pmc.ncbi.nlm.nih.gov

Mini-Review: Antibiotic-Resistant Escherichia coli from Farm Animal-Associated Sources

Abstract

Escherichia coli is one of the most frequent causes of gastro-intestinal and extra-intestinal diseases in animals and humans. Due to overuse and misuse of antibiotics, recent years have seen a rapidly increasing prevalence of antibiotic-resistant (AR) Escherichia coli globally; particularly, AR E. coli from farm animal-associated sources and its antibiotic resistance genes (ARGs) are becoming a global concern, with clinical negative effects on both human and animal health. The aim of this review was to explore the prevalence trends of AR E. coli from farm animals, waste treatment, and aquatic environments. The disinfection methods of AR E. coli and possible alternatives to antibiotics were also highlighted. The current review highlights that the prevalence of AR E. coli from food animals, products, and animal waste is increasing at an alarming rate, but is reduced at waste treatment plants. Ultraviolet (UV) treatment, surface plasma oxidation, and biochar are commonly used to effectively eliminate AR E. coli. Some probiotics, plant extracts, and antimicrobial peptides (AMPs) are arousing interest as promising alternatives to antibiotics to fight against AR E. coli. The current review suggests that AR E. coli from farm animal-associated sources is prevalent and poses a serious global threat to public health. This review provides an avenue for further research, development, and application of novel strategies to minimize antibiotic resistance in E. coli of farm animal origin.

Keywords: antibiotic resistance, Escherichia coli, farm animals, alternatives, disinfection

1. Introduction

Escherichia coli is found in the environment, food, and the guts of animals and humans. It is an opportunistic pathogen that can cause gastro-intestinal and extra-intestinal diseases, such as diarrhea, enteritis, bacteremia, urinary tract infection, and other infections in animals and humans [1,2,3,4,5]. E. coli is also found in a major portion of feces from animals [6,7]. Due to overuse and misuse of antibiotics, E. coli of animal origin displays resistance against various antibiotics, including tetracyclines, aminoglycosides, β-lactams, fluoroquinolones, third-generation cephalosporins, etc. [8,9,10,11]. It has been demonstrated that more than 90% of E. coli isolated from food animals (including healthy broiler chickens, cattle, and pigs) in Korea during 2010–2020 exhibited high resistance to quinolones and cephalosporins [12]. Meanwhile, antibiotic-resistant (AR) E. coli that carries antibiotic resistance genes (ARGs) is also present in multiple hosts and environmental compartments as a normal inhabitant or a temporary or persistent colonizer, and can be globally transmitted between animals and humans [13]. In some waste treatment plants and aquatic environments, AR E. coli concentrations were up to 10–105 CFU/mL, higher than the requirement for irrigation use of water (10 CFU/100 mL) [14,15,16], posing a serious threat to public health [3,4,17,18,19].

The dissemination of AR E. coli and its ARGs is considered to occur frequently in farm animal-associated conditions [20,21]. Animals and products serve as potential reservoirs and vectors for the spread of AR E. coli. AR E. coli that carries ARGs (such as blaCTX-M, sul1, tetA, tetB, etc.) on livestock farms can transfer into the surrounding environment, such as water bodies, soils, etc. [1,20,22,23]. Moreover, AR E. coli and its ARGs of animal origin can also be transferred to other bacteria through horizontal gene transfer (HGT), which plays a key role in the acquisition, accumulation, and dissemination of ARGs in bacteria [24,25,26,27]. Some ARGs (including sul3, cmLA, aadA1, aadA2, tetR, tetA, and dhrfI) from a commensal E. coli strain isolated from food animals such as broilers and pigs could be transferred to humans [28,29]. Noticeably, multi-drug resistant (MDR) E. coli isolates from livestock are identical to those of human-origin isolates, indicating high transferability of AR E. coli [26]. AR E. coli and its ARGs pose serious risks to animal and human health [5], requiring effective strategies to combat them.

To fight against AR E. coli of animal origin, some traditional and novel strategies, including ultraviolet (UV) treatment, surface plasma oxidation, and biochar, have been reported to effectively kill AR E. coli by inhibiting DNA replication and destroying the cell membrane [30,31,32]. A few ARGs (including tetC, tetW, blaTEM-1, ampC, etc.) of E. coli of animal origin were remarkably removed or reduced after plasma or biochar oxidation treatment, and conjugative transfer of ARGs (such as integron gene-intI1) was dramatically inhibited [31,33]. The advantage of using these methods is that they display high efficiency, simple equipment, and no/low exogenous chemical residues [30,33,34]. It is worth mentioning that recently, some potential alternatives to antibiotics, such as probiotics, plant extracts, antimicrobial peptides (AMPs), etc., are emerging to address the emergence and spread of AR E. coli due to their potent biological functions, with health benefits [35,36,37,38]. Especially for AMPs, a class of effector molecules with less than 100 amino acids, are found in almost all living organisms and display potent antibacterial activity against AR bacteria (ARB) and low risk of the development of drug resistance [39,40]. Hitherto, several AMPs (such as microcin, magainin, cathelicidin, etc.) are regarded as a promising class of antimicrobial agents to overcome AR E. coli [40,41,42,43,44].

In this review, we introduce a brief outline of the current situation of AR E. coli from farm animal-associated sources (including farm animals, sewage/manure treatments, and aquatic environments), as well as strategies in the battle against AR E. coli. The possible routes of transmission of AR E. coli and its ARGs are summarized in Figure 1. By studying current AR E. coli of animal origin, we hope that more people can clearly understand its adverse effects, which may help develop more efficient strategies to fight against bacterial resistance from farm animal-associated sources.

Figure 1.

Figure 1

Multiple pathways involved in the transfer of AR E. coli and its ARGs in animals, humans, and the environment. Antibiotics used in farm animals may lead to AR E. coli, which is present in food products, feces, manure, waste, treatment plants, etc. AR E. coli and its ARGs can be transferred from farm animals to the surrounding environment, other animals, or even humans by multiple routes (including foods, waste, surface water, river, rainwater, drinking systems, etc.).

2. Prevalence of AR E. coli from Farm Animal-Associated Sources

2.1. AR E. coli from Farm Animals

2.1.1. Food Animals and Products

Animals may serve as potential reservoirs and vectors for the dissemination of ARB, including E. coli, which is a growing concern worldwide. Monitoring AR E. coli from food animals and products is vital to determine the emergence of antibiotic resistance and its associated risk to humans [20,45,46,47].

Avian pathogenic E. coli, which can cause avian colibacillosis and is common in Germany, Egypt, Pakistan, etc., displays high levels of resistance to ampicillin, tetracycline, ciprofloxacin, and other antibiotics [48,49,50]. Colistin-resistant E. coli and the mcr-1 gene were found in broilers in Germany [49], posing a threat to human health by potential zoonoses [51]. A high prevalence of AR E. coli (100%), especially against tetracycline, gentamicin, colistin, imipenem, and β-lactams, has been observed in different poultry products and in poultry meat from different types of retailers; the majority of resistant genes were tetA and blaTEM [10]. Aklilu et al. analyzed broilers and retail chickens in food animals in Malaysia and found that 37.5% (27/72) of E. coli was positive for at least one antibiotic-resistant gene [52]. The prevalence was even more severe in Vietnam; colistin-resistant E. coli was found in about half of chicken samples, and most of AR E. coli contained the mcr-1 gene [53]. Abdallah et al. analyzed retail lamb samples from Zagazig, Egypt, and found AR E. coli in nearly one-fifth of the samples [54].

Colistin-resistant E. coli was isolated from 78% (51/65) of raw beef and 53% (24/45) of ready-to-eat beef products in Egypt, with individual transmission in cattle [55]. Ahmad et al. surveyed raw milk samples from farms, milk vendors, and shops in the Peshawar district of Pakistan for MDR E coli. Among 28 isolated E. coli, six isolates were MDR E. coli and all identified blaCTXM resistance genes [56]. Furthermore, in recent years (2016–), AR E. coli was also found in ready-to-eat street foods in small and roadside outlets, which is a significant risk for human health (Table 1) [4,57]. Some 16.9–72.9% of E. coli in ready-to-eat street food (containing chicken) was resistant to cefepime, cefotaxime, imipenem, and meropenem; the most prevalent ARGs included blaTEM (40.68%), blaCTX (32.20%), blaSHV (10.17%), and blaNDM, indicating a potential risk of transmission from food to humans [4]. Meanwhile, AR E. coli was found in fresh seafood such as fish and shellfish sold in a retail market in Mumbai, India [3]. Some 71.58–95% of E. coli isolates were resistant to β-lactams and cephalosporins (including cefotaxime, cefpodoxime, and ceftazidime), with blaCTX-M (62.37%), blaSHV (23.35%), blaTEM (2.6%), blaOXA (7.06%), blaNDM (4.42%), and blaVIM (0.88%), indicating a high risk of transmission of MDR E. coli in seafood consumers and handlers [3]. Shellfish in marine environments were affected by effluents including rivers, domestic effluents, and sewage treatment plants that carry AR E. coli [58].

Table 1.

AR E. coli and its ARGs in food animals and products (2016–2022).

