Indian Journal of Animal Research

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Detection of Antimicrobial Resistance Genes from Shiga Toxin Producing Escherichia coli by Multiplex PCR

 

Ramya Putturu1,*, Manyam Shashi kumar1, Angalakudithi Jagdeeshbabu1, Sujatha singh1, Eevuri Tirupathi Reddy1, Alla Gopala Reddy1
1Department of Veterinary Public Health and Epidemiology, Sri Venkateswara Veterinary University, Tirupathi-517 502, Andhra Pradesh, India.

ABSTRACT

Background: Shiga toxin-producing Escherichia coli (STEC) strains are considered to be most common food-borne enteric zoonotic pathogen, causing various disease conditions in both animals and humans and are highly pathogenic to human in low infectious doses. Resistance against antibiotics by STEC is also a big concern now a days. Hence in view of the public health significance of STEC, present work was planned to know the combination of phenotypic and genotypic resistance patterns against certain most commonly used antibiotics by using disk diffusion method and multiplex PCR respectively.

Methods: A total of 426 PCR confirmed STEC isolates isolated from pooled samples (animal faecal(179), farm water(122) and human faecal samples (125) of different livestock farms in and around Proddatur andhra Pradesh, were subjected to antibiotic sensitivity test by using disc diffusion method. The isolates that showed resistance for tetracycline, streptomycin, sulphonamides and ampicillin were selected and subjected to multiplex PCR for the detection of resistance genes.

Result: Disk diffusion assay revealed highest phenotypic resistance for STEC isolates against Cepahlothin (100%), followed by Ampicillin (99.06%), Tetracycline (97.2%), Streptomycin (94.3%), Sulphonamides (90.8%) and Trimethoprim (84.5%). Pooled samples also revealed the presence of antimicrobial resistance genes like tetA(59.2%), tetB(43.5%), tetC (9.2%), strA (39.3%), strB(54.1%), sul1 (40.8%), sul2 (58.7%), sul3 (3.8%) and blaTEM(83.4%). These findings indicate the highest prevalence of antimicrobial resistance among the STEC isolates, which alarms indiscriminate use of antibiotics both for therapeutic purpose and as growth promoters. Strict hygienic, sanitation and HACCP programmes should be applied to counter STEC prevalence.
 

INTRODUCTION

Escherichia coli is one of the main inhabitants of the intestinal tract of most mammalian species, including humans. Hence recovery of Escherichia coli from livestock products and environmental samples like water is used as reliable indicator of faecal contamination and indicates a possible presence of enteropathogenic and/or toxigenic microorganisms, which constitute a public health hazard. Shiga toxin producing Escherichia coli (STEC) forms major food borne pathogen that produces shiga 1 and shiga 2 toxins that affects human health (Koutsoumanis et al., 2020).
       
Most pathogenic E. coli are transmitted by fecal-oral route from food materials, water, animals and environment. Humans may also acquire STEC infections primarily from consumption of undercooked beef, raw milk, meat and dairy products, vegetables, unpasteurized fruit juices and water contaminated with faeces of animal (Molina et al., 2003). These STEC isolates, specially those with stx2, cause a variety of human illnesses ranging from diarrhoea to hemorrhagic colitis (HC), thrombotic thrombocytopenia purpurea (TTP) and hemolytic uremic syndrome (HUS) with fatal consequences (Walker et al., 2012).
              
Antibiotic usage is probably the most important factor that promotes the emergence, selection and dissemination of antibiotic resistance in both veterinary and human medicine. The increase in antimicrobial resistance in STEC is an emerging problem worldwide, as this resistant bacteria disseminates resistance to human pathogens. The resistance genetic mechanisms involved in the transfer of resistance from one strain of STEC to other may be by transfer of plasmids or by mobile genetic elements (Schwarz and Dancla, 2001). As much work has not carried on the antibiotic resistance of STEC isolates from animal and human sources of our area, the present work was carried out to study the antibiogram of STEC isolates and the genes responsible for specific antibiotic resistance from faecal samples of animals and humanbeings along with water samples of different farms as a part of PhD research work

MATERIALS AND METHODS

Antibiotic susceptibility testing
 
Out of 838 E. coli isolates isolated from pooled samples, (426-animal faecal, 196-farm water and 216- human faecal samples) 426 isolates (179 animal faecal, 122 farm water and 125 human faecal samples) were confirmed as STEC by multiplex PCR in a previous study conducted at Department of Veterinary Public Health and Epidemiology, College of Veterinary Science, Proddatur, YSR Kadapa District andhrapradesh, India. In the present study, all the confirmed STEC isolates were subjected to antibiotic sensitivity test by using disc diffusion method (Bauer et al., 1966) with Muller Hinton agar, against 10 different antibiotics (Hi MEDIA Laboratories) and the results were documented as sensitive (S), intermediate (I) and resistant (R).
 
