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Production systems and important antimicrobial resistant-pathogenic bacteria in poultry: a review

Abstract

Economic losses and market constraints caused by bacterial diseases such as colibacillosis due to avian pathogenic Escherichia coli and necrotic enteritis due to Clostridium perfringens remain major problems for poultry producers, despite substantial efforts in prevention and control. Antibiotics have been used not only for the treatment and prevention of such diseases, but also for growth promotion. Consequently, these practices have been linked to the selection and spread of antimicrobial resistant bacteria which constitute a significant global threat to humans, animals, and the environment. To break down the antimicrobial resistance (AMR), poultry producers are restricting the antimicrobial use (AMU) while adopting the antibiotic-free (ABF) and organic production practices to satisfy consumers’ demands. However, it is not well understood how ABF and organic poultry production practices influence AMR profiles in the poultry gut microbiome. Various Gram-negative (Salmonella enterica serovars, Campylobacter jejuni/coli, E. coli) and Gram-positive (Enterococcus spp., Staphylococcus spp. and C. perfringens) bacteria harboring multiple AMR determinants have been reported in poultry including organically- and ABF-raised chickens. In this review, we discussed major poultry production systems (conventional, ABF and organic) and their impacts on AMR in some potential pathogenic Gram-negative and Gram-positive bacteria which could allow identifying issues and opportunities to develop efficient and safe production practices in controlling pathogens.

Introduction

Poultry meat is an important animal protein and one of the most popular meat consumed by humans worldwide. Its consumption is projected to increase 17.8% by 2030 according to the OECD-FAO; the highest increase among all types of animal meats [1]. This significant increase is due to the rapidly growing poultry industry (annual global production of about 120 million tons) through genetic selection and the adoption of various measures to improve birds’ health and performance. Intensive poultry production driven by consumer’s demand continue to increase, especially in South America, Asia and Africa, possibly due to their recent change in diets for a more animal protein option [2]. Antibiotic use in the poultry industry revolutionized the therapeutic and economical gains by improving meat yield, bird’s health, and cost-efficient production. However, the growing concerns of the increasing prevalence of antimicrobial resistance (AMR), particularly against antibiotics of human importance have led to restrictions of antimicrobial use (AMU) in poultry in several countries. Despite these restrictions and the use of alternative production practices to reduce AMR in poultry, there have been multiple reports of AMR bacteria associated with poultry which present food safety concerns [3,4,5].

The gastrointestinal tract (GIT) plays a crucial role in poultry health as it provides the first-line of defense against foreign pathogens while also allowing nutrient absorption [6]. In addition to maintaining the homeostasis and nutrient processing, populations of different bacteria including Lactobacillus, Clostridium, Ruminococcus, Salmonella enterica serovars, Enterococcus spp., and E. coli inhabit the GIT to constitute the gut microbiota. Through horizontal gene transfer of mobile genetic elements such as transposons and plasmids, the gut microbiota can be a reservoir for antimicrobial resistance genes (ARGs). The addition of antibiotics to poultry diets can modulate the gut microbiota by decreasing the pathogenic bacteria load, increased the intestinal nutrient absorption, and ultimately improved growth parameters [7]. Thus, it is important to understand how dietary practices modulate the poultry gut microbiome [6, 8].

Necrotic enteritis (NE) caused by a Gram-positive anaerobic spore-forming bacterium C. perfringens is one of the major poultry diseases costing $6 billion per year to the global poultry industry [9]. This bacterium, representing also a food safety issue, is widespread and commonly found in the environment and in the gut of humans and animals [10]. Sub-clinical NE lead to production losses associated with reduced weight gains and poor feed conversion ratios [11]. Intestinal damages induced by C. perfringens give bacteria access to the bile duct and blood stream, consequently damaging additional organs in birds [12]. Typical antibiotics such as avilamycin and bacitracin methylene disalicylate are used to prevent NE in poultry. Therefore, with the AMU restrictions in poultry, controlling this pathogen has become highly imperative not only for poultry gut health, but also from a food safety perspective [9]. Coccidiosis is also a major poultry intestinal disease caused by Eimeria spp. parasites which, invade and replicate in the intestine [13]. This parasitic disease causes annual losses greater than $600 million in the United States and $3.2 billion worldwide [13, 14]. Eimeria infections have also been associated with the promotion of NE [15, 16].

In poultry production, the type of feeding program is extremely important to ensure nutrient and health requirements are met. Feeding programs are selected based on cost efficiency, effectiveness to improve health and growth. Conventional feeding programs relied on AMU to improve growth performance while simultaneously preventing infectious diseases. However, increasing concerns over AMR resulted in the development and adoption of alternative productions known as antibiotic-free (ABF) productions, also called no antibiotic ever (NAE) or raised without antibiotic (RWA) and organic productions. Harmonization of the definitions used for the terms ABF, NAE and RWA is necessary, so “ABF” will be used for consistency in this review. Research on the effectiveness of alternative feeding programs to reduce AMR is needed to identify best production practices in preserving gut heath [17,18,19]. Substantial efforts are needed to not only understand the underlying mechanisms behind alternative feeding programs but also to understand their true impacts on AMR profiles in the gut microbiota.

In this review, we will discuss the significance of conventional, ABF and organic poultry productions by outlining the AMU concerns and the use of alternatives to antibiotics. Moreover, a summarization of some important antimicrobial agents and alternative products in poultry production is presented to highlight pathogenic bacteria of concern and opportunity for improvements for their efficient control while highlighting that AMR issues should be addressed by a “One Health” approach.

Poultry feeding and production practices

Feed is a significant component in poultry production. Feed quality, nutrient composition, and consumption rate by birds are critical parameters to monitor for their health and productivity. Nutrients of poultry feed can be categorized into five different groups: carbohydrates, lipids, proteins, minerals and vitamins. High quantity and quality water is also essential. Each feed ingredient plays a vital role in either, energy acquisition and utilization, metabolism or health of poultry. For several years, sub-therapeutic levels of antibiotics have been used in broiler feed to maximize their productivity [20]. This practice contributed to meet the rapidly increasing chicken meat demands of the growing world population. However, AMR concerns led to alternative poultry feeding programs and production practices to be adopted. These alternative feeding programs include ABF and organic production which, in definition may vary by country around the world. However, organic and ABF poultry production requires alternative solutions to maintain or improve health. Moreover, the impact of alternative poultry feeding program on AMR deserve to be explored further.

Conventional production

Conventional production practices were widely adopted to shape the livestock industry to what it is today. One key difference between conventional production and ABF or organic production is the use of antibiotics in healthy animal during conventional production. Justifications of antibiotics used in poultry production include growth promotion and prevention of important diseases. The World Health Organization (WHO) created a global critically important antibiotics (CIA) list that categorize antibiotics into three different classes based on their importance in human medicine; important, highly important, and critically important [21]. In addition to WHO, CIA lists were created by different countries with varying discrepancies in antibiotic classification. For example, the Public Health Agency of Canada CIA’s list classify antibiotics in four categories (I, II, III, and IV), where agents in category I are “very high importance” and those in category IV have “low importance” in human medicine. The Chicken Farmers of Canada (CFC) progressively eliminated the preventive use of Category I to III antibiotics by 2020. Accordingly, about 60% of broilers were raised without antibiotics in the United State of America in 2019 [22]. The trend to remove antibiotics from poultry production slowly increased in the past years, but concerns about bird's health and cost-efficiency remain to be issues in the development of antibiotic replacements.

Organic production

Organic production typically raise animals naturally while maintaining optimal health, welfare and living conditions. More and more poultry producers are opting for organic production due to the sustainability and harmony with the environment. Each country has their own standards and regulations of organic production systems, such as the United States Department of Agriculture’s National Organic Program and the Standards Council of Canada’s CAN/CGSB-32-Organic Production Systems [23, 24]. Despite slight differences on the definition of organic production by country, the common rule of thumb requires free range systems (outdoor access on pasture), ecological sustenance, and compliance with all applicable regulatory requirements of substances [24]. However, the organic production requirements place heavy limitations that reintroduce health and management issues. For example, access to the outdoor pasture increases the risk of exposure to environmental microbes such as Salmonella, Campylobacter and C. perfringens [25], which are food safety and bird’s heath concerns. There is a perception among consumers that organically produced foods are more “natural” and therefore healthier than conventionally produced ones [26, 27]. However, organic broiler production costs were estimated to be 70%–86% higher than those of conventional production which consequently increased retail market costs of poultry products [28]. Furthermore, in organic production there is a high risk of colonization by pathogens that can cause diseases such as NE and coccidiosis in chicken (chicken health) and salmonellosis in human (food safety) [26]. Colonized pathogenic bacteria consequently may contaminate meat during processing. For example, it has been reported that organic broiler meat, at the end of processing after chilling, was more frequently contaminated with Campylobacter spp. than conventional broiler carcasses, possibly due to the organic bird’s free access to pasture where they could be more exposured to environmental of bacterial pathogens [29]. These authors also reported relative risks of 1.7 times increased risk of Campylobacter illnesses following consumption of contaminated organic broiler meat, compared to conventional broiler meat in Denmark. These reports on organic poultry production indicate that investigation are needed to develop cost-efficient methods to improve the gut health, reduce risks to consumers, and minimize negative impacts of production on the environment.

Antibiotic-free production

Antibiotic-free production is similar to conventional production, with the exception of AMU as a prophylactic and for growth promotion. Thus, the potential health and production issues in ABF production requires alternative solutions (Section Alternatives to antibiotics in poultry production). Consumer perception and rising concerns about the food attributes direct attention to ABF-based poultry production; they are willing to pay premium prices for these products. However, the general consumer’s understanding of ABF is limited to positive advertisement and method of communication and do not discuss the negative issues of ABF production. According to Agri-Stats data in 2018, the mortality rate in ABF and conventionally raised birds were reported to be approximately 4.2% and 2.9%, respectively [30]. Growth promoting properties of antibiotics are used to evaluate the efficacy of alternatives products in controlling coccidiosis, NE and maintaining gut health [31]. In ABF production, vaccinations, high-quality feed and water, and heightened control of production environments are required to decrease stresses in birds while maintaining their health and performance [32, 33]. Despite these efforts, health and growth performance issues could arise due to ineffective prevention of diseases and the potential of negative side effects from antibiotic alternatives [17, 19, 32]. Moreover, even if these problems could be surmounted, it would be at the cost of expense [17]. For the prevention of coccidiosis, ABF production rely on vaccinations or chemically synthesized non-antibiotic coccidiostats [19]. However, studies indicated that, when compared to ionophores, chemical coccidiostats could promote the development of anticoccidials drug resistance and are typically more expensive than ionophores [19]. Surprisingly, it has also been observed that some chemical coccidiostats without the co-administration with antibiotics could induce NE [19].

Alternatives to antibiotics in poultry production

Many different alternatives to antibiotics have been investigated in poultry production at an attempt to replicate their multifunctions. A list of alternatives investigated and/or used in poultry production include probiotics, prebiotics, organic acids, phytochemicals, vaccines, in-feed enzymes, and essential oils (Table 1). A description of each antibiotic alternative, their benefits in poultry health, and their effective function are briefly described below.

Table 1 Different categories of alternatives to antibiotics in poultry production

Probiotics

They are live microbial feed additives to help maintain intestinal microbial balance and benefit the host’s health [34,35,36,37]. Mostly identified as Gram-positive and some Gram-negative, Khan and Naz [37] reviewed commonly used probiotics including various Lactobacillus spp. (L. bulgaricus, L. plantarum, L. acidophilus, L. helveticus, L. lactis, L. salivarius, L. casei, L. reuteri), Enterococcus faecium and E. faecalis, Streptococcus thermophilus, and Bacillus subtilis in poultry. They function by interfering with the colonization of the gut by pathogenic bacteria through competitive exclusion [35,36,37]. Moreover, probiotics stimulate the immune system as shown by various studies correlating probiotic administration with elevated humoral and cellular immune responses by increasing T cell, CD+, B cells, and anti-inflammatory cytokine production [37, 55, 56]. Probiotics have been reported to improve body weight and feed-conversion ratio in commercial broilers [55]. However, the effectiveness of probiotics seems strain-dependent [36]. Probiotics naturally produce volatile fatty and organic acids and assist in digestion by breaking down insoluble fibers and improve nutrient absorption metabolism as well as lowering the pH of the gut to levels affecting pathogenic bacteria such as E. coli and Salmonella spp. [37]. Moreover, dietary probiotic B. subtilis was found to improve hen’s performance and egg quality at a lower dose while improving the protein quality in the eggs at a high dose [57]. In contrast, Sohail et al. [58] did not observe a positive impact on beneficial gut bacteria when investigating the effects of probiotics on the cecal and tracheal microbiota.

Prebiotics

They are carbohydrate-based polymers such as fructooligosaccharides (FOS), galactooligosaccharides, and mannanoligosaccharides (MOS) that function to promote beneficial bacteria in the gut, aid in digestion, and inhibit colonization by pathogenic bacteria [38]. Prebiotics are not utilized by the host but, they could be substrates for gut bacteria such as Bifidobacterium and other lactic acid bacteria. The prebiotic FOS indirectly alters the gut microbiota community through increased production of short-chain fatty acids (SCFA), some of which favour fermentation. The SCFAs are important in the GIT and immune function but, they also elicit acid stress to pathogenic bacteria [35, 38]. However, MOS can directly affect adhesion of pathogens such as E. coli and Salmonella to intestinal cells by binding to their flagella, which are important in their motility and attachment to intestinal epithelial cells [38]. Poultry cannot digest prebiotics because they are resistant to digestive enzymatic actions [38]. A study conducted by Ricke [39], indicated the potential of FOS as a beneficial prebiotic with its fermentation being limited to certain lactic acid bacteria. Prebiotics have been also reported to dose-dependently improve mineral absorption and immune function in poultry with minor adverse side effects [35].

Organic acids

These compounds have acquired a favourable reputation in the poultry industry due to their strong nutritional and antimicrobial properties. Moreover, organic acids have already been applied for feed preservation and performance enhancement in livestock production. These compounds have a carboxylic acid (R-COOH) group in common, in the simple monocarboxylic (formate, acetate, butyrate and propionate), hydroxyl (tartrate, citrate, lactate, and malate), or short-chain (fumarate, sorbate) form [19]. They acidify through lowering the pH of the gut to inhibit pathogenic bacterial growth, thus decreasing their prevalence and product contaminations while improving nutrient digestibility [40,41,42]. Butyrate and propionate have positive effects on the gut microbiota, such as down-regulation of the Salmonella pathogenicity islands which are important virulence-encoding genes in Salmonella. However, lactate has been identified to fuel Salmonella growth due to the utilization of the lactate-degrading respiratory lactate dehydrogenases LldD (converts L-lactate into pyruvate) and Dld (oxidates D-lactate to quinones) [59]. Moreover, acetate restored barA gene function in mutant S. typhimurium barA; this gene encodes for the BarA sensor kinase important in the interaction with SirA to shift Salmonella from mobility to virulence [60].

