Indian Journal of Animal Sciences 93 (6): 566–571, June 2023/Article

https://doi.org/10.56093/ijans.v93i6.126892

Prevalence and characterisation of antimicrobial resistance pattern of ESBL-

producing Escherichia coli isolated from poultry in Banaskantha district, India
MITUL A PATEL1*, APARNA PANDEY1, SANDIP S PATEL2, ARUN C PATEL2, SUSHIL K MOHAPATRA2,
HARSHAD C CHAUHAN2, KISHAN K SHARMA2, BHAVESH I PRAJAPATI2 and
BHARATSINGH S CHANDEL2

Sardarkrushinagar Dantiwada Agricultural University, Sardarkrushinagar, Banaskantha, Gujarat 385 505 India

Received: 13 August 2022 ; Accepted: 30 April 2023

ABSTRACT
Resistance to antimicrobial drugs among bacterial pathogens is an emerging problem. Bacterial resistance to beta-
lactam antibiotics has grown significantly. The present study aims at isolation, identification, phenotypic confirmation
of ESBL-producer, and antimicrobial resistance pattern of Escherichia coli isolated from poultry faecal samples. A
total of 120 samples were collected from 30 different poultry farms in Banaskantha district. 108 out of 120 samples
were confirmed as E. coli using microscopic, biochemical tests, followed by species-specific 16S rRNA PCR; among
them, broiler 65 (92.85%) and layer 43 (86%) were confirmed as E. coli. The phenotypic ESBL-production was
detected in 54 (50%) isolates with broiler (29.62%) and layer (20.28%) farms. The antibiotic sensitivity pattern
revealed the highest resistance was identified against Cefpodoxime 100%, followed by Tetracycline 97.22%,
Amoxicillin + Clavulanic acid 95.37%, Nalidixic Acid 94.44%, Enrofloxacin 91.66%, Co-trimaxazole 90.74%,
Ampicillin 78.70% and Amikacin 57.40%. The 95.37% and 77.77% isolates showed susceptibility to Imipenem and
Cefoxitin, respectively. Thus, it may be concluded that in the current study, isolates revealed multidrug resistance
against antimicrobial agents commonly used in veterinary and human practice. This implies that the existing practice
of misuse and improper use of antibiotics in poultry accelerates antimicrobial resistance in poultry.
Keywords: Antibiotics, Antimicrobial resistance, E. coli, India, PCR, Poultry

Antimicrobial resistance is caused by developing the intestine’s natural flora. Some strains of E. coli are a
and disseminating multidrug-resistant bacteria that have frequent cause of intestinal and urinary tract infections
developed new resistance mechanisms and are becoming in animals and humans (Ramos et al. 2020) and are
a growing threat to public health (Racewicz et al. 2022). transmitted via the fecal-oral route. E. coli causes disease
Misuse and overusage of antibiotics in livestock have been in poultry, generally referred to as avian pathogenic E. coli
associated with the emergence and spread of bacterial (APEC). Nowadays, the emergence of extended-spectrum
resistance (Manyi-Loh et al. 2018). In India, the poultry beta-lactamase (ESBL) is increasing globally. ESBL is an
industry is fastest growing in the agriculture sector. India enzyme commonly found in gram-negative bacteria and
is the world’s fourth-largest producer of chicken and eggs inactivates the many antibiotics used to treat bacterial
after China, Brazil, and the US (APEDA). Globally, many infections. ESBL E. coli has resistance to third-generation
poultry farmers often use low doses of antibiotics as growth- cephalosporin and quinolones antibiotics (Kettani et al.
promoting agents and preventive chemotherapy (Van et al. 2021).
2019). It has been estimated that 80% of food-producing Antimicrobial resistance is one of the top ten global
animals and birds received antibiotics throughout the health issues for 2019, and according to the World Health
majority of their lives (Husain et al. 2021). India is among Organization (WHO) India has among the highest bacterial
the top consumers worldwide, accounting for 3% of global infections in the world. Resistance is rapidly increased by
consumption of antibiotics. spreading resistance genes using mobile genetic elements
Escherichia coli is a commensal bacterium found in or horizontal gene transfer mechanisms (Patel et al. 2022).
In the last two decades, AMR in animals has grown by 50%,
Present address: 1Department of Biochemistry, Narsinhbhai compared to several years’ usual approval time for new
Patel Dental College, Sankalchand Patel University, Saduthala- antibiotics (Boeckel et al. 2019). In recent years, several
Kamana-Udalpur Rd, SPCE Campus, Visnagar, Gujarat. studies have identified the prevalence of beta-lactamase
2
Veterinary Science and Animal Husbandry, Sardarkrushinagar
antibiotic resistance in E. coli from poultry (Tansawai et
Dantiwada Agricultural University, Sardarkrushinagar,
Banaskantha, Gujarat. *Corresponding author email:
al. 2019). Therefore, the study aimed to isolate phenotypic
[email protected] confirmation of ESBL-production and antimicrobial

