coli and 13 K. pneumoniae isolates were found to possess more than one biofilm-producing gene in this study which was also supported by Bakhtiari and Javadmakoei (2017) and Banerjee and Acharyya (2020).

Table 3: Distribution of the biofilm genes in E. coli and K. pneumoniae isolates.



This study showed that 30.43% ESBL-E. coli and 47.82% biofilm-producing E. coli to possess virulence genes, but 56 ESBL-E. coli were positive for biofilm production too. Again only 02 isolates were positive for the ESBL, Biofilm producing and virulence genes as revealed in this study. This reveals a significant relationship were also reported by Jegadeesh Kumar et al., (2016) and Fattahi et al., (2015), which confirms these present findings too.

All the ESBL and biofilm-producing E. coli isolates were resistant to ampicillin and approx. 61-86% resistant to norfloxacin, ertapenem, ciprofloxacin, tetracycline and ceftazidime respectively (Table 4). Na et al., (2019) also reported resistance to tetracycline (59.3%) and other drugs of E. coli in their study.

​

Table 4: Antibiogram of ESBL and biofilm-producing E. coli isolates (n=56).



A total of 95.24% of all ESBL and biofilm-producing K. pneumoniae isolates (n=21) were resistant to ampicillin followed by 85.71%, 85.71%, 80.95%, 76.19%, 57.14% and 52.38% resistant to cefotaxime, ticarcillin/ clavulanic acid, ertapenem, ceftazidime, norfloxacin and ciprofloxacin respectively. Sensitivity was detected against chloramphenicol, co-trimoxazole and gentamicin (@61-92%) [Table 5]. Almost similar reports were shown by Nnachi et al., (2015) and Kumar et al., (2022), thus the current result stands confirmed.

​

Table 5: Antibiogram of ESBL and biofilm-producing Klebsiella pneumoniae isolates (n=21).

CONCLUSION

The prevalence of Escherichia coli and Klebsiella pneumoniae was quite significant in duck samples and environmental samples. Twelve different E. coli serogroups were found in this study and O120 was the most prevalent one. The frequency of the blaAmpC gene was the highest among all the ESBL/ACBL producing E. coli and K. pneumoniae isolates. Approx. 65% and 18% of all the E. coli isolates were positive for biofilm production and the presence of virulence genes. Most of the ESBL and biofilms producing Escherichia coli and Klebsiella pneumoniae isolates showed resistance towards ampicillin, cefotaxime, ticarcillin/clavulanic acid, ertapenem, ceftazidime, norfloxacin and ciprofloxacin in antibiotic sensitivity assay.

ACKNOWLEDGEMENT

The authors thank the University Authorities and the Faculties of the Department of Veterinary Microbiology, West Bengal University of Animal and Fishery Sciences, West Bengal for providing the necessary funds, research facilities and support for this study. They are also thankful to the farm owners and local Veterinarians for their technical and field support. Financial support from the Department of Science and Technology and Biotechnology, Govt. of West Bengal sponsored project on duck health management (ST/P/S&T/17G-2/2018) is duly acknowledged.

Conflict of interest

None

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