Sources Resistance to Antibiotics ARGs Location References
Eggs Florophenicol NN Slovenia [45]
Turkey ampicillin, ampicillin–sulbactam, cefazolin, and tetracycline uidA America [46]
Broiler chicken Colistin, ampicillin, tetracycline, and chloramphenicol strA, strB, and blaTEM-135 Germany [49]
Fresh seafood in retail markets Cephalosporins cefotaxime, cefpodoxime, ceftazidime, imipenem, cefoxitin, and meropenem blaCTX-M, blaSHV, blaTEM, blaOXA, blaNDM, and blaVIM India [3]
Raw beef Colistin and cefotaxime mcr-1 and
ECTX-M-28 		Egypt [55]
Ready-to-eat beef products Colistin and cefotaxime mcr-1 and
blaTEM-116 		Egypt [55]
Milk Amoxicillin–clavulanic acid, ampicillin, ceftriaxone, kanamycin, streptomycin, trimethoprim sulfamethoxazole, and vancomycin blaCTX-M, blaTEM-1,
blaNDM-1, blaOXA-48,
blaVIM, and blaSHV 		Pakistan [56]
Malaysian broiler chicken Carbapenem and colistin mcr-1, blaTEM-52, blaNDM, blaOXA-48, and blaIMP Malaysia [52]
Vietnam broiler chicken Colistin blaCTX-M, mcr-1, blaTEM, and blaCMY-2 Vietnam [53]
Retail mutton Trimethoprim, sulfamethoxazole, aminoglycosides, quinolones, and nitrofurantoin blaCTX-M, blaTEM, and blaSHV Egypt [54]

Therefore, the use of antibiotics in food animals has resulted in the selection of drug-resistant bacteria across the farm-to-fork continuum. It is essential to improve sanitary conditions and take intersectoral actions coordinated by the different organizations involved.

2.1.2. Animal Waste

Animal waste is a large pool of ARB containing E. coli and its ARGs (Table 2), leading to the dissemination of AR E. coli and its ARGs into the environment, representing an important and dangerous environmental pollutant [59].

Table 2.

AR E. coli and its ARGs in animal waste (2016–2022).

Sources Resistance to Antibiotics ARGs Strategies Location References
Veal calf Tetracycline, ampicillin, sulfonamides,
streptomycin, and trimethoprim		 intI1 and intI2 NN French [60]
South African herbivores Gentamicin, tobramycin, ceftazidime, and aztreonam NN Antibiotics used in human medicine should be avoided in veterinary medicine South Africa [61]
Free-grazing food animals Ampicillin, ceftriaxone, chloramphenicol, gentamicin, streptomycin, sulfonamide, tetracycline, etc. dfrA, orfF, aadA, sul1, and qacEΔ1 NN China [62]
Meat duck deep litter Ceftiofur, enrofloxacin, ofloxacin, and gentamicin NN The deep litter should be treated with appropriate antibiotic resistant bacteria China [8]
Dog Cefazolin and fluoroquinolone blaSHV, blaTEM, blaOXA, and blaCTX-M NN Taiwan, China [2]
Intensively produced poultry Ampicillin, tetracycline, nalidixic acid, trimethoprim-sulfamethoxazole, and chloramphenicol blaCTX-M, sul1, tetA, and tetB NN South Africa [23]
Open pig farm Chlortetracycline, tetracycline, tilmicosin, amoxicillin, and doxycycline NN Legislation to clarify the boundary between antibiotics for human use and antibiotics for veterinary use Thailand [63]
Deer and Pigs Ciprofloxacin and nalidixic acid qnrS and qnrB NN Germany [64]
Cow farm Tetracycline tetA, tetB, and tetM Veterinarian supervisor, administration history for all individuals, and the rearing environment is strictly managed Japan [65]

An investigation of E. coli isolated from the feces of native South African herbivores (including wildebeest, zebra, and giraffe), pets, and farm pigs was performed to analyze dissemination patterns of drug resistance [61]. The results suggested that herbivores native to South Africa may be important carriers in the transmission of AR E. coli [61]. The occurrence of integrons in AR E. coli strains isolated from free-grazing food animals (such as chickens, piglets, and yaks) in China was firstly determined by Rehman et al. [62]. A total of 432 E. coli strains isolated from free-ranging food animals in China were resistant to at least one class of antibiotics, including ampicillin, ceftriaxone, chloramphenicol, gentamicin, streptomycin, sulfonamide, tetracycline, etc. Integrons were detected in 6% of AR E. coli strains, indicating that precautionary measures are invoked to prevent the transfer of AR E. coli [62]. Weiss et al. analyzed a total of 1685 E. coli fecal samples from domestic animals, humans, and wild primates in western Uganda, and found that 499 E. coli isolates were resistant to 11 antibiotics tested [66]. The frequency of resistance was 57.4%, 19.5%, and 16.3% in E. coli isolates from people, domestic animals, and wild primates, respectively. The percentage of AR E. coli decreased with increasing local price of antibiotics. Moreover, 33.2% of resistant isolates with class 1 integrons were widely distributed in E. coli strains from different host species [66]. In Germany, researchers analyzed feces from a variety of animals, including ducks and pigs, and found that quinolone-resistant E. coli was widespread in livestock and food [64]. One survey from 2010 to 2020 showed that more than 90% of E. coli isolated from the feces of healthy broiler chickens, cattle, and pigs in Korea exhibited high resistance to quinolones and cephalosporins [12]. Additionally, AR E. coli, including cefazolin-resistant (43.1%), fluoroquinolone-resistant (22.1%), and β-lactam-resistant ones (9.4%), were found in dog feces, indicating the possible transmission of drug resistance in companion animals [2].

The epidemiology of AR E. coli in intensively produced poultry was investigated in South Africa by McIver et al. [23]. The results showed that 67.3% of E. coli isolates from the poultry industry were resistant to ampicillin (48.1%), tetracycline (27.4%), nalidixic acid (20.3%), trimethoprim–sulfamethoxazole (13.9%), and chloramphenicol (11.7%), which was similar to the antibiotics used in the poultry industry. The most frequently detected ARGs were blaCTX-M (100%), sul1 (80%), tetA (77%), and tetB (71%). It indicated that intensive poultry farming may be a reservoir and a potential vehicle for the transmission of bacterial antibiotic resistance; some prompt measures must be taken to reduce the spread of bacterial resistance from the poultry industry to humans [23]. AR E. coli and Salmonella with resistance to third-generation cephalosporins or quinolones were detected in feces from cattle, goats, pigs, and poultry in Rwanda’s eastern province [11]. Suzuki et al. studied cow feces in animal farms and found that in farms where antibiotics are used carefully, AR E. coli has less impact on the surrounding wildlife and environment [65].

The percentage of AR E. coli in wastewater from adult cattle and veal calf slaughterhouses ranged from 5% to 87.5%; approximately 1,010 strains of MDR E. coli were detected to be released into contaminated rivers every day [60]. One pathogenic E. coli O157:H7 strain was transmitted into the environment by land application [60]. The prevalence of AR E. coli and antibiotic residues in open pig farm systems were analyzed by Wandee et al. [63]. They observed high levels of AR E. coli populations in open pig farm systems, probably due to antibiotic contamination in the water supply and additional application of antibiotics, such as neomycin or colistin, having a significant impact on the prevalence of AR E. coli in pig manure [63]. This suggests that more appropriate waste management guidelines should be proposed to reduce the spread of pathogenic MDR E. coli and its ARGs.

Furthermore, mismanagement, such as the continuous use of antibiotics in feed or the accumulation of antibiotics in meat duck deep litter, may also be responsible for the evolution of bacterial resistance [8]. E. coli isolates from duck farms and meat deep litter were resistant to various antibiotics, including tetracycline, ampicillin, doxycycline, ofloxacin, gentamicin, etc., indicating a high prevalence of multi-antibiotic resistance in E. coli. Deep litter is considered an ideal environment for the evolution of bacterial resistance [8].

2.2. AR E. coli in Waste Treatment Plants

Waste treatment plants commonly contain antibiotics, biocides, metals, and diverse microorganisms, being potential hotspots for ARB and their ARGs [67]. Approximately 103–105 CFU/mL AR E. coli was found in wastewater treatment plants (Table 3) [14,68,69], and a variety of drug resistance genes and virulence genes were detected [70]. Thus, the prevalence of AR E. coli and its associated ARGs in wastewater cannot be ignored.

In a survey of a city’s sewage treatment plants, the numbers of ampicillin- and chloramphenicol-resistant E. coli in municipal wastewater were up to 3 × 104 CFU/mL, but greatly reduced (<10 CFU/100 mL) after treatment with peracetic acid (Table 3) [71]. In Norwegian treatment plants, all E. coli, including AR E. coli, were completely removed from wastewater by using ultrafiltration (UF) and nanofiltration (NF) membranes [67]. AR E. coli in municipal wastewater and river water was identified by Kaźmierczak et al. [68]; approximately 99.9% of AR E. coli was removed from wastewater treatment plants. However, AR E. coli isolates were at least one order of magnitude lower in summer than in winter. Residual resistant bacteria were up to 103–105 CFU/mL in treated wastewater, indicating a high spread risk of ARB in the environment. It revealed that despite the high efficiency of bacterial removal in wastewater treatment processes, considerable amounts of ARB are released into the environment with treated wastewater, and the percentage of ARB in total bacterial counts increases after wastewater treatment [68]. Yuan et al. found 35 MDR Escherichia spp. from animal farms, hospitals, and municipal wastewater treatment plants [72]. Each Escherichia isolate carried 21–26 ARGs and 8–12 mobile genetic elements (MGEs), and the isolates from livestock manure and wastewater treatment plants had greater diversity in plasmid profiles than hospital wastewater; more gene cassettes were also found in Escherichia isolates from livestock manure, which is possibly related to a higher occurrence of residual antibiotics or heavy metals [72].

The residual bacteria were less than 10 CFU/100 mL, which was compatible with the irrigation application of treated water. E. coli isolates with resistance to neomycin, florfenicol, amoxicillin, chlortetracycline, and sulfamethoxazole were found in pig farming (Table 3) [63]. Higher levels of E. coli and antibiotic residues were present in open farming systems than in closed systems, and there was no AR E. coli in the original excreta and wastewater. Meanwhile, an increased prevalence of AR E. coli was found in the sludge of anaerobic digestion and the waste stabilization pond [63]. Summerlin et al. (2021) found that the concentrations of ampicillin- and cephalothin-resistant E. coli in wastewater treatment plants were 2.5 ± 0.6–2.6 ± 2.0 log CFU/100 mL, higher than that of irrigation water (126 CFU/100 mL), posing potential health risks [73].

Table 3.

AR E. coli and its ARGs in waste treatment plants (2016–2021).