Phytogenics

The immune-stimulatory potential of fruit products in poultry have been recently reviewed [61]. Berry fruit pomace, a major solid by-product from the juice industry, contains phenolic compounds such as flavonoids [45]. These compounds have antioxidant properties, which have been positively correlated with their antimicrobial activity [8, 46]. Islam et al. [8] investigated effects of low-bush blueberry pomace (LBBP) on gut microbiota of free-range birds when administered through feed and reported that Lactobacillus population in LBBP-fed birds were more abundant than those fed a control diet from 21 to 42 days old birds. Moreover, Das et al. [46] reported significant improvements of body weight along with improved intestinal health when supplementing feed with cranberry and blueberry by-products. These authors also reported that dietary cranberry products modulated the innate immune genes (caspase 1, apoptosis–related cysteine peptidase, chemokine receptor-5, interferon gamma, myeloid differentiation primary response gene 88, and Toll-like receptor 3) and suppressed proinflammatory cytokines in broilers [46].

Essential oils

They are known to have antioxidant and antimicrobial properties [53]. With the increasing demand for ABF production, essential oils as feed additives in poultry production have become more popular. Dietary cinnamaldehyde (Cinnamomum) and citral (3,7-dimethyl-2-6-octadienal) were found to reduce the severity and incidence of NE and coccidiosis [54], and the proportion of antibiotic resistant E. coli while improving the intestinal digestibility, the overall performance and the meat quality in broilers [54, 62]. Broilers fed a natural blend of essential oils (basil, caraway, lemon, laurel, sage, thyme, oregano, tea) showed a significant increase in weight gain and feed-to-gain ratio, with an overall increase in carcass weight, breast weight, and relative percentage of breast meat [63].

Enzymes

These biological catalysts are typically administered to assist in digestion of certain feedstuffs [49]. Enzymes for poultry feed are mostly derived from fungi and bacteria, with xylanase and glucanase constituting majority (> 80%) of the global market for carbohydrase [49]. In-feed enzymes are more recently investigated in broiler production due to the rising costs of feed ingredients such as soybean meal and corn, so cheaper feed alternatives that contain non-starch polysaccharides (NSP) were considered. Since NSP are not completely digestible in broilers, in-feed enzymes are added in response to the adverse effects of NSP [64]. The impacts of enzymes on ruminant performance and health have been studied extensively but such extensive studies are lacking in non-ruminants including poultry. However, it is well understood that feed enzymes are required to fully degrade certain chemical bonds of feedstuffs allowing access to amino acids and minerals where the host normally could not access alone [50]. One naturally available enzyme in poultry is phytase, which hydrolyzes phytic acids allowing the host to have a better access to phosphorus; which is one of the most expensive nutrients of feed [51]. Contrasting studies conflict on the effect of enzymes on growth rate and feed intake, but other studies all agreed on an increased nutrient digestibility when administering in-feed enzymes [65, 66].

Several health and economic challenges arise when implementing ABF productions using the alternative products. Despite promised beneficial activities, the efficacy of antibiotic alternatives is quite variable by study. It is hypothesized that combination of these individual alternatives may provide optimal activities. This probably could explain in the decrease of overall performance (average daily gain, feed conversion ratio, meat yield, mortality, etc.) with a single alternative product when compared to traditional antibiotics [17, 19]. Requiring more feed, time, and space to mitigate these deficits will be more costly compared to antibiotics, as well as increased carbon foot-printing. Nevertheless, assuming that all of these factors were somehow managed, readjustment of production practices would result in higher costs than conventional production which will affect the price of broiler meat in retail markets. Furthermore, the impacts including AMR, of these alternatives to antibiotics in production deserve investigations under a “One Health” perspective.

Antimicrobial use and concerns

Antimicrobials significantly contribute to the treatment and prevention of infectious diseases, the improvement of poultry performance, and overall yield [67,68,69]. However, concerns arose regarding the excessive AMU with the most significant issues being the emergence and spread of AMR among bacteria [70, 71] through selection of antibiotic resistant strains and dissemination of genes conferring AMR by horizontal gene transfer [72,73,74]. Antimicrobial resistance causes loss in therapeutic efficacy of antibiotics resulting in increased morbidity and mortality rates due to infectious diseases in both animals and humans [70, 75, 76] thus constituting significant socio-economic and public health issues.

Several studies reported links between AMU in food animal production and the prevalence of AMR in bacteria [77, 78]. The prevalence of AmpC-like β-lactamase blaCMY-2 genes harboring Salmonella enterica and E. coli from infected humans were positively correlated to ceftiofur-resistant Salmonella and E. coli from chicken meat [79]. Action plans to decrease AMR are being implemented under a “One Health” approach in several countries. Moreover, WHO responded with a Global Action Plan, outlining important objectives to succeed in the fight against AMR. However, it was reported that 73%–80% of all antibiotics sold worldwide were used specifically for food animal production [2, 80]. Due to the AMR crisis, several poultry producing countries including Canada, United States of America, Brazil, China and the European Union have restricted the use of antibiotics as growth promoters and for disease prevention in animal production [81, 82].

Some antimicrobials used in conventional poultry

Typical conventional broilers are raised in barns from hatching to 36–42 d during which each bird can consume 3.2 to 4.0 kg of feed to reach a body weight of about 1.8 to 2.2 kg [7]. Conventional broiler feeds which, are generally formulated according to the growth phases (starter, grower and finisher), are mainly grain-based to which protein, minerals and vitamins are added for nutritional requirements along with antibiotics. Major antibiotics used for therapy in poultry feed include aminoglycosides (gentamicin, neomycin, spectinomycin, and streptomycin), β-lactams (penicillin and amoxicillin), sulfonamides and tetracyclines [83]. Antibiotics that have been used for disease prevention and growth promotion in poultry include glycolipids (bambermycin), polypeptides (bacitracin), ionophores (salinomycin), streptogramin (virginiamycin), and orthosomycin (avilamycin). However, the accurate estimates for the number and amount of antibiotics used in poultry production systems globally are lacking [2, 84]. Some common antimicrobials used for disease prevention and growth promotion in broiler production are discussed below.

Avilamycin

Is an orthosomycin antibiotic from Streptomyces viridochromogenes, targeting Gram-positive bacteria such as C. perfringens to prevent NE in broiler chickens [85]. It has been used as a growth promoter in poultry production [67, 68]. Avilamycin is unclassified in the WHO list of critically important antimicrobials for human medicine (WHO CIA), justifying its use in current poultry production [21]. Avilamycin inhibits bacterial protein synthesis by binding to their 50S ribosomal subunit’s helices 89 and 91 interfering thus, with tRNA and initiation factor 2 [85, 86]. Resistance to avilamycin can be mediated by mutations in helix 89 and 91 of the 23S rRNA [86] or in the ribosomal protein L16 [87, 88]. Various avilamycin resistance bacteria such as Enterococcus faecium have been reported in broiler fecal from several farms in Denmark and France [89, 90].

Bambermycin

Is also known as flavomycin, flavophospholipol or moenomycin. This phosphoglycolipid antibiotic originating from various strains of Streptomyces including S. bambergiensis and S. ghanaensis is not categorized in the WHO/CIA list as important in human medicine, but used in poultry production [91]. Targeting primarily Gram-positive, bambermycin inhibits peptidoglycan synthesis through disruption of the penicillin-binding proteins (PBPs) transglycosylase activities, affecting bacterial cell wall production [67, 92]. Resistance mechanisms against bambermycin are not fully understood. However, due to its similar mechanism of actions to β-lactam (targeting PBPs), mechanism of actions for resistance to bambermycin could be related to β-lactam resistance.

Bacitracin

This cyclic polypeptide antibiotic produced by Bacillus licheniformis and B. subtilis strains is categorized as important in the WHO/CIA list [93]. Primarily targeting Gram-positive bacteria, bacitracin interferes with the dephosphorylation function of C55-isoprenyl pyrophosphate which is a lipid carrier involved in bacterial peptidoglycan synthesis [93, 94]. Dephosphorylation of C55-isoprenyl pyrophosphate results in the prevention of transport of N-acetylglucosamine (NAG) and β-(1–4)-N-acetylmuramic acid (NAM) to build the peptidoglycan wall [95]. Bacitracin is widely used for prevention of NE in broiler production. It is typically administered in the form of bacitracin methylene disalicylate (BMD) or zinc-bacitracin (BACN-Z) [95, 96]. Bacitracin resistance has been correlated with the presence of the bcrR gene encoding a unique membrane-bound one-component system through a putative ATP-binding cassette (bcrAB) transporter [97, 98].

Monocarboxylic polyether ionophores

Salinomycin, narasin, and monensin belonged to this group and are unclassified in the WHO/CIA list [21]. They are produced by Streptomyces albus, S. aureofaciens, and S. cinnamonensis, respectively. Salinomycin use dates back to its discovery in 1974, demonstrating effectiveness against Gram-positive bacteria and coccidiosis [99]. Salinomycin has been reported to improve bird's performance and prevent infectious diseases presumably by altering the composition and activities of intestinal microflora in broiler. Historically, salinomycin was considered less important in human medicine, however, it is now a well-known inhibitor of human cancer stem cells and has been suggested to suppress the growth of colorectal cancer by disrupting the β-catenin/TCF complex [100]. Ionophores facilitate the transport of cations into target organisms such as Eimeria spp. by disrupting their osmoregulation [101]. The mechanisms of resistance against ionophores are not fully understood, but ionophores are suspected to be excluded from cell membranes by an extracellular polysaccharide called glycocalyx [102].

Mechanisms in poultry

Antibiotics and their alternatives on livestock or poultry may have complex direct or indirect mechanism of actions [103]. Antibiotics in broiler diets can alter the composition and activities of the bird’s gut microflora by killing, inhibiting or promoting bacteria resulting in improved health and advantageous economic outcomes [67]. More research is needed to systematically evaluate effects of specific antibiotics on the overall dynamics of gut microflora as well as on the distribution of ARGs among bacteria in chicken. Justifications for certain antibiotics used for growth promotion (i.e. avilamycin and bambermycin) need to be established as concerns for cross-resistance and co-selection to traditional antibiotics important in human medicine has been legitimated. An example includes bacteria showing resistance to avilamycin and cross-resistance to evernimicin, an antibiotic which inhibits the 50S ribosomal subunit formation in Staphylococcus aureus cells and are used to treat humans [86, 90, 104, 105]. Isolates of S. enterica serovar Heidelberg showed resistance to the third-generation cephalosporin ceftiofur (used in animals only) and ceftriaxone (very important in treating bacterial infections in human) [79]. This raised significant concerns to human health due to possible cross-resistance between third-generation cephalosporins such as ceftiofur, ceftriaxone and cephamycin [106, 107].

Antibiotics may also have important effects on animal physiology that are not studied in detail despite their significant effects against bacteria. Thus, it is important to study their effects on host’s physiology and immunology to better understand their interactions and design better alternative production practices. An example of this interaction was reported with bacitracin, showing modulation of the poultry blood serum metabolite profiles through increasing the alanine aminotransferase and decreasing albumin/globulin ratio levels (Fig. 1) [46]. The reduced albumin/globulin ratio in bacitracin-fed birds could indicate acute or chronic inflammatory processes due to an elevated globulin level or other uncharacterised mechanisms. Interestingly, Das et al. [47] reported a 22.55-fold, 12.34-fold, and 7.97-fold expression in CATH2, MPO, and IL-5 genes respectively, in immune organs of bacitracin-fed birds compared to a control diet (Fig. 1). Understanding the mechanisms of how other health management practices such as how prebiotics, probiotics and vaccines interact with broilers is critical in the development of improved production systems [90, 108].

Fig. 1
figure 1

Bacitracin effect on broiler chicken cecal microbiota, blood metabolites, and immune gene modulation. ALP: Alkaline phosphatase; AGR: Albumin-globulin ratio; AMY: Amylase; CATH2: Cathelicidin antimicrobial peptide; MPO: Myeloperoxidase; CASP1: Caspase 1; MX1: Myxovirus resistance 1; CCR4: Chemokine receptor 4; CRP: C-reactive protein; JAK2: Janus kinase 2 "Updated from Das et al. [47]"

Poultry production systems and AMR bacteria

Various studies have been conducted on the AMU in food animals and their consequences on AMR in foodborne bacteria [4, 7, 90, 97, 109,110,111]. Here, the impacts of conventional and alternative production systems on AMR are presented to clarify concerns moving from conventional to ABF or organic production and the consequential effect on AMR in the birds and their products. The most common AMR reported in poultry pathogenic bacteria such as S. enterica serovars, Campylobacter jejuni, E. coli, Staphylococcus aureus, and C. perfringens are discussed (Table 2). Antibiotic-resistant non-typhoidal S. enterica serovars, E. coli, or Campylobacter spp. can infect humans through contact or consumption of contaminated food (food safety). A positive association between consumption of antibiotics in poultry and corresponding antibiotic resistance in some bacteria has been reported in Europe [83]. It is clear on how conventional production affects AMR; however, it is unclear on how organic or ABF production affects AMR. There are limited studies on AMR in organic and ABF systems. A summary of antibiotic-resistant E. coli, Salmonella spp., and Campylobacter spp. reported worldwide in poultry is presented in Fig. 2 and a schematic overview of mechanisms of AMR in bacteria is presented in Fig. 3. Organic and ABF production practices have been adopted to reduce AMU; however, various multi-drug resistant (MDR) bacteria from poultry raised from these alternative production practices have been reported (Table 3). Understanding on how these production practices truly affect the AMR profiles of the poultry gut microbiome (resistome) need to be established.