Genomic DNA extraction
 
STEC isolates that showed resistance for tetracycline, streptomycin, sulphonamides and ampicillin were tested for the presence of AMR genes by PCR for which template is needed, extracted by Boiling and Snap chilling method (Lee, 2003). The suspensions were boiled, cooled and centrifuged and the supernatant was used as template for multiplex PCR.
 
Detection of antibiotic resistance genes
 
The multiplex PCR protocol was standardized in a volume of 25 ìl of reaction mixture. Thermal cycling was performed using the 96-Well Q-Sat 96 Thermal Cycler® and the PCQB software. Cyclic conditions followed are an initial denaturation at 95°C for 4 min, followed by 35 cycles of denaturation at 95°C for 1 min, annealing at 58°C for tetA, tetB and tetC, 55°C for strA and strB, 68°C for sul1, 66°C for sul2, 51°C for sul3,  55°C for blaTEM for 1 min and elongation at 72°C for 1 min and final elongation at 72°C for 7 min (Boerlin et al., 2005). The primers used for the detection of different genes are listed in the Table 1. The multiplex PCR products were visualized after agarose gel electrophoresis using UV transilluminater.
 

Table 1: Primers used for the detection of resistant genes among STEC isolates.

RESULTS AND DISCUSSION

Antibiotic resistance/sensitivity
 
The present study evaluated prevalence of antimicrobial resistance and molecular profile of STEC isolates from animal, human and environmental origin and it is noteworthy to find resistance for different antibiotics (Table 2) along with the presence of resistance genes for antibiotics like ampicillin, tetracycline, streptomycin and sulphonamides. The results in the present study were similar to the reports of Collelo et al., (2018), Gentle et al., (2020), Parvez-Munoz et al., (2021) and many other researchers. Antimicrobial treatment for STEC infections is controversial (Begum et al., 2018) and it is generally not recommended, but the indirect selection for multiresistant strains could occur due to the antibiotic induced selection pressure on other diseases causing bacteria. In addition, antimicrobials are widely used prophylactically, metaphylactically and as growth promoters in animal husbandry (Cabello and Godfrey, 2016).
 

Table 2: Antibiotic resistance of STEC positive pooled samples (n=426) from three sources by phenotypic methods.


 
Genotypic identification of tetracycline resistance genes
 
Phenotypically tetracycline resistant STEC isolates from different samples were subjected for mPCR to detect tetA (Fig 1), tetB and tetC genes (Table 3). Among 171, 121, 123 tetracycline resistant STEC isolates respectively from pooled animal faecal samples, water samples and human faecal samples, highest prevalence of tetA was noticed ranging from 53.7% to 65%. The prevalence (59.1%) of tetA observed in the present study was almost similar to the prevalence (60%) reported by Rao et al., (2011), higher than the prevalence (50%) observed by Hameed et al., (2017) and lower than the prevalence (65.1%) observed by Meselle et al., (2017). In the present study tetA was dominant gene and similar observations were made by Li et al., (2013), whereas on contrary Tang et al., (2011) reported higher prevalence of tetB (49.8%) than tetA (24.0%) in E. coli isolates from pigs raised under overuse of antimicrobials in China. Bryan et al., (2004) and Srinivasan et al., (2007) reported dominance of tetB and tetC, whereas Velusamy et al., (2007) reported the higher prevalence of tetA and tetC than tetB. Diarra et al., (2009) reported the prevalence of tetB only. Rao et al., (2011) reported lower prevalence (27%) of tetB and slightly higher prevalence (12%) of tetC compared to the present findings. Bok et al., (2015) reported a very low prevalence of tetA, tetB and tetC genes as 25.7%, 2.9% and 2.9%. Velusamy et al., (2007) reported that 79.8% of STEC O157H7 and 91.7% O157H7-isoalates carried one or more antimicrobial resistant genes regardless of whether phenotypically resistant or susceptible.
 

Fig 1: Results of STEC isolates possessing tetA gene.


 

Table 3: Genotypic identification of antibiotic resistance from pooled samples.


 
All most all tetracycline resistant isolates harbored tetA and/or tetB as the tetracycline has been used worldwide in both human and veterinary medicine due to being able to select resistance strains (Maynard et al., 2003). Resistance to tetracycline is encoded by more than 40 genes (tet-genes) and they are divided into 11 classes, with a majority of classes (60%) encoding for membrane-associated efflux proteins. These efflux pumps selectively transport tetracycline from the cytosol to the periplasm, thereby limiting the access of tetracycline to the ribosomes in the cell (Tuckman et al., 2007). Tet (A) is the most common efflux pump type found in commensal and clinical Escherichia coli animal isolates (Zhang et al., 2012). The absence of all the above three genes in any of the phenotypically tetracycline resistant isolates might have carried other genes like tetM (Chopra and Roberts, 2001).
 