Resistance to Antibiotics ARGs Contents of AR E. coli Sources Location References
Ampicillin and chloramphenicol bla and cat 3 × 104 CFU/mL Municipal wastewater Italy [71]

Ampicillin and trimethoprim–sulfamethoxazole		 NN NN Influent wastewater Norway [67]
β-lactams and tetracycline NN 1.25 × 105 CFU/mL in winter and 1.25 × 103 CFU/mL in summer Upstream and downstream from the effluent discharge point Poland [68]
Aminoglycosides, sulfonamides, and quinolones aac-Ib, aacC2, aadA1, blaCTX-M, oqxB, qnrS, sul1, sul2, dfrA7, tetA, and tetG NN Municipal wastewater treatment plants China [72]
Trimethoprim/sulfamethoxazole and tetracycline blaCTX-M-1, blaTEM, tetA, and tetB 1.49–2.11 × 105 CFU/ml Urban wastewater treatment facility America [69]

Ampicillin, nalidixic acid, tetracycline, cotrimoxazole, and streptomycin		 Cit, Int1, Tn3, CTX-M1, IMP, and qnrS NN Municipal and animal wastewater Slovakia [70]

Neomycin, florfenicol, norfloxacin, amoxicillin, colistin, chlortetracycline, and sulfamethoxazole		 NN 3.0 × 103–2.1 × 105 CFU/mL Aerobic digestion and waste stabilization pond Thailand [63]

2.3. AR E. coli in the Aquatic Environment

At present, the rising emergence of AR and MDR E. coli is ubiquitous in the aquatic environment, which is a great concern for animal and human health [74]. Among them, the transfer effect of HGT has a significant influence on the spread of antibiotic resistance [75]. Hamelin et al. detected ARGs in E. coli isolates from different surface water areas within the St. Clair River and Detroit River by the DNA microarray method [76]. It was found that 48% of E. coli isolates carrying at least one ARG were downstream of wastewater effluent outfalls in an urban site, higher than that of other sites (24%). This suggests that AR E. coli from municipal wastewater may be widely transmitted in aquatic ecosystems [76]. The horizontal spread of MDR E. coli in small water bodies such as streams was mainly caused by runoff and leaching, which affect adjacent water bodies or large water bodies. During a rainfall period with grazing, the percentages of AR E. coli increased to 30–35%, higher than that of a dry period for grazing (<7%). Both chloramphenicol and tetracycline were most often found in water. Additionally, MDR E. coli, even with resistance to eight different antibiotics, accounted for 23% of the total resistant isolates, and they originated from both animals and humans. This indicated that drinking water from groundwater in a rural karst terrain is vulnerably polluted by ARB [77]. Zhang et al. (2014) found that the residue of 61 antibiotics (including quinolones, tetracyclines, and sulfonamides) in the Wenyu River basin was associated with quinolone-resistant E. coli [78]. The concentrations of AR E. coli in both an urban and a rural river ranged from 10 to 100 CFU/mL in New Zealand; ampicillin-resistant E. coli was the most common in both rivers [15].

Malema et al. investigated the prevalence and antibiotic resistance of pathogenic E. coli strains in harvested rainwater in South Africa by using PCR and disc-diffusion methods [79]. The result showed that E. coli isolates had the highest resistance to cephalosporin (76%), and 52% of isolates had multiple antibiotic resistance; all tested pathogenic E. coli isolates were sensitive to gentamicin, indicating that collected rainwater is not suitable for human drinking before treatment.

A total of 436 E. coli isolates with resistance to 17 antibiotics were found in water from representative interconnected sites (including streams, swallow caves, springs, and wells) in rural karst water systems in France [77]. Fakhr et al. (2016) investigated the contamination of drinking water by diarrheagenic AR E. coli in Zagazig City, northeastern Egypt [80]. The results showed that 16 E. coli strains were isolated from 300 potable water samples. All E. coli isolates were resistant to at least to one antibiotic, and 62.5% of E. coli displayed resistance to three or more antibiotics. E. coli exhibited high resistance to cefotaxime, tetracycline, and ampicillin (50–62.5%). High frequency of fecal contamination of drinking water indicates a high risk of diarrhea caused by AR E. coli [80]. Bong et al. (2022) investigated prevalence and diversity of AR E. coli from the anthropogenic-impacted Larut River and found that the concentration of AR E. coli carrying tet and sul genes was 4.1 × 103–4.7 × 103 CFU/mL in wastewater effluents, higher than in the river water; this indicated that E. coli is a key carrier of ARGs in freshwater river environments [74]. More effective measures should be taken to prevent and control the prevalence and risk of transmission of AR E. coli [79,81].

2.4. Modes of HGT in AR E. coli

Vertical gene transfer (VGT) and HGT are the two major mechanisms for the spread of AGRs in E. coli [25]. VGT is defined as a gene transferring from a parent to their offspring. Comparably, HGT, the process by which an organism passes genetic material to other cells rather than to its offspring, makes gene transfer more complicated. HGT is regarded as the most common mechanism of action and plays an important role in the rapid spread of antibiotic resistance in E. coli of animal origin, leading to the swift and wide transmission of ARGs between E. coli and other bacteria [29]. The transmission of AR E. coli by HGT depends mainly on the fact that resistant plasmids can be transmitted between different environments and hosts [27,82,83]. HGT mainly involves ARGs carried in MGEs, such as transposons, plasmids, and integrons [84,85]. The transfer of ARGs between E. coli of animal origin and other bacterial populations by HGT is governed mainly by three mechanism modes, including conjugation, transformation, and transduction [84,86,87]. Among them, conjugation is the primary mode of HGT, in which plasmids are transferred between donor and recipient cells that are in physical contact with one another through the mating pore pilus. The plasmids carrying ARGs such as mcr-1 gene in E. coli from food animals were transferred to recipients of E. coli and Salmonella spp. of humans by conjugation, conferring resistance to polymyxin, apramycin, chloramphenicol, etc. [88,89]. Transformation refers to the transfer of short free DNA from the environment, which does not need living donor cells, and incorporation into recipient cells. Transduction is the process of transfer of DNA via bacteriophages [84,85]. Tetracyclines with sub-minimum inhibitory concentration (MIC) can promote conjugate transfer of E. coli plasmid (PR4) and accelerate HGT effects [90]. These mechanisms may cause the rapid evolution of E. coli because HGT can increase their fitness in the presence of antibiotics [91].

3. Disinfection of AR E. coli and Its ARGs

3.1. Traditional UV Treatment

UV treatment systems can effectively eliminate AR E. coli by destroying nucleotide base pairs in DNA molecules and inhibiting DNA replication (Figure 2) [92]. UV treatment does not produce any chemical by-products and is becoming more common in the treatment of AR E. coli and its ARGs in wastewater and drinking water.

Figure 2.

Figure 2

Strategies to eliminate AR E. coli and its ARGs.

Rizzo et al. (2013) evaluated the effects of UV radiation on AR E. coli from an urban wastewater treatment plant [93]. AR E. coli was inactivated after UV irradiation for 1 h (at a dose of 1.25 × 104 μW s/cm2), while the traditional chlorination disinfection process (at a concentration of 2 mg/L) did not affect the antibiotic resistance of the investigated E. coli strains. Additionally, UV treatment did not change the amoxicillin and sulfamethoxazole resistance of E. coli (MIC > 256 or > 1024 μg/mL), but affected resistance to ciprofloxacin (MIC decreased by 33–50%). Conventional disinfection may be ineffective in the inactivation of ARB, which may be linked to UV levels [93].

It is vital to use suitable UV levels to eliminate AR E. coli. Pang et al. (2016) found that the UV dose of 40 mJ/cm2 led to a 5.5-log reduction in ampicillin-resistant E. coli, but E. coli was more resistant at lower UV doses (5–20 mJ/cm2) [94]. Zhang et al. (2017) isolated AR E. coli from a sewage treatment plant and evaluated the effects of UV irradiation on bacteria and their ARGs [34]. It was found that MDR E. coli was more resistant to UV disinfection at lower UV doses; the inactivation curves entered the tailing phase at a dose of 20 mJ/cm2, higher than that of antibiotic-sensitive E. coli (8 mJ/cm2). MDR E. coli was completely inactivated at a UV dose of 400 mJ/cm2. Moreover, ARGs (tetracycline- and sulfamethoxazole-resistant genes tetA, tetB, and sul2) of E. coli with 107–108 copies/mL were not effectively eliminated by UV disinfection; the reduced rates of relative abundance of ARGs reached 0.85–6 log after 80 mJ/cm2 UV irradiation [34]. O’Flaherty et al. (2018) detected the effects of different UV levels and lamp types on AR and antibiotic-sensitive E. coli in water treatments [57]. It was found that 7.5–8.4 mJ/cm2 UV lamp treatment led to a 6-log reduction in AR E. coli, higher that in antibiotic-sensitive E. coli (7.3–8.1 mJ/cm2); the UV levels were lower than the recommended level of 40 mJ/cm2 [57]. In general, UV treatment significantly reduced the number of viable AR E. coli cells, which is associated with the UV levels.

3.2. Surface Plasma Oxidation

Surface plasma oxidation can destroy the bacterial cell membrane, change the conformational structure of proteins, and destroy nucleotide bases of DNA (Figure 2) [73]. In recent years, more attention has been given to surface plasma in various bacteria inactivation due to its high efficiency, simple equipment, and no exogenous chemical residues [95].

Li et al. (2021) studied the effects of surface plasma on the elimination of AR E. coli and its ARGs from water environments [73]. The result showed that after plasma treatment for 10 min, 6.6 log E. coli was inactivated and the tetracycline, gentamicin, and amoxicillin resistance of E. coli significantly decreased, which may be associated with reactive oxygen and nitrogen species. Moreover, some ARGs (including tet(C), tet(W), blaTEM-1, and aac(3)-II) of E. coli were remarkably removed after the plasma treatment, and the conjugative transfer of ARGs (such as integron gene-intI1) was dramatically inhibited. This result highlights that plasma has potential application in removing AR E. coli and its ARGs from water environments [73].