Table 2 Important antimicrobial-resistant bacteria reported in conventional poultry
Fig. 2
figure 2

Antibiotic resistance in Salmonella, E. coli and Camplylobacter spp. reported in major poultry production countries from 2000 to 2020. Information obtained from: Brazil [41, 121,122,123,124,125,126,127,128,129], Europe [130,131,132], USA [133,134,135,136,137,138,139], China [140,141,142,143]

Fig. 3
figure 3

Schematic representation of Gram-positive and Gram-negative antimicrobial resistance mechanisms. 1. Decreased permeability of antibiotics due to outer membrane, 2. Increased expression of efflux pumps, 3. Modification/mutation of target sites (i.e. topoisomerases, ribosomes, penicillin-binding proteins (PBPs), fluoroquinolones, etc.), 4. Inactivation and modification of antibiotics via inactivating enzymes (i.e. β-lactamases, tetracycline-inactivating enzymes)

Table 3 Important antimicrobial resistant bacteria reported in organic poultry

AMR in Gram-negative bacteria

A wide variety of Gram-negative bacteria can cause diseases in poultry (E. coli, Salmonella Pullorum/Gallinarum, Gallibacterium anatis, Pasteurella multocida, Klebsiella spp.) and foodborne illness in human (S. enterica serovars and Campylobacter jejuni/coli). The complexity of the Gram-negative bacterial cell surface provides intrinsic resistance against various antibiotics [149]. Antibiotics such as cephalosporins, carbapenems and fluoroquinolones are effective against Gram-negative bacteria, however, Gram-negative bacteria resistant to these antibiotics have been reported (Fig. 2). Resistance in Gram-negative bacteria can be acquired and/or intrinsic, with an overview of mechanisms of resistance being presented in Fig. 3.

Escherichia coli

Escherichia coli is a commensal bacterium of the gastrointestinal microflora. Some strains of this bacterium are known to cause diseases such as colibacillosis, cystitis, pyelonephritis, sepsis/meningitis, and gastroenteritis in both humans and animals due to the presence of various virulence factors [150]. The extraintestinal pathogenic E. coli (ExPEC) strains are epidemiologically and phylogenetically distinct from both intestinal pathogenic and commensal strains [151]. Avian pathogenic E. coli (APEC) is an ExPEC responsible for significant economic losses in the poultry industry [152] and was suggested to cause urinary tract infections and meningitis in humans, highlighting their safety risks [153].

In conventional poultry production, AMU has been correlated to the increased prevalence of AMR in E. coli [7, 62, 150, 154]. Antibiotics belonging to cephalosporins, quinolones, aminoglycosides and sulfonamides are used against E. coli infections. Multiple resistance to amoxicillin–clavulanic acid, ceftiofur, ceftriaxone, cefoxitin, gentamicin, sulfonamide and tetracycline in commensal and APEC isolates have been documented in poultry [7, 62, 150, 154]. Antibiotic resistance genes blaTEM, blaSHV, blaCMY-2, aac (3)-Via, aadA1, aph (3)-Ib, aph (6)-Id, sul1, sul2, tet(A) and tet(B), were observed in corresponding resistance phenotypes. Mobile genetic elements including pAPEC-O2-R, IncA/C2 and IncI1 plasmids as well as Class I integrons carrying antibiotic resistance genes tet(A), sul1, and blaTEM able to be transferred to a recipient bacterium have been also observed in E. coli from broilers [150]. Dietary bambermycin, penicillin, salinomycin, and bacitracin or a combination of salinomycin plus bacitracin in broiler resulted in a higher incidence of ceftiofur, spectinomycin, and gentamicin resistance in E. coli isolates than those from the non-medicated feeds [7]. Interestingly, these authors observed a higher prevalence of sul1, aadA, and Class 1 integrons in salinomycin-fed chickens than in control or other treatment groups [7]. Regardless of antimicrobial feeding, they also noted multiple antibiotic-resistant E. coli isolates harboring corresponding genes such as blaCMY-2, blaTEM, tetB, sul1, and aadA [7]. Oral administration of tetracycline was not found to significantly induce changes in the chicken cecal bacterial community, however, population of tetracycline resistance E. coli harboring tet(A) or tet(B) increased [155]. Extended-spectrum β-lactamase-producing E. coli and Klebsiella pneumoniae were reported in local and imported chicken meat [156]. From conventional commercial broiler chickens, E. fergusonii harboring resistance to ampicillin, streptomycin and tetracycline were isolated, but the antibiotic usage from the studied farm was unknown [157]. These authors reported that 94.5% of the ampicillin-resistant E. fergusonii isolates tested contained the β-lactam (blaCMY-2), aminoglycoside (aadA1, strA, strB), trimethoprim (dfrV, dfrA1), tetracycline (tet(A), tet(B), tet(C), tet(E)), and sulfonamide (sul1, sul2) resistance genes [157].

As organic and ABF poultry production systems are becoming popular, their efficacy to reduce AMR deserves investigations. Recently, the prevalence of antimicrobial resistant commensal E. coli was found to be lower in organic and ABF broilers compared to conventionally produced ones [117]. However, E. coli isolated from organic, ABF and conventional production systems demonstrated high frequencies of resistance (> 50%) to ampicillin, cefazolin, sulfonamides, streptomycin and tetracycline [117]. It has been reported that E. coli isolates from conventional poultry meat were more MDR than those from organic poultry meat [27]. Even though the possible effectiveness of organic acids as an alternative to antibiotics have potential, some bacteria such as E. coli and Lactobacilli can survive in acidic environments due to their innate acid resistance properties [158]. Davis et al. [133] reported no significant difference between conventional, RWA and organic productions for the overall prevalence of antimicrobial resistant E. coli in chicken and turkeys, although differences were noted in specific antibiotic resistant phenotypes. Moreover, a higher prevalence of resistant E. coli to ampicillin, ampicillin-sulbactam, cefazolin, cefoxitin, ceftriaxone, and trimethoprim-sulfamethoxazole was found in conventionally raised turkeys compared to organic and RWA produced ones [133]. However, Sanchez et al. [134] reported a 56.2% and 60.7% resistance to ampicillin in E. coli when fed conventional and ABF, respectively [134]. In the Netherlands, extended-spectrum β-lactamase (ESBL)-producing E. coli harboring blaCTX-M-1 and blaCMY-2 genes have been isolated from commercial organic broilers [147].

Non-typhoidal Salmonella enterica (NTS)

In food production animals, NTS induces diarrhea with fever, anorexia, and dehydration. However, poultry can be asymptomatic carriers of these pathogens and exposure to antimicrobials could promote AMR isolates that may be transmitted to humans [5, 159]. It has been estimated that NTS causes 1.35 million infections (212,500 infections due to AMR isolates), 26,500 hospitalizations, and 420 deaths each year in the United States, resulting in about $400 million in direct medical costs [160]. Most cases of human salmonellosis (diarrhea) do not require antibiotic treatments. However, severe cases in elderly, children, or those with underlying comorbidities may require antimicrobial treatment, such as invasive infection resulting in life-threatening bloodstream infections. Recommended antimicrobials to treat NTS include ciprofloxacin, ceftriaxone, trimethoprim/sulfamethoxazole, or in last resort cases, amoxicillin and carbapenem. Several NTS serovars from conventional poultry farms showing resistance to ampicillin, amoxicillin-clavulanic acid, ceftiofur, cefoxitin, and ceftriaxone were reported [113]. Moreover, genes associated with aminoglycoside (aadA1, aadA2, strA), β-lactams (blaCMY-2, blaSHV, blaTEM), tetracycline (tet(A), tet(B)) and sulfonamides (sul1) were detected in these Salmonella isolates [113]. Fosfomycin is an antibiotic approved to treat urinary tract infection cases, but its use is restricted in poultry production. However, a fosfomycin resistance gene, fosA7, was identified in S. enterica serovar Heidelberg isolated from conventional broilers [161]. In China, it has been reported that 60.1% of all non-duplicate Salmonella isolated from retail raw poultry meats were MDR to at least three different classes of antimicrobials, which included nalidixic acid, ampicillin and streptomycin [140]. Co-resistance to ciprofloxacin and ceftriaxone was most prevalent (84.1%) in S. enterica serovar Indiana [140]. A clonal group of S. enteritidis known as SE86, a frequently identified poultry Salmonella isolate in Brazil associated with foodborne outbreaks, has been reported to be resistant to ciprofloxacin (41.9%) and sulfafurazole (75%) [121]. A persistent septicemia causing S. enteritidis (SE_TAU19) resistant to nalidixic acid and sulfadimethaxine was reported [162]. Quesada et al. [130] found the mcr-1 gene (colistin resistance) in E. coli and S. enterica from poultry and swine. From commercial poultry farms, Liljebjelke et al. [135] reported MDR Salmonella resistant to streptomycin, gentamycin, sulfadimethaxine, trimethoprim, and tetracycline. A recent report from Europe indicated no associations between consumption of cephalosporins and quinolone in poultry and resistance to these antibiotics in Salmonella isolates from humans [83].

A few studies on AMR Salmonella have been conducted in organic and ABF poultry production systems [144, 145, 163, 164]. The prevalence of amoxicillin-clavulanate, ampicillin, cefoxitin, ceftiofur, and ceftriaxone-resistant Salmonella isolates from large-scale organic poultry production farms was significantly lower than isolates from conventional broiler production [144, 163]. In contrast, a significantly higher AMR Salmonella isolates were found in ABF broiler than in those from conventional production [145]. Salmonella isolated from US conventional retail poultry meat showed 2.6 times higher resistance prevalence compared to those from organic retail meats [164].

Campylobacter spp.

Campylobacter spp. (C. jejuni and C. coli) are important foodborne pathogenic bacteria associated with poultry. These bacteria are microaerophilic and certain environmental stresses such as exposure to air, drying, low pH, and prolonged storage can be detrimental to their survival. In humans, these pathogens cause a self-limiting diarrheal disease from improperly prepared or contaminated food, including poultry products. In the United States, Campylobacter are responsible for an estimated 2 million cases of gastroenteritis annually. Antibiotics belonging to the macrolides (erythromycin), fluoroquinolone, tetracyclines and aminoglycosides (gentamicin) classes are used against Campylobacteriosis [165]. Despite an interprovincial observed difference in the AMR profile, a Canadian study suggested that AMR observed in Campylobacter isolates from chicken could be originated from upstream [166]. These authors reported more quinolone-resistant Campylobacter isolated in British Columbia, while those isolated in Quebec and Ontario provinces were predominantly resistant to tetracyclines, macrolides, ketolides, and lincosamides [166]. The emergence of fluoroquinolone resistance among Campylobacter from poultry led to the restriction or ban of sarafloxacin and enrofloxacin used in poultry [167]. An extremely high (88.6%–100%) prevalence of resistance to macrolides, tetracyclines, quinolones, and chloramphenicol was found in Campylobacter spp. isolated from conventionally-raised broiler chickens [168]. Moreover, it was reported that majority of the Campylobacter spp. isolated from turkeys were resistant to over seven antimicrobials [169]. Correlation between the prevalence of macrolide-resistant Campylobacter and the use of macrolides along with a trend of increasing prevalence of erm(B) gene in isolates were observed in poultry [170, 171].

Limited studies investigated the presence of antibiotic resistant Campylobacter in ABF and organic poultry productions. However, a study reported a significantly lower fluoroquinolone resistant Campylobacter prevalence (< 2%) in organic than in conventional (46%) poultry farms [136]. Susceptibility test of 157 Campylobacter isolates from organic (n = 77) and conventional (n = 80) chickens showed that all organic isolates were sensitive to all antibiotics, except two that were resistant to tetracycline, while resistance to quinolones and tetracycline were observed among the 80 isolates from conventional chickens [172]. Despite limitations, fecal, carcasses, equipment, water and air sample analyses from organic and conventional processing methods suggested that raising birds without the use of antimicrobials is not effective in decreasing the incidence of AMR Campylobacter in poultry products [146]. However, effects of Canadian AMU reduction on AMR in major poultry-associated foodborne pathogenic Gram-negative bacteria (Salmonella, Escherichia coli, and Campylobacter) showed the potential for progressive transitions from conventional to antibiotic-free broiler production [173]. The above review indicated the lack of studies investigating AMR in different production and alternative gut health management practices in poultry.

AMR in Gram-positive bacteria

Gram-positive bacteria including Enterococcus spp., Staphylococcus spp., and C. perfringens are common in poultry and can be commensal or pathogenic. According to a meta-analysis performed by Cardinal et al. [174], the most frequently used antibiotics in broiler during the last 30 years predominately targeted Gram-positive bacteria. As shown in Fig. 3, these bacteria lack an outer membrane which is compensated by a thicker (30–100 nm) peptidoglycan cell wall [175]. Examples of major AMR Gram-positive bacteria of concerns include methicillin-resistant S. aureus (MRSA), vancomycin-resistant S. aureus (VRSA), MDR Streptococcus pneumoniae, and vancomycin-resistant E. faecium (VRE). Several MDR Gram-positive bacteria have been isolated from conventional, organic and ABF poultry productions [4, 27, 97, 176, 177].

Enterococcus spp.

They were initially described as Micrococcus and fecal streptococci more than 113 years ago [178] belonging to the Firmicutes phylum of Bacilli class, Lactobacillales order, Enterococcaceae family, and Enterococcus genus (more than 40 species). Enterococcus spp. particularly E. faecalis, E. faecium and E. cecorum have been associated with diseases in both human and poultry [179, 180]. Therapeutic options of enterococcal infections include a combination of penicillin (ampicillin or penicillin) and aminoglycoside (gentamicin or streptomycin), vancomycin and quinupristin-dalfopristin (for E. faecium only). Newer antibiotics (linezolid, daptomycin, tigecycline and 5th-generation cephalosporins) or older antibiotics (chloramphenicol, doxycycline, minocycline and nitrofurantoin) have been also considered to fight against Enterococcus. However, these bacteria are characterised by intrinsic resistance to important antibiotic classes and to tolerate low concentrations of β-lactams, quinolones, aminoglycosides, and lincosamides, as well as being able to metabolise preformed folic acid (trimethoprim and sulphonamides). Furthermore, Enterococci have developed a high ability to acquire exogenous resistance genes via conjugative transposons and plasmids [181]. In conventional production, AMU has been associated with increased AMR Enterococci isolates and a potential zoonotic transmission of AMR isolates has been suggested [97, 182]. Association between the use of virginiamycin and virginiamycin-resistant E. faecium was reported in a surveillance study conducted by Aarestrup et al. [183]. Subsequent studies reported a strong correlation between the presence of streptogramin resistance genes in E. faecium in humans and the use of virginiamycin [81]. A case-control study in France determined a significant correlation (risk factor of 2.3) between the prevalence of avilamycin-resistant E. faecium and avilamycin use during broiler production [90]. Avilamycin-resistant E. faecium has also been reported to be cross-resistance to evernimicin [86, 90, 104, 105] and demonstrated MDR to other antibiotics such as penicillin, tetracycline, streptomycin and erythromycin [111]. All avilamycin-resistant E. faecium isolates contained the emtA gene encoding a methyltransferase which inhibits avilamycin and evernimicin function [111, 184]. Such emtA positive E. faecium has also been found to harbor vancomycin, gentamicin, tetracyclines, and erythromycin and streptogramin resistance genes in chickens [88]. Enterococcus faecium isolated from broiler chickens treated with virginiamycin demonstrated resistance to quinupristin-dalfopristin, supporting previous observations on the induction of quinupristin-dalfopristin resistance from the use of virginiamycin [185, 186]. Ciprofloxacin, macrolides, penicillin and tetracycline resistant E. faecium strains were isolated from broilers fed bambermycin, penicillin, salinomycin, bacitracin, or a salinomycin/bacitracin combination [4]. Moreover, MDR E. faecium and E. faecalis isolates showing resistance phenotypes and genotypes against bacitracin, erythromycin, tylosin, lincomycin, streptomycin, gentamycin, tetracycline and ciprofloxacin were reported in commercial broiler [97].

As there are a limited number of studies that investigated resistance profiles of important Gram-positive bacteria in organic and ABF poultry production, it is imperative to broaden this topic of research. Miranda et al. [176] reported lower prevalence of resistant Enterococcus spp. from organic chickens compared to conventional chickens. Moreover, prevalence of MDR Enterococcus spp. was higher in conventional chickens compared to organic chickens [176]. In South Korea, organically-produced poultry demonstrated less prevalence of resistance to ciprofloxacin and erythromycin (commonly used in veterinary medicine) compared to conventionally-produced poultry [187]. Interestingly, Kilonzo-Nthenge et al. [148] reported increased total Enterococcus spp. but less AMR Enterococcus spp. in organic chicken compared to conventional chickens, predominantly showing resistance to streptomycin and erythromycin.

Staphylococcus spp.

Staphylococci are widespread in nature and comprise of coagulase-positive and coagulase-negative species able to induce minor and major infections in poultry and human [188]. The coagulase-positive Staphylococcus aureus can cause infections such as omphalitis, pneumonia and arthritis [189]. The treatment of S. aureus infections becomes difficult due to the emergency of multiple antibiotic resistant isolates including MRSA resulting from AMU in both animal and human. In Belgium, MRSA also resistant to antimicrobials including tylosin, amoxicillin, trimethoprim-sulfamethoxazole, lincomycin, tetracycline, and colistin were isolated from broiler [190]. Penicillin, tetracycline and ciprofloxacin-resistant S. aureus strains have been reported in different conventional broiler production operations in Korea along with four MRSA isolates from three different operations [191]. South Africa investigations of antibiotic resistance by Amoako et al. [192] in S. aureus from poultry and their products using the “Farm to Fork” approach showed a prevalence of 31.25% (n = 120/384) of S. aureus in analyzed samples: farm (40), transport (15), abattoir (30), and retail point (35) [192]. The authors reported that isolates were resistant to tetracycline (61.7%), penicillin (55.8%), erythromycin (54.2%), clindamycin (43.3%), doxycycline (36.7%), ampicillin (34.17%), moxifloxacin (30.8%), amikacin (30.83%), trimethoprim-sulfamethoxazole (30.0%), and levofloxacin (23.3%) with 100% of isolates being susceptibility to tigecycline, teicoplanin, vancomycin, nitrofurantoin, chloramphenicol, and linezolid [192]. In 2006, S. aureus isolated from poultry demonstrated increased resistance against antibiotics compared to S. aureus isolates from 1970s [193]. Multidrug-resistant S. aureus strains in farm could contaminate chicken meat during processing. Accordingly, MDR S. aureus isolated from raw poultry meats were reported, with a highest resistance prevalence being observed towards β-lactams, macrolides, quinolones, and fluoroquinolones [177]. There was significantly more doxycycline-resistant S. aureus from conventional poultry meat than from organic poultry meat [27]. From conventional bioaerosols, coagulase-negative S. xylosus isolates resistant to nalidixic acid, novobiocin, penicillin, oxacillin, ampicillin, lincomycin, tetracycline, erythromycin, bacitracin, and streptomycin were observed [194]. These resistant isolates harbored tetK (tetracycline), linA (lincomycin), ermB (erythromycin) and blaZ (β-lactam) genes.

Clostridium perfringens

Isolates of C. perfringens resistant to bacitracin, penicillin, streptomycin, tetracyclines and gentamicin have been reported in poultry [195]. Moreover, C. perfringens isolated from conventionally produced broilers demonstrated resistance to tetracycline and bacitracin, and intermediate resistance to lincomycin [196]. Bambermycin resistance also was observed in C. perfringens from poultry, pig, and cattle in Belgium farms [197]. Antimicrobial resistance in Clostridium including C. perfringens and other anaerobes has been reviewed recently [198]. High prevalence of AMR were reported in C. perfringens isolated from broiler chickens in Egypt, namely neomycin, colistin, pefloxacin, trimethoprim-sulfamethoxazole, gentamicin, streptomycin, lincomycin, oxalinic acid, erythromycin and spiramycin [199]. Despite the importance of C. perfringens on poultry health, there are a lack of studies that investigated the prevalence of AMR C. perfringens in organic and ABF poultry production. Thus, more research is warranted to better understand the impact of organic and ABF poultry production on AMR in C. perfringens.

Conclusion

The poultry industry is rapidly growing due to market and consumer’s demand. However, adopting alternative poultry production practices to improve bird health and performance while decreasing AMU is imperative due to AMR concerns. In poultry production systems, complex environmental and genetic factors could contribute to the prevalence and spread of AMR and their related ARGs despite existence of correlations between AMU and AMR. In ABF and organic poultry productions, several antibiotic alternatives and vaccines are currently being applied. However, cost-effective benefits for most of the alternatives to antibiotics in poultry remain to be established. These alternative products appear to have pleotropic activities including antimicrobial, antioxidant, immune stimulatory and anti-inflammatory actions indicating that more investigations are required to determine their mechanism of action both against bacteria including their AMR profiles and birds. Overall this review indicates that AMR was present in poultry production systems that did not use any antimicrobials but a significant lower prevalence than in conventional poultry. However, more studies to investigate AMR in organic/ABF poultry production need to be done. Furthermore, understanding how feeding programs impact the commensal gut microbiota, pathogenic bacteria, and AMR will help guide dietary and bird health management practices. Accordingly, extensive efforts using integrative One Health approaches are imperative to breakdown the emergence and spread of AMR in poultry.

Availability of data and materials

Not applicable.

Abbreviations

AMU:

Antimicrobial use

AMR:

Antimicrobial resistance

GIT:

Gastrointestinal tract

ARG:

Antimicrobial resistance genes

NE:

Necrotic enteritis

ABF:

Antibiotic-free

NAE:

No antibiotic ever

RWA:

Raised without antibiotics

CIA:

Critically important antibiotics

CFC:

Chicken farmers of Canada

FOS:

Fructooligosaccharides

MOS:

Mannanoligosaccharides

SCFA:

Short-chain fatty acids

LBBP:

Low-bush blueberry pomace

NSP:

Non-starch polysaccharides

PBPs:

Penicillin-binding proteins

NAG:

N-acetylglucosamine

NAM:

β-(1–4)-N-acetylmuramic acid

BMD:

Bacitracin methylene disalicylate

BACN-Z:

Zinc-bacitracin

ExPEC:

Extraintestinal pathogenic E. coli

APEC:

Avian pathogenic E. coli

MDR:

Multi-drug resistance

MRSA:

Methicillin-resistant Staphylococcus aureus

VRSA:

Vancomycin-resistant Staphylococcus aureus

VRE:

Vancomycin-resistant Enterococcus faecium

References

  1. Food and Agriculture Organization of the United Nations. OECD-FAO Agricultural Outlook 2021–2030. Paris: Political Science: OECD; 2021. p. 337. (OECD-FAO Agricultural Outlook). https://doi.org/10.1787/19428846-en.

  2. Van Boeckel TP, Pires J, Silvester R, Zhao C, Song J, Criscuolo NG, et al. Global trends in antimicrobial resistance in animals in low- and middle-income countries. Science. 2019;365(6459). https://doi.org/10.1126/science.aaw1944.

  3. Diarra MS, Malouin F. Antibiotics in Canadian poultry productions and anticipated alternatives. Front Microbiol. 2014;5(282):1–15. https://doi.org/10.3389/fmicb.2014.00282.

    Article  Google Scholar 

  4. Rehman MA, Yin X, Zaheer R, Goji N, Amoako KK, McAllister T, et al. Genotypes and phenotypes of enterococci isolated from broiler chickens. Front Sustain Food Syst. 2018;2:1–28. https://doi.org/10.3389/fsufs.2018.00083.

    Article  Google Scholar 

  5. Rehman MA, Hasted TL, Persaud-Lachhman MG, Yin X, Carrillo C, Diarra MS. Genome analysis and multiplex PCR method for the molecular detection of coresistance to Cephalosporins and Fosfomycin in Salmonella enterica serovar Heidelberg. J Food Prot. 2019;82(11):1938–49. https://doi.org/10.4315/0362-028X.JFP-19-205.

  6. Pan D, Yu Z. Intestinal microbiome of poultry and its interaction with host and diet. Gut Microbes. 2014;5(1):108–19. https://doi.org/10.4161/gmic.26945.

    Article  Google Scholar 

  7. Diarra MS, Silversides FG, Diarrassouba F, Pritchard J, Masson L, Brousseau R, et al. Impact of feed supplementation with antimicrobial agents on growth performance of broiler chickens, Clostridium perfringens and Enterococcus counts, and antibiotic resistance phenotypes and distribution of antimicrobial resistance determinants in Escheric. Appl Environ Microbiol. 2007;73(20):6566–76. https://doi.org/10.1128/AEM.01086-07.

    Article  CAS  Google Scholar 

  8. Islam MR, Lepp D, Godfrey DV, Orban S, Ross K, Delaquis P, et al. Effects of wild blueberry (Vaccinium angustifolium) pomace feeding on gut microbiota and blood metabolites in free-range pastured broiler chickens. Poult Sci. 2019;98(9):3739–55. https://doi.org/10.3382/ps/pez062.

    Article  CAS  Google Scholar 

  9. McDevitt RM, Brooker JD, Acamovic T, Sparks NHC. Necrotic enteritis; a continuing challenge for the poultry industry. Worlds Poult Sci J. 2006;62(2):221–48. https://doi.org/10.1079/WPS200593.

    Article  Google Scholar 

  10. Collier CT, Van der Klis JD, Deplancke B, Anderson DB, Gaskins HR. Effects of tylosin on bacterial mucolysis, Clostridium perfringens colonization, and intestinal barrier function in a chick model of necrotic enteritis. Antimicrob Agents Chemother. 2003;47(10):3311–7. https://doi.org/10.1128/AAC.47.10.3311-3317.2003.

    Article  CAS  Google Scholar 

  11. Stutz MW, Lawton GC. Effects of diet and antimicrobials on growth, feed efficiency, intestinal Clostridium perfringens, and ileal weight of broiler chicks. Poult Sci. 1984;63(10):2036–42. https://doi.org/10.3382/ps.0632036.

    Article  CAS  Google Scholar 

  12. Timbermont L, Haesebrouck F, Ducatelle R, Van Immerseel F. Necrotic enteritis in broilers: an updated review on the pathogenesis. Avian Pathol. 2011;40(4):341–7. https://doi.org/10.1080/03079457.2011.590967.

    Article  CAS  Google Scholar 

  13. Soutter F, Werling D, Tomley FM, Blake DP. Poultry coccidiosis: design and interpretation of vaccine studies. Front Vet Sci. 2020;7:1–12. https://doi.org/10.3389/fvets.2020.00101.

    Article  Google Scholar 

  14. Lee JW, Kim DH, Kim YB, Jeong SB, Oh ST, Cho SY, et al. Dietary encapsulated essential oils improve production performance of coccidiosis-vaccine-challenged broiler chickens. Animals. 2020;10(481):481. https://doi.org/10.3390/ani10030481.

  15. Williams RB. Intercurrent coccidiosis and necrotic enteritis of chickens: rational, integrated disease management by maintenance of gut integrity. Avian Pathol. 2005;34(3):159–80. https://doi.org/10.1080/03079450500112195.

    Article  CAS  Google Scholar 

  16. Al-Sheikhly F, Al-Saieg A. Role of Coccidia in the occurrence of necrotic enteritis of chickens. Avian Dis. 1980;24(2):324–33. https://doi.org/10.2307/1589700.

    Article  CAS  Google Scholar 

  17. Smith JA. Experiences with drug-free broiler production. Poult Sci. 2011;90(11):2670–8. https://doi.org/10.3382/ps.2010-01032.

    Article  CAS  Google Scholar 

  18. Hajati H. Application of organic acids in poultry nutrition. Int Int J Avian Wildl Biol. 2018;3(4):324–9. https://doi.org/10.15406/ijawb.2018.03.00114.

    Article  Google Scholar 

  19. Smith JA. Broiler production without antibiotics: United States field perspectives. Anim Feed Sci Technol. 2019;250:93–8. https://doi.org/10.1016/j.anifeedsci.2018.04.027.

    Article  Google Scholar 

  20. Moore PR, Evenson A. Use of sulfasuxidine, streptothricin, and streptomycin in nutritional studies with the chick. J Biol Chem. 1946;165(2):437–41. https://doi.org/10.1016/s0021-9258(17)41154-9.

    Article  CAS  Google Scholar 

  21. Critically important antimicrobials for human medicine, 6th revision. Geneva: World Health Organization; 2019. Licence: CC BY-NC-SA 3.0 IGO.

  22. Poultry Health Today. Nearly 60% of US broilers now raised without antibiotics, but that number may have peaked. Available from: https://poultryhealthtoday.com/nearly-60-of-us-broilers-now-raised-without-antibiotics-but-that-number-may-have-peaked/ [cited 10 Jun 2021].

  23. Fanatico AC, Owens CM, Emmert JL. Organic poultry production in the United States: broilers. J Appl Poult Res. 2009;18(2):355–66. https://doi.org/10.3382/japr.2008-00123.

    Article  Google Scholar 

  24. Standards Council of Canada. Organic production systems: general principles and management standards. 2nd ed. Ottawa: Canadian General Standards Board: Standards Council of Canada; 2021. p. 75.

    Google Scholar 

  25. Berg C. Health and welfare in organic egg production. Acta Vet Scand. 2001;95:37–45.

    CAS  Google Scholar 

  26. Bailey JS, Cosby DE. Salmonella prevalence in free-range and certified organic chickens. J Food Prot. 2005;68(11):2451–3. https://doi.org/10.4315/0362-028X-68.11.2451.

  27. Miranda JM, Vázquez BI, Fenti CA, Calo-Mata P, Cepeda A, Franco CM. Comparison of antimicrobial resistance in Escherichia coli, Staphylococcus aureus, and listeria monocytogenes strains isolated from organic and conventional poultry meat. J Food Prot. 2008;71(12):2537–42. https://doi.org/10.4315/0362-028X-71.12.2537.

    Article  CAS  Google Scholar 

  28. Cobanoglu F, Kucukyilmaz K, Cinar M, Bozkurt M, Catli AU, Bintas E. Comparing the profitability of organic and conventional broiler production. Rev Bras Cienc Avic. 2014;16(4):403–10. https://doi.org/10.1590/1516-635x1604403-410.

    Article  Google Scholar 

  29. Rosenquist H, Boysen L, Krogh AL, Jensen AN, Nauta M. Campylobacter contamination and the relative risk of illness from organic broiler meat in comparison with conventional broiler meat. Int J Food Microbiol. 2013;162(3):226–30. https://doi.org/10.1016/j.ijfoodmicro.2013.01.022.

    Article  Google Scholar 

  30. Ritter GD, Acuff GR, Bergeron G, Bourassa MW, Chapman BJ, Dickson JS, et al. Antimicrobial-resistant bacterial infections from foods of animal origin: understanding and effectively communicating to consumers. Ann N Y Acad Sci. 2019;1441(1):40–9. https://doi.org/10.1111/nyas.14091.

    Article  Google Scholar 

  31. Adhikari P, Kiess A, Adhikari R, Jha R. An approach to alternative strategies to control avian coccidiosis and necrotic enteritis. J Appl Poult Res. 2020;29(2):515–34. https://doi.org/10.1016/j.japr.2019.11.005.

    Article  CAS  Google Scholar 

  32. Cervantes HM. Antibiotic-free poultry production: is it sustainable? J Appl Poult Res. 2015;24(1):91–7. https://doi.org/10.3382/japr/pfv006.

    Article  CAS  Google Scholar 

  33. Johnson TJ, Youmans BP, Noll S, Cardona C, Evans NP, Peter Karnezos T, et al. A consistent and predictable commercial broiler chicken bacterial microbiota in antibiotic-free production displays strong correlations with performance. Appl Environ Microbiol. 2018;84(12):1–18. https://doi.org/10.1128/AEM.00362-18.

    Article  Google Scholar 

  34. Fuller Afrc R. Probiotics in man and animals. J Appl Bacteriol. 1989;66(5):365–78. https://doi.org/10.1111/j.1365-2672.1989.tb05105.x.

    Article  Google Scholar 

  35. Patterson JA, Burkholder KM. Application of prebiotics and probiotics in poultry production. Poult Sci. 2003;82(4):627–31. https://doi.org/10.1093/ps/82.4.627.

    Article  CAS  Google Scholar 

  36. Jha R, Das R, Oak S, Mishra P. Probiotics (direct-fed microbials) in poultry nutrition and their effects on nutrient utilization, growth and laying performance, and gut health: a systematic review. Animals. 2020;10(10):1863. https://doi.org/10.3390/ani10101863.

  37. Khan RU, Naz S. The applications of probiotics in poultry production. Worlds Poult Sci J. 2013;69(3):621–32. https://doi.org/10.1017/S0043933913000627.

    Article  Google Scholar 

  38. Ricke SC. Impact of prebiotics on poultry production and food safety. Yale J Biol Med. 2018;91(2):151–9.

    CAS  Google Scholar 

  39. Ricke SC. Potential of fructooligosaccharide prebiotics in alternative and nonconventional poultry production systems. Poult Sci. 2015;94(6):1411–8. https://doi.org/10.3382/ps/pev049.

    Article  CAS  Google Scholar 

  40. Polycarpo GV, Andretta I, Kipper M, Cruz-Polycarpo VC, Dadalt JC, Rodrigues PHM, et al. Meta-analytic study of organic acids as an alternative performance-enhancing feed additive to antibiotics for broiler chickens. Poult Sci. 2017;96(10):3645–53. https://doi.org/10.3382/ps/pex178.

    Article  CAS  Google Scholar 

  41. Papatsiros VG, Katsoulos PD, Koutoulis KC, Karatzia M, Dedousi A, Christodoulopoulos G. Alternatives to antibiotics for farm animals. CAB Rev Ag Vet Sci Nutr Res. 2013;8:1–15. https://doi.org/10.1079/PAVSNNR20138032.

    Article  Google Scholar 

  42. Dibner JJ, Buttin P. Use of organic acids as a model to study the impact of gut microflora on nutrition and metabolism. J Appl Poult Res. 2002;11(4):453–63. https://doi.org/10.1093/japr/11.4.453.

    Article  CAS  Google Scholar 

  43. Mani-López E, García HS, López-Malo A. Organic acids as antimicrobials to control Salmonella in meat and poultry products. Food Res Int. 2012;45(2):713–21. https://doi.org/10.1016/j.foodres.2011.04.043.

    Article  CAS  Google Scholar 

  44. Van Immerseel F, Russell JB, Flythe MD, Gantois I, Timbermont L, Pasmans F, et al. The use of organic acids to combat Salmonella in poultry: A mechanistic explanation of the efficacy. Avian Pathol. 2006;35(3):182–8. https://doi.org/10.1080/03079450600711045.

    Article  CAS  Google Scholar 

  45. Ross KA, Ehret D, Godfrey D, Fukumoto L, Diarra M. Characterization of pilot scale processed Canadian organic cranberry (Vaccinium macrocarpon) and blueberry (Vaccinium angustifolium) juice pressing residues and phenolic-enriched extractives. Int J Fruit Sci. 2017;17(2):202–32. https://doi.org/10.1080/15538362.2017.1285264.

    Article  Google Scholar 

  46. Das Q, Islam MR, Lepp D, Tang J, Yin X, Mats L, et al. Gut microbiota, blood metabolites, and spleen immunity in broiler chickens fed berry pomaces and phenolic-enriched extractives. Front Vet Sci. 2020;7:1–19. https://doi.org/10.3389/fvets.2020.00150.

    Article  Google Scholar 

  47. Das Q, Tang J, Yin X, Ross K, Warriner K, Marcone MF, et al. Organic cranberry pomace and its ethanolic extractives as feed supplement in broiler: impacts on serum Ig titers, liver and bursal immunity. Poult Sci. 2021;100(2):517–26. https://doi.org/10.1016/j.psj.2020.09.044.

    Article  CAS  Google Scholar 

  48. Lund M, Jensen JD. A real options approach to biotechnology investment policy-the case of developing a Campylobacter vaccine to poultry. Prev Vet Med. 2016;128:58–69. https://doi.org/10.1016/j.prevetmed.2016.04.006.

    Article  Google Scholar 

  49. Adeola O, Cowieson AJ. Board-invited review: opportunities and challenges in using exogenous enzymes to improve nonruminant animal production. J Anim Sci. 2011;89(10):3189–218. https://doi.org/10.2527/jas.2010-3715.

    Article  CAS  Google Scholar 

  50. Kiarie E, Romero LF, Nyachoti CM. The role of added feed enzymes in promoting gut health in swine and poultry. Nutr Res Rev. 2013;26(1):71–88. https://doi.org/10.1017/S0954422413000048.

    Article  Google Scholar 

  51. Selle PH, Ravindran V. Microbial phytase in poultry nutrition. Anim Feed Sci Technol. 2007;135(1–2):1–41. https://doi.org/10.1016/j.anifeedsci.2006.06.010.

    Article  CAS  Google Scholar 

  52. Alagawany M, Abd El-Hack ME, Farag MR, Sachan S, Karthik K, Dhama K. The use of probiotics as eco-friendly alternatives for antibiotics in poultry nutrition. Environ Sci Pollut Res. 2018;25(11):10611–8. https://doi.org/10.1007/s11356-018-1687-x.

    Article  CAS  Google Scholar 

  53. Brenes A, Roura E. Essential oils in poultry nutrition: Main effects and modes of action. Anim Feed Sci Technol. 2010;158(1–2):1–14. https://doi.org/10.1016/j.anifeedsci.2010.03.007.

    Article  CAS  Google Scholar 

  54. Yang C, Kennes YM, Lepp D, Yin X, Wang Q, Yu H, et al. Effects of encapsulated cinnamaldehyde and citral on the performance and cecal microbiota of broilers vaccinated or not vaccinated against coccidiosis. Poult Sci. 2020;99(2):936–48. https://doi.org/10.1016/j.psj.2019.10.036.

    Article  CAS  Google Scholar 

  55. Panda AK, Reddy MR, Rama Rao SV, Praharaj NK. Production performance, serum/yolk cholesterol and immune competence of White Leghorn layers as influenced by dietary supplementation with probiotic. Trop Anim Health Prod. 2003;35(1):85–94. https://doi.org/10.1023/A:1022036023325.

    Article  CAS  Google Scholar 

  56. Chichlowski M, Croom J, McBride BW, Havenstein GB, Koci MD. Metabolic and physiological impact of probiotics or direct-fed-microbials on poultry: a brief review of current knowledge. Int J Poult Sci. 2007;6:694–704.

    Article  Google Scholar 

  57. Neijat M, Shirley RB, Barton J, Thiery P, Welsher A, Kiarie E. Effect of dietary supplementation of Bacillus subtilis DSM29784 on hen performance, egg quality indices, and apparent retention of dietary components in laying hens from 19 to 48 weeks of age. Poult Sci. 2019;98(11):5622–35. https://doi.org/10.3382/ps/pez324.

    Article  CAS  Google Scholar 

  58. Sohail MU, Hume ME, Byrd JA, Nisbet DJ, Shabbir MZ, Ijaz A, et al. Molecular analysis of the caecal and tracheal microbiome of heat-stressed broilers supplemented with prebiotic and probiotic. Avian Pathol. 2015;44(2):67–74. https://doi.org/10.1080/03079457.2015.1004622.

    Article  CAS  Google Scholar 

  59. Stecher B, Jung K. LACTATEing Salmonella: A host-derived fermentation product fuels pathogen growth. Cell Host Microbe. 2018;23(1):3–4. https://doi.org/10.1016/j.chom.2017.12.012.

    Article  CAS  Google Scholar 

  60. Lawhon SD, Maurer R, Suyemoto M, Altier C. Intestinal short-chain fatty acids alter Salmonella typhimurium invasion gene expression and virulence through BarA/SirA. Mol Microbiol. 2002;46(5):1451–64. https://doi.org/10.1046/j.1365-2958.2002.03268.x.

    Article  CAS  Google Scholar 

  61. Hasted TL, Sharif S, Boerlin P, Diarra MS. Immunostimulatory potential of fruits and their extracts in poultry. Front Immunol. 2021;12:1–11. https://doi.org/10.3389/fimmu.2021.641696.

    Article  CAS  Google Scholar 

  62. Yang C, Rehman MA, Yin X, Carrillo CD, Wang Q, Yang C, et al. Antimicrobial resistance phenotypes and genotypes of Escherichia coli isolates from broiler chickens fed encapsulated cinnamaldehyde and citral. J Food Prot. 2021;84(8):1385–99. https://doi.org/10.4315/JFP-21-033.

    Article  CAS  Google Scholar 

  63. Khattak F, Ronchi A, Castelli P, Sparks N. Effects of natural blend of essential oil on growth performance, blood biochemistry, cecal morphology, and carcass quality of broiler chickens. Poult Sci. 2014;93(1):132–7. https://doi.org/10.3382/ps.2013-03387.

    Article  CAS  Google Scholar 

  64. Alagawany M, Elnesr SS, Farag MR. The role of exogenous enzymes in promoting growth and improving nutrient digestibility in poultry. Iran J Vet Res. 2018;19(3):157–64.

    CAS  Google Scholar 

  65. Ramesh KR, Devegowda G, Khosravinia H. Effects of enzyme addition to broiler diets containing varying levels of double zero rapeseed meal. Asian Australas J Anim Sci. 2006;19(9):1354–60. https://doi.org/10.5713/ajas.2006.1354.

    Article  CAS  Google Scholar 

  66. Alagawany M, Attia A. Effects of feeding sugar beet pulp and Avizyme supplementation on performance, egg quality, nutrient digestion and nitrogen balance of laying Japanese quail. Avian Biol Res. 2015;8(2):79–88. https://doi.org/10.3184/175815515X14274754281188.

    Article  Google Scholar 

  67. Butaye P, Devriese LA, Haesebrouck F. Antimicrobial growth promoters used in animal feed: effects of less well known antibiotics on gram-positive bacteria. Clin Microbiol Rev. 2003;16(2):175–88. https://doi.org/10.1128/CMR.16.2.175-188.2003.

    Article  CAS  Google Scholar 

  68. Castanon JIR. History of the use of antibiotic as growth promoters in European poultry feeds. Poult Sci. 2007;86(11):2466–71. https://doi.org/10.3382/ps.2007-00249.

    Article  CAS  Google Scholar 

  69. Costa MC, Bessegatto JA, Alfieri AA, Weese JS, Filho JAB, Oba A. Different antibiotic growth promoters induce specific changes in the cecal microbiota membership of broiler chicken. PLoS One. 2017;12(2):1–13. https://doi.org/10.1371/journal.pone.0171642.

    Article  CAS  Google Scholar 

  70. Collignon PC, Conly JM, Andremont A, McEwen SA, Aidara-Kane A, Griffin PM, et al. World health organization ranking of antimicrobials according to their importance in human medicine: A critical step for developing risk management strategies to control antimicrobial resistance from food animal production. Clin Infect Dis. 2016;63(8):1087–93. https://doi.org/10.1093/cid/ciw475.

    Article  CAS  Google Scholar 

  71. De Oliveira DMP, Forde BM, Kidd TJ, Harris PNA, Schembri MA, Beatson SA, et al. Antimicrobial resistance in ESKAPE pathogens. Clin Microbiol Rev. 2020;33(3). https://doi.org/10.1128/CMR.00181-19.