26
June 2023] PREVALENCE OF ESBL ESCHERICHIA COLI IN POULTRY 567

resistance profile of E. coli isolated from poultry farms primer :- 5’CACACGCTGACGCTGACCA 3’, and then
(broiler and layers) in Banaskantha, India. 8.5 µl nuclease free water was added to get a total volume
of 25 µl. The PCR cyclic condition for ECO-1 was initial
MATERIALS AND METHODS
denaturation at 94°C for 5 minutes, followed by 30 cycles
Study area and sample collection: Cloacal swabs of denaturation at 94°C for 30 sec, annealing at 53°C for
(120) were randomly collected from 30 different poultry 1 min, an extension at 72°C for 1 min, and a final extension
farms (four from each farm) in semi-arid climate area of at 72°C for 8 min.
Gujarat. Following aseptic precautions, sterile swab was Phenotypic confirmation of extended spectrum beta-
gently inserted into the cloaca of the chicken and carefully lactamase producing E. coli: The extended-spectrum
swabbed on the mucosal wall several times. Samples beta-lactamase-producing E. coli was determined by the
were packed carefully and transported immediately to a combined disk diffusion method (Zali et al. 2000) using
laboratory at 4°C. The sick and dead chickens (broiler and cefotaxime (CTX-30 μg) alone and cefotaxime/clavulanic
layer) were eliminated from the study. acid (CEC 30/10 μg ) and ceftazidime (CAZ 30 μg)
Isolation and identification of Escherichia coli: Primary alone and ceftazidime/clavulanic acid (CAC 30/10 μg) as
isolation was done by inoculation of the cloacal swab into recommended by CLSI 2018. The production of ESBL was
MacConkey broth for pre-enrichment and incubated at indicated by a difference in the zone of inhibition of ≥5 mm
37°C for 24 h. Then the incubated culture was streaked on between cephalosporin discs and their Cephalosporin +
MacConkey agar and incubated at 37°C for 24 h. Lactose
Clavulanic acid containing discs.
fermenting pink presumptive colonies was purified by
Antimicrobial susceptibility testing: Antimicrobial
streaked on Eosin Methylene Blue (EMB) agar for
sensitivity test of E. coli isolates were performed as per
selective isolation. The plates were incubated at 37°C for
the Kirby-Bauer method (Bauer et al. 1966) and according
24 h, and colonies showing a greenish metallic sheen were
to guidelines provided by the Clinical and Laboratory
considered confirmatory for E. coli.
Standards Institute of the USA (CLSI 2018). A single pure
The microscopic morphology of the isolates was studied
colony obtained from EMB agar was suspended in 2 ml of
by Gram’s staining method, followed by biochemical
tests like Oxidase, catalase, Indole, Methyl red, Voges- sterile normal saline and adjusted its turbidity to the 0.5
Proskauer, and Citrate were employed to confirm E. coli as McFarland standards. Thereafter, sterile cotton swab was
per the methods described by Quinn (2002). dipped into the suspension and rotated several times. The
Genotypic confirmation of E. coli isolates using PCR swab was streaked over the entire surface of the Mueller
method: The DNA was extracted from the presumptively Hinton Agar (MHA) plate three times to ensure equal
confirmed bacterial colonies using the DNeasy Blood distribution of the inoculum. A total of 15 antibiotic discs
and Tissue Kit (Qiagen), following the manufacturer’s with known concentration were placed on MHA agar plate
protocols. E. coli isolates were identified using species- and incubated at 37°C for 24 h. The name and concentration
specific 16S rRNA gene amplification as per the of antibiotic discs were mentioned in Table 1. A zone of
method described by Fratamico et al. (2000). The PCR inhibition was measured, compared and interpreted as
reaction was prepared by adding 12.5 µl master mix, 2 resistance, intermediate of susceptible according to the
µl DNA template, 1 µl of each ECO-1 forward primer size interpretative chart furnished by the CLSI guidelines-
:- 5’GACCTCGGTTTAGTTCACAGA 3’ and reverse VET0819.