Song et al. (2021) found that after surface plasma treatment for 10 min, 7.0 log AR E. coli in water was inactivated; its associated ARGs (including tetC, tetW, blaTEM-1, aac(3)-II, and intI1) decreased by 1.04–2.3 log copies, which may be attributed to oxidizing substances (such as H2O2, O3, NO2−, etc.) [31]. Additionally, the tetracycline, amoxicillin, and gentamicin resistance of E. coli decreased by 96.9–98.4%, and HGT of ARGs was suppressed by 63% after the plasma treatment. Overall, surface plasma treatment may be an effective method to remove AR E. coli and associated ARGs from water environments [31].

3.3. Others

Other strategies, such as biochar, phage, oxidants, etc., have been developed to inactivate AR E. coli and remove its associated ARGs from water (Figure 2) [30,31].

Combined biochar and polyvalent bacteriophage (phage) were used to inactivate AR E. coli and its ARGs in a soil–plant system [30]. The abundance of AR E. coli K-12 and its ARGs (such as tetM, tetQ, tetW, ampC, etc.) significantly decreased in the soil and in lettuce tissues following combined treatment for 63 d. A novel biotechnology used in this work provides insights into the targeted inactivation of AR E. coli and its ARGs, therein reducing their dispersion risks in the soil–plant–human system [30].

Disinfection efficiencies of AR E. coli and the sulfonamide-resistant gene sul1 were carried out in sterilized pond water by three fishery oxidants (bromine, chlorine, and KMnO4) [32]. After treatment with the dosages of 5–15 mg/L of the three oxidants, AR E. coli was completely inactivated and sul1 was efficiently removed. Chlorine had a higher ability to eliminate AR E. coli than bromine and KMnO4; chlorine and bromine had moderate removal efficiency of sul1. The results indicated that oxidative treatments may help with practical disinfection to prevent the spread of ARB and their ARGs in aquaculture environments [32]. Additionally, other biological or chemical methods (such as peracetic acid) effectively eliminated AR E. coli (<102 CFU/mL) in wastewater [14,71].

4. Alternatives to Antibiotics to Combat AR E. coli from the Farm Animal-Associated Sources

Some strategies have been taken to minimize antibiotic resistance, including the complete restriction of antibiotics used in food animals, the prudent use of conventional antibiotics, the development of alternatives to antibiotics, etc. [96,97,98]. At present, over 128 countries, including in Europe (such as Sweden in 1986, Denmark and Norway in 1995, Germany in 1996, etc.) and Asia (such as Japan in 2008, Korea in 2011, Vietnam in 2017, China in 2020, etc.) and the United States (in 2017), have taken action to regulate the use of antibiotics in food animals by banning, restricting, and reducing the amount of growth-promoting antibiotics in animal feed [99,100]. Moreover, some probiotics, herbal medicines, and AMPs have been developed to replace the use of antibiotics.

4.1. Probiotics/Prebiotics

Probiotics are one of the potential alternatives to antibiotics due to their modulation of the gut microbiota and enhancement of growth performance in animals (Figure 3).

Figure 3.

Figure 3

Alternatives to antibiotics to fight against AR E. coli.

Bacillus subtilis can enhance the immune response and it maintains the balance of intestinal flora; it increases the abundance of lactic acid bacteria and bifidobacterial, and reduces coliform bacteria and Clostridium perfringens. Moreover, short-chain fatty acids produced by B. subtilis can enhance intestinal health [101]. The B. velezensis ZBG17 strain exhibited high stability towards gastroenteric fluid in animal guts [102]. B. velezensis ZBG17 completely inhibited bacterial pathogens such as AR E. coli and Salmonella enteritidis within 6–8 h, and significantly improved the feed efficiency and humoral immune response in broilers. This highlights that B. velezensis ZBG17 is a prospective alternative to antibiotics in broiler production [102]. Bilal et al. found that the growth of E. coli O78 was inhibited by feeding 1.5 g/kg Saccharomyces cerevisiae (2 × 106 CFU/g) and Lactobacillus fermentum (1 × 107 CFU/g) that serves as a prebiotic and probiotic [103]. The supplement of prebiotics and probiotics into animal feed can improve animal welfare and productivity by promoting and protecting the villus structure and reducing pathogen colonization, such as E. coli in the poultry intestinal tract [103]. The data provide a new concept of a commercially viable alternative to antibiotics in the broiler feed industry.

4.2. Plant Extracts

Botanicals play an important role in bacteriostasis and they are being tested as alternatives to antibiotics due to their positive effects on coliform diarrhea caused by AR E. coli (Figure 3) [37].

Dell’Anno et al. investigated the effects of quebracho/chestnut tannins (0.75%) extracts, leonardite (0.25%), and tributyrin (0.2%) on porcine colibacillosis [104]. It was found that the combination of plant extracts increased the ratio of Lactobacillus to coliform in feces and reduced the incidence of diarrhea in weaned piglets [104]. This indicates that plant extracts are regarded as potential alternatives to antibiotics to maintain swine health and performance. Plant extract-concentrated tannin showed efficient antibacterial activity toward avian AR E. coli in vitro [105].

Recent studies showed that various plant essential oils (including terpenoids and phenylpropenes) have potent antimicrobial activity and could effectively reduce pathogens such as E. coli [106,107,108]. The counts of precaecal E. coli in broilers significantly reduced after the supplement of cinnamon bark oils with 300–600 mg/kg of diet [109]. Meanwhile, essential oils can maintain intestinal health and promote growth, indicating that they can be green alternatives to antibiotics in animal production to combat AR E. coli [108].

4.3. AMPs

It has been demonstrated that a few AMPs (such as plectasin, AA139, LL-37, hLF1-11, ZY4, etc.) in different phases of clinical trials (phase I–III) against ARB are more effective than conventional antibiotics due to their low resistance (Figure 3) [110,111,112,113]. AMPs have potent antibacterial activity, increasing the permeability of the bacterial inner and outer membrane, destroying the cell membrane, and promoting the leakage of intracellular substance, which may result in low resistance [114]. Bacteriocin is a kind of peptide or precursor peptide with potent antibacterial activity against E. coli [115]. Several Ib-M peptides (with the length of 20 amino acids) displayed potent activity against aminoglycoside-resistant E. coli O157:H7 AC188 with the MIC value of 1.6–6.3 μM; after exposure to 1 × MIC Ib-M peptides for 4 h, the population of E. coli reduced by more than 95%, indicating potential promising molecules for the development of new alternatives to antibiotics to combat AR E. coli [116].

Microcins produced by Gram-negative bacteria have been regarded as potential alternatives to antibiotics [117]. Lu et al. (2019) demonstrated that microcin PDI (MccPDI) generated by E. coli could inhibit MDR E. coli and Shigella isolates by the disruption of the bacterial membrane, indicating its potential as an alternative to antibiotics [118].

Other AMPs, such as dermaseptins, cathelicidin-OH-CATH30, and magainin-PGLa, have provided alternative therapies against MDR bacteria, including E. coli [41,42,43]. Generally, although several AMPs provide a promising revenue to reduce ARB, the road ahead is still long due to high production costs, poor stability in vivo, and other side effects [119,120].

5. Conclusions

The increasing use of antibiotics in farm animals has led to the spread of AR E. coli and its ARGs. Here, we have reviewed the prevalence of AR E. coli of farm animal origin. Disinfection methods (such as UV treatment, surface plasma oxidation, biochar, oxidants, etc.) and a few alternatives to antibiotics (including probiotics, plant extracts, and AMPs) to combat AR E. coli were highlighted, which may help us address the issues of bacterial antibiotic resistance from the farm animal-associated sources.

Author Contributions

C.X. helped to investigate, supervise, and write the manuscript. L.K. wrote the manuscript and prepared the figures. Y.L., Y.T., H.L. and Q.W. helped to investigate and review the manuscript. X.W. conceptualized and writing the manuscript. All authors have read and agreed to the published version of the manuscript.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data are contained within the article.

Conflicts of Interest

The authors declare no conflict of interest.

Funding Statement

The authors thank the Open Research Fund Program of Key Laboratory of Cleaner Production and Integrated Resource Utilization of China National Light Industry (grant no. CP2022YB10) and the National Natural Science Foundation of China (grant no. 32072770) for providing financial support.

Footnotes

Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

  • 1.Bernadether T.R., Douglas R.C., Gaspary O.M., Murugan S., Joram B. Comparison of the prevalence of antibiotic-resistant Escherichia coli isolates from commercial-layer and free-range chickens in Arusha district, Tanzania. Afr. J. Microbiol. Res. 2016;10:1422–1429. doi: 10.5897/AJMR2016.8251. [DOI] [Google Scholar]
  • 2.Chen J.W., Huang H.H., Chang S.M., Scaria J., Chiu Y.L., Chen C.M., Ko W.C., Wang J.L. Antibiotic-resistant Escherichia coli and sequence type 131 in fecal colonization in dogs in Taiwan. Microorganisms. 2020;8:1439. doi: 10.3390/microorganisms8091439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Singh A.S., Nayak B.B., Kumar S.H. High prevalence of multiple antibiotic-resistant, extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli in fresh seafood sold in retail markets of Mumbai, India. Vet. Sci. 2020;7:46. doi: 10.3390/vetsci7020046. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Giri S., Kudva V., Shetty K., Shetty V. Prevalence and characterization of extended-spectrum beta-lactamase-producing antibiotic-resistant Escherichia coli and Klebsiella pneumoniae in ready-to-eat street foods. Antibiotics. 2021;10:850. doi: 10.3390/antibiotics10070850. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Ewers C., Antao E.M., Diehl I., Philipp H.C., Wieler L.H. Intestine and environment of the chicken as reservoirs for extraintestinal pathogenic Escherichia coli strains with zoonotic potential. Appl. Environ. Microbiol. 2009;75:184–192. doi: 10.1128/AEM.01324-08. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Knutson K. Food Safety Lessons for Cannabis-Infused Edibles. Academic Press; Cambridge, MA, USA: 2020. Nobody is talking about environmental monitoring; pp. 111–137. [Google Scholar]
  • 7.Ji Y., Jang W., Carolyn J. A brief overview of Escherichia coli O157:H7 and its plasmid O157. J. Microbiol. Biotechnol. 2010;20:5–14. doi: 10.4014/jmb.0908.08007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Lin Y., Zhao W., Shi Z.D., Gu H.R., Zhang X.T., Ji X., Zou X.T., Gong J.S., Yao W. Accumulation of antibiotics and heavy metals in meat duck deep litter and their role in persistence of antibiotic-resistant Escherichia coli in different flocks on one duck farm. Poult. Sci. 2017;96:997–1006. doi: 10.3382/ps/pew368. [DOI] [PubMed] [Google Scholar]
  • 9.Sorbara M.T., Dubin K., Littmann E.R., Moody T.U., Fontana E., Seok R., Leiner I.M., Taur Y., Peled J.U., van den Brink M.R.M., et al. Inhibiting antibiotic-resistant Enterobacteriaceae by microbiota-mediated intracellular acidification. J. Exp. Med. 2019;216:84–98. doi: 10.1084/jem.20181639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Garcia-Bejar B., de Blas Martin I.G., Arevalo-Villena M., Perez A.B. High prevalence of antibiotic-resistant Escherichia coli isolates from retail poultry products in Spain. Animals. 2021;11:3197. doi: 10.3390/ani11113197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Manishimwe R., Moncada P.M., Musanayire V., Shyaka A., Scott H.M., Loneragan G.H. Antibiotic-resistant Escherichia coli and Salmonella from the feces of food animals in the east province of Rwanda. Animals. 2021;11:1013. doi: 10.3390/ani11041013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Song H.J., Kim S.J., Moon D.C., Mechesso A.F., Choi J.H., Kang H.Y., Boby N., Yoon S.S., Lim S.K. Antimicrobial resistance in Escherichia coli isolates from healthy food animals in South Korea, 2010–2020. Microorganisms. 2022;10:524. doi: 10.3390/microorganisms10030524. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Levy S.B., Marshall B. Antibacterial resistance worldwide: Causes, challenges and responses. Nat. Med. 2004;10:S122–S129. doi: 10.1038/nm1145. [DOI] [PubMed] [Google Scholar]
  • 14.Reinthaler F.F., Posch J., Feierl G., Wust G., Haas D., Ruckenbauer G., Mascher F., Marth E. Antibiotic resistance of E. coli in sewage and sludge. Water Res. 2003;37:1685–1690. doi: 10.1016/S0043-1354(02)00569-9. [DOI] [PubMed] [Google Scholar]
  • 15.Van Hamelsveld S., Adewale M.E., Kurenbach B., Godsoe W., Harding J.S., Remus-Emsermann M.N.P., Heinemann J.A. Prevalence of antibiotic-resistant Escherichia coli isolated from urban and agricultural streams in Canterbury, New Zealand. FEMS Microbiol. Lett. 2019;366:fnz104. doi: 10.1093/femsle/fnz104. [DOI] [PubMed] [Google Scholar]
  • 16.Administration D. Standards for Growing, Harvesting, Packing, and Holding of Produce for Human Consumption. Deparment of Health and Human Services, Food and Drug Administration; College Park, MD, USA: 2015. [Google Scholar]
  • 17.Van Driel A., Notermans D., Meima A., Mulder M., Donker G., Stobberingh E., Verbon A. Antibiotic resistance of Escherichia coli isolated from uncomplicated UTI in general practice patients over a 10-year period. Eur. J. Clin. Microbiol. Infect. Dis. 2019;38:2151–2158. doi: 10.1007/s10096-019-03655-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Bhardwaj D.K., Taneja N.K., Dp S., Chakotiya A., Patel P., Taneja P., Sachdev D., Gupta S., Sanal M.G. Phenotypic and genotypic characterization of biofilm forming, antimicrobial resistant, pathogenic Escherichia coli isolated from Indian dairy and meat products. Int. J. Food Microbiol. 2021;336:108899. doi: 10.1016/j.ijfoodmicro.2020.108899. [DOI] [PubMed] [Google Scholar]
  • 19.Bean D.C., Livermore D.M., Papa I., Hall L.M. Resistance among Escherichia coli to sulphonamides and other antimicrobials now little used in man. J. Antimicrob. Chemother. 2005;56:962–964. doi: 10.1093/jac/dki332. [DOI] [PubMed] [Google Scholar]
  • 20.Brynildsen M.P., Winkler J.A., Spina C.S., MacDonald I.C., Collins J.J. Potentiating antibacterial activity by predictably enhancing endogenous microbial ROS production. Nat. Biotechnol. 2013;31:160–165. doi: 10.1038/nbt.2458. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Yang H., Chen S., White D.G., Zhao S., McDermott P., Walker R., Meng J. Characterization of multiple-antimicrobial-resistant Escherichia coli isolates from diseased chickens and swine in China. J. Clin. Microbiol. 2004;42:3483–3489. doi: 10.1128/JCM.42.8.3483-3489.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Zhang X., Li Y., Liu B., Wang J., Feng C., Gao M., Wang L. Prevalence of veterinary antibiotics and antibiotic-resistant Escherichia coli in the surface water of a livestock production region in northern China. PLoS ONE. 2014;9:e111026. doi: 10.1371/journal.pone.0111026. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.McIver K.S., Amoako D.G., Abia A.L.K., Bester L.A., Chenia H.Y., Essack S.Y. Molecular epidemiology of antibiotic-resistant Escherichia coli from farm-to-fork in intensive poultry production in KwaZulu-Natal, South Africa. Antibiotics. 2020;9:850. doi: 10.3390/antibiotics9120850. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Schink A.K., Kadlec K., Kaspar H., Mankertz J., Schwarz S. Analysis of extended-spectrum-beta-lactamase-producing Escherichia coli isolates collected in the GERM-Vet monitoring programme. J. Antimicrob. Chemother. 2013;68:1741–1749. doi: 10.1093/jac/dkt123. [DOI] [PubMed] [Google Scholar]
  • 25.Messerer M., Fischer W., Schubert S. Investigation of horizontal gene transfer of pathogenicity islands in Escherichia coli using next-generation sequencing. PLoS ONE. 2017;12:e0179880. doi: 10.1371/journal.pone.0179880. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Poole T.L., Callaway T.R., Norman K.N., Scott H.M., Loneragan G.H., Ison S.A., Beier R.C., Harhay D.M., Norby B., Nisbet D.J. Transferability of antimicrobial resistance from multidrug-resistant Escherichia coli isolated from cattle in the USA to E. coli and Salmonella Newport recipients. J. Glob. Antimicrob. Resist. 2017;11:123–132. doi: 10.1016/j.jgar.2017.08.001. [DOI] [PubMed] [Google Scholar]
  • 27.Blahna M.T., Zalewski C.A., Reuer J., Kahlmeter G., Foxman B., Marrs C.F. The role of horizontal gene transfer in the spread of trimethoprim-sulfamethoxazole resistance among uropathogenic Escherichia coli in Europe and Canada. J. Antimicrob. Chemother. 2006;57:666–672. doi: 10.1093/jac/dkl020. [DOI] [PubMed] [Google Scholar]
  • 28.Lambrecht E., Van Coillie E., Boon N., Heyndrickx M., Van de Wiele T. Transfer of antibiotic resistance plasmid from commensal E. coli towards human intestinal microbiota in the M-SHIME: Effect of E. coli dosis, human individual and antibiotic use. Life. 2021;11:192. doi: 10.3390/life11030192. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Vines J., Cusco A., Napp S., Alvarez J., Saez-Llorente J.L., Rosas-Rodoreda M., Francino O., Migura-Garcia L. Transmission of similar mcr-1 carrying plasmids among different Escherichia coli lineages isolated from livestock and the farmer. Antibiotics. 2021;10:313. doi: 10.3390/antibiotics10030313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Ye M., Sun M., Zhao Y., Jiao W., Xia B., Liu M., Feng Y., Zhang Z., Huang D., Huang R., et al. Targeted inactivation of antibiotic-resistant Escherichia coli and Pseudomonas aeruginosa in a soil-lettuce system by combined polyvalent bacteriophage and biochar treatment. Environ. Pollut. 2018;241:978–987. doi: 10.1016/j.envpol.2018.04.070. [DOI] [PubMed] [Google Scholar]
