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Review

Staphylococcus aureus and MRSA in Livestock: Antimicrobial Resistance and Genetic Lineages

by
Vanessa Silva
1,2,3,4,
Sara Araújo
1,2,
Andreia Monteiro
1,
José Eira
1,
José Eduardo Pereira
1,5,6,
Luís Maltez
1,5,6,
Gilberto Igrejas
2,3,4,
Teresa Semedo Lemsaddek
6,7,* and
Patricia Poeta
1,5,6,*
1
Microbiology and Antibiotic Resistance Team (MicroART), Department of Veterinary Sciences, University of Trás-os-Montes and Alto Douro (UTAD), 5000-801 Vila Real, Portugal
2
Department of Genetics and Biotechnology, University of Trás-os-Montes and Alto Douro (UTAD), 5000-801 Vila Real, Portugal
3
Functional Genomics and Proteomics Unit, University of Trás-os-Montes and Alto Douro (UTAD), 5000-801 Vila Real, Portugal
4
Associated Laboratory for Green Chemistry (LAQV-REQUIMTE), University NOVA of Lisboa, 1099-085 Lisbon, Portugal
5
Veterinary and Animal Research Centre (CECAV), University of Trás-os-Montes and Alto Douro (UTAD), 5000-801 Vila Real, Portugal
6
Associate Laboratory for Animal and Veterinary Sciences (AL4AnimalS), University of Trás-os-Montes and Alto Douro (UTAD), 5000-801 Vila Real, Portugal
7
Centro de Investigação Interdisciplinar em Sanidade Animal (CIISA), Faculdade de Medicina Veterinária, Av. Universidade Técnica de Lisboa, 1300-477 Lisboa, Portugal
*
Authors to whom correspondence should be addressed.
Microorganisms 2023, 11(1), 124; https://doi.org/10.3390/microorganisms11010124
Submission received: 21 December 2022 / Revised: 27 December 2022 / Accepted: 30 December 2022 / Published: 3 January 2023
(This article belongs to the Special Issue Pathogens and Antimicrobial Drug Resistance in the Food Chain)
Review Reports Versions Notes

Abstract

:
Animal production is associated with the frequent use of antimicrobial agents for growth promotion and for the prevention, treatment, and control of animal diseases, thus maintaining animal health and productivity. Staphylococcus aureus, in particular methicillin-resistant S. aureus (MRSA), can cause a variety of infections from superficial skin and soft tissue infections to life-threatening septicaemia. S. aureus represents a serious public health problem in hospital and community settings, as well as an economic and animal welfare problem. Livestock-associated MRSA (LA-MRSA) was first described associated with the sequence (ST) 398 that was grouped within the clonal complex (CC) 398. Initially, LA-MRSA strains were restricted to CC398, but over the years it has become clear that its diversity is much greater and that it is constantly changing, a trend increasingly associated with multidrug resistance. Therefore, in this review, we aimed to describe the main clonal lineages associated with different production animals, such as swine, cattle, rabbits, and poultry, as well as verify the multidrug resistance associated with each animal species and clonal lineage. Overall, S. aureus ST398 still remains the most common clone among livestock and was reported in rabbits, goats, cattle, pigs, and birds, often together with spa-type t011. Nevertheless, a wide diversity of clonal lineages was reported worldwide in livestock.

1. Staphylococci—An Overview

Staphylococci are Gram-positive cocci-shaped cells arranged in irregular clusters similar to grape clusters [1]. Although S. aureus is the major bacterium of its genus, more than 50 Staphylococcus species are registered in the List of Prokaryotic Names with Standing in Nomenclature database [2]. These bacteria are facultative anaerobes, catalase positive and salt (NaCl) tolerant [3]. The Staphylococcus genus is divided in two main groups, the coagulase-negative staphylococci (CoNS) and coagulase-positive staphylococci (CoPS). Staphylococcus species were first characterized by Friedrich Rosenbach, who established that yellow/orange colonies corresponded to CoPS species and white colonies to CoNS [4]. In general, staphylococci are natural inhabitants of skin and mucous membranes of human beings and animals, while the prevalence of species varies widely according to the host [2]. However, they can cause various types of infections ranging from skin infections to severe infections like necrotizing pneumonia or sepsis [5]. Staphylococci tolerate a wide range of temperatures, from 7 to 40 ℃, and survive under unfavourable conditions like dryness and dehydration, making them a persistent and widespread pathogen in the environment [3]. Among Staphylococci, Staphylococcus aureus and Staphylococcus epidermidis are the most frequently isolated species of the CoPS and CoNS groups, respectively, which is why S. epidermidis is the species most focused on in CoNS studies [4]. Staphylococcus aureus has been the major pathogen associated with nosocomial infections in humans [1]. However, more recently, infections caused by CoNS like S. epidermidis, S. haemolyticus and S. saprophyticus have emerged in hospitals [6]. Moreover, although to a lesser extent, CoNS are known to colonize both farm and domestic animals. For instance, several bovine mastitis infections associated with CoNS have increasingly been reported over the years [7,8,9]. CoNS have also been detected as contaminants in food products [10,11,12,13] becoming more frequent and harmful to both animals and humans, affecting public health and taking a huge economic burden.

2. Methicillin-Resistant Staphylococci

Penicillin is an antibiotic in the β-lactam family. It was introduced in clinical practice in 1941 and, only a year later, penicillin resistance in S. aureus was described. Ten years later, more than half of the isolates in large hospitals were already resistant to penicillin [14]. The need to create compounds resistant to the action of β-lactamases produced by staphylococci led to the development of other antimicrobials such as methicillin. However, shortly after the introduction of this antibiotic, methicillin-resistant S. aureus (MRSA) was isolated [15]. MRSA is now recognized as a high-priority pathogen according to the World Health Organization (WHO), since an emergence of these strains has been observed [16]. The mechanism of resistance to methicillin is based on the synthesis of a new penicillin-binding protein (PBP), the PBP2a, with little affinity for methicillin and other β-lactams, which blocks the arrival of the antibiotic at its target site and thus creates resistance [17]. The mecA gene is the main gene responsible for resistance to methicillin. This gene is found on the genetic loci called staphylococcal cassette chromosome mec (SCCmec). The expression of the mecA gene depends on two genes, mecR1, which regulates transcription, and mecI, which encodes the repressor protein [18]. There are two other mechanisms that result in weak resistance to methicillin and oxacillin in which the presence of the mecA gene is not clear. Strains with modifications in the affinity of PBP 1, 3, and 4 exhibit weak resistance to methicillin, and strains that hyper-produce β-lactamases have a limited resistance to oxacillin [19]. Although the mecA gene is the most common PBP2a-encoding gene, recently, the detection of a new mec gene was reported. mecC is part of the SCCmec type XI and has been detected in both S. aureus and CoNS in animal and environmental samples [20,21]. Two less frequent mec genes have been described, mecB and mecD, both detected in Macrococcus caseolyticus, although the mecB gene has been recently reported in S. aureus [22,23].
Staphylococcus spp. have the ability to quickly acquire resistance to antibiotics. This started with the first strains resistant to penicillin reported a few years after its introduction. The successive introduction of other antibiotics, such as macrolides, tetracycline, and chloramphenicol, had a similar result: that is, the rapid appearance of resistant strains which, in turn, led to the proliferation and dissemination of bacteria with a broad spectrum of resistance and a remarkable ability to survive in different environments [24,25]. One interesting fact about most of these strains is that they are generally resistant to β-lactams [26]. Different species have a wide range of antibiotic resistances and monoresistant and multiresistant strains have been found in the environment, in particular in the aquatic environment [27].

2.1. Mechanisms of Antibiotic Resistance in S. aureus

Antimicrobials are substances that inhibit or eliminate the growth of microorganisms and are therefore commonly used in the treatment and prevention of infections. They can be classified as bactericidal or bacteriostatic. Bactericidal drugs act by directly eliminating the microorganism, while bacteriostatic drugs inhibit bacterial growth and multiplication [28]. Among the main groups of bactericidal antibiotics are aminoglycosides, β-lactams, fluoroquinolones, and glycopeptides, while lincosamides, oxazolidinones, and macrolides are some of the drugs with bacteriostatic action [29].
Bacterial resistance to antimicrobials can be manifested through several mechanisms such as inhibition of cell wall synthesis, inhibition of cytoplasmic membrane synthesis or damage, inhibition of protein synthesis in ribosomes, changes in the synthesis of nucleic acids, and alteration of cellular metabolisms [30]. The resistance of bacteria to antibiotics can have an intrinsic typology, depending a lot on the typical and specific biology of the bacterium, or extrinsic, through horizontal gene transfer, where there is the acquisition of new genes, transported by plasmids, transposons, integrons, or bacteriophages, also known as phages [31].
Genetic alterations promoted by the mechanisms described here may provide bacteria with the ability to carry out certain biochemical mechanisms such as: enzymatic inactivation, efflux pumps, or target modification which can be specific for different classes of antimicrobials, as shown in Table 1 [32,33].

2.2. Virulence Factors in S. aureus

S. aureus is one of the first pathogens described and remains one of the most common causes of life-threatening infections of the bloodstream, skin, soft tissues, and even the lower respiratory tract, and serious deep-seated infections such as endocarditis, mastitis, and osteomyelitis [34]. The degree of pathogenicity of S. aureus depends on several components of the bacterial surface and extracellular proteins. The expression of most virulence factors in S. aureus is controlled by the agr locus (accessory gene regulator) which encodes a two-component signaling pathway whose activation ligand is a bacterial density sensor peptide (autoinducer peptide) which is also encoded by agr [35]. Thus, the agr system is directly involved in controlling the expression of virulence factors in S. aureus [35].
Four hemolysins have been identified: alpha, beta, gamma, and delta. They have hemolytic and cytolytic capacity and act on some cells of the host such as macrophages, leukocytes and fibroblasts. α-hemolysin is the most studied. It is responsible for the hemolysis zone observed around the S. aureus colonies and has its effect on eukaryotic cell membranes and erythrocytes. β-hemolysin is an active sphingomyelinase that acts on different cells, and γ and δ hemolysins, found in some strains of S. aureus, have the ability to lyse a variety of different cells [36]. Only 5–10% of S. aureus produce exfoliative toxins. Two serotypes of exfoliative toxins have been reported, A and B, which are biochemically and immunologically different, but with similar biological functions [37]. Exfoliative toxin A is chromosomal encoded whereas B is plasmid encoded. Both have proteolytic activity, dissolve the mucopolysaccharide matrix of the epidermis, and act as superantigens [38]. Enterotoxins are responsible for food poisoning with emesis and enterocolitis symptoms and are produced by 30–50% of S. aureus strains [39]. Toxic shock toxin is a thermostable protein synthesized by chromosomal genes. They are considered superantigens since they are capable of producing the massive proliferation of T lymphocytes and thus the production of cytokines, which leads to toxic shock syndrome [38]. Panton–Valentine’s leucocidin is a cytolytic toxin and is formed by two proteins, LukS-PV and LukF-PV, which form pores across the membrane of leukocytes causing efflux of the cell content, leading to lysis [40].

3. The Issue of Antimicrobial Resistance in Livestock

In animal production farms, the main goal is to raise healthy animals for food consumption by humans. In such places, animals should be provided with good nutrition, a clean and dry environment, good ventilation, and supervision by veterinarians [41]. Just like in humans, animals get sick with bacterial infections and need antibiotic treatment. Treatment of sick animals with antibiotics is of prime importance because sometimes there are no other alternatives, and that is the only choice to stop the illness spreading to the rest of the herd or flock, promoting animal welfare, and contributing to food safety. However, antibiotics have been used for a long time for non-medical purposes. In subtherapeutic levels, these medicines improve growth rate, reduce mortality and morbidity, and improve reproductive performance in production animals, allowing industries to achieve a highly efficient production [41]. Besides all the benefits provided by antibiotics with respect to animal health and welfare, the continuous use of those medications at low levels brings risks to public health due to the emergence of resistant microorganisms.
In low-middle-income countries, antimicrobials are frequently used as prophylactic drugs in animal production. Because of the easy access to these medicines and their non-restricted use, antimicrobial consumption in the animal production system almost double human consumption [42]. In developing countries unqualified animal healthcare providers play a significant role in this problematic situation [42].
The use of antibiotics in food animals for purposes of disease treatment and prevention and growth promotion are frequently associated with the global rise of AR. In fact, estimated global antibiotic consumption in 2010 was 63,151 ± 1, 560 tons and it is estimated that, by 2030, this number will increase by 67% [43,44].
In order to promote responsible use of antibiotics, international and national guidelines are available with the purpose of ensuring therapeutic efficacy and mitigating antimicrobial resistance. However, compliance with such guidelines is very variable among countries.
Most of the literature focuses on the risks of bacteria resistance directly transferred from production animals to people, affecting public health. However, the consequences of antibiotic resistance of animal origin are beyond that. In production animals, the bacterial diseases can bring on, behind all the suffering, huge economic losses. In several species, respiratory and enteric diseases are very common, while in others—like cows, goats and, sheep and other animals kept for milk production—mastitis is the major problem [45]. Because these infections are contagious, the problem grows when animals are kept in large groups and close to each other. In aquaculture, bacterial diseases are also important because the animals, such as fish and shrimps, are raised in large numbers with close contact [45].
The first cases of antibiotic resistance in food animals were observed in turkeys in 1951, after streptomycin was fed to those animals [46]. Since then, resistance to antibiotics, such as tetracyclines, sulfonamides, β-lactams, and penicillin, have increasingly been observed [43].
In terms of public health, two major routes of antimicrobial-resistant bacteria transmission to humans exist. They are direct acquisition through contact with food producing infected animals or indirect acquisition through the food chain or via exposure to niches with high antimicrobial pollution [47]. Several studies have found a high prevalence rate of antimicrobial resistance among individuals like farm workers and veterinarians that have a close relationship with food-producing animals [48,49,50].
Relative to environmental pollution caused by antibiotics in animal-producing sectors, it is known that only a small amount of the administered antibiotics participates in animal metabolism and are effectively used [51]. In fact, it is estimated that 30–90% of antibiotics are excreted in animal urine or faeces in the form of main metabolites [52]. High concentrations of these metabolites can enter the soil and water environment in various ways, causing pollution to the ecological environment [52]. Subsequently, the microbial species that occupy the soil or water will suffer a selective pressure that results in the emergence of antibiotic-resistant phenotypes. It is a very similar process that occurs when we talk about the antibiotic use in agriculture. If these phenotypes emerge on a mobile genetic element, like a plasmid, they can be horizontally transmitted to animals or humans, which may pose a considerable public health threat [47].
Taken together, it can be assumed that the use of antibiotics in animal settings, specifically their massive use for growth promotion, can lead to the emergence of antibiotic-resistant bacteria. That will affect not only animal wellbeing, but also public health, because humans interact directly or indirectly with them. Finally, the economic burden from antimicrobial resistance is still a problem worldwide.

4. Staphylococcus aureus in Livestock

In this review article, we gathered information from studies that detected and characterized S. aureus in pigs, goats, horses, sheep, buffaloes, cattle, rabbits, and poultry. LA-MRSA isolates are genetically distinct from human isolates. Table 2 presents a general summary of the molecular characteristics of LA-MRSA clones worldwide.
Although few, some studies investigated the presence of S. aureus in rabbits (Table 3). A study carried out by Ruiz-Ripa et al., in rabbits from Spain, in which nasal and rectal samples from 103 mammals were analysed, detected the presence of three mecC-positive MRSA isolated from rabbits, which belonged to the ST130 clonal lineage, the complex clonal CC130 and the spa-type t843; in addition, they showed resistance to cefoxitin and penicillin [53]. Another study also carried out in rabbits in China analysed 691 samples (lung, mastitis, and foot dermatitis) and isolated S. aureus strains belonging to clonal strains ST121 and ST398. In addition, most isolates had a multidrug-resistance phenotype showing resistance to many antimicrobials such as streptomycin, kanamycin, gentamicin, penicillin, ciprofloxacin, and azithromycin, even though the samples were collected from different provinces in China. Regarding virulence, S. aureus isolates had the genes encoding for the virulence factors hla, hlb, clfA, clfB, and fnbpA [54]. A less recent study, carried out by Holmes et al. in the United Kingdom, more specifically in England and Scotland, reported a wide variety of genetic lineages among S. aureus isolated from rabbits: ST30, CC30, ST3126, CC291, ST15, CC15, ST6, CC6, ST3120, ST121, CC425, CC121, ST3092, ST39, ST2257, and CC22. Regarding spa-types, the following were detected: t021, t1614, t2574, t5413, t13114, t645, t15410, t15409, and t1977 [55]. The S. aureus isolates from the same study were mostly susceptible to the antimicrobials tested, with some isolates showing resistance to penicillin, fusidic acid, tetracycline, and fluroquinolones encoded by the genes blaZ, tet (38), and norA. On the other hand, a high diversity of virulence genes were found among the isolates: fnbA, fnbB, sdrD, sdrE, efb, cna, sea, seb, sei, sen, seo, seg, sep, tst, sak, and scn [55]. Indrawattana et al. carried out a study in rabbits in Thailand, in which 67 purulent samples were studied. From these samples, different S. aureus strains were isolated and were ascribed to ST4209, ST4212, and ST4213. Furthermore, resistances to penicillin, aminoglycosides, and lincosamides were detected in S. aureus isolates conferred by the blaZ, mecA, aacA-aphD, and mrs (A) genes [56]. Another study conducted in Portugal by Silva et al. investigated the presence of MRSA in 66 purulent samples from rabbits. Most isolates were ascribed to ST2855 and spa type t1190. Nevertheless, other genetic lineages were also identified including CC97, ST105, CC5, ST5, ST582, CC15, ST22, CC22, ST1, and CC1 and spa types t002, t2802, t1094, t084, t032, and t1491 [57]. In the same study article, the authors also reported the presence of strains showing a multidrug-resistant phenotype with resistance to cefoxitin, penicillin, tetracycline, erythromycin, clindamycin, gentamicin, tobramycin, ciprofloxacin, and fusidic acid associated with the mecA, tet (K), tet (L), erm (B), msr (A/B), linB, erm (C), vgaB, vgaA, aac (6′)-Ie-aph (2′’)-Ia genes. Finally, in that study, the presence of the virulence genes hlb, cna and etA, as well as the immune evasion cluster (IEC) type B and C-related genes scn, chp, and sak, was also detected [57]. In a study carried out with rabbits from Spain and Portugal, 240 samples were analysed. These samples were recovered from mastitis (n = 86), skin abscesses (n = 33), pododermatitis (n = 31), dermatitis (n = 21), otitis (n = 13), metritis (n = 12), peritonitis (n = 2), conjunctivitis (n = 11), pneumonia (n = 9), rhinitis (n = 3), hepatitis (n = 3), osteomyelitis (n = 1), pericarditis (n = 1), and nasal samples (n = 14). Among these samples, the prevalence of MRSA varied between 4.8% and 100% and the isolates were ascribed to ST146, ST398, ST2855, and ST4774 [58]. Some MRSA isolates carried the mecC gene, which confers resistance to methicillin, and were also ascribed to SCCmec types IV, V, and III. Regarding resistance and virulence, MRSA isolates presented a wide variety of resistances, including resistance to vancomycin, and some isolates were categorized as IEC type E [58].
Table
Table 3. Molecular characteristics of LA-MRSA clones in different continents [22].
Table 3. Molecular characteristics of LA-MRSA clones in different continents [22].
AnimalLocationClonal LineagesVirulenceReferences
MLSTspa TypeIEC TypesOutros Genes
RabbitsChinaST121, ST398 nuc, hla, hlb, clfA, clfB, fnbpA[54]
EnglandST30, ST3126, ST15, ST6t021, t1614, t2574, t5413 fnbA, efb, cna, sea, seb, sei, sen, sea, sep, tsst, sak, scn, sdrD, sdrE, efb[55]
ScotlandST3120, ST121, ST3092, ST39, ST2257,t13114, t645, t15410, t15409, t1977 fnbA, fnbB, sdrD, sdrE, cna, sea, sec, sei, sen, sep[55]
ThailandST4209, ST4212, ST4213 [56]
SwitzerlandCC5, CC7, CC8, CC15, CC96, CC101, CC121, ST890t160, t179, t8456, t14871, t091, t681, t4770, t085, t745, t1190, t056, t741, t1773 sea, sea, seb, sed, egc, sej, ser[59]
PortugalST2855, ST105, ST5, ST582, ST22, ST1t1190, t002, t2802, t2802, t1094, t084, t032, t1491B, Chlb, can, eta, cna[57]
SpainST146, ST398, ST2855, ST4774 E [58]
PortugalST2855 [58]
GoatKoreaST72, ST398t324, t571, t324, t664 lukED, seg, sei, sem, sen, seo, seq[60]
Greece t1336 [61]
IranST97, ST522/2057, ST2079, CC5, CC522,t267, t1534, t7305, t5428 [62]
SheepGreece t3586 [61]
Czech RepublicST398t011 [63]
IranST522/2057, ST130, CC522, CC130t1534, t16958, t12270 [62]
CattleGreece t3586 [61]
Czech RepublicST398, ST361, ST1t011, t034, t2346, t1255, t315, t127 [63]
Czech RepublicST398t011 [63]
IranST6, ST15, ST291, CC5, CC398t304, t084, t937 [62]
IndiaST5220 [64]
BuffaloPhilippinesST2454, ST9t091, t800 [65]
PigsItalyCC97, CC398t1730, t899, t4795 [66]
Northern IrelandST30, ST398t749, t011 lukM, lukF-P38[67]
ItalyST398, ST9, ST97, ST1t011, t034, t899, t1451, t1456, t4474, t588, t1793, t4795, t1730, t9301, t127 [67]
Czech RepublicST398t011, t034, t2123, t2346, t4661 [63]
Latvia t011, t1333, t808, t808, t400, t400, t1580, t1985, t2383 [68]
SwitzerlandST752, ST398t011, t034 [69]
ItalyST398t899, t034, t011 [70]
DenmarkCC398t034, t011 [71]
SpainST398t011, t034, t2346, t108, t1197, t1456, t1451 [72]
PolandST398, ST9, ST433, ST12, ST2950t011, t034, t108, t4389, t318, t1580, t1928, t4387, t1255, t337, t1430, t8893, t5817, t021, t156, t005 seg, sei[73]
FinlandCC1, CC398t127, t1381, t011, t034, t108, t2741 [74]
ItalyST398t011, t108, t899, t034, t571, t1606, t5524, t1793, t10485, t2876 [75]
PigletsPortugalST398, ST1t011, t1451, t108, t1491 hla, hlb, hld, hlg, hlgy[76]
ChickensBelgiumST398, ST239t011, t037, t899 [77]
DenmarkST398, ST8, ST5, ST1t011, t108, t008/, t347, t002, t034, t273 [78]
Switzerland [79]
The NetherlandsST398t011, t034, t108, t899, t3015 [80]
ItalyST612, ST8, ST30t1257, t018 [81]
Egypt [82]
South Africa [83]
Chickens and turkeysGermanyST398, ST9, ST5, ST1791t011, t034, t899, t023, t6574 lukD, lukE,
hla, hlb, cna, fib		[84]
Switzerland t011, t034 [85]
The USAST5, ST6, ST8, ST15, ST406, ST544, ST699, ST398 [86]
Chickens, turkeys and geesePolandST398, ST5t002, t034, t214, t436, t127, t912, t663, t1422 egc1, seh[87]
QuailsPortugalST398, ST6831t011, t9747 hla, hlb, hld, scn[88]
DucksThe NetherlandsST398t011 [89]
TurkeysGermanyST398t011, t002, t1456, t034 [90]
Abbreviations. MLST: multilocus sequence typing; IEC: immune invasion cluster; ST: sequence type.
Regarding samples from cattle, in a study carried out in Korea by Mechesso et al., nasal samples (n = 431) and carcass samples (n = 50) of goats were analysed. Among the samples, a prevalence of 1.2% of MRSA was detected and the strains belonged to ST72, ST398, spa types t324, t571, and t664 and SCCmec types IV and V. Finally, some virulence genes were identified including lukED, seg, sei, sem, sen, seo, and seq [60]. Another study, carried out by Papadopoulos et al., in cows (n = 89), sheep (n = 104), and goats (n = 84), reported a prevalence of MRSA that varied between 1.10% and 2.90%. The isolates were ascribed to spa types t3586 and t1336 and showed resistance to penicillin, oxacillin, sulfamethoxazole-trimethoprim, gentamicin, kanamycin, and tetracycline [61]. In the Czech Republic, a study was carried out in cattle (n = 34), goats (n = 38), and sheep (n = 25), in which the prevalence of MRSA was between 0.6% and 11.30%, the isolates belonged mainly to ST398, ST361, and ST1 and the spa types t011, t034, t2346, t1255, and t315 [63]. A study conducted by Dastmalchi Saei et al., with goats (n = 10), cows (n = 9), and sheep (n = 8) samples from Iran detected S. aureus isolated belonging to ST6, ST15, ST291, CC5, CC398, ST522, ST2057, ST130, CC522, CC130, ST97, ST2079, CC522 and spa types t304, t084, t937, t1534, t16958, t12270, t267, t7305, and t5428. In addition, the isolates showed resistance to penicillin, erythromycin, clindamycin, and tetracycline [62]. Finally, another study conducted with cattle from Indian samples reported the detection of one S. aureus isolate which belonged to ST5220 and SCCmec V [64].