  72. Shousha A, Awaiwanont N, Sofka D, Smulders FJM, Paulsen P, Szostak MP, et al. Bacteriophages isolated from chicken meat and the horizontal transfer of antimicrobial resistance genes. Appl Environ Microbiol. 2015;81(14):4600–6. https://doi.org/10.1128/AEM.00872-15.

    Article  CAS  Google Scholar 

  73. Yu T, Jiang X, Liang Y, Zhu Y, Tian J, Ying H, et al. Characterization and horizontal transfer of antimicrobial resistance genes and integrons in bacteria isolated from cooked meat products in China. J Food Prot. 2017;80(12):2048–55. https://doi.org/10.4315/0362-028X.JFP-17-119.

    Article  CAS  Google Scholar 

  74. Le Roux F, Blokesch M. Eco-evolutionary dynamics linked to horizontal gene transfer in vibrios. Annu Rev Microbiol. 2018;72:89–110. https://doi.org/10.1146/annurev-micro-090817-062148.

    Article  CAS  Google Scholar 

  75. Lode HM. Clinical impact of antibiotic-resistant gram-positive pathogens. Clin Microbiol Infect. 2009;15:212–7.

    Article  CAS  Google Scholar 

  76. Scott AM, Beller E, Glasziou P, Clark J, Ranakusuma RW, Byambasuren O, et al. Is antimicrobial administration to food animals a direct threat to human health? A rapid systematic review. Int J Antimicrob Agents. 2018;52(3):316–23. https://doi.org/10.1016/j.ijantimicag.2018.04.005.

    Article  CAS  Google Scholar 

  77. Silbergeld EK, Graham J, Price LB. Industrial food animal production, antimicrobial resistance, and human health. Annu Rev Public Health. 2008;29:151–69. https://doi.org/10.1146/annurev.publhealth.29.020907.090904.

    Article  Google Scholar 

  78. Marshall BM, Levy SB. Food animals and antimicrobials: impacts on human health. Clin Microbiol Rev. 2011;24(4):718–33. https://doi.org/10.1128/CMR.00002-11.

    Article  CAS  Google Scholar 

  79. Dutil L, Irwin R, Finley R, Ng LK, Avery B, Boerlin P, et al. Ceftiofur resistance in Salmonella enterica serovar Heidelberg from chicken meat and humans, Canada. Emerg Infect Dis. 2010;16(1):48–54. https://doi.org/10.3201/eid1601.090729.

    Article  Google Scholar 

  80. Food and Drug Administration. FDA releases annual summary report on antimicrobials sold or distributed in 2018 for use in food-producing animals. 2019. Available from: https://www.fda.gov/animal-veterinary/cvm-updates/fda-releases-annual-summary-report-antimicrobials-sold-or-distributed-2018-use-food-producing

    Google Scholar 

  81. Cogliani C, Goossens H, Greko C. Restricting antimicrobial use in food animals: lessons from Europe. Microbe. 2011;6:274–9. https://doi.org/10.1128/microbe.6.274.1.

    Article  Google Scholar 

  82. Xiao Y, Li L. China’s national plan to combat antimicrobial resistance. Lancet Infect Dis. 2016;16(11):1216–8. https://doi.org/10.1016/S1473-3099(16)30388-7.

    Article  Google Scholar 

  83. ECDC (European Centre for Disease Prevention and Control), EFSA (European Food Safety Authority), EMA (European Medicines Agency). Third joint inter-agency report on integrated analysis of consumption of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from humans and food-producing animals in the EU/EEA. EFSA J. 2021;19(6):6712. https://doi.org/10.2903/j.efsa.2021.6712.

    Article  CAS  Google Scholar 

  84. Hao H, Cheng G, Iqbal Z, Ai X, Hussain HI, Huang L, et al. Benefits and risks of antimicrobial use in food-producing animals. Front Microbiol. 2014;5:1–11. https://doi.org/10.3389/fmicb.2014.00288.

    Article  Google Scholar 

  85. Wolf H. Avilamycin, an inhibitor of the 30 S ribosomal subunits function. FEBS Lett. 1973;36(2):181–6. https://doi.org/10.1016/0014-5793(73)80364-3.

    Article  CAS  Google Scholar 

  86. Kofoed CB, Vester B. Interaction of avilamycin with ribosomes and resistance caused by mutations in 23S rRNA. Antimicrob Agents Chemother. 2002;46(11):3339–42. https://doi.org/10.1128/AAC.46.11.3339-3342.2002.

    Article  CAS  Google Scholar 

  87. Aarestrup FM, Jensen LB. Presence of variations in ribosomal protein L16 corresponding to susceptibility of enterococci to oligosaccharides (avilamycin and evernimicin). Antimicrob Agents Chemother. 2000;44(12):3425–7. https://doi.org/10.1128/AAC.44.12.3425-3427.2000.

    Article  CAS  Google Scholar 

  88. Petsaris O, Miszczak F, Gicquel-Bruneau M, Perrin-Guyomard A, Humbert F, Sanders P, et al. Combined antimicrobial resistance in enterococcus faecium isolated from chickens. Appl Environ Microbiol. 2005;71(5):2796–9. https://doi.org/10.1128/AEM.71.5.2796-2799.2005.

    Article  CAS  Google Scholar 

  89. Aarestrup FM, Bager F, Andersen JS. Association between the use of avilamycin for growth promotion and the occurrence of resistance among Enterococcus faecium from broilers: epidemiological study and changes over time. Microb Drug Resist. 2000;6(1):71–5. https://doi.org/10.1089/mdr.2000.6.71.

    Article  CAS  Google Scholar 

  90. Chauvin C, Gicquel-Bruneau M, Perrin-Guyomard A, Humbert F, Salvat G, Guillemot D, et al. Use of avilamycin for growth promotion and avilamycin-resistance among Enterococcus faecium from broilers in a matched case-control study in France. Prev Vet Med. 2005;70(3–4):155–63. https://doi.org/10.1016/j.prevetmed.2005.03.004.

    Article  CAS  Google Scholar 

  91. Pfaller MA. Flavophospholipol use in animals: positive implications for antimicrobial resistance based on its microbiologic properties. Diagn Microbiol Infect Dis. 2006;56(2):115–21. https://doi.org/10.1016/j.diagmicrobio.2006.03.014.

    Article  CAS  Google Scholar 

  92. Huber G, Nesemann G. Moenomycin, an inhibitor of cell wall synthesis. Biochem Biophys Res Commun. 1968;30(1):7–13. https://doi.org/10.1016/0006-291X(68)90704-3.

    Article  CAS  Google Scholar 

  93. Pavli V, Kmetec V. Pathways of chemical degradation of polypeptide antibiotic bacitracin. Biol Pharm Bull. 2006;29(11):2160–7. https://doi.org/10.1248/bpb.29.2160.

    Article  CAS  Google Scholar 

  94. Stone KJ, Strominger JL. Mechanism of action of bacitracin: complexation with metal ion and C 55 -isoprenyl pyrophosphate. Proc Natl Acad Sci U S A. 1971;68(12):3223–7. https://doi.org/10.1073/pnas.68.12.3223.

    Article  CAS  Google Scholar 

  95. Miles RD, Butcher GD, Henry PR, Littell RC. Effect of antibiotic growth promoters on broiler performance, intestinal growth parameters, and quantitative morphology. Poult Sci. 2006;85(3):476–85. https://doi.org/10.1093/ps/85.3.476.

    Article  CAS  Google Scholar 

  96. Attia YA, Bovera F, Abd El-Hamid AE, Tag El-Din AE, Al-Harthi MA, El-Shafy AS. Effect of zinc bacitracin and phytase on growth performance, nutrient digestibility, carcass and meat traits of broilers. J Anim Physiol Anim Nutr (Berl). 2016;100(3):485–91. https://doi.org/10.1111/jpn.12397.

    Article  CAS  Google Scholar 

  97. Diarra MS, Rempel H, Champagne J, Masson L, Pritchard J, Topp E. Distribution of antimicrobial resistance and virulence genes in enterococcus spp. and characterization of isolates from broiler chickens. Appl Environ Microbiol. 2010;76(24):8033–43. https://doi.org/10.1128/AEM.01545-10.

    Article  CAS  Google Scholar 

  98. Darnell RL, Nakatani Y, Knottenbelt MK, Gebhard S, Cook GM. Functional characterization of bcrr: A one-component transmembrane signal transduction system for bacitracin resistance. Microbiology (Reading). 2019;165(4):475–87. https://doi.org/10.1099/mic.0.000781.

    Article  CAS  Google Scholar 

  99. Miyazaki Y, Shibuya M, Sugawara H, Kawaguchi O, Hirose C, Nagatsu J, et al. Salinomycin, a new polyether antibiotic. J Antibiot (Tokyo). 1974;27(11):814–21. https://doi.org/10.7164/antibiotics.27.814.

    Article  CAS  Google Scholar 

  100. Wang Z, Zhou L, Xiong Y, Yu S, Li H, Fan J, et al. Salinomycin exerts anti-colorectal cancer activity by targeting the β-catenin/T-cell factor complex. Br J Pharmacol. 2019;176(17):3390–406. https://doi.org/10.1111/bph.14770.

    Article  CAS  Google Scholar 

  101. Mitani M, Yamanishi T, Miyazaki Y. Salinomycin: A new monovalent cation ionophore. Biochem Biophys Res Commun. 1975;66(4):1231–6. https://doi.org/10.1016/0006-291X(75)90490-8.

    Article  CAS  Google Scholar 

  102. Russell JB, Houlihan AJ. Ionophore resistance of ruminal bacteria and its potential impact on human health. FEMS Microbiol Rev. 2003;27(1):65–74. https://doi.org/10.1016/S0168-6445(03)00019-6.

    Article  CAS  Google Scholar 

  103. Brown K, Uwiera RRE, Kalmokoff ML, Brooks SPJ, Inglis GD. Antimicrobial growth promoter use in livestock: a requirement to understand their modes of action to develop effective alternatives. Int J Antimicrob Agents. 2017;49(1):12–24. https://doi.org/10.1016/j.ijantimicag.2016.08.006.

    Article  CAS  Google Scholar 

  104. Aarestrup FM, McNicholas PM. Incidence of high-level evernimicin resistance in Enterococcus faecium among food animals and humans. Antimicrob Agents Chemother. 2002;46(9):3088–90. https://doi.org/10.1128/AAC.46.9.3088-3090.2002.

    Article  CAS  Google Scholar 

  105. Boucher HW, Thauvin-Eliopoulos C, Loebenberg D, Eliopoulos GM. In vivo activity of evernimicin (SCH 27899) against methicillin-resistant Staphylococcus aureus in experimental infective endocarditis. Antimicrob Agents Chemother. 2001;45(1):208–11. https://doi.org/10.1128/AAC.45.1.208-211.2001.

    Article  CAS  Google Scholar 

  106. Fey PD, Safranek TJ, Rupp ME, Dunne EF, Ribot E, Iwen PC, et al. Ceftriaxone-resistant salmonella infection acquired by a child from cattle. N Engl J Med. 2000;342(17):1242–9. https://doi.org/10.1056/nejm200004273421703.

    Article  CAS  Google Scholar 

  107. Dunne EF, Fey PD, Kludt P, Reporter R, Mostashari F, Shillam P, et al. Emergence of domestically acquired ceftriaxone-resistant Salmonella infections associated with AmpC β-lactamase. J Am Med Assoc. 2000;284(24):3151–6. https://doi.org/10.1001/jama.284.24.3151.

    Article  CAS  Google Scholar 

  108. Torok VA, Allison GE, Percy NJ, Ophel-Keller K, Hughes RJ. Influence of antimicrobial feed additives on broiler commensal posthatch gut microbiota development and performance. Appl Environ Microbiol. 2011;77(10):3380–90. https://doi.org/10.1128/AEM.02300-10.

    Article  CAS  Google Scholar 

  109. Aarestrup FM, Seyfarth AM, Emborg HD, Pedersen K, Hendriksen RS, Bager F. Effect of abolishment of the use of antimicrobial agents for growth promotion on occurrence of antimicrobial resistance in fecal enterococci from food animals in Denmark. Antimicrob Agents Chemother. 2001;45(7):2054–9. https://doi.org/10.1128/AAC.45.7.2054-2059.2001.

    Article  CAS  Google Scholar 

  110. Diarrassouba F, Diarra MS, Bach S, Delaquis P, Pritchard J, Topp E, et al. Antibiotic resistance and virulence genes in commensal Escherichia coli and Salmonella isolates from commercial broiler chicken farms. J Food Prot. 2007;70(6):1316–27. https://doi.org/10.4315/0362-028X-70.6.1316.

    Article  CAS  Google Scholar 

  111. Zhao S, Li C, Mukherjee S, Hsu CH, Singh R, Gilbert J, et al. Complete genome sequences of two avilamycin-resistant Enterococcus faecium strains isolated from chicken in the United States. Microbiol Resour Announc. 2019;8(47):6–8. https://doi.org/10.1128/mra.00957-19.

    Article  Google Scholar 

  112. Varga C, Guerin MT, Brash ML, Slavic D, Boerlin P, Susta L. Antimicrobial resistance in fecal Escherichia coli and Salmonella enterica isolates: A two-year prospective study of small poultry flocks in Ontario, Canada. BMC Vet Res. 2019;15(1):1–10. https://doi.org/10.1186/s12917-019-2187-z.

    Article  CAS  Google Scholar 

  113. Diarra MS, Delaquis P, Rempel H, Bach S, Harlton C, Aslam M, et al. Antibiotic resistance and diversity of Salmonella enterica serovars associated with broiler chickens. J Food Prot. 2014;77(1):40–9. https://doi.org/10.4315/0362-028.JFP-13-251.

    Article  CAS  Google Scholar 

  114. Abay S, Kayman T, Otlu B, Hizlisoy H, Aydin F, Ertas N. Genetic diversity and antibiotic resistance profiles of Campylobacter jejuni isolates from poultry and humans in Turkey. Int J Food Microbiol. 2014;178:29–38. https://doi.org/10.1016/j.ijfoodmicro.2014.03.003.

    Article  CAS  Google Scholar 

  115. Perez-Boto D, Garcia-Peña FJ, Abad-Moreno JC, Echeita MA. Dynamics of populations of Campylobacter jejuni in two grandparent broiler breeder farms: persistent vs. transient strains. Vet Microbiol. 2012;159(1–2):204–11. https://doi.org/10.1016/j.vetmic.2012.03.042.

    Article  CAS  Google Scholar 

  116. Dan SD, Tăbăran A, Mihaiu L, Mihaiu M. Antibiotic susceptibility and prevalence of foodborne pathogens in poultry meat in Romania. J Infect Dev Ctries. 2015;9(1):035–41. https://doi.org/10.3855/jidc.4958.

    Article  CAS  Google Scholar 

  117. Pesciaroli M, Magistrali CF, Filippini G, Epifanio EM, Lovito C, Marchi L, et al. Antibiotic-resistant commensal Escherichia coli are less frequently isolated from poultry raised using non-conventional management systems than from conventional broiler. Int J Food Microbiol. 2020;314:108391. https://doi.org/10.1016/j.ijfoodmicro.2019.108391.

    Article  CAS  Google Scholar 

  118. Bernier-Lachance J, Arsenault J, Usongo V, Parent E, Labrie J, Jacques M, et al. Prevalence and characteristics of livestock- associated methicillin-resistant staphylococcus aureus (LA-MRSA) isolated from chicken meat in the province of Quebec, Canada. PLoS One. 2020;15(1):1–20. https://doi.org/10.1371/journal.pone.0227183.

    Article  CAS  Google Scholar 

  119. Lepp D, Roxas B, Parreira VR, Marri PR, Rosey EL, Gong J, et al. Identification of novel pathogenicity loci in Clostridium perfringens strains that cause avian necrotic enteritis. PLoS One. 2010;5(5). https://doi.org/10.1371/journal.pone.0010795.

  120. Charlebois A, Jalbert LA, Harel J, Masson L, Archambault M. Characterization of genes encoding for acquired bacitracin resistance in Clostridium perfringens. PLoS One. 2012;7(9):e44449. https://doi.org/10.1371/journal.pone.0044449.

    Article  CAS  Google Scholar 

  121. Borges KA, Furian TQ, De Souza SN, Menezes R, Salle CTP, De Souza Moraes HL, et al. Phenotypic and molecular characterization of Salmonella Enteritidis SE86 isolated from poultry and salmonellosis outbreaks. Foodborne Pathog Dis. 2017;14(12):742–54. https://doi.org/10.1089/fpd.2017.2327.

    Article  CAS  Google Scholar 

  122. Braga JFV, Chanteloup NK, Trotereau A, Baucheron S, Guabiraba R, Ecco R, et al. Diversity of Escherichia coli strains involved in vertebral osteomyelitis and arthritis in broilers in Brazil. BMC Vet Res. 2016;12(1):1–12. https://doi.org/10.1186/s12917-016-0762-0.

    Article  CAS  Google Scholar 

  123. Carvalho D, Finkler F, Grassotti TT, Kunert Filho HC, de Lima FES, Soares BD, et al. Antimicrobial susceptibility and pathogenicity of Escherichia coli strains of environmental origin. Ciência Rural. 2015;45(7):1249–55. https://doi.org/10.1590/0103-8478cr20141020.

    Article  CAS  Google Scholar 

  124. Duarte DAM, Ribeiro AR, Vasconcelos AMM, Santos SB, Silva JVD, de Andrade PLA, et al. Occurrence of Salmonella spp. in broiler chicken carcasses and their susceptibility to antimicrobial agents. Braz J Microbiol. 2009;40(3):569–73. https://doi.org/10.1590/S1517-83822009000300020.

    Article  Google Scholar 

  125. Gazal LES, Puno-Sarmiento JJ, Medeiros LP, Cyoia PS, Da Silveira WD, Kobayashi RKT, et al. Presence of pathogenicity islands and virulence genes of extraintestinal pathogenic Escherichia coli (ExPEC) in isolates from avian organic fertilizer. Poult Sci. 2015;94(12):3025–33. https://doi.org/10.3382/ps/pev278.

    Article  CAS  Google Scholar 

  126. Lima-Filho JV, Martins LV, de Nascimento DCO, Ventura RF, Batista JEC, Silva AFB, et al. Zoonotic potential of multidrug-resistant extraintestinal pathogenic Escherichia coli obtained from healthy poultry carcasses in Salvador, Brazil. Braz J Infect Dis. 2013;17(1):54–61. https://doi.org/10.1016/j.bjid.2012.09.004.

    Article  Google Scholar 

  127. Palmeira A, dos Santos LR, Borsoi A, Rodrigues LB, Calasans M, do Nascimento VP. Serovars and antimicrobial resistance of Salmonella spp. isolated from Turkey and broiler carcasses in southern Brazil between 2004 and 2006. Rev Inst Med Trop Sao Paulo. 2016;58(1):1–6. https://doi.org/10.1590/S1678-9946201658019.

    Article  Google Scholar 

  128. Stella AE, de Oliveira MC, da Fontana VLDS, Maluta RP, Borges CA, de Ávila FA. Characterization and antimicrobial resistance patterns of Escherichia coli isolated from feces of healthy broiler chickens. Arq Inst Biol (Sao Paulo). 2016;83(0):1–5. https://doi.org/10.1590/1808-1657000392014.

    Article  Google Scholar 

  129. Vaz RV, Gouveia GV, Andrade NMJ, da Costa MM, Lima-Filho JV. Phylogenetic characterization of serum plus antibiotic-resistant extraintestinal Escherichia coli obtained from the liver of poultry carcasses in Pernambuco. Pesqui Vet Bras. 2017;37(10):1069–73. https://doi.org/10.1590/S0100-736X2017001000005.

    Article  Google Scholar 

  130. Quesada A, Ugarte-Ruiz M, Iglesias MR, Porrero MC, Martínez R, Florez-Cuadrado D, et al. Detection of plasmid mediated colistin resistance (MCR-1) in Escherichia coli and Salmonella enterica isolated from poultry and swine in Spain. Res Vet Sci. 2016;105:134–5. https://doi.org/10.1016/j.rvsc.2016.02.003.

    Article  CAS  Google Scholar 

  131. de Jong A, Stephan B, Silley P. Fluoroquinolone resistance of Escherichia coli and Salmonella from healthy livestock and poultry in the EU. J Appl Microbiol. 2012;112(2):239–45. https://doi.org/10.1111/j.1365-2672.2011.05193.x.

    Article  CAS  Google Scholar 

  132. European Food Safety Authority EC for DP and C. The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2017. EFSA J. 2019;17(2). https://doi.org/10.2903/j.efsa.2019.5598.

  133. Davis GS, Waits K, Nordstrom L, Grande H, Weaver B, Papp K, et al. Antibiotic-resistant Escherichia coli from retail poultry meat with different antibiotic use claims. BMC Microbiol. 2018;18(1):1–7. https://doi.org/10.1186/s12866-018-1322-5.

    Article  CAS  Google Scholar 

  134. Sanchez HM, Whitener VA, Thulsiraj V, Amundson A, Collins C, Duran-Gonzalez M, et al. Antibiotic resistance of escherichia coli isolated from conventional, no antibiotics, and humane family owned retail broiler chicken meat. Animals. 2020;10(12):1–17. https://doi.org/10.3390/ani10122217.

    Article  Google Scholar 

  135. Liljebjelke KA, Hofacre CL, White DG, Ayers S, Lee MD, Maurer JJ. Diversity of antimicrobial resistance phenotypes in Salmonella isolated from commercial poultry farms. Front Vet Sci. 2017;4:1–9. https://doi.org/10.3389/fvets.2017.00096.

    Article  Google Scholar 

  136. Luangtongkum T, Jeon B, Han J, Plummer P, Logue CM, Zhang Q. Antibiotic resistance in Campylobacter: emergence, transmission and persistence. Future Microbiol. 2009;4(2):189–200. https://doi.org/10.2217/17460913.4.2.189.

    Article  CAS  Google Scholar 

  137. Johnson JR, Sannes MR, Croy C, Johnston B, Clabots C, Kuskowski MA, et al. Antimicrobial drug-resistant Escherichia coli from humans and poultry products, Minnesota and Wisconsin, 2002-2004. Emerg Infect Dis. 2007;13(6):838–46. https://doi.org/10.3201/eid1306.061576.

    Article  CAS  Google Scholar 

  138. Nair DVT, Venkitanarayanan K, Johny AK. Antibiotic-resistant Salmonella in the food supply and the potential role of antibiotic alternatives for control. Foods. 2018;7(10). https://doi.org/10.3390/foods7100167.

  139. Zhao S, Mukherjee S, Chen Y, Li C, Young S, Warren M, et al. Novel gentamicin resistance genes in Campylobacter isolated from humans and retail meats in the USA. J Antimicrob Chemother. 2014;70(5):1314–21. https://doi.org/10.1093/jac/dkv001.

    Article  CAS  Google Scholar 

  140. Yang X, Huang J, Zhang Y, Liu S, Chen L, Xiao C, et al. Prevalence, abundance, serovars and antimicrobial resistance of Salmonella isolated from retail raw poultry meat in China. Sci Total Environ. 2020;713(100):136385. https://doi.org/10.1016/j.scitotenv.2019.136385.

    Article  CAS  Google Scholar 

  141. Chen X, Naren GW, Wu CM, Wang Y, Dai L, Xia LN, et al. Prevalence and antimicrobial resistance of Campylobacter isolates in broilers from China. Vet Microbiol. 2010;144(1–2):133–9. https://doi.org/10.1016/j.vetmic.2009.12.035.

    Article  CAS  Google Scholar 

  142. Jiang HX, Lü DH, Chen ZL, Wang XM, Chen JR, Liu YH, et al. High prevalence and widespread distribution of multi-resistant Escherichia coli isolates in pigs and poultry in China. Vet J. 2011;187(1):99–103. https://doi.org/10.1016/j.tvjl.2009.10.017.

    Article  Google Scholar 

  143. Wang Y, Xu C, Zhang R, Chen Y, Shen Y, Hu F, et al. Changes in colistin resistance and mcr-1 abundance in Escherichia coli of animal and human origins following the ban of colistin-positive additives in China: an epidemiological comparative study. Lancet Infect Dis. 2020;20(10):1161–71. https://doi.org/10.1016/S1473-3099(20)30149-3.

    Article  CAS  Google Scholar 

  144. Sapkota AR, Kinney EL, George A, Hulet RM, Cruz-Cano R, Schwab KJ, et al. Lower prevalence of antibiotic-resistant Salmonella on large-scale U.S. conventional poultry farms that transitioned to organic practices. Sci Total Environ. 2014;476–477:387–92. https://doi.org/10.1016/j.scitotenv.2013.12.005.

    Article  CAS  Google Scholar 

  145. Bailey M, Taylor R, Brar J, Corkran S, Velásquez C, Novoa-Rama E, et al. Prevalence and antimicrobial resistance of Salmonella from antibiotic-free broilers during organic and conventional processing. J Food Prot. 2020;83(3):491–6. https://doi.org/10.4315/0362-028X.JFP-19-269.

    Article  Google Scholar 

  146. Bailey MA, Taylor RM, Brar JS, Corkran SC, Velásquez C, Novoa Rama E, et al. Prevalence and antimicrobial resistance of Campylobacter from antibiotic-free broilers during organic and conventional processing. Poult Sci. 2019;98(3):1447–54. https://doi.org/10.3382/ps/pey486.

    Article  CAS  Google Scholar 

  147. Huijbers PMC, van Hoek AHAM, Graat EAM, Haenen APJ, Florijn A, Hengeveld PD, et al. Methicillin-resistant Staphylococcus aureus and extended-spectrum and AmpC β-lactamase-producing Escherichia coli in broilers and in people living and/or working on organic broiler farms. Vet Microbiol. 2015;176(1–2):120–5. https://doi.org/10.1016/j.vetmic.2014.12.010.

    Article  Google Scholar 

  148. Kilonzo-Nthenge A, Brown A, Nahashon SN, Long D. Occurrence and antimicrobial resistance of enterococci isolated from organic and conventional retail chicken. J Food Prot. 2015;78(4):760–6. https://doi.org/10.4315/0362-028X.JFP-14-322.

    Article  CAS  Google Scholar 

  149. Miller SI. Antibiotic resistance and regulation of the gram-negative bacterial outer membrane barrier by host innate immune molecules. MBio. 2016;7(5):5–7. https://doi.org/10.1128/mBio.01541-16.

    Article  Google Scholar 

  150. Bonnet C, Diarrassouba F, Brousseau R, Masson L, Topp E, Diarra MS. Pathotype and antibiotic resistance gene distributions of Escherichia coli isolates from broiler chickens raised on antimicrobial-supplemented diets. Appl Environ Microbiol. 2009;75(22):6955–62. https://doi.org/10.1128/AEM.00375-09.

    Article  CAS  Google Scholar 

  151. Dho-moulin M, Fairbrother JM. Avian pathogenic Escherichia coli (APEC). Vet Res. 1999;30:299–316.

    CAS  Google Scholar 

  152. Nolan LK, Vaillancourt JP, Barbieri NL, Logue CM. Colibacillosis. In: Swayne DE, editor. Diseases of poultry. 14th ed. Hoboken: Wiley; 2020. p. 770–830. https://doi.org/10.1002/9781119371199.ch18.

  153. Jørgensen SL, Stegger M, Kudirkiene E, Lilje B, Poulsen LL, Ronco T, et al. Diversity and population overlap between avian and human Escherichia coli belonging to sequence type 95. mSphere. 2019;4(1). https://doi.org/10.1128/msphere.00333-18.

  154. Poirel L, Madec JY, Lupo A, Schink AK, Kieffer N, Nordmann P, et al. Antimicrobial resistance in Escherichia coli. Aarestrup FM, Schwarz S, Shen J, Cavaco L, editors. Microbiol Spectr. 2018;6(4):979–80. https://doi.org/10.1128/microbiolspec.ARBA-0026-2017.

    Article  Google Scholar 

  155. Fairchild AS, Smith JL, Idris U, Lu J, Sanchez S, Purvis LB, et al. Effects of orally administered tetracycline on the intestinal community structure of chickens and on tet determinant carriage by commensal bacteria and Campylobacter jejuni. Appl Environ Microbiol. 2005;71(10):5865–72. https://doi.org/10.1128/AEM.71.10.5865-5872.2005.

    Article  CAS  Google Scholar 

  156. Eibach D, Dekker D, Gyau Boahen K, Wiafe Akenten C, Sarpong N, Belmar Campos C, et al. Extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in local and imported poultry meat in Ghana. Vet Microbiol. 2018;217:7–12. https://doi.org/10.1016/j.vetmic.2018.02.023.

    Article  Google Scholar 

  157. Simmons K, Islam MR, Rempel H, Block G, Topp E, Diarra MS. Antimicrobial resistance of Escherichia fergusonii isolated from broiler chickens. J Food Prot. 2016;79(6):929–38. https://doi.org/10.4315/0362-028X.JFP-15-575.

    Article  CAS  Google Scholar 

  158. Yang H, Yu Y, Fu C, Chen F. Bacterial acid resistance toward organic weak acid revealed by RNA-seq transcriptomic analysis in acetobacter pasteurianus. Front Microbiol. 2019;10:1–14. https://doi.org/10.3389/fmicb.2019.01616.

    Article  Google Scholar 

  159. Canadian antimicrobial resistance surveillance system report. Canadian antimicrobial resistance surveillance system - Update 2020. 2020.

  160. Center for Disease Control and Prevention. Drug-resistant nontyphoidal Salmonella (2019). Available from: https://www.cdc.gov/drugresistance/pdf/threats-report/nt-salmonella-508.pdf [cited 20 May 2020].

    Google Scholar 

  161. Rehman MA, Yin X, Persaud-Lachhman MG, Diarra MS. First detection of a fosfomycin resistance gene, fosA7, in Salmonella enterica serovar Heidelberg isolated from broiler chickens. Antimicrob Agents Chemother. 2017;61(8):1–6. https://doi.org/10.1128/AAC.00410-17.

    Article  Google Scholar 

  162. Walker GK, Suyemoto MM, Hull DM, Gall S, Jimenez F, Chen LR, et al. Genomic characterization of a Nalidixic acid-resistant Salmonella Enteritidis strain causing persistent infections in broiler chickens. Front Vet Sci. 2021;8:1–8. https://doi.org/10.3389/fvets.2021.725737.

    Article  Google Scholar 

  163. Gad AH, Abo-Shama UH, Harclerode KK, Fakhr MK. Prevalence, serotyping, molecular typing, and antimicrobial resistance of Salmonella isolated from conventional and organic retail ground poultry. Front Microbiol. 2018;9:1–10. https://doi.org/10.3389/fmicb.2018.02653.

    Article  Google Scholar 

  164. Yin X, M’ikanatha NM, Nyirabahizi E, McDermott PF, Tate H. Antimicrobial resistance in non-Typhoidal Salmonella from retail poultry meat by antibiotic usage-related production claims – United States, 2008–2017. Int J Food Microbiol. 2021;342:109044. https://doi.org/10.1016/j.ijfoodmicro.2021.109044.

    Article  CAS  Google Scholar 

  165. Allos BM. Campylobacter jejuni infections: update on emerging issues and trends. Clin Infect Dis. 2001;32(8):1201–6. https://doi.org/10.1086/319760.

    Article  CAS  Google Scholar 

  166. Dramé O, Leclair D, Parmley EJ, Deckert A, Ouattara B, Daignault D, et al. Antimicrobial resistance of Campylobacter in broiler chicken along the food chain in Canada. Foodborne Pathog Dis. 2020;17(8):512–20. https://doi.org/10.1089/fpd.2019.2752.

    Article  CAS  Google Scholar 

  167. Nelson JM, Chiller TM, Powers JH, Angulo FJ. Fluoroquinolone-resistant Campylobacter species and the withdrawal of fluoroquinolones from use in poultry: A public health success story. Clin Infect Dis. 2007;44(7):977–80. https://doi.org/10.1086/512369.

    Article  CAS  Google Scholar 

  168. Gharbi M, Béjaoui A, Ben Hamda C, Jouini A, Ghedira K, Zrelli C, et al. Prevalence and antibiotic resistance patterns of campylobacter spp. isolated from broiler chickens in the north of Tunisia. Biomed Res Int. 2018;2018. https://doi.org/10.1155/2018/7943786.

  169. Noormohamed A, Fakhr MK. Prevalence and antimicrobial susceptibility of Campylobacter spp. in Oklahoma conventional and organic retail poultry. Open Microbiol J. 2014;8(1):130–7. https://doi.org/10.2174/1874285801408010130.

    Article  Google Scholar 

  170. Wang Y, Dong Y, Deng F, Liu D, Yao H, Zhang Q, et al. Species shift and multidrug resistance of Campylobacter from chicken and swine, China, 2008-14. J Antimicrob Chemother. 2016;71(3):666–9. https://doi.org/10.1093/jac/dkv382.

    Article  CAS  Google Scholar 

  171. Liu D, Liu W, Lv Z, Xia J, Li X, Hao Y, et al. Emerging Erm(B)-mediated macrolide resistance associated with novel multidrug resistance genomic islands in Campylobacter. Antimicrob Agents Chemother. 2019;63(7). https://doi.org/10.1128/AAC.00153-19.

  172. Hansson I, Ellström P, Nilsson O, Chaba M, Skarin M, Fernström LL, et al. Differences in genotype and antimicrobial resistance between Campylobacter spp. isolated from organic and conventionally produced chickens in Sweden. Pathogens. 2021;10(12). https://doi.org/10.3390/pathogens10121630.

  173. Huber L, Agunos A, Gow SP, Carson CA, Van Boeckel TP. Reduction in antimicrobial use and resistance to Salmonella, Campylobacter, and Escherichia coli in broiler chickens, Canada, 2013-2019. Emerg Infect Dis. 2021;27(9):2434–44. https://doi.org/10.3201/eid2709.204395.

    Article  CAS  Google Scholar 

  174. Cardinal KM, Kipper M, Andretta I, Ribeiro AML. Withdrawal of antibiotic growth promoters from broiler diets: performance indexes and economic impact. Poult Sci. 2019;98(12):6659–67. https://doi.org/10.3382/ps/pez536.

    Article  CAS  Google Scholar 

  175. Silhavy TJ, Kahne D, Walker S. The bacterial cell envelope. Cold Spring Harb Perspect Biol. 2010;2(5):a000414. https://doi.org/10.1101/cshperspect.a000414.

    Article  CAS  Google Scholar 

  176. Miranda JM, Guarddon M, Mondragón A, Vázquez BI, Fente CA, Cepeda A, et al. Antimicrobial resistance in Enterococcus spp. strains isolated from organic chicken, conventional chicken, and Turkey meat: a comparative survey. J Food Prot. 2007;70(4):1021–4. https://doi.org/10.4315/0362-028X-70.4.1021.

    Article  CAS  Google Scholar 

  177. Buzón-Durán L, Capita R, Alonso-Calleja C. Microbial loads and antibiotic resistance patterns of Staphylococcus aureus in different types of raw poultry-based meat preparations. Poult Sci. 2017;96(11):4046–52. https://doi.org/10.3382/ps/pex200.

    Article  CAS  Google Scholar 

  178. Maccallum WG, Hastings TW. A case of acute endocarditis caused by micrococcus zymogenes (nov. spec.), with a description of the microorganism. J Exp Med. 1899;4(5–6):521–34. https://doi.org/10.1084/jem.4.5-6.521.

    Article  CAS  Google Scholar 

  179. Moellering RC. Emergence of enterococcus as a significant pathogen. Clin Infect Dis. 1992;14(6):1173–6 https://doi.org/https://www.jstor.org/stable/4456494.

    Article  Google Scholar 

  180. Jung A, Chen LR, Suyemoto MM, Barnes HJ, Borst LB. A review of Enterococcus cecorum infection in poultry. Avian Dis. 2018;62(3):261–71. https://doi.org/10.1637/11825-030618-Review.1.

    Article  Google Scholar 

  181. Arias CA, Murray BE. The rise of the Enterococcus: beyond vancomycin resistance. Nat Rev Microbiol. 2012;10(4):266–78. https://doi.org/10.1038/nrmicro2761.

    Article  CAS  Google Scholar 

  182. Kelesidis T. The zoonotic potential of daptomycin non-susceptible enterococci. Zoonoses Public Health. 2015;62(1):1–6. https://doi.org/10.1111/zph.12091.

    Article  CAS  Google Scholar 

  183. Aarestrup FM, Bager F, Jensen NE, Madsen M, Meyling A, Wegener HC. Surveillance of antimicrobial resistance in bacteria isolated from food animals to antimicrobial growth promoters and related therapeutic agents in Denmark. Apmis. 1998;106(6):606–22. https://doi.org/10.1111/j.1699-0463.1998.tb01391.x.

    Article  CAS  Google Scholar 

  184. Mann PA, Xiong L, Mankin AS, Chau AS, Mendrick CA, Najarian DJ, et al. EmtA, a rRNA methyltransferase conferring high-level evernimicin resistance. Mol Microbiol. 2001;41(6):1349–56. https://doi.org/10.1046/j.1365-2958.2001.02602.x.

    Article  CAS  Google Scholar 

  185. Hershberger E, Donabedian S, Konstantinou K, Zervos MJ. Quinupristin-dalfopristin resistance in gram-positive bacteria: mechanism of resistance and epidemiology. Clin Infect Dis. 2004;38(1):92–8. https://doi.org/10.1086/380125.

    Article  CAS  Google Scholar 

  186. McDermott PF, Cullen P, Hubert SK, McDermott SD, Bartholomew M, Simjee S, et al. Changes in antimicrobial susceptibility of native Enterococcus faecium in chickens fed virginiamycin. Appl Environ Microbiol. 2005;71(9):4986–91. https://doi.org/10.1128/AEM.71.9.4986-4991.2005.

    Article  CAS  Google Scholar 

  187. Kim YJ, Park JH, Seo KH. Comparison of the loads and antibiotic-resistance profiles of Enterococcus species from conventional and organic chicken carcasses in South Korea. Poult Sci. 2018;97(1):271–8. https://doi.org/10.3382/ps/pex275.

    Article  CAS  Google Scholar 

  188. Bannerman TL. Staphylococcus, Micrococcus, and other catalase-positive cocci that grow aerobically. In: Murray P, Baron E, Jorgensen J, Pfaller M, Yolken R, editors. Manual of clinical microbiology. 8th ed. Washington DC: American Society for Microbiology; 2003. p. 384–404.

    Google Scholar 

  189. Park S, Ronholm J. Staphylococcus aureus in agriculture: lessons in evolution from a multispecies pathogen. Clin Microbiol Rev. 2021;34(2). https://doi.org/10.1128/CMR.00182-20.

  190. Persoons D, Van Hoorebeke S, Hermans K, Butaye P, de Kruif A, Haesebrouck F, et al. Methicillin-resistant Staphylococcus aureus in poultry. Emerg Infect Dis. 2009;15(3):452–3. https://doi.org/10.3201/eid1503.080696.

    Article  Google Scholar 

  191. Kim YB, Seo KW, Jeon HY, Lim SK, Lee YJ. Characteristics of the antimicrobial resistance of Staphylococcus aureus isolated from chicken meat produced by different integrated broiler operations in Korea. Poult Sci. 2018;97(3):962–9. https://doi.org/10.3382/ps/pex357.

    Article  CAS  Google Scholar 

  192. Amoako DG, Somboro AM, Abia ALK, Molechan C, Perrett K, Bester LA, et al. Antibiotic resistance in Staphylococcus aureus from poultry and poultry products in uMgungundlovu district, South Africa, using the “farm to fork” approach. Microb Drug Resist. 2020;26(4):402–11. https://doi.org/10.1089/mdr.2019.0201.

    Article  CAS  Google Scholar 

  193. Nemati M, Hermans K, Lipinska U, Denis O, Deplano A, Struelens M, et al. Antimicrobial resistance of old and recent Staphylococcus aureus isolates from poultry: first detection of livestock-associated methicillin-resistant strain ST398. Antimicrob Agents Chemother. 2008;52(10):3817–9. https://doi.org/10.1128/AAC.00613-08.

    Article  CAS  Google Scholar 

  194. Vela J, Hildebrandt K, Metcalfe A, Rempel H, Bittman S, Topp E, et al. Characterization of Staphylococcus xylosus isolated from broiler chicken barn bioaerosol. Poult Sci. 2012;91(12):3003–12. https://doi.org/10.3382/ps.2012-02302.

    Article  CAS  Google Scholar 

  195. Anju K, Karthik K, Divya V, Mala Priyadharshini ML, Sharma RK, Manoharan S. Toxinotyping and molecular characterization of antimicrobial resistance in Clostridium perfringens isolated from different sources of livestock and poultry. Anaerobe. 2021;67:102298. https://doi.org/10.1016/j.anaerobe.2020.102298.

    Article  CAS  Google Scholar 

  196. Silva ROS, Salvarani FM, Assis RA, Martins NRS, Pires PS, Lobato FCF. Antimicrobial susceptibility of Clostridium perfringens strains isolated from broiler chickens. Braz J Microbiol. 2009;40(2):262–4. https://doi.org/10.1590/s1517-83822009000200010.

    Article  CAS  Google Scholar 

  197. Devriese LA, Daube G, Hommez J, Haesebrouck F. In vitro susceptibility of Clostridium perfringens isolated from farm animals to growth-enhancing antibiotics. J Appl Bacteriol. 1993;75(1):55–7. https://doi.org/10.1111/j.1365-2672.1993.tb03407.x.

    Article  CAS  Google Scholar 

  198. Archambault M, Rubin JE. Antimicrobial resistance in Clostridium and Brachyspira spp. and other anaerobes. Microbiol Spectr. 2020;8(1). https://doi.org/10.1128/microbiolspec.arba-0020-2017.

  199. Osman KM, Elhariri M. Antibiotic resistance of Clostridium perfringens isolates from broiler chickens in Egypt. OIE Rev Sci Tech. 2013;32(3):841–50. https://doi.org/10.20506/rst.32.2.2212.

    Article  CAS  Google Scholar 

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Acknowledgements

The authors would like to thank X. Yin and Q. Das (GRDC, AAFC, Guelph, ON) for providing assistance and trainings.

Funding

This work was supported by Agriculture and Agri-Food Canada to M.S. Diarra through the Genomics Research and Development Initiative (PSS #1858 J-001262) and A-Base (PSS #3441, J-002363) projects on “Mitigating Antimicrobial Resistance”.

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MSD (principal investigator) conceptualized the review design. PM and MAR wrote the review with major contributions of MSD, ET and EGK. MSD provided overall guidance, mentorship, and resources throughout the scope of this review. All authors approved this work for publication.

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Mak, P.H.W., Rehman, M.A., Kiarie, E.G. et al. Production systems and important antimicrobial resistant-pathogenic bacteria in poultry: a review. J Animal Sci Biotechnol 13, 148 (2022). https://doi.org/10.1186/s40104-022-00786-0

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