  • 31.Song R., Li H., Kang Z., Zhong R., Wang Y., Zhang Y., Qu G., Wang T. Surface plasma induced elimination of antibiotic-resistant Escherichia coli and resistance genes: Antibiotic resistance, horizontal gene transfer, and mechanisms. Sep. Purif. Technol. 2021;275:119185. doi: 10.1016/j.seppur.2021.119185. [DOI] [Google Scholar]
  • 32.Zhao X., Su H., Xu W., Hu X., Xu Y., Wen G., Cao Y. Removal of antibiotic resistance genes and inactivation of antibiotic-resistant bacteria by oxidative treatments. Sci. Total Environ. 2021;778:146348. doi: 10.1016/j.scitotenv.2021.146348. [DOI] [PubMed] [Google Scholar]
  • 33.Li H., Kang Z., Jiang E., Song R., Zhang Y., Qu G., Wang T., Jia H., Zhu L. Plasma induced efficient removal of antibiotic-resistant Escherichia coli and antibiotic resistance genes, and inhibition of gene transfer by conjugation. J. Hazard. Mater. 2021;419:126465. doi: 10.1016/j.jhazmat.2021.126465. [DOI] [PubMed] [Google Scholar]
  • 34.Zhang C.M., Xu L.M., Wang X.C., Zhuang K., Liu Q.Q. Effects of ultraviolet disinfection on antibiotic-resistant Escherichia coli from wastewater: Inactivation, antibiotic resistance profiles and antibiotic resistance genes. J. Appl. Microbiol. 2017;123:295–306. doi: 10.1111/jam.13480. [DOI] [PubMed] [Google Scholar]
  • 35.De Mandal S., Panda A.K., Murugan C., Xu X., Senthil Kumar N., Jin F. Antimicrobial peptides: Novel source and biological function with a special focus on entomopathogenic nematode/bacterium symbiotic complex. Front. Microbiol. 2021;12:555022. doi: 10.3389/fmicb.2021.555022. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Jiang C., Ding L., Dong Q., Wang X., Wei H., Hu C., Ma C., Yan Q., Zhou Y., Degen A.A. Effects of root extracts of three traditional Chinese herbs as dietary supplements on dry matter intake, average daily gain, rumen fermentation and ruminal microbiota in early weaned yak calves. Anim. Feed Sci. Technol. 2021;278:115002. doi: 10.1016/j.anifeedsci.2021.115002. [DOI] [Google Scholar]
  • 37.Rabelo-Ruiz M., Ariza-Romero J.J., Zurita-Gonzalez M.J., Martin-Platero A.M., Banos A., Maqueda M., Valdivia E., Martinez-Bueno M., Peralta-Sanchez J.M. Allium-based phytobiotic enhances egg production in laying hens through microbial composition changes in ileum and cecum. Animals. 2021;11:448. doi: 10.3390/ani11020448. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38.Ramirez S.Y., Penuela-Sierra L.M., Ospina M.A. Effects of oregano (Lippia origanoides) essential oil supplementation on the performance, egg quality, and intestinal morphometry of Isa Brown laying hens. Vet. World. 2021;14:595–602. doi: 10.14202/vetworld.2021.595-602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 39.Rima M., Rima M., Fajloun Z., Sabatier J.M., Bechinger B., Naas T. Antimicrobial peptides: A potent alternative to antibiotics. Antibiotics. 2021;10:1095. doi: 10.3390/antibiotics10091095. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 40.Xia J., Ge C., Yao H. Antimicrobial peptides from black soldier fly (Hermetia illucens) as potential antimicrobial factors representing an alternative to antibiotics in livestock farming. Animals. 2021;11:1937. doi: 10.3390/ani11071937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41.Li S.A., Lee W.H., Zhang Y. Efficacy of OH-CATH30 and its analogs against drug-resistant bacteria In vitro and in mouse models. Antimicrob. Agents Chemother. 2012;56:3309–3317. doi: 10.1128/AAC.06304-11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42.Zaïri A., Ferrières L., Latour-Lambert P., Beloin C., Tangy F., Ghigo J.-M., Hani K. In vitro activities of dermaseptins K4 S4 and K4K20S4 against Escherichia coli, Staphylococcus aureus, and Pseudomonas aeruginosa planktonic growth and biofilm formation. Antimicrob. Agents Chemother. 2014;58:2221–2228. doi: 10.1128/AAC.02142-13. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43.Bechinger B., Juhl D.W., Glattard E., Aisenbrey C. Revealing the mechanisms of synergistic action of two magainin antimicrobial peptide. Front. Med. Technol. 2020;2:615494. doi: 10.3389/fmedt.2020.615494. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 44.Büyükkiraz M., Kesmen Z. Antimicrobial peptides (AMPs): A promising class of antimicrobial compounds. J. Appl. Microbiol. 2022;132:1573–1596. doi: 10.1111/jam.15314. [DOI] [PubMed] [Google Scholar]
  • 45.Krizman M., Avgustin J.A., Zdovc I., Golob M., Trkov M., Ciglenecki U.J., Biasizzo M., Kirbis A. Antimicrobial resistance and molecular characterization of extended-spectrum beta-lactamases and other Escherichia coli isolated from food of animal origin and human intestinal isolates. J. Food Prot. 2017;80:113–120. doi: 10.4315/0362-028X.JFP-16-214. [DOI] [PubMed] [Google Scholar]
  • 46.Davis G.S., Waits K., Nordstrom L., Grande H., Weaver B., Papp K., Horwinski J., Koch B., Hungate B.A., Liu C.M., et al. Antibiotic-resistant Escherichia coli from retail poultry meat with different antibiotic use claims. BMC Microbiol. 2018;18:174. doi: 10.1186/s12866-018-1322-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 47.Balcazar J.L. How do bacteriophages promote antibiotic resistance in the environment? Clin. Microbiol. Infect. 2018;24:447–449. doi: 10.1016/j.cmi.2017.10.010. [DOI] [PubMed] [Google Scholar]
  • 48.Azam M., Mohsin M., Sajjad Ur R., Saleemi M.K. Virulence-associated genes and antimicrobial resistance among avian pathogenic Escherichia coli from colibacillosis affected broilers in Pakistan. Trop. Anim. Health Prod. 2019;51:1259–1265. doi: 10.1007/s11250-019-01823-3. [DOI] [PubMed] [Google Scholar]
  • 49.Hornsey M., Betts J.W., Mehat J.W., Wareham D.W., van Vliet A.H.M., Woodward M.J., La Ragione R.M. Characterization of a colistin-resistant avian pathogenic Escherichia coli ST69 isolate recovered from a broiler chicken in Germany. J. Med. Microbiol. 2019;68:111–114. doi: 10.1099/jmm.0.000882. [DOI] [PubMed] [Google Scholar]
  • 50.Awad A.M., El-Shall N.A., Khalil D.S., Abd El-Hack M.E., Swelum A.A., Mahmoud A.H., Ebaid H., Komany A., Sammour R.H., Sedeik M.E. Incidence, pathotyping, and antibiotic susceptibility of avian pathogenic Escherichia coli among diseased broiler chicks. Pathogens. 2020;9:114. doi: 10.3390/pathogens9020114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 51.Wang P., Zhang J., Chen Y., Zhong H., Wang H., Li J., Zhu G., Xia P., Cui L., Li J., et al. ClbG in avian pathogenic Escherichia coli contributes to meningitis development in a mouse model. Toxins. 2021;13:546. doi: 10.3390/toxins13080546. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 52.Aklilu E., Harun A., Singh K.K.B. Molecular characterization of blaNDM, blaOXA-48, mcr-1 and blaTEM-52 positive and concurrently carbapenem and colistin resistant and extended spectrum beta-lactamase producing Escherichia coli in chicken in Malaysia. BMC Vet. Res. 2022;18:190. doi: 10.1186/s12917-022-03292-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 53.Nakayama T., Le Thi H., Thanh P.N., Minh D.T.N., Hoang O.N., Hoai P.H., Yamaguchi T., Jinnai M., Do P.N., Van C.D., et al. Abundance of colistin-resistant Escherichia coli harbouring mcr-1 and extended-spectrum beta-lactamase-producing E. coli co-harbouring blaCTX-M-55 or -65 with blaTEM isolates from chicken meat in Vietnam. Arch. Microbiol. 2022;204:137. doi: 10.1007/s00203-021-02746-0. [DOI] [PubMed] [Google Scholar]
  • 54.Abdallah H.M., Al Naiemi N., Elsohaby I., Mahmoud A.F.A., Salem G.A., Vandenbroucke-Grauls C. Prevalence of extended-spectrum beta-lactamase-producing Enterobacterales in retail sheep meat from Zagazig city, Egypt. BMC Vet. Res. 2022;18:191. doi: 10.1186/s12917-022-03294-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 55.Sabala R.F., Usui M., Tamura Y., Abd-Elghany S.M., Sallam K.I., Elgazzar M.M. Prevalence of colistin-resistant Escherichia coli harbouring mcr-1 in raw beef and ready-to-eat beef products in Egypt. Food Control. 2021;119:107436. doi: 10.1016/j.foodcont.2020.107436. [DOI] [Google Scholar]
  • 56.Ahmad I., Khattak S., Ali R., Nawaz N., Ullah K., Khan S.B., Ali M., Patching S.G., Mustafa M.Z. Prevalence and molecular characterization of multidrug-resistant Escherichia coli O157:H7 from dairy milk in the Peshawar region of Pakistan. J. Food Saf. 2021;41:e12941. doi: 10.1111/jfs.12941. [DOI] [Google Scholar]
  • 57.O’Flaherty E., Borrego C.M., Balcazar J.L., Cummins E. Human exposure assessment to antibiotic-resistant Escherichia coli through drinking water. Sci. Total Environ. 2018;616–617:1356–1364. doi: 10.1016/j.scitotenv.2017.10.180. [DOI] [PubMed] [Google Scholar]
  • 58.Jeong S.H., Kwon J.Y., Shin S.B., Choi W.S., Lee J.H., Kim S.J., Ha K.S. Antibiotic resistance in shellfish and major inland pollution sources in the drainage basin of Kamak Bay, Republic of Korea. Environ. Monit. Assess. 2021;193:471. doi: 10.1007/s10661-021-09201-z. [DOI] [PubMed] [Google Scholar]
