Abstract
Antimicrobial resistance represents a major threat to human health. As a result, we are faced with potential antimicrobial therapeutic failure, thus forcing physicians to use last resort antimicrobials, such as carbapenems, glycopeptides or polypeptides. During the last fifty years, the number of companion animals has substantially increased and there is a growing concern related to the use of antimicrobials in companion animals as a potential source for antimicrobial resistance to humans. Problems related with antimicrobial resistance and infection control in small animal hospitals are mimicking those in human hospitals. Transmission of pathogens or resistance genes such as methicillin-resistant staphylococci, extended spectrum beta-lactamase- or carbapenemase-producing and colistin-resistant Enterobacteriaceae between people and their pets have been documented or suggested. The public health risks associated with the transfer of antimicrobial-resistant bacteria from companion animals were recently reviewed by the European Medicine Agency which warned to the existence of antimicrobial resistance microbiological hazards coming from companion animals to humans. The magnitude to which these occur, and the risks posed by the different animal species is still inadequately studied. This is the main goal of the JPI-EC-AMR JTC 2016 Pet-Risk Consortium (Portugal, Germany, Switzerland, UK, Canada) JPIAMR/0002/2016 under the CIISA Antibiotic Lab Team Leader Coordination.
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Keywords
1 The Antimicrobial Use in Veterinary Medicine
The increase in antimicrobial resistance represents a major threat to human and animal health (WHO 2017a). As a result, we are now faced with the reduction of treatment options and with potential therapeutic failure leading veterinarians to use antimicrobials off-label and physicians to use last resort antimicrobials.
There is a growing concern related to the use of antimicrobials in food-producing and companion animals as a potential source for antimicrobial resistance to humans (Greko et al. 2009; Catry et al. 2010; van Duijkeren et al. 2014; Pomba et al. 2017). In fact, it is known that the use of antimicrobials increases the risk of antimicrobial resistance and the risk of colonization with antimicrobial-resistant bacteria (Barza and Travers 2002; Belas et al. 2014).
Since 2010, the European Medicine Agency started reporting data on antimicrobial sales for companion animals (EMA 2017b). Beta-lactams, including potentiated penicillins, were the most frequently sold for companion animals in most European countries, including Portugal (EMA 2017b). Furthermore, fluoroquinolones were the second most sold in Portugal.
It should be noted that the most sold antimicrobials in companion animals worldwide overlap those routinely used in human medicine and are considered as critically important antimicrobials to humans by the World Health Organization (WHO 2016b). Interestingly, the problems of antimicrobial resistance development and infection control in small animal hospitals are mimicking those in human hospitals (ECDC 2017). Furthermore, in contrast to food-producing animals, the prescription of antimicrobials only approved for human use may occur under the cascade principles in companion animals (Pomba et al. 2017). This represents an additional antimicrobial resistance selective pressure towards last resorts antimicrobials and warