Animal-Associated Methicillin-Resistant Staphylococcus aureus: History
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Contributor:
Martyna Kasela
,
Mateusz Ossowski
,
Ewelina Dzikoń
,
Katarzyna Ignatiuk
,
Łukasz Wlazło
,
Anna Malm
Methicillin-resistant Staphylococcus aureus (MRSA) remains an important etiological factor of human and animal infectious diseases, causing significant economic losses not only in human healthcare but also in the large-scale farming sector. The constantly changing epidemiology of MRSA observed globally affects animal welfare and raises concerns for public health. High MRSA colonization rates in livestock raise questions about the meaning of reservoirs and possible transmission pathways, while the prevalence of MRSA colonization and infection rates among companion animals vary and might affect human health in multiple ways.
  • MRSA
  • Staphylococcus aureus
  • epidemiology
  • transmission
  • animals

1. Introduction

Staphylococcus aureus, including methicillin-resistant S. aureus (MRSA), is not only one of the most common etiological factors of human infectious disease but also a pathogen with a profound impact on animal welfare because of increasing antibiotic resistance and the resulting economic burden [1][2]. The first reports concerning MRSA date back to the years 1959–1960, when it evolved from a susceptible S. aureus strain as a result of the implementation of methicillin as a new antimicrobial drug in hospitals. Additionally, the first observations suggested that it originated from one epidemic clone as all investigated strains exhibited the same antimicrobial resistance profile (penicillin, streptomycin, and tetracycline), [3]. Described by the Centers for Disease Control and Prevention as an note-threating microorganism quickly acquiring antibiotic resistance, MRSA gradually spread around the world, resulting in a high epidemiological burden both for humans as well as animals [4]. The strains are all characterized by the presence of an acquired type of resistance to β-lactam antibiotics encoded by genes from the mec group (mecA, mecB, and mecC) located in the staphylococcal chromosomal cassette (SCCmec). Genes encode for novel types of the penicillin-binding protein exhibiting decreased affinity to β-lactams resulting in inactivation of an antibiotic [5]. Depending on the setting, where the MRSA infection has been first reported, strains are divided into certain subpopulations. For human infections, the most prevalent hospital-associated MRSA (HA-MRSA) and community-associated MRSA (CA-MRSA) inform as to whether the strains were isolated in a nosocomial environment or outside, respectively. The third subpopulation—animal-associated MRSA (AA-MRSA), sometimes limited only to livestock-associated-MRSA (LA-MRSA)—includes pathogens isolated from animals [6][7]. The determination of subpopulation type can be helpful in epidemiological investigation by providing information about certain MRSA clone origins; however, the dynamic spread and transmission of MRSA worldwide blur the formerly clear line between clones of human and animal origin.
Since first MRSA was discovered, it has consequently gained resistance to other classes of antibiotics, like macrolides and tetracyclines, or chemotherapeutics, like fluoroquinolones, resulting in difficulties in the development of successful antimicrobial therapy in infected individuals [8]. While even more health-threatening S. aureus strains have emerged, including vancomycin-resistant S. aureus (VRSA) often characterized by multi-drug resistance, MRSA still remains the main therapeutic challenge worldwide [9]. Depending on the character and location of infection, routine antimicrobial therapy of MRSA infections consists of the application of several antimicrobial drugs, i.e., vancomycin in the case of MRSA bacteremia, daptomycin in the treatment of soft-tissue infections, or mupirocin for skin infections. For infections caused by multi-drug-resistant strains, novel antimicrobial agents are often applied, e.g., linezolid antibiotic, or multiple semisynthetic drugs, such as tigecycline, dalbavancin, oritavancin, iclaprim, cethromycin, or delafloxacin [10]. Except standard antibiotic therapy, alternative treatments and agents supporting antibiotic therapy are being developed as a new approach for the treatment of MRSA infections. The above-mentioned strategies consist of combining known antimicrobial agents with substances or compounds of natural origin or the application of a combination of two or more antimicrobial agents [8]. In spite of all these efforts, the emergence of resistance to new antimicrobials is being observed. MRSA strains resistant to daptomycin were described just years after the official Food and Drug Administration approval for the treatment of S. aureus in 2006. A similar situation has been noted for linezolid, implemented for treatment in the year 2000, to which resistance was first described in 2005. Since then, S. aureus has developed several resistance mechanisms [11].
The growing antibiotic resistance to so called “last resort” antibiotics in the treatment of serious bacterial infections drastically limits the current therapeutic options. There are several factors that increase the risk of acquiring antibiotic resistance in bacteria. They include: the excessive use of antimicrobial agents creating selective pressure enabling resistance to develop and persist in the environment, the emergence of novel sources of drug-resistant bacteria as well as novel routes for these bacteria to spread which allows not only the direct transmission of MRSA but also the occurrence of the horizontal transfer of resistance factors [12]. In the recent years, animals have become a profound secondary source of MRSA in the environment, and the frequent contact between animals and humans create a significant route of their transmission [13]. Therefore, to further fight antibiotic resistance in S. aureus, it is indispensable to investigate and understand novel reservoirs of antibiotic-resistant bacteria and the evolutionary consequences of their global spread. The epidemiology of MRSA is changing dynamically due to intensive circulation within the community and farming environment [14]. However, the transfer of microorganisms between humans and animals seems to be a part of the natural process of microbial adaptation. The interspecies transmission of antibiotic-resistant bacteria raises significant concerns for public health. The prevalence and risk factors for colonization and subsequent infection with multidrug-resistant microbes among humans are well established when compared with animal populations [15]. MRSA colonizes and infects companion animals and wild animals as well as livestock, causing serious diseases of worldwide significance, e.g., in poultry or dairy cows [16].

2. Methicillin-Resistant Staphylococcus aureus in Companion Animals

Companion animals might be a significant reservoir of MRSA circulating in the environment. The presence of multi-drug-resistant bacterial strains in households poses a threat not just to human and animal health but especially for people who are immunocompromised because of various medical conditions as well as those undergoing immunosuppressive treatment. Therefore, epidemiological investigations on MRSA colonization rates in companion animals provide valuable data on the scale of the problem.
Studies have shown that the nares, mouth, and perineum are the major colonization sites in cats and dogs; however, the persistence of carriage itself remains poorly investigated [17]. Both animals and owners can be colonized by S. aureus as an effect of indirect everyday interaction with each other as well as contact with contaminated surfaces within the household [18][19]. Multiple studies have detected the presence of MRSA in not only pets, mainly dogs and cats [20][21][22][23][24][25][26][27][28], but also other companion species like birds, guinea pigs, turtles [29], or hamsters [30]. This wide dissemination proves that MRSA is well adapted to colonize a wide spectrum of animal hosts.
The methicillin-resistant S. aureus colonization rates given by multiple studies are highly diversified and depend on various factors, including geographical location, the animal population studied, household hygienic conditions, and many others. Recent studies have shown alarmingly high MRSA colonization rates in most common species of companion animals—dogs and cats. Moreover, taking into consideration the number of cats and dogs kept as companion animals worldwide, the scale at which transmission between pets and the owners might occur is disturbing. In the study conducted by Strommenger et al. in Germany, all S. aureus strains isolated from pet dogs and cats harbored the mecA gene [31]. Similarly, relatively high MRSA colonization rates were observed in France, where MRSA colonized 39.3% of dogs, 26.5% of cats, and as high as 47.1% of horses [24]. Also, Drougka et al., whose study was located in Greece, investigated the prevalence of S. aureus among companion dogs and cats and found 37% and 30% methicillin-susceptible S. aureus (MSSA) isolation rates, respectively, while the overall MRSA prevalence rate accounted for 10.8% [32]. The prevalence of certain clonal lineages of MRSA isolated from companion animals remains similar within European countries and, according to the authors, often reflects dominating lineages of MRSA of human origin (Table 1). In contrast to dogs and cats, only horses are usually colonized by MRSA strains typical for livestock, e.g., in France, as many as 72.1% of MRSA strains isolated from horses belonged to CC398 [24].
Table 1. Metihicillin-resistant Staphylococcus aureus lineages isolated from pet animals.
Country Years of Isolation Animals MLST Literature
Germany 2003–2004 Dogs and cats CC22 (ST22) [31]
2010–2012 CC22, CC5, CC398, CC8 [33]
England 2007–2008 Dogs CC30 (ST36) [34]
Cats CC22
Horses CC22, CC8 (ST239)
Switzerland 2017 Horse ST338 [35]
Hungary 2017 Horse ST130 [36]
France 2010–2015 Dogs CC8, CC398, CC5, CC22, CC45, CC1, CC59 [24]
Cats CC8, CC398, CC5, CC22, CC130
Horses CC398, CC8, CC130, CC49
Serbia 2016 Dogs CC239, CC45, CC5 [21]
Cat CC1
Portugal 1999–2018 Dogs CC22 (ST22), CC1 (ST188, ST6565, ST1), CC8 (ST72, ST6566), CC5 (ST105, ST5, ST6535), CC398 (ST398) [37]
Cats CC22 (ST22), CC8 (ST72), CC97 (ST97), CC7 (ST7), CC15 (ST15), CC5 (ST5), CC398 (ST398)
Rabbits CC22 (ST22), CC121 (ST121), CC398 (ST398)
Horse ST816
US 2010 Dogs, cats, and a hamster CC5 [30]
Brazil 2010 Cat ST30 [38]
2010–2013 Dogs ST1, ST5, ST30, ST239 [39]
Japan 2016–2018 Cats ST5, ST764, ST512, ST1863, ST1, ST2725, ST4775, ST4779, ST8, ST4224, ST4777 [40]
Dogs ST72, ST4776, ST5, ST4778, ST2725, ST8, ST380
Rabbits ST4768
Australia 2019 Dogs ST1, ST5, ST72, ST93 [41]
Thailand 2017–2020 Dogs ST398, ST5926, ST6563 [42]
Cats ST398
Malaysia 2007–2008 Dogs ST59 [43]
Cats ST55
Zambia 2012 Dogs ST 152, ST398, ST15, ST1416 [44]
Fewer researchers have focused on the possibility of interspecies transmission between pets and their owners and conducted studies with the use of genotyping methods [21]. Researchers suggest that transmission from humans to companion animals occurs more prevalently due to overlapping of their habitats [45]. Moreover, multiple studies have proven that humans are the main source of the MRSA colonizing companion animals, which would explain the high colonization rates in cats and dogs maintaining close contact with owners and living in an area of limited space. These animals might become a profound secondary source for human and animal infections, which is emphasized by the fact that strains of human origin, especially HA-MRSA, often carry more antibiotic-resistance and virulence genes than strains of animal origin [24]. The reports of typical nosocomial MRSA strains’ isolation from dogs and cats (e.g., ST5, ST45, and ST239) prove that pets might act as a secondary reservoir for virulent S. aureus strains in the environment [21]. The enhanced virulence of MRSA is often connected with the production of specific toxins resulting in more severe disease symptoms in the case of infection. The production of Panton–Valentine leucocidin toxin, strongly associated with skin and soft-tissue infections and tissue necrosis in community-acquired pneumonia, might have serious health implications not only for immunocompromised people but also for young and healthy individuals [46]. The high isolation rates of pvl-positive S. aureus strains from healthy dogs and cats in certain European regions, ranging from 25% to even 87.5%, underlining the need for epidemiological monitoring of MRSA colonizing pet animals, especially in the context of pet owners predisposed to community-acquired staphylococcal infections [23][32][47].
The main concern about S. aureus transmission between humans and animals is the spread of zoonotic diseases in the general population; nevertheless, a recent study conducted by Bierowiec et al. proved that close contact with owners predisposed companion cats to significantly higher S. aureus colonization rates than free-living, domestic cats. Moreover, the prevalence of MRSA was also found to be higher among pet cats, which confirms the assumed direction of MRSA transmission from owners to companion animals [20]. Other factors recently discovered to be significantly associated with the S. aureus colonization of both dogs and cats are the young age of the animals (<12 mo.), living in rural areas, possessing skin diseases at the time of swab collection, and simultaneous colonization with coagulase-negative staphylococci [32].
Recent studies clearly show the growing importance of companion animals as a secondary reservoir of drug-resistant pathogens in the environment. Human infections caused by MRSA isolated simultaneously from companion animals occur rarely; however, researchers emphasize the role of proper hygienic conditions in households in limiting the risk of colonization and subsequent infection in pet owners [22][30].

3. Methicillin-Resistant Staphylococcus aureus in Livestock Animals

The human population is steadily expanding into new geographical areas, which together with the increase in the number of large-scale animal farms generates new transmission pathways that ease the spread of MRSA in the environment. High MRSA colonization rates in livestock farming environments and the emergence of LA-MRSA in humans raise questions regarding its origin and possible transmission pathways [48]. Similar to companion animals, MRSA colonizing livestock can act as a significant reservoir for drug-resistance genes. The transmission of these genes is a significant epidemiological concern, because of the possible share in acquiring MRSA that colonizes humans. The high diversification of LA-MRSA isolation rates and their genetic variants in animal farming environments is common and clearly seen in studies from different parts of the world.
Researchers suggest that the current spread of LA-MRSA in Europe is connected to the international pig market [49]. What is more, the prevalence of LA-MRSA in pigs is rising constantly, with ST398 LA-MRSA lineage domination observed in most European countries [50][51]. Despite this, the epidemiological situation in other parts of the world differs. The domination of certain lineages of LA-MRSA in livestock farming environments is being observed (Table 2). The distribution of MRSA sequence types among livestock depends not only on geographical location [52][53] but also the major clonal lineages causing infections in humans, e.g., in Australian piggeries, as many as 84% of MRSA strains were classified as ST93—the most common CA-MRSA in the country. Additionally, MRSA isolation rates were high and accounted for 76% in animals and 60% in pig farm workers [54].
Table 2. Methicillin-resistant Staphylococcus aureus lineages isolated from livestock animals.
Country Years of Isolation Animals MLST Literature
Denmark 2004–2007 Pigs ST398 [55]
2013–2014 Ducks and turkeys [56]
Belgium 2011 Chickens ST398, ST239 [57]
Switzerland 2017 Pigs ST398 [35]
Spain 2009–2010 Pigs ST398 [50]
2017–2018
Portugal 2020 Quails ST398, ST6831 [58]
Italy 2010 Pigs CC398, CC97 [59]
2018 Dairy cows CC22 [60]
Czech Republic 2017 Goats ST398 [61]
Spain
and Portugal		 2014–2017 Rabbits ST2855, ST146, ST398 [62]
Australia 2015 Pigs ST398, ST93, ST30 [54]
China 2011–2016 Pigs ST9, ST764 [53]
Chickens ST9
Ducks ST9, ST398
2017–2018 Pigs ST9, ST3653-6356, ST1376, ST59, ST398 [63]
India 2020 Goats ST772, ST22, ST368 [64]
Africa (Cote d’Ivoire) 2012 Goats ST15, ST152, ST6, ST8, ST1472 [45]
Sheep ST15, ST88, ST152, ST567, ST121
Chicken ST152
USA 2006 Pigs ST398 [65]
2013–2014 ST9, ST398, ST2007, ST1, ST5 [52]
Staphylococcus aureus remains a major etiological factor of bovine mastitis [66][67], and it is estimated that methicillin-resistant strains are responsible for approximately 12% of infections [68][69]. Recent findings confirm that MRSA strains circulating among humans are capable of causing infection in cows [70]. Juhász-Kaszanyitzky et al. found that subclinical mastitis in cows on a Hungarian farm was caused by MRSA genetically undistinguishable from a strain isolated from a farm worker. Moreover, an alarmingly high percentage of MRSA strains isolated from dairy cows harbor multiple enterotoxin genes simultaneously (seg, sei, sem, sen, seo, and seu), making a possible outbreak from contaminated milk more health-threatening to humans [60].
Methicillin-resistant strains are also present in poultry [48][56][57][71] and poultry-derived products [72][73]. In some countries, the prevalence of MRSA among poultry has been found to be relatively high. In Algeria, as many as 57% of laying hens and 50% of broiler chickens were found to be colonized with MRSA. The authors also found that the poultry were significantly more often colonized than the bovine animals (31%), [48]. The poultry were found to be colonized not only by livestock-associated CC398 but also by strains of human origin [57]; thus, the epidemiological situation regarding poultry market should be carefully monitored in order to limit the spread of virulent MRSA strains in the environment.
In comparison to the environment of large-scale farms with bovine, swine or poultry, the epidemiology of S. aureus differs in small dairy-ruminant herds. Carfora et al. observed low intra-farm prevalence of both MSSA and MRSA among sheep. In total, 2.16% of milk samples were found S. aureus positive and only 0.34% MRSA positive, however, genotyping revealed that all MRSA collected from animals and farm workers belonged to the same MLST variant (ST1), [74]. MRSA is also being isolated from goats. Loncaric et al. described a case of necropsy in a goat caused by LA-MRSA ST398. The same strain was isolated earlier from the goat’s owner, proving the infectious potential of LA-MRSA transmitted from the human host to the animal [75]. In the Czech Republic, LA-MRSA ST398 was isolated on a goat farm, both from animals and personnel, indicating circulation of S. aureus in a given environment; however, the authors did not detect any MRSA strains among sheep and pig farms in the same homestead [61]. The presence of MRSA was also found in rabbits; S. aureus was detected both as a colonizing agent as well as an etiological factor causing lesions. Large-scale studies in commercial rabbitries located on the Iberian Peninsula revealed the presence of MRSA in 19 out of 89 farms with an 11.25% colonization rate among rabbits [62].
The presence of MRSA in the large-scale farming environment challenges current epidemiological approaches limiting the circulation of pathogens between animals and humans. Moreover, it increases the probability of the emergence of new pathogenic microorganisms, making agro-ecosystems a global threat to public health.

This entry is adapted from the peer-reviewed paper 10.3390/antibiotics12061079

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