  • 59.Checcucci A., Trevisi P., Luise D., Modesto M., Blasioli S., Braschi I., Mattarelli P. Exploring the animal waste resistome: The spread of antimicrobial resistance genes through the use of livestock manure. Front. Microbiol. 2020;11:1416. doi: 10.3389/fmicb.2020.01416. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 60.Um M.M., Barraud O., Kerouredan M., Gaschet M., Stalder T., Oswald E., Dagot C., Ploy M.C., Brugere H., Bibbal D. Comparison of the incidence of pathogenic and antibiotic-resistant Escherichia coli strains in adult cattle and veal calf slaughterhouse effluents highlighted different risks for public health. Water Res. 2016;88:30–38. doi: 10.1016/j.watres.2015.09.029. [DOI] [PubMed] [Google Scholar]
  • 61.King T.L.B., Schmidt S. Assessment of three indigenous South African herbivores as potential reservoirs and vectors of antibiotic-resistant Escherichia coli. Eur. J. Wildl. Res. 2017;63:44. doi: 10.1007/s10344-017-1100-y. [DOI] [Google Scholar]
  • 62.Rehman M.U., Zhang H., Huang S., Iqbal M.K., Mehmood K., Luo H., Li J. Characteristics of integrons and associated gene cassettes in antibiotic-resistant Escherichia coli isolated from free-ranging food animals in China. J. Food Sci. 2017;82:1902–1907. doi: 10.1111/1750-3841.13795. [DOI] [PubMed] [Google Scholar]
  • 63.Wandee S., Chan R., Chiemchaisri W., Chiemchaisri C. Alteration of antibiotic-resistant phenotypes and minimal inhibitory concentration of Escherichia coli in pig farming: Comparison between closed and open farming systems. Sci. Total Environ. 2021;781:146743. doi: 10.1016/j.scitotenv.2021.146743. [DOI] [PubMed] [Google Scholar]
  • 64.Juraschek K., Deneke C., Schmoger S., Grobbel M., Malorny B., Kasbohrer A., Schwarz S., Meemken D., Hammerl J.A. Phenotypic and genotypic properties of fluoroquinolone-resistant, qnr-carrying Escherichia coli isolated from the German food chain in 2017. Microorganisms. 2021;9:1308. doi: 10.3390/microorganisms9061308. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 65.Suzuki Y., Hiroki H., Xie H., Nishiyama M., Sakamoto S.H., Uemura R., Nukazawa K., Ogura Y., Watanabe T., Kobayashi I. Antibiotic-resistant Escherichia coli isolated from dairy cows and their surrounding environment on a livestock farm practicing prudent antimicrobial use. Int. J. Hyg. Environ. Health. 2022;240:113930. doi: 10.1016/j.ijheh.2022.113930. [DOI] [PubMed] [Google Scholar]
  • 66.Weiss D., Wallace R.M., Rwego I.B., Gillespie T.R., Chapman C.A., Singer R.S., Goldberg T.L. Antibiotic-resistant Escherichia coli and class 1 integrons in humans, domestic animals, and wild primates in rural Uganda. Appl. Environ. Microbiol. 2018;84:e01632-18. doi: 10.1128/AEM.01632-18. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 67.Schwermer C.U., Krzeminski P., Wennberg A.C., Vogelsang C., Uhl W. Removal of antibiotic resistant E. coli in two Norwegian wastewater treatment plants and by nano- and ultra-filtration processes. Water Sci. Technol. 2018;77:1115–1126. doi: 10.2166/wst.2017.642. [DOI] [PubMed] [Google Scholar]
  • 68.Kaźmierczak B., Osińska A., Korzeniewska E., Harnisz M., Niestępski S., Jachimowicz P., Jadwiszczak P., Kutyłowska M., Miller U. The occurrence of antibiotic-resistant bacteria, including Escherichia coli, in municipal wastewater and river water. E3S Web Conf. 2019;100:00061. doi: 10.1051/e3sconf/201910000061. [DOI] [Google Scholar]
  • 69.Brandon B., Jennifer S., Rachelle B., Caitlin C., Elizabeth L., Munoz-Price L.S., Krassimira R.H., Troy S. Antibiotic resistance patterns of Escherichia coli isolates from the clinic through the wastewater pathway. Int. J. Hyg. Environ. Health. 2021;238:113863. doi: 10.1016/j.ijheh.2021.113863. [DOI] [PubMed] [Google Scholar]
  • 70.Gregova G., Kmet V., Szaboova T. New insight on antibiotic resistance and virulence of Escherichia coli from municipal and animal wastewater. Antibiotics. 2021;10:1111. doi: 10.3390/antibiotics10091111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 71.Zanotto C., Bissa M., Illiano E., Mezzanotte V., Marazzi F., Turolla A., Antonelli M., De Giuli Morghen C., Radaelli A. Identification of antibiotic-resistant Escherichia coli isolated from a municipal wastewater treatment plant. Chemosphere. 2016;164:627–633. doi: 10.1016/j.chemosphere.2016.08.040. [DOI] [PubMed] [Google Scholar]
  • 72.Yuan W., Tian T., Yang Q., Riaz L. Transfer potentials of antibiotic resistance genes in Escherichia spp. strains from different sources. Chemosphere. 2020;246:125736. doi: 10.1016/j.chemosphere.2019.125736. [DOI] [PubMed] [Google Scholar]
  • 73.Summerlin H.N., Pola C.C., McLamore E.S., Gentry T., Karthikeyan R., Gomes C.L. Prevalence of Escherichia coli and antibiotic-resistant bacteria during fresh produce production (romaine lettuce) using municipal wastewater effluents. Front. Microbiol. 2021;12:660047. doi: 10.3389/fmicb.2021.660047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 74.Bong C.W., Low K.Y., Chai L.C., Lee C.W. Prevalence and diversity of antibiotic resistant Escherichia coli from anthropogenic-impacted larut river. Front. Public Health. 2022;10:794513. doi: 10.3389/fpubh.2022.794513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 75.Shao S., Hu Y., Cheng J., Chen Y. Research progress on distribution, migration, transformation of antibiotics and antibiotic resistance genes (ARGs) in aquatic environment. Crit. Rev. Biotechnol. 2018;38:1195–1208. doi: 10.1080/07388551.2018.1471038. [DOI] [PubMed] [Google Scholar]
  • 76.Hamelin K., Bruant G., El-Shaarawi A., Hill S., Edge T.A., Fairbrother J., Harel J., Maynard C., Masson L., Brousseau R. Occurrence of virulence and antimicrobial resistance genes in Escherichia coli isolates from different aquatic ecosystems within the St. Clair River and Detroit River areas. Appl. Environ. Microb. 2007;73:477–484. doi: 10.1128/AEM.01445-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 77.Laroche E., Petit F., Fournier M., Pawlak B. Transport of antibiotic-resistant Escherichia coli in a public rural karst water supply. J. Hydrol. 2010;392:12–21. doi: 10.1016/j.jhydrol.2010.07.022. [DOI] [Google Scholar]
  • 78.Zhang Q., Jia A., Wan Y., Liu H., Wang K., Peng H., Dong Z., Hu J. Occurrences of three classes of antibiotics in a natural river basin: Association with antibiotic-resistant Escherichia coli. Environ. Sci. Technol. 2014;48:14317–14325. doi: 10.1021/es503700j. [DOI] [PubMed] [Google Scholar]
  • 79.Malema M.S., Abia A.L.K., Tandlich R., Zuma B., Mwenge Kahinda J.M., Ubomba-Jaswa E. Antibiotic-resistant pathogenic Escherichia coli isolated from rooftop rainwater-harvesting tanks in the eastern cape, South Africa. Int. J. Environ. Res. Public Health. 2018;15:892. doi: 10.3390/ijerph15050892. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 80.Fakhr A.E., Gohar M.K., Atta A.H. Impact of some ecological factors on fecal contamination of drinking water by diarrheagenic antibiotic-resistant Escherichia coli in Zagazig city, Egypt. Int. J. Microbiol. 2016;2016:6240703. doi: 10.1155/2016/6240703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 81.Ahmed W., Hodgers L., Masters N., Sidhu J.P., Katouli M., Toze S. Occurrence of intestinal and extraintestinal virulence genes in Escherichia coli isolates from rainwater tanks in Southeast Queensland, Australia. Appl. Environ. Microbiol. 2011;77:7394–7400. doi: 10.1128/AEM.06047-11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 82.Zhou Z., Shuai X., Lin Z., Liu Y., Zhu L., Chen H. Prevalence of multi-resistant plasmids in hospital inhalable particulate matter (PM) and its impact on horizontal gene transfer. Environ. Pollut. 2021;270:116296. doi: 10.1016/j.envpol.2020.116296. [DOI] [PubMed] [Google Scholar]
  • 83.Yang D., Wang J., Qiu Z., Jin M., Shen Z., Chen Z., Wang X., Zhang B., Li J.W. Horizontal transfer of antibiotic resistance genes in a membrane bioreactor. J. Biotechnol. 2013;167:441–447. doi: 10.1016/j.jbiotec.2013.08.004. [DOI] [PubMed] [Google Scholar]
  • 84.Liu G., Thomsen L.E., Olsen J.E. Antimicrobial-induced horizontal transfer of antimicrobial resistance genes in bacteria: A mini-review. J. Antimicrob. Chemother. 2022;77:556–567. doi: 10.1093/jac/dkab450. [DOI] [PubMed] [Google Scholar]
  • 85.Vinayamohan P., Pellissery A., Venkitanarayanan K. Role of horizontal gene transfer in the dissemination of antimicrobial resistance in food animal production. Curr. Opin. Food Sci. 2022;47:100882. doi: 10.1016/j.cofs.2022.100882. [DOI] [Google Scholar]
  • 86.Loayza F., Graham J.P., Trueba G. Factors obscuring the role of E. coli from domestic animals in the global antimicrobial resistance crisis: An evidence-based review. Int. J. Environ. Res. Public Health. 2020;17:3061. doi: 10.3390/ijerph17093061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 87.Zhang S., Abbas M., Rehman M.U., Huang Y., Zhou R., Gong S., Yang H., Chen S., Wang M., Cheng A. Dissemination of antibiotic resistance genes (ARGs) via integrons in Escherichia coli: A risk to human health. Environ. Pollut. 2020;266:115260. doi: 10.1016/j.envpol.2020.115260. [DOI] [PubMed] [Google Scholar]
  • 88.Liu Y., Wang Y., Walsh T., Yi L., Zhang R., Spencer J., Doi Y., Tian G., Dong B., Huang X., et al. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: A microbiological and molecular biological study. Lancet Infect. Dis. 2016;16:161–168. doi: 10.1016/S1473-3099(15)00424-7. [DOI] [PubMed] [Google Scholar]
  • 89.Blake D.P., Hillman K., Fenlon D.R., Low J.C. Transfer of antibiotic resistance between commensal and pathogenic members of the Enterobacteriaceae under ileal conditions. J. Appl. Microbiol. 2003;95:428–436. doi: 10.1046/j.1365-2672.2003.01988.x. [DOI] [PubMed] [Google Scholar]