Genotypic identification of streptomycin resistance genes
 
Phenotypically streptomycin resistant STEC isolates were subjected for mPCR to detect strA and strB (Fig 2) genes (Table 3). Out of 167, 116, 119 streptomycin resistant STEC isolates respectively from pooled animal faecal samples, farm water samples and human faecal samples, highest prevalence of strB (53.8% to 56.9%) was noticed from all the three types of samples. Very low prevalence of 17% for strB genes among phenotypically streptomycin resistant isolates, suggesting that such resistance might be mediated by other yet undescribed genes. A lower prevalence than the present study for strA (15.6%) and strB (15.6%) was reported by Day et al., (2017).

Fig 2: Results of STEC isolates possessing strB gene.


 
Genotypic identification of sulphonamide resistance genes
 
The sulfonamides resistant Escherichia coli is generally attributed to the presence of sul1, sul2 (Fig 3) and/or sul3 genes (Table 3) (Hammerum et al., 2006). So phenotypically sulphonamide resistant STEC isolates were subjected for mPCR to detect sul1, sul2 and sul3 genes. Out of 161, 112 and 114 sulphonamide resistant STEC isolates respectively from animal faecal, farm water and human faecal samples, most of the isolates have shown the presence of sul2 (57.9% to 60.2%). The results were in consistant with the findings of Trobos et al., (2008) and Li et al., (2013). On contrary, Momtaz et al., (2012) reported higher prevalence of sul1 (47.36%), whereas Katakweba et al., (2014) reported high prevalence of sul3 among buffalo faecal samples compared to other animal samples.  Higher prevalence (59% and 54%) of sul1 than the present study (40.9%) was reported by Guerra et al., (2006) and Meselle et al., (2017) respectively, whereas Li et al., (2013) reported very low prevalence of sul1 (5.5%). Low prevalence (3.7%) of sul3 was observed in the present study, which was slightly higher than the prevalence (2.3%) reported by Li et al., (2013). sul1, sul2 and sul3 plays equal importance for sulphonamides resistance in E. coli strains (Ho et al., 2009; Zhang et al., 2012). This result agrees with the fact that the sul2 gene is part of the 30CS in class 1 integron. The sulphonamide resistance genes may be present in diverse mobile genetic elements (such as integrons) that can be easily disseminated to other bacteria. The use of this antimicrobial in veterinary medicine or food animals may contribute to their maintenance of Escherichia coli strains (Srinivasan et al., 2007).
 

Fig 3: Results of STEC isolates possessing having sul2 gene.


 
Genotypic identification of ampicillin resistance genes
 
Phenotypically ampicillin resistant STEC isolates were subjected for mPCR to detect blaTEM gene. Among 179,118 and 125 Ampicillin resistant STEC isolates respectively from pooled animal faecal samples, farm water samples and human faecal samples, almost all the samples (80.4% to 89.6%) had shown the presence of blaTEM gene (Fig 4) (Table 3). Guerra et al., (2006) reported higher prevalence (94%) of blaTEM in pooled animal faecal samples than the present study, whereas Bok et al., (2015) reported lower prevalence (19.4%) than the present study. The â-lactamase gene TEM-1 (blaTEM-1) is the most prevalent â-lactamase in gram-negative bacteria which is usually located on conjugative plasmids facilitating its spread among different species (Arvand et al., 2015). Some authors reported blaTEM-1 in STEC, not only isolated from food or animals but also from humans (Cergolle-Novella et al., 2011). In contrary to the present study, Day et al., (2017) and Elsayed et al., (2021) reported a very low prevalence of (2% and 5% respectively) blaTEM gene among the STEC isolates.

Fig 4: Results of STEC isolates possessing blaTEM gene.


 

CONCLUSION

In summary antibiotic resistance towards most commonly used antibiotics was developed by most of the STEC isolates isolated from animal, human and environmental samples of our region, which alarms indiscriminate use of antibiotics both for therapeutic purpose and as growth promoters. This study also concluded with similar pattern of distribution of resistance genes among the isolates of different origin which indicates the interrelation between the components of epidemiological triad. Although antimicrobials are not usually used in the treatment of STEC infections, the presence of MDR in isolates collected from farm and other sources represents a risk for animal and human health as they can spread their resistance genes to other bacteria. Therefore, some measures must be taken to ensure a reasonable use of antimicrobials in the animal husbandry and strict hygienic, sanitation and HACCP programmes should be applied to counter STEC prevalence.

ACKNOWLEDGEMENT

The authors are grateful to the PVNRTVU, Hyderabad and SVVU, Tirupathi for providing facilities to carry out the work.

CONFLICT OF INTEREST

None

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