The presence of S. aureus and MRSA in the swine population was widely studied. In a study carried out in pigs in Italy, there was a prevalence of MRSA of 51.40% mostly associated with CC97, CC398 and spa types t1730, t899, and t4795. In addition, the MRSA strains showed resistance to cefoxitin, gentamicin, clindamycin, tetracycline, rifampicin, enrofloxacin, and erythromycin and carried the virulence genes clfA, lukE, cna, lukE-lukD, and fmtB [66]. In 2016, several studies associated with the detection and characterization of S. aureus in pigs were published. One of these studies was carried out in Northern Ireland, in which the clonal lineage ST30, the spa type t749 and SCCmec Vt were detected among S. aureus isolates. Regarding antimicrobial resistance, the strains showed resistance mainly to penicillin and tetracycline and carried the blaZ and tet (K) genes. On the other hand, with regard to virulence, the lukM and lukF-P38 genes were detected [67]. Another study carried out in 2016 in Ireland reported that all pig isolates belonged to CC398, spa types t034 and t011 and SCCmec Vt. In addition, some isolates were multidrug resistant and harboured the blaZ, erm (A), erm (B), aacA-aphD, aadD, tet (K), tet (M), tet (L), fexA, dfrG, and dfrK genes [91]. Another study conducted in Spain, more specifically in Catalonia, reported a prevalence of MRSA between 10% and 80% among pigs, with ST398 being the only sequence type detected. The isolates were ascribed to the spa types t011, t034, t2346, t108, t1197, t1456, and t1451. Finally, MRSA isolates were reported to be resistant to tetracycline, clindamycin, ciprofloxacin, erythromycin, gentamicin, tobramycin, and sulfamethoxazole-trimethoprim [72]. Another study carried out in Finland showed the presence of S. aureus CC1 and CC398, spa types t127, t1381, t011, t034, t2741, and t108, SCCmec V in pigs. These isolates also showed resistance to multiple antimicrobial classes conferred by the mecA, bla (Z), tet (K), tet (M), aadD, and erm (B) genes [74]. Other studies have been conducted in pigs with MRSA and S. aureus isolates being mostly associated with ST398 (CC398), and spa type t011, SCCmec type V and resistance to tetracycline [63,68,69,70,71,73,75]. A study conducted with piglets in Portugal revealed a prevalence of MRSA of between 98% and 100%. Once again, the clonal lineage ST398 and the spa types t011 and t108 were detected. Furthermore, all isolates were resistant to tetracycline and some were resistant to erythromycin, clindamycin, sulfamethoxazole-trimethoprim, and gentamicin [92]. In a study conducted in Poland, S. aureus isolated from pig samples were ascribed to a high diversity of genetic lineages including CC398, ST398, CC30, ST433, CC9, ST9, CC12, ST12, CC22, ST2950, spa types t011, t034, t108, t4389, t318, t1580, t1928, t4387, t1255, t337, t1430, t8893, t5817, t021, t156, and t005, and SCCmec types V (5C2&5), V (5C2), and IV (2B) [71]. In another study performed with pig samples from Italy, several different genetic lineages were also detected in MRSA isolates: ST398, ST9, ST97, ST1, the spa types t011, t034, t899 t1451, t1456, t4474, t588, t1793, t4795, t1730, t9301 and t127, and SCCmec V and IVa [93].
Regarding birds, a few studies conducted worldwide reported the presence of MRSA strains among food-producing birds including chickens, turkeys, geese, and ducks. MRSA CC398 was the most frequent clone detected in several countries across Europe in ducks, chickens, and turkeys (Table 3). Most strains from birds showed a multidrug-resistant profile showing resistance mostly to tetracycline, oxacillin, erythromycin, clindamycin, kanamycin, gentamicin, ciprofloxacin, chloramphenicol, and sulfamethoxazole trimethoprim. In the study of Nemeghaire et al., only 0.8% of chicken samples were colonized by MRSA in Belgium. However, the strains carried resistance to a wide range of antimicrobial classes and belonged to ST398 and ST239 and spa types t011, t037, and t899 [77]. In another study conducted in chickens in Denmark, the frequency of MRSA detection among chicken samples was 4%. S. aureus strains belonged to ST398, ST8, ST5, and ST1, and spa types t011, t108, t008, t347, t002, t034, and t273. Regarding the antimicrobial resistance, the isolates were resistant to tetracycline, erythromycin, clindamycin, and ciprofloxacin [78]. Feßler et al. reported a moderate prevalence (37.2%) of MRSA in chickens and turkeys in Germany. The isolates were ascribed mostly to ST398 but also to ST9, ST5, and ST1791, and spa types t011, t034, t899, t023, and t6574. MRSA isolates harboured several virulence genes (lukD, lukE, hla, hlb, can, and fib) and showed resistance to clindamycin, erythromycin, tetracycline, and enrofloxacin [84]. In another study conducted in Germany with chickens and turkeys, several different clonal lineages were detected among the MRSA isolates: ST398, ST5, ST9, ST7, and ST15, and spa types t002, t1430, t011, and t034. These MRSA isolates showed resistance to several isolates and a wide diversity of genes encoding virulence factors were also detected, namely, seg/i, selm/n/o/u, lukF/S/hlgA, lukD/E, sea, lukF/S/hlgA, and sak [94]. In a more recent study, Silva et al. investigated the prevalence of MRSA in quails. Among the 100 samples tested, 29 were colonized by MRSA. Most strains belonged to ST398 and spa type t011 and the remaining isolates were ascribed to ST6831 and spa type t9747. All MRSA from quails were multidrug-resistant including resistance to penicillin, ciprofloxacin, erythromycin, clindamycin, tetracycline, aminoglycosides, chloramphenicol, and fusidic acid [88]. In the USA, Waters et al. showed that 54.1% of chickens and turkeys carried MRSA strains which were ascribed to several lineages: ST5, ST6, ST8, ST15, ST406, ST544, ST699, and ST398; however, the spa type was not investigated. The isolates also showed resistance to erythromycin, oxacillin, penicillin, tetracycline, and vancomycin [86]. In 2019, Amoako et al. carried out a study in chickens from South Africa and reported a 20% frequency of MRSA carriage with resistance to cefoxitin, clindamycin, erythromycin, gentamycin, penicillin, and tetracycline. Nevertheless, the genetic lineages were not investigated [83].
As shown in previous studies, MRSA ST2855 is the most prevalent clonal lineage in rabbits. Moreover, MRSA ST2855 has only been reported in studies carried out in wild hares and farm rabbits. Regarding the spa type, none showed a significant prevalence. In cattle, MRSA ST398 was the most prevalent, in addition to MRSA ST9 and ST72. MRSA ST398 was initially detected in pigs, however, later it was also detected in companion and food chain animals, as well as in humans, mainly in those who perform professions in which they have frequent contact with animals [95,96]. MRSA ST9 has already been described as a cause of infections in humans and animals, in addition to that it is constantly related to pigs [93,97,98]. Finally, MRSA ST72 is included in the CC8 clonal complex and is found throughout the community and hospitals [99,100]. The most prevalent spa types in pigs were t664, t011, and t800. Regarding the studies carried out in pigs, the MRSA that showed a higher prevalence was ST398, which was initially isolated in pigs; later it was isolated in several other animals and even in humans, as previously mentioned. The most prevalent spa type was t011, mostly associated with ST398. In Europe, the ST398 clonal lineage is the most frequent lineage detected in MRSA from poultry. Of the 16 studies presented with birds, this lineage was found in 14 (87.5%), followed by ST5 and ST8 (30% and 40%, respectively) [101,102,103]. Resistance among S. aureus from birds is very high particularly to penicillin and methicillin; these two antimicrobials are used in most of the studies presented here.
This acquisition of antimicrobial resistance effectively presents a major challenge for the medical world, in human and veterinary terms, regarding the treatment and control of MRSA and S. aureus infections.