  • 90.Zhang Y., Ma Q., Su B., Chen R., Lin J., Lin Z., Wang D., Yu Y. A study on the role that quorum sensing play in antibiotic-resistant plasmid conjugative transfer in Escherichia coli. Ecotoxicology. 2018;27:209–216. doi: 10.1007/s10646-017-1886-0. [DOI] [PubMed] [Google Scholar]
  • 91.Hiltunen T., Virta M., Laine A.L. Antibiotic resistance in the wild: An eco-evolutionary perspective. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2017;372:20160039. doi: 10.1098/rstb.2016.0039. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 92.Zimmer J., Slawson R. Potential repair of Escherichia coli DNA following exposure to UV radiation from both medium- and low-pressure UV sources used in drinking water treatment. Appl. Environ. Microbiol. 2002;68:3293–3299. doi: 10.1128/AEM.68.7.3293-3299.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 93.Rizzo L., Fiorentino A., Anselmo A. Advanced treatment of urban wastewater by UV radiation: Effect on antibiotics and antibiotic-resistant E. coli strains. Chemosphere. 2013;92:171–176. doi: 10.1016/j.chemosphere.2013.03.021. [DOI] [PubMed] [Google Scholar]
  • 94.Pang Y., Huang J.J., Xi J., Hu H., Zhu Y. Effect of ultraviolet irradiation and chlorination on ampicillin-resistant Escherichia coli and its ampicillin resistance gene. Front. Environ. Sci. Eng. 2016;10:522–530. doi: 10.1007/s11783-015-0779-9. [DOI] [Google Scholar]
  • 95.Li H., Song R., Wang Y., Zhong R., Zhang Y., Zhou J., Wang T., Jia H., Zhu L. Inhibited conjugative transfer of antibiotic resistance genes in antibiotic resistant bacteria by surface plasma. Water Res. 2021;204:117630. doi: 10.1016/j.watres.2021.117630. [DOI] [PubMed] [Google Scholar]
  • 96.Lee C.R., Cho I.H., Jeong B.C., Lee S.H. Strategies to minimize antibiotic resistance. Int. J. Environ. Res. Public Health. 2013;10:4274–4305. doi: 10.3390/ijerph10094274. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 97.Lee C.R., Lee J.H., Kang L.W., Jeong B.C., Lee S.H. Educational effectiveness, target, and content for prudent antibiotic use. BioMed Res. Int. 2015;2015:214021. doi: 10.1155/2015/214021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 98.Uchil R.R., Kohli G.S., Katekhaye V.M., Swami O.C. Strategies to combat antimicrobial resistance. J. Clin. Diagn. Res. 2014;8:ME01–ME04. doi: 10.7860/JCDR/2014/8925.4529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 99.Salim H.M., Huque K.S., Kamaruddin K.M., Beg M. Global restriction of using antibiotic growth promoters and alternative strategies in poultry production. Sci. Prog. 2018;101:52–75. doi: 10.3184/003685018X15173975498947. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 100.Schoenmakers K. How China is getting its farmers to kick their antibiotics habit. Nature. 2020;586:S60–S62. doi: 10.1038/d41586-020-02889-y. [DOI] [Google Scholar]
  • 101.Qiu K., Li C.L., Wang J., Qi G.H., Gao J., Zhang H.J., Wu S.G. Effects of dietary supplementation with bacillus subtilis, as an alternative to antibiotics, on growth performance, serum immunity, and intestinal health in broiler chickens. Front. Nutr. 2021;8:786878. doi: 10.3389/fnut.2021.786878. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 102.Soni R., Keharia H., Bose A., Pandit N., Doshi J., Rao S.V.R., Paul S.S., Raju M. Genome assisted probiotic characterization and application of Bacillus velezensis ZBG17 as an alternative to antibiotic growth promoters in broiler chickens. Genomics. 2021;113:4061–4074. doi: 10.1016/j.ygeno.2021.10.012. [DOI] [PubMed] [Google Scholar]
  • 103.Bilal R.M., Hassan F.U., Saeed M., Rafeeq M., Zahra N., Fraz A., Saeed S., Khan M.A., Mahgoub H.A.M., Farag M.R., et al. Role of yeast and yeast-derived products as feed additives in broiler nutrition. Anim. Biotechnol. 2021:1–10. doi: 10.1080/10495398.2021.1942028. [DOI] [PubMed] [Google Scholar]
  • 104.Dell’Anno M., Reggi S., Caprarulo V., Hejna M., Sgoifo Rossi C.A., Callegari M.L., Baldi A., Rossi L. Evaluation of tannin extracts, leonardite and tributyrin supplementation on diarrhoea incidence and gut microbiota of weaned piglets. Animals. 2021;11:1693. doi: 10.3390/ani11061693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 105.Dakheel M.M., Alkandari F.A.H., Mueller-Harvey I., Woodward M.J., Rymer C. Antimicrobial in vitro activities of condensed tannin extracts on avian pathogenic Escherichia coli. Lett. Appl. Microbiol. 2020;70:165–172. doi: 10.1111/lam.13253. [DOI] [PubMed] [Google Scholar]
  • 106.Oussalah M., Caillet S., Saucier L., Lacroix M. Inhibitory eVects of selected plant essential oils on the growth of four pathogenic bacteria: E. coli O157:H7, Salmonella typhimurium, Staphylococcus aureus and Listeria monocytogenes. Food Control. 2007;18:414–420. doi: 10.1016/j.foodcont.2005.11.009. [DOI] [Google Scholar]
  • 107.Abd E., Ismail M. Tackling experimental colisepticaemia in broiler chickens using phytobiotic essential oils and antibiotic alone or in combination. Iran. J. Vet. Res. 2014;15:110–115. [Google Scholar]
  • 108.Abd El-Hack M.E., El-Saadony M.T., Saad A.M., Salem H.M., Ashry N.M., Abo Ghanima M.M., Shukry M., Swelum A.A., Taha A.E., El-Tahan A.M., et al. Essential oils and their nanoemulsions as green alternatives to antibiotics in poultry nutrition: A comprehensive review. Poult. Sci. 2022;101:101584. doi: 10.1016/j.psj.2021.101584. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 109.Chowdhury S., Mandal G.P., Patra A.K., Kumar P., Samanta I., Pradhan S., Samanta A.K. Different essential oils in diets of broiler chickens: 2. Gut microbes and morphology, immune response, and some blood profile and antioxidant enzymes. Anim. Feed Sci. Technol. 2018;236:39–47. doi: 10.1016/j.anifeedsci.2017.12.003. [DOI] [Google Scholar]
  • 110.Nibbering P.H., Ravensbergen E., Welling M.M., van Berkel L.A., van Berkel P.H., Pauwels E.K., Nuijens J.H. Human lactoferrin and peptides derived from its N terminus are highly effective against infections with antibiotic-resistant bacteria. Infect. Immun. 2001;69:1469–1476. doi: 10.1128/IAI.69.3.1469-1476.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 111.Mygind P.H., Fischer R.L., Schnorr K.M., Hansen M.T., Sonksen C.P., Ludvigsen S., Raventos D., Buskov S., Christensen B., De Maria L., et al. Plectasin is a peptide antibiotic with therapeutic potential from a saprophytic fungus. Nature. 2005;437:975–980. doi: 10.1038/nature04051. [DOI] [PubMed] [Google Scholar]
  • 112.Mwangi J., Yin Y., Wang G., Yang M., Li Y., Zhang Z., Lai R. The antimicrobial peptide ZY4 combats multidrug-resistant Pseudomonas aeruginosa and Acinetobacter baumannii infection. Proc. Natl. Acad. Sci. USA. 2019;116:52. doi: 10.1073/pnas.1909585117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 113.Elliott A.G., Huang J.X., Neve S., Zuegg J., Edwards I.A., Cain A.K., Boinett C.J., Barquist L., Lundberg C.V., Steen J., et al. An amphipathic peptide with antibiotic activity against multidrug-resistant Gram-negative bacteria. Nat. Commun. 2020;11:3184. doi: 10.1038/s41467-020-16950-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 114.Miao J., Liu G., Ke C., Fan W., Li C., Chen Y., Dixon W., Song M., Cao Y., Xiao H. Inhibitory effects of a novel antimicrobial peptide from kefir against Escherichia coli. Food Control. 2016;65:63–72. doi: 10.1016/j.foodcont.2016.01.023. [DOI] [Google Scholar]
  • 115.Almeida-Santos A.C., Novais C., Peixe L., Freitas A.R. Enterococcus spp. as a producer and target of bacteriocins: A double-edged sword in the antimicrobial resistance crisis context. Antibiotics. 2021;10:1215. doi: 10.3390/antibiotics10101215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 116.Prada-Prada S., Flórez-Castillo J., Farfán-García A., Guzmán F., Hernández-Peñaranda I. Antimicrobial activity of Ib-M peptides against Escherichia coli O157: H7. PLoS ONE. 2020;15:e0229019. doi: 10.1371/journal.pone.0229019. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 117.Yang S., Lin C., Sung C., Fang J. Antibacterial activities of bacteriocins: Application in foods and pharmaceuticals. Front. Microbiol. 2014;5:241. doi: 10.3389/fmicb.2014.00683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 118.Lu S.Y., Graca T., Avillan J.J., Zhao Z., Call D.R. Microcin PDI inhibits antibiotic-resistant strains of Escherichia coli and shigella through a mechanism of membrane disruption and protection by homotrimer self-immunity. Appl. Environ. Microbiol. 2019;85:e00371-19. doi: 10.1128/AEM.00371-19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 119.Divyashree M., Mani M.K., Reddy D., Kumavath R., Ghosh P., Azevedo V., Barh D. Clinical applications of antimicrobial peptides (AMPs): Where do we stand now? Protein Pept. Lett. 2020;27:120–134. doi: 10.2174/0929866526666190925152957. [DOI] [PubMed] [Google Scholar]
  • 120.Zhang Q.Y., Yan Z.B., Meng Y.M., Hong X.Y., Shao G., Ma J.J., Cheng X.R., Liu J., Kang J., Fu C.Y. Antimicrobial peptides: Mechanism of action, activity and clinical potential. Mil. Med. Res. 2021;8:48. doi: 10.1186/s40779-021-00343-2. [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The data are contained within the article.