Table 1. Antimicrobial resistance pattern of ESBL E. coli

Name of antibiotics Resistance Intermediate Sensitivity
Cefpodoxime (10 mcg) 108 (100%) 0 0
Tetracycline (30 mcg) 105 (97.22%) 0 3 (2.77%)
Amoxicllin +Clavunic acid (20/10 mcg) 103(95.37%) 0 5 (4.62%)
Nalidixic Acid (30 mcg) 102 (94.44%) 2 (1.85%) 4 (3.70 %)
Enrofloxacin (5 mcg) 99 (91.66%) 0 9 (8.33%)
Co-trimaxazole (1.25/23.75 mcg) 98 (90.74%) 1 (0.92%) 9 (8.33%)
Ampicillin (10 mcg) 85 (78.70%) 8 (7.80%) 15 (13.88%)
Amikacin (30 mcg) 62 (57.40%) 5 (4.62%) 41 (37.96%)
Chloramphenocol (30 mcg) 60 (55.55%) 15 (13.88%) 33 (30.55%)
Ceftriaxone (30mcg) 41 (37.96%) 8 (7.40%) 59 (54.62%)
Cefoxitin + coxacillin (30/200 mcg) 36 (33.33 %) 60 (55.55%) 12 (11.11%)
Aztreaxone (30 mcg) 28 (25.92%) 19 (17.59%) 61 (56.48%)
Cefoxitin (30 mcg) 12 (11.11%) 12 (11.11%) 84 (77.77%)
Colistin (10 mcg) 05 (4.62%) 58 (53.70%) 45 (41.66%)
Imipenam (10 mcg) 0 5 (4.62%) 103 (95.37%)

27
 568 PATEL ET AL. [Indian Journal of Animal Sciences 93 (6)