Author Contributions

Conceptualization, V.S.; validation, P.P., J.E.P. and L.M.; investigation, V.S. and S.A.; data curation, J.E.; writing—original draft preparation, V.S., S.A. and A.M.; writing—review and editing, V.S.; supervision, G.I., T.S.L. and P.P. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Associate Laboratory for Green Chemistry-LAQV, which is financed by national funds from FCT/MCTES (UIDB/50006/2020 and UIDP/50006/2020) and by the projects UIDB/CVT/00772/2020 and LA/P/0059/2020 funded by the Portuguese Foundation for Science and Technology (FCT). This research was funded by CIISA—Centro de Investigação Interdisciplinar em Sanidade Animal, Faculdade de Medicina Veterinária, Universidade de Lisboa, Project UIDB/00276/2020 (funded by FCT—Fundação para a Ciência e Tecnologia IP). Teresa Semedo-Lemsaddek is financially supported by national funds through FCT under the Transitional Standard—DL57/2016/CP1438/CT0004.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Silva, V.; Caniça, M.; Capelo, J.L.; Igrejas, G.; Poeta, P. Diversity and genetic lineages of environmental staphylococci: A surface water overview. FEMS Microbiol. Ecol. 2020, 96, fiaa191. [Google Scholar] [CrossRef] [PubMed]
  2. Rossi, C.C.; Pereira, M.F.; Giambiagi-deMarval, M. Underrated Staphylococcus species and their role in antimicrobial resistance spreading. Genet. Mol. Biol. 2020, 43, e20190065. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. Gnanamani, A.; Hariharan, P.; Paul-Satyaseela, M. Staphylococcus aureus: Overview of bacteriology, clinical diseases, epidemiology, antibiotic resistance and therapeutic approach. In Frontiers in Staphylococcus aureus; IntechOpen Limited: London, UK, 2017; Volume 4. [Google Scholar]
  4. França, A.; Gaio, V.; Lopes, N.; Melo, L.D.R. Virulence Factors in Coagulase-Negative Staphylococci. Pathogens 2021, 10, 170. [Google Scholar] [CrossRef] [PubMed]
  5. Furuya, E.Y.; Lowy, F.D. Antimicrobial-resistant bacteria in the community setting. Nat. Rev. Microbiol. 2006, 4, 36–45. [Google Scholar] [CrossRef] [PubMed]
  6. Kim, E.; Kim, H.-J.; Yang, S.-M.; Kim, C.-G.; Choo, D.-W.; Kim, H.-Y. Rapid Identification of Staphylococcus Species Isolated from Food Samples by Matrix-Assisted Laser Desorption/Ionization Time-of-Flight Mass Spectrometry. J. Microbiol. Biotechnol. 2019, 29, 548–557. [Google Scholar] [CrossRef]
  7. Cervinkova, D.; Vlkova, H.; Borodacova, I.; Makovcova, J.; Babak, V.; Lorencova, A.; Vrtkova, I.; Marosevic, D.; Jaglic, Z. Prevalence of mastitis pathogens in milk from clinically healthy cows. Vet. Med. 2013, 58, 567–575. [Google Scholar] [CrossRef] [Green Version]
  8. Mello, P.L.; Riboli, D.F.M.; Martins, L.A.; Brito, M.A.V.P.; Victória, C.; Calixto Romero, L.; Ribeiro de Souza da Cunha, M.L. Staphylococcus spp. isolated from bovine subclinical mastitis in different regions of Brazil: Molecular typing and biofilm gene expression analysis by RT-qPCR. Antibiotics 2020, 9, 888. [Google Scholar] [CrossRef]
  9. Song, X.; Huang, X.; Xu, H.; Zhang, C.; Chen, S.; Liu, F.; Guan, S.; Zhang, S.; Zhu, K.; Wu, C. The prevalence of pathogens causing bovine mastitis and their associated risk factors in 15 large dairy farms in China: An observational study. Vet. Microbiol. 2020, 247, 108757. [Google Scholar] [CrossRef]
  10. Mubarak, A. Prevalence and Genetic Diversity of Coagulase Negative Staphylococcus in Food Products Collected from Riyadh Region. J. Pure Appl. Microbiol. 2021, 15, 1987–1995. [Google Scholar] [CrossRef]
  11. Organji, S.R.; Abulreesh, H.H.; Elbanna, K.; Osman, G.E.H.; Almalki, M.H.K. Diversity and characterization of Staphylococcus spp. in food and dairy products: A foodstuff safety assessment. J. Microbiol. Biotechnol. Food Sci. 2021, 2021, 586–593. [Google Scholar] [CrossRef]
  12. Scherrer, D.; Corti, S.; Muehlherr, J.E.; Zweifel, C.; Stephan, R. Phenotypic and genotypic characteristics of Staphylococcus aureus isolates from raw bulk-tank milk samples of goats and sheep. Vet. Microbiol. 2004, 101, 101–107. [Google Scholar] [CrossRef]
  13. Veras, J.F.; do Carmo, L.S.; Tong, L.C.; Shupp, J.W.; Cummings, C.; Dos Santos, D.A.; Cerqueira, M.M.O.P.; Cantini, A.; Nicoli, J.R.; Jett, M. A study of the enterotoxigenicity of coagulase-negative and coagulase-positive staphylococcal isolates from food poisoning outbreaks in Minas Gerais, Brazil. Int. J. Infect. Dis. 2008, 12, 410–415. [Google Scholar] [CrossRef] [Green Version]
  14. Shlaes, D.M.; Projan, S.J. Antimicrobial Resistance Versus the Discovery and Development of New Antimicrobials BT-Antimicrobial Drug Resistance: Mechanisms of Drug Resistance; Mayers, D.L., Ed.; Humana Press: Totowa, NJ, USA, 2009; pp. 43–50. ISBN 978-1-59745-180-2. [Google Scholar]
  15. Stapleton, P.D.; Taylor, P.W. Methicillin resistance in Staphylococcus aureus: Mechanisms and modulation. Sci. Prog. 2002, 85, 57–72. [Google Scholar] [CrossRef]
  16. WHO. World Health Organization Global Priority List of Antibiotic-Resistant Bacteria to Guide Research, Discovery, and Development of New Antibiotics; WHO: Geneva, Switzerland, 2017. [Google Scholar]
  17. Fishovitz, J.; Hermoso, J.A.; Chang, M.; Mobashery, S. Penicillin-binding protein 2a of methicillin-resistant Staphylococcus aureus. IUBMB Life 2014, 66, 572–577. [Google Scholar] [CrossRef] [Green Version]
  18. Shore, A.C.; Deasy, E.C.; Slickers, P.; Brennan, G.; O’Connell, B.; Monecke, S.; Ehricht, R.; Coleman, D.C. Detection of staphylococcal cassette chromosome mec type XI carrying highly divergent mecA, mecI, mecR1, blaZ, and ccr genes in human clinical isolates of clonal complex 130 methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 2011, 55, 3765–3773. [Google Scholar] [CrossRef] [Green Version]
  19. Chan, L.C.; Gilbert, A.; Basuino, L.; da Costa, T.M.; Hamilton, S.M.; dos Santos, K.R.; Chambers, H.F.; Chatterjee, S.S. PBP 4 Mediates High-Level Resistance to New-Generation Cephalosporins in Staphylococcus aureus. Antimicrob. Agents Chemother. 2016, 60, 3934–3941. [Google Scholar] [CrossRef] [Green Version]
  20. MacFadyen, A.C.; Harrison, E.M.; Ellington, M.J.; Parkhill, J.; Holmes, M.A.; Paterson, G.K. A highly conserved mecC-encoding SCCmec type XI in a bovine isolate of methicillin-resistant Staphylococcus xylosus. J. Antimicrob. Chemother. 2018, 73, 3516–3518. [Google Scholar] [CrossRef]
  21. Porrero, M.C.; Harrison, E.; Fernández-Garayzábal, J.F.; Paterson, G.K.; Díez-Guerrier, A.; Holmes, M.A.; Domínguez, L. Detection of mecC-Methicillin-resistant Staphylococcus aureus isolates in river water: A potential role for water in the environmental dissemination. Environ. Microbiol. Rep. 2014, 6, 705–708. [Google Scholar] [CrossRef]
  22. Lakhundi, S.; Zhang, K. Methicillin-Resistant Staphylococcus aureus: Molecular Characterization, Evolution, and Epidemiology. Clin. Microbiol. Rev. 2018, 31, e00020-18. [Google Scholar] [CrossRef] [Green Version]
  23. Becker, K.; van Alen, S.; Idelevich, E.A.; Schleimer, N.; Seggewiß, J.; Mellmann, A.; Kaspar, U.; Peters, G. Plasmid-Encoded Transferable mecB-Mediated Methicillin Resistance in Staphylococcus aureus. Emerg. Infect. Dis. 2018, 24, 242–248. [Google Scholar] [CrossRef]
  24. Fair, R.J.; Tor, Y. Antibiotics and Bacterial Resistance in the 21st Century. Perspect. Medicin. Chem. 2014, 6, 25–64. [Google Scholar] [CrossRef] [Green Version]
  25. Kaur, D.C.; Chate, S.S. Study of Antibiotic Resistance Pattern in Methicillin Resistant Staphylococcus Aureus with Special Reference to Newer Antibiotic. J. Glob. Infect. Dis. 2015, 7, 78–84. [Google Scholar] [CrossRef] [PubMed]
  26. Foster, T.J. Antibiotic resistance in Staphylococcus aureus. Current status and future prospects. FEMS Microbiol. Rev. 2017, 41, 430–449. [Google Scholar] [CrossRef] [PubMed]
  27. Gómez, P.; Casado, C.; Sáenz, Y.; Ruiz-Ripa, L.; Estepa, V.; Zarazaga, M.; Torres, C. Diversity of species and antimicrobial resistance determinants of staphylococci in superficial waters in Spain. FEMS Microbiol. Ecol. 2017, 93, fiw208. [Google Scholar] [CrossRef] [Green Version]
  28. Crofts, T.S.; Gasparrini, A.J.; Dantas, G. Next-generation approaches to understand and combat the antibiotic resistome. Nat. Rev. Microbiol. 2017, 15, 422–434. [Google Scholar] [CrossRef] [Green Version]
  29. Nemeth, J.; Oesch, G.; Kuster, S.P. Bacteriostatic versus bactericidal antibiotics for patients with serious bacterial infections: Systematic review and meta-analysis. J. Antimicrob. Chemother. 2015, 70, 382–395. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  30. Tenover, F.C. Mechanisms of Antimicrobial Resistance in Bacteria. Am. J. Med. 2006, 119, S3–S10. [Google Scholar] [CrossRef]
  31. Brown-Jaque, M.; Calero-Cáceres, W.; Muniesa, M. Transfer of antibiotic-resistance genes via phage-related mobile elements. Plasmid 2015, 79, 1–7. [Google Scholar] [CrossRef]
  32. Giedraitienė, A.; Vitkauskienė, A.; Naginienė, R.; Pavilonis, A. Antibiotic resistance mechanisms of clinically important bacteria. Medicina 2011, 47, 19. [Google Scholar] [CrossRef]
  33. Kapoor, G.; Saigal, S.; Elongavan, A. Action and resistance mechanisms of antibiotics: A guide for clinicians. J. Anaesthesiol. Clin. Pharmacol. 2017, 33, 300. [Google Scholar] [CrossRef]
  34. Kwiecinski, J.M.; Horswill, A.R. Staphylococcus aureus bloodstream infections: Pathogenesis and regulatory mechanisms. Curr. Opin. Microbiol. 2020, 53, 51–60. [Google Scholar] [CrossRef]
  35. Jenul, C.; Horswill, A.R. Regulation of Staphylococcus aureus virulence. Microbiol. Spectr. 2019, 7, 2–7. [Google Scholar] [CrossRef] [PubMed]
  36. Oliveira, D.; Borges, A.; Simões, M. Staphylococcus aureus Toxins and Their Molecular Activity in Infectious Diseases. Toxins 2018, 10, 252. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  37. Bukowski, M.; Wladyka, B.; Dubin, G. Exfoliative toxins of Staphylococcus aureus. Toxins 2010, 2, 1148–1165. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  38. Abed, S.M.; Raoof, W.M.; Assie, A.H.A.; Al-Jaafari, E.N.I.; Hadi, Y.A. Multiplex PCR for Detection of Exfoliative Toxins, and Toxic Shock Syndrome Toxin 1 Genes in MRSA Strains of Clinical Staphylococcus aureus Isolates. Tikrit J. Pure Sci. 2018, 21, 39–44. [Google Scholar]
  39. Okuyama, Y.; Yoshida, N. Staphylococcal food poisoning and MRSA enterocolitis. Nihon Rinsho. 2012, 70, 1362–1365. [Google Scholar]
  40. Darboe, S.; Dobreniecki, S.; Jarju, S.; Jallow, M.; Mohammed, N.I.; Wathuo, M.; Ceesay, B.; Tweed, S.; Basu Roy, R.; Okomo, U.; et al. Prevalence of Panton-Valentine Leukocidin (PVL) and Antimicrobial Resistance in Community-Acquired Clinical Staphylococcus aureus in an Urban Gambian Hospital: A 11-Year Period Retrospective Pilot Study. Front. Cell. Infect. Microbiol. 2019, 9, 170. [Google Scholar] [CrossRef] [Green Version]
  41. Kasimanickam, V.; Kasimanickam, M.; Kasimanickam, R. Antibiotics use in food animal production: Escalation of antimicrobial resistance: Where are we now in combating AMR? Med. Sci. 2021, 9, 14. [Google Scholar] [CrossRef]
  42. Chowdhury, S.; Ghosh, S.; Aleem, M.A.; Parveen, S.; Islam, M.A.; Rashid, M.M.; Akhtar, Z.; Chowdhury, F. Antibiotic Usage and Resistance in Food Animal Production: What Have We Learned from Bangladesh? Antibiotics 2021, 10, 1032. [Google Scholar] [CrossRef]
  43. Feiyang, M.; Shixin, X.; Zhaoxin, T.; Zekun, L.; Lu, Z. Use of antimicrobials in food animals and impact of transmission of antimicrobial resistance on humans. Biosaf. Health 2021, 03, 32–38. [Google Scholar] [CrossRef]
  44. Tiseo, K.; Huber, L.; Gilbert, M.; Robinson, T.P.; Van Boeckel, T.P. Global trends in antimicrobial use in food animals from 2017 to 2030. Antibiotics 2020, 9, 918. [Google Scholar] [CrossRef] [PubMed]
  45. Bengtsson, B.; Greko, C. Antibiotic resistance—Consequences for animal health, welfare, and food production. Ups. J. Med. Sci. 2014, 119, 96–102. [Google Scholar] [CrossRef] [PubMed]
  46. Starr, M.P.; Reynolds, D.M. Streptomycin resistance of coliform bacteria from turkeys fed streptomycin. Am. J. Public Health Nations Health 1951, 41, 1375–1380. [Google Scholar] [CrossRef] [PubMed]
  47. Vidovic, N.; Vidovic, S. Antimicrobial resistance and food animals: Influence of livestock environment on the emergence and dissemination of antimicrobial resistance. Antibiotics 2020, 9, 52. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  48. Jackson, J.; Villarroel, A. A survey of the risk of zoonoses for veterinarians. Zoonoses Public Health 2012, 59, 193–201. [Google Scholar] [CrossRef]
  49. Nadimpalli, M.L.; Stewart, J.R.; Pierce, E.; Pisanic, N.; Love, D.C.; Hall, D.; Larsen, J.; Carroll, K.C.; Tekle, T.; Perl, T.M. Face mask use and persistence of livestock-associated Staphylococcus aureus nasal carriage among industrial hog operation workers and household contacts, USA. Environ. Health Perspect. 2018, 126, 127005. [Google Scholar] [CrossRef] [Green Version]
  50. Peng, Z.; Maciel-Guerra, A.; Baker, M.; Zhang, X.; Hu, Y.; Wang, W.; Rong, J.; Zhang, J.; Xue, N.; Barrow, P. Whole-genome sequencing and gene sharing network analysis powered by machine learning identifies antibiotic resistance sharing between animals, humans and environment in livestock farming. PLoS Comput. Biol. 2022, 18, e1010018. [Google Scholar] [CrossRef]
  51. Tian, M.; He, X.; Feng, Y.; Wang, W.; Chen, H.; Gong, M.; Liu, D.; Clarke, J.L.; van Eerde, A. Pollution by antibiotics and antimicrobial resistance in livestock and poultry manure in China, and countermeasures. Antibiotics 2021, 10, 539. [Google Scholar] [CrossRef]
  52. Cheng, D.; Feng, Y.; Liu, Y.; Xue, J.; Li, Z. Dynamics of oxytetracycline, sulfamerazine, and ciprofloxacin and related antibiotic resistance genes during swine manure composting. J. Environ. Manag. 2019, 230, 102–109. [Google Scholar] [CrossRef]
  53. Ruiz-Ripa, L.; Alcalá, L.; Simón, C.; Gómez, P.; Mama, O.M.; Rezusta, A.; Zarazaga, M.; Torres, C. Diversity of Staphylococcus aureus clones in wild mammals in Aragon, Spain, with detection of MRSA ST130-mecC in wild rabbits. J. Appl. Microbiol. 2019, 127, 284–291. [Google Scholar] [CrossRef]
  54. Wang, J.; Sang, L.; Sun, S.; Chen, Y.; Chen, D.; Xie, X. Characterisation of Staphylococcus aureus isolated from rabbits in Fujian, China. Epidemiol. Infect. 2019, 147, e256. [Google Scholar] [CrossRef]
  55. Holmes, M.A.; Harrison, E.M.; Fisher, E.A.; Graham, E.M.; Parkhill, J.; Foster, G.; Paterson, G.K. Genomic analysis of companion rabbit Staphylococcus aureus. PLoS ONE 2016, 11, e0151458. [Google Scholar] [CrossRef] [PubMed]
  56. Indrawattana, N.; Pumipuntu, N.; Suriyakhun, N.; Jangsangthong, A.; Kulpeanprasit, S.; Chantratita, N.; Sookrung, N.; Chaicumpa, W.; Buranasinsup, S. Staphylococcus argenteus from rabbits in Thailand. Microbiologyopen 2019, 8, e00665. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  57. Silva, V.; de Sousa, T.; Gómez, P.; Sabença, C.; Vieira-Pinto, M.; Capita, R.; Alonso-Calleja, C.; Torres, C.; Capelo, J.L.; Igrejas, G.; et al. Livestock-Associated Methicillin-Resistant Staphylococcus aureus (MRSA) in Purulent Subcutaneous Lesions of Farm Rabbits. Foods 2020, 9, 439. [Google Scholar] [CrossRef] [Green Version]
  58. Moreno-Grúa, E.; Pérez-Fuentes, S.; Muñoz-Silvestre, A.; Viana, D.; Fernández-Ros, A.B.; Sanz-Tejero, C.; Corpa, J.M.; Selva, L. Characterization of Livestock-Associated Methicillin-Resistant Staphylococcus aureus Isolates Obtained From Commercial Rabbitries Located in the Iberian Peninsula. Front. Microbiol. 2018, 9, 1812. [Google Scholar] [CrossRef] [Green Version]
  59. Merz, A.; Stephan, R.; Johler, S. Genotyping and DNA microarray based characterization of Staphylococcus aureus isolates from rabbit carcasses. Meat Sci. 2016, 112, 86–89. [Google Scholar] [CrossRef] [PubMed]
  60. Mechesso, A.F.; Moon, D.C.; Ryoo, G.-S.; Song, H.-J.; Chung, H.Y.; Kim, S.U.; Choi, J.-H.; Kim, S.-J.; Kang, H.Y.; Na, S.H. Resistance profiling and molecular characterization of Staphylococcus aureus isolated from goats in Korea. Int. J. Food Microbiol. 2021, 336, 108901. [Google Scholar] [CrossRef] [PubMed]
  61. Papadopoulos, P.; Angelidis, A.S.; Papadopoulos, T.; Kotzamanidis, C.; Zdragas, A.; Papa, A.; Filioussis, G.; Sergelidis, D. Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) in bulk tank milk, livestock and dairy-farm personnel in north-central and north-eastern Greece: Prevalence, characterization and genetic relatedness. Food Microbiol. 2019, 84, 103249. [Google Scholar] [CrossRef]
  62. Dastmalchi Saei, H.; Panahi, M. Genotyping and antimicrobial resistance of Staphylococcus aureus isolates from dairy ruminants: Differences in the distribution of clonal types between cattle and small ruminants. Arch. Microbiol. 2020, 202, 115–125. [Google Scholar] [CrossRef] [PubMed]
  63. Tegegne, H.A.; Koláčková, I.; Karpíšková, R. Diversity of livestock associated methicillin-resistant Staphylococcus aureus. Asian Pac. J. Trop. Med. 2017, 10, 929–931. [Google Scholar] [CrossRef] [PubMed]
  64. Venugopal, N.; Mitra, S.; Tewari, R.; Ganaie, F.; Shome, R.; Rahman, H.; Shome, B.R. Molecular detection and typing of methicillin-resistant Staphylococcus aureus and methicillin-resistant coagulase-negative staphylococci isolated from cattle, animal handlers, and their environment from Karnataka, Southern Province of India. Vet. World 2019, 12, 1760. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  65. Badua, A.T.; Boonyayatra, S.; Awaiwanont, N.; Gaban, P.B.V.; Mingala, C.N. Antibiotic resistance and genotyping of mecA-positive methicillin-resistant Staphylococcus aureus (MRSA) from milk and nasal carriage of dairy water buffaloes (Bubalus bubalis) in the Philippines. J. Adv. Vet. Anim. Res. 2020, 7, 397. [Google Scholar] [CrossRef] [PubMed]
  66. Locatelli, C.; Cremonesi, P.; Caprioli, A.; Carfora, V.; Ianzano, A.; Barberio, A.; Morandi, S.; Casula, A.; Castiglioni, B.; Bronzo, V.; et al. Occurrence of methicillin-resistant Staphylococcus aureus in dairy cattle herds, related swine farms, and humans in contact with herds. J. Dairy Sci. 2017, 100, 608–619. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  67. Lahuerta-Marin, A.; Guelbenzu-Gonzalo, M.; Pichon, B.; Allen, A.; Doumith, M.; Lavery, J.F.; Watson, C.; Teale, C.J.; Kearns, A.M. First report of lukM-positive livestock-associated methicillin-resistant Staphylococcus aureus CC30 from fattening pigs in Northern Ireland. Vet. Microbiol. 2016, 182, 131–134. [Google Scholar] [CrossRef] [PubMed]
  68. Ivbule, M.; Miklaševičs, E.; Čupāne, L.; Bērziņa, L.; Bālinš, A.; Valdovska, A. Presence of methicillin-resistant Staphylococcus aureus in slaughterhouse environment, pigs, carcasses, and workers. J. Vet. Res. 2017, 61, 267. [Google Scholar] [CrossRef] [Green Version]
  69. Kittl, S.; Brodard, I.; Heim, D.; Andina-Pfister, P.; Overesch, G. Methicillin-resistant Staphylococcus aureus strains in Swiss pigs and their relation to isolates from farmers and veterinarians. Appl. Environ. Microbiol. 2020, 86, e01865-19. [Google Scholar] [CrossRef]
  70. Tegegne, H.A.; Koláčková, I.; Florianová, M.; Wattiau, P.; Gelbíčová, T.; Boland, C.; Madec, J.-Y.; Haenni, M.; Karpíšková, R. Genomic insights into methicillin-resistant Staphylococcus aureus spa type t899 isolates belonging to different sequence types. Appl. Environ. Microbiol. 2021, 87, e01994-20. [Google Scholar] [CrossRef]
  71. Islam, M.Z.; Espinosa-Gongora, C.; Damborg, P.; Sieber, R.N.; Munk, R.; Husted, L.; Moodley, A.; Skov, R.; Larsen, J.; Guardabassi, L. Horses in Denmark Are a Reservoir of Diverse Clones of Methicillin-Resistant and -Susceptible Staphylococcus aureus. Front. Microbiol. 2017, 8, 543. [Google Scholar] [CrossRef] [Green Version]
  72. Reynaga, E.; Navarro, M.; Vilamala, A.; Roure, P.; Quintana, M.; Garcia-Nuñez, M.; Figueras, R.; Torres, C.; Lucchetti, G.; Sabrià, M. Prevalence of colonization by methicillin-resistant Staphylococcus aureus ST398 in pigs and pig farm workers in an area of Catalonia, Spain. BMC Infect. Dis. 2016, 16, 716. [Google Scholar] [CrossRef] [Green Version]
  73. Mroczkowska, A.; Żmudzki, J.; Marszałek, N.; Orczykowska-Kotyna, M.; Komorowska, I.; Nowak, A.; Grzesiak, A.; Czyżewska-Dors, E.; Dors, A.; Pejsak, Z. Livestock-associated Staphylococcus aureus on Polish pig farms. PLoS ONE 2017, 12, e0170745. [Google Scholar] [CrossRef] [Green Version]
  74. Heikinheimo, A.; Johler, S.; Karvonen, L.; Julmi, J.; Fredriksson-Ahomaa, M.; Stephan, R. New dominant spa type t2741 in livestock-associated MRSA (CC398-MRSA-V) in Finnish fattening pigs at slaughter. Antimicrob. Resist. Infect. Control 2016, 5, 6. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  75. Pirolo, M.; Visaggio, D.; Gioffrè, A.; Artuso, I.; Gherardi, M.; Pavia, G.; Samele, P.; Ciambrone, L.; Di Natale, R.; Spatari, G. Unidirectional animal-to-human transmission of methicillin-resistant Staphylococcus aureus ST398 in pig farming; evidence from a surveillance study in southern Italy. Antimicrob. Resist. Infect. Control 2019, 8, 1–10. [Google Scholar] [CrossRef] [PubMed]
  76. Santos, V.; Gomes, A.; Ruiz-Ripa, L.; Mama, O.M.; Sabença, C.; Sousa, M.; Silva, V.; Sousa, T.; Vieira-Pinto, M.; Igrejas, G.; et al. Methicillin-Resistant Staphylococcus aureus CC398 in Purulent Lesions of Piglets and Fattening Pigs in Portugal. Microb. Drug Resist. 2020, 26, 850–856. [Google Scholar] [CrossRef] [PubMed]
  77. Nemeghaire, S.; Roelandt, S.; Argudín, M.A.; Haesebrouck, F.; Butaye, P. Characterization of methicillin-resistant Staphylococcus aureus from healthy carrier chickens. Avian Pathol. 2013, 42, 342–346. [Google Scholar] [CrossRef]
  78. Tang, Y.; Larsen, J.; Kjeldgaard, J.; Andersen, P.S.; Skov, R.; Ingmer, H. Methicillin-resistant and -susceptible Staphylococcus aureus from retail meat in Denmark. Int. J. Food Microbiol. 2017, 249, 72–76. [Google Scholar] [CrossRef]
  79. Zogg, A.L.; Zurfluh, K.; Nüesch-Inderbinen, M.; Stephan, R. Characteristics of ESBL-producing Enterobacteriaceae and Methicillinresistant Staphylococcus aureus (MRSA) isolated from Swiss and imported raw poultry meat collected at retail level. Schweiz. Arch. Tierheilkd. 2016, 158, 451–456. [Google Scholar] [CrossRef] [Green Version]
  80. Geenen, P.L.; Graat, E.A.M.; Haenen, A.; Hengeveld, P.D.; Van Hoek, A.H.A.M.; Huijsdens, X.W.; Kappert, C.C.; Lammers, G.A.C.; Van Duijkeren, E.; Van De Giessen, A.W. Prevalence of livestock-associated MRSA on Dutch broiler farms and in people living and/or working on these farms. Epidemiol. Infect. 2013, 141, 1099–1108. [Google Scholar] [CrossRef]
  81. Pesavento, G.; Ducci, B.; Comodo, N.; Nostro, A. Lo Antimicrobial resistance profile of Staphylococcus aureus isolated from raw meat: A research for methicillin resistant Staphylococcus aureus (MRSA). Food Control 2007, 18, 196–200. [Google Scholar] [CrossRef]
  82. Karmi, M. Prevalence of methicillin-resistant Staphylococcus aureus in poultry meat in Qena, Egypt. Vet. World 2013, 6, 711–715. [Google Scholar] [CrossRef]
  83. Amoako, D.G.; Somboro, A.M.; Abia, A.L.K.; Allam, M.; Ismail, A.; Bester, L.; Essack, S.Y. Genomic analysis of methicillin-resistant Staphylococcus aureus isolated from poultry and occupational farm workers in Umgungundlovu District, South Africa. Sci. Total Environ. 2019, 670, 704–716. [Google Scholar] [CrossRef]
  84. Feßler, A.T.; Kadlec, K.; Hassel, M.; Hauschild, T.; Eidam, C.; Ehricht, R.; Monecke, S.; Schwarz, S. Characterization of methicillin-resistant Staphylococcus aureus isolates from food and food products of poultry origin in Germany. Appl. Environ. Microbiol. 2011, 77, 7151–7157. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  85. Hauschild, T.; Feßler, A.T.; Kadlec, K.; Billerbeck, C.; Schwarz, S. Detection of the novel vga (E) gene in methicillin-resistant Staphylococcus aureus CC398 isolates from cattle and poultry. J. Antimicrob. Chemother. 2012, 67, 503–504. [Google Scholar] [CrossRef] [PubMed]
  86. Waters, A.E.; Contente-Cuomo, T.; Buchhagen, J.; Liu, C.M.; Watson, L.; Pearce, K.; Foster, J.T.; Bowers, J.; Driebe, E.M.; Engelthaler, D.M. Multidrug-resistant Staphylococcus aureus in US meat and poultry. Clin. Infect. Dis. 2011, 52, 1227–1230. [Google Scholar] [CrossRef] [PubMed]
  87. Bystroń, J.; Podkowik, M.; Piasecki, T.; Wieliczko, A.; Molenda, J.; Bania, J. Genotypes and enterotoxin gene content of S. aureus isolates from poultry. Vet. Microbiol. 2010, 144, 498–501. [Google Scholar] [CrossRef] [PubMed]
  88. Silva, V.; Vieira-Pinto, M.; Saraiva, C.; Manageiro, V.; Reis, L.; Ferreira, E.; Caniça, M.; Capelo, J.L.; Igrejas, G.; Poeta, P. Prevalence and Characteristics of Multidrug-Resistant Livestock-Associated Methicillin-Resistant Staphylococcus aureus (LA-MRSA) CC398 Isolated from Quails (Coturnix Coturnix Japonica) Slaughtered for Human Consumption. Animals 2021, 11, 2038. [Google Scholar] [CrossRef]
  89. van Duijkeren, E.; Hengeveld, P.; Zomer, T.P.; Landman, F.; Bosch, T.; Haenen, A.; van de Giessen, A. Transmission of MRSA between humans and animals on duck and turkey farms. J. Antimicrob. Chemother. 2016, 71, 58–62. [Google Scholar] [CrossRef] [Green Version]
  90. Richter, A.; Sting, R.; Popp, C.; Rau, J.; Tenhagen, B.-A.; Guerra, B.; Hafez, H.M.; Fetsch, A. Prevalence of types of methicillin-resistant Staphylococcus aureus in turkey flocks and personnel attending the animals. Epidemiol. Infect. 2012, 140, 2223–2232. [Google Scholar] [CrossRef] [Green Version]
  91. Brennan, G.I.; Abbott, Y.; Burns, A.; Leonard, F.; McManus, B.A.; O’Connell, B.; Coleman, D.C.; Shore, A.C. The Emergence and Spread of Multiple Livestock-Associated Clonal Complex 398 Methicillin-Resistant and Methicillin-Susceptible Staphylococcus aureus Strains among Animals and Humans in the Republic of Ireland, 2010–2014. PLoS ONE 2016, 11, e0149396. [Google Scholar] [CrossRef]
  92. Conceição, T.; De Lencastre, H.; Aires-De-Sousa, M. Frequent isolation of methicillin resistant Staphylococcus aureus (MRSA) ST398 among healthy pigs in Portugal. PLoS ONE 2017, 12, e0175340. [Google Scholar] [CrossRef]
  93. Parisi, A.; Caruso, M.; Normanno, G.; Latorre, L.; Miccolupo, A.; Fraccalvieri, R.; Intini, F.; Manginelli, T.; Santagada, G. MRSA in swine, farmers and abattoir workers in Southern Italy. Food Microbiol. 2019, 82, 287–293. [Google Scholar] [CrossRef]
  94. Monecke, S.; Ruppelt, A.; Wendlandt, S.; Schwarz, S.; Slickers, P.; Ehricht, R.; Jäckel, S.C. de Genotyping of Staphylococcus aureus isolates from diseased poultry. Vet. Microbiol. 2013, 162, 806–812. [Google Scholar] [CrossRef] [PubMed]
  95. Silva, V.; Monteiro, A.; Pereira, J.E.; Maltez, L.; Igrejas, G.; Poeta, P. MRSA in Humans, Pets and Livestock in Portugal: Where We Came from and Where We Are Going. Pathogens 2022, 11, 1110. [Google Scholar] [CrossRef] [PubMed]
  96. Schmithausen, R.M.; Schulze-Geisthoevel, S.V.; Heinemann, C.; Bierbaum, G.; Exner, M.; Petersen, B.; Steinhoff-Wagner, J. Reservoirs and Transmission Pathways of Resistant Indicator Bacteria in the Biotope Pig Stable and along the Food Chain: A Review from a One Health Perspective. Sustainability 2018, 10, 3967. [Google Scholar] [CrossRef] [Green Version]
  97. Tanomsridachchai, W.; Changkaew, K.; Changkwanyeun, R.; Prapasawat, W.; Intarapuk, A.; Fukushima, Y.; Yamasamit, N.; Flav Kapalamula, T.; Nakajima, C.; Suthienkul, O.; et al. Antimicrobial Resistance and Molecular Characterization of Methicillin-Resistant Staphylococcus aureus Isolated from Slaughtered Pigs and Pork in the Central Region of Thailand. Antibiotics 2021, 10, 206. [Google Scholar] [CrossRef] [PubMed]
  98. Wu, S.; Huang, J.; Zhang, F.; Wu, Q.; Zhang, J.; Pang, R.; Zeng, H.; Yang, X.; Chen, M.; Wang, J. Prevalence and characterization of food-related methicillin-resistant Staphylococcus aureus (MRSA) in China. Front. Microbiol. 2019, 10, 304. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  99. Kang, K.-M.; Park, J.-H.; Kim, S.H.; Yang, S.-J. Potential role of host defense antimicrobial peptide resistance in increased virulence of health care-associated MRSA strains of sequence type (ST) 5 versus livestock-associated and community-associated MRSA strains of ST72. Comp. Immunol. Microbiol. Infect. Dis. 2019, 62, 13–18. [Google Scholar] [CrossRef]
  100. Yang, E.; Kim, E.; Chung, H.; Lee, Y.W.; Bae, S.; Jung, J.; Kim, M.J.; Chong, Y.P.; Kim, S.-H.; Choi, S.-H. Changing characteristics of S. aureus bacteremia caused by PVL-negative, MRSA strain over 11 years. Sci. Rep. 2021, 11, 15677. [Google Scholar] [CrossRef]
  101. Kluytmans, J. Methicillin-resistant Staphylococcus aureus in food products: Cause for concern or case for complacency? Clin. Microbiol. Infect. 2010, 16, 11–15. [Google Scholar] [CrossRef] [Green Version]
  102. Pu, S.; Han, F.; Ge, B. Isolation and characterization of methicillin-resistant Staphylococcus aureus strains from Louisiana retail meats. Appl. Environ. Microbiol. 2009, 75, 265–267. [Google Scholar] [CrossRef] [Green Version]
  103. Van Loo, I.H.M.; Diederen, B.M.W.; Savelkoul, P.H.M.; Woudenberg, J.H.C.; Roosendaal, R.; Van Belkum, A.; Lemmens-den Toom, N.; Verhulst, C.; Van Keulen, P.H.J.; Kluytmans, J.A.J.W. Methicillin-resistant Staphylococcus aureus in meat products, the Netherlands. Emerg. Infect. Dis. 2007, 13, 1753. [Google Scholar] [CrossRef]
Table
Table 1. Mechanisms of action and resistance of the most important classes of antibiotics.
Table 1. Mechanisms of action and resistance of the most important classes of antibiotics.
Class of AntibioticsMechanisms of ActionMechanisms of Resistance
PenicillinsInhibition of cell wall biosynthesis.Production of β-lactamases; PBP’s changed; efflux pumps.
Cephalosporins
AminoglycosidesInhibition of protein synthesis by binding to the 30S ribosomal subunit.efflux pumps; modification of the target (ribosome).
Macrolides
LincosamidesInhibition of protein synthesis by binding to the 30S ribosomal subunit.Modification of the target (ribosome).
QuinolonesInhibition of DNA synthesis.Target modification (DNA gyrase and DNA topoisomerase).
TetracyclinesInhibition of protein synthesis at the level of peptide elongation.Efflux pumps; modification of the target (ribosome).
PhenicolsInhibition of the peptidyltransferase reaction in the 50S ribosomal subunit.efflux pumps; target modification (enzyme and ribosome).
SulfonamidesInhibition of folic acid synthesis.Target modification (enzymes).
Table
Table 2. Molecular characteristics of LA-MRSA clones in different continents [22].
Table 2. Molecular characteristics of LA-MRSA clones in different continents [22].
LocationCloneMolecular Characteristics
MLSTspa TypeSCCmec Typeagr Type
USA/
Canada		ST398-MRSA VST398t571/t011/t034/t1197/t1250/t1451/t1456/t2510V1
ST5-MRSA IVST5t002/t003/t311IV2
EuropeST398-MRSA VST398t571/t011/t034/t1197/t1250/t1451/t1456/t2510III/IV/V/1
ST9ST9t100/t411/t899/t4358 2
ST97-MRSA VST97t1234V/IV1
ST1379-MRSA VST1379t3992V1
ST1-MRSA IVST1t128/t127/t125/t1178IV3
ST130-MRSA XIST130t373XI
AfricaST398-MRSA IVST398t571/t011/t034/t1197/t1250/t1451/t1456/t2510IV1
AsiaST9-MRSAST9t100/t411/t899/t4358III/IV/V/NT2
ST398-MRSA VST398t571/t011/t034/t1197/t1250/t1451/t1456/t2510IV1
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Silva, V.; Araújo, S.; Monteiro, A.; Eira, J.; Pereira, J.E.; Maltez, L.; Igrejas, G.; Lemsaddek, T.S.; Poeta, P. Staphylococcus aureus and MRSA in Livestock: Antimicrobial Resistance and Genetic Lineages. Microorganisms 2023, 11, 124. https://doi.org/10.3390/microorganisms11010124

AMA Style

Silva V, Araújo S, Monteiro A, Eira J, Pereira JE, Maltez L, Igrejas G, Lemsaddek TS, Poeta P. Staphylococcus aureus and MRSA in Livestock: Antimicrobial Resistance and Genetic Lineages. Microorganisms. 2023; 11(1):124. https://doi.org/10.3390/microorganisms11010124

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Silva, Vanessa, Sara Araújo, Andreia Monteiro, José Eira, José Eduardo Pereira, Luís Maltez, Gilberto Igrejas, Teresa Semedo Lemsaddek, and Patricia Poeta. 2023. "Staphylococcus aureus and MRSA in Livestock: Antimicrobial Resistance and Genetic Lineages" Microorganisms 11, no. 1: 124. https://doi.org/10.3390/microorganisms11010124

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