RESULTS AND DISCUSSION layer 22 (20.38%) were positive for extended-spectrum

beta-lactamase-producing E. coli, which is consistent
Isolation, identification and biochemical
with the findings of Hiroi et al. (2012), who revealed 44%
characterization of E. coli: The overall prevalence of E.
ESBL-producing E. coli from a rectal sample from the
coli from poultry fecal samples according to this study was
slaughterhouse. The occurrence of ESBL-production in
108 (90%), with broiler (92.85%) and layers (86%), which
E. coli (25%) and Salmonella (27.5%) was identified in
was similar to a study conducted in Bangladesh (Mandal
West Bengal (Chowdhury et al. 2021), which is slightly
et al. 2022) and in Maharashtra, India (Mahadewaswami
equivalent to the present finding. Kharate et al. (2019)
et al. 2021). In contrast, the present study showed a higher
found 54.54% and 52.04% ESBL prevalence in layers
prevalence in broilers chickens compared to research
and broilers, respectively in Karnataka, India, which was
conducted in West Bengal, India, by Sarkar et al. (2013).
higher than the current study.
Confirmation of E. coli by PCR technique using ECO-1
Antimicrobial sensitivity pattern study: All E. coli (ESBL
primer: Based on the PCR technique, 108 (90%) samples
+ non-ESBL) isolated from poultry fecal matter were found
out of 120 were confirmed to be positive for E. coli. Out of
to be resistant to Cefpodoxime (Fig. 3). This result agreed
selected isolates, 65 (92.85%) from broilers and 43 (86%)
with the findings of broiler chickens in Ghana (Rasmussen
from layers of chickens were confirmed as E. coli. (Fig.1).
et al. 2015). In Indonesia, Indrawati et al. (2021) identified
The sample given a positive result for the 16S rRNA gene
E. coli from poultry, drinking water, and litter and showed
with an amplicon size of 585 bp (Fig. 2) was correlated
89% and 94% resistance against tetracycline and nalidixic
with the finding of Godambe et al. (2017) and Ibrahim
acid, respectively similar to the current study. Alvarez
et al. (2019).
et al. (2022) isolated E. coli from broiler farms in Portugal
Phenotypic confirmation of ESBL-producing E. coli:
and found no resistance to imipenem antibiotics, consistent
Bacteria produce beta-lactamase enzymes, making them
with the current investigation’s findings. In the present
resistant to beta-lactam antibiotics such as penicillin and
study, higher resistance levels were also recorded for
3rd generation cephalosporins. E. coli is the most prevalent
amoxicillin + clavunic, co-trimxazole, and ampicillin
ESBL generator (Andrews et al. 2018). In the current study,
(Table 1); a similar observation was also reported by
a total of 54 (50%) isolates with broiler 32 (29.62%) and
Olowe et al. (2015) from animal fecal samples in Ado
150
No. of positive samples Akiti, Nigeria, (Osei et al. 2021) from water supply used
No. of samples/Percentage of positive samples

Percentage of positive samples

for poultry production in Ghana. None or lower usage of
antibiotics such as imipenem, Aztreaxone, and ceftriaxone
100
in poultry industries due to their not being accessible for
usage or not being used for treatment and growth promoter,
the current study revealed susceptibility to these antibiotics
50
in E. coli isolates. Gundran et al. (2019) observed similar
antibiotic susceptibility trends in the poultry sector in the
Philippines and Egypt (Badr et al. 2022).
0
Higher resistance may develop in an organism because
es

er
r
le

of readily available antimicrobial agents in the Indian

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ECo-1 gene

Fig. 1. Detection of E. coli using PCR method. antibiotics as a growth promoter in chickens by poultry
farmers leads to the development of resistance; this
100
M P N 1 2 3 4 statement is also supported by Aworh et al. (2021) in
Resistance
Nigeria, who reported that developing economies have easy
access to antimicrobials for both human and animal usage.
Intermediate

LeeSusceptible
et al. (2004) reported the MIC range for enrofloxacin,
ciprofloxacin, norfloxacin, and ofloxacin grew significantly
during the same time period because of a parallel rise in
Number of percentage

1500 BP the rate of gyrA mutations. A similar finding also identified

high resistance to enrofloxacin in the current study.
50 In the present study, non-ESBL-producing isolates
500 BP showed resistance against cephalosporin, tetracycline,
penicillin, quinolone, and the sulfonamide class of
antibiotics. While compared to ESBL and non-ESBL
585 BP
isolates, ESBL isolates showed more resistance than non-
100 BP
ESBL isolates. Similar results was recorded in Benin
Fig. 2. PCR amplification of 16S rRNA gene of E. coli. (Anago et al. 2015). Jocoby (2009) reported that AmpC
(Lane M-100 bp plus ladder; Lane P- Positive control; Lane N- beta-lactamase genes mediate resistance to cephalosporin,
0 control; Lane 1,2,3,4- E. coli samples)
Negative cefazolin, and penicillin class of antibiotics. The existence
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To
ECo-1 gene
June 2023] PREVALENCE OF ESBL ESCHERICHIA COLI IN POULTRY 569

100 Resistance
Intermediate
Susceptible
Number of percentage

50

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Fig. 3. Antimicrobial sensitivity pattern of E. coli isolates from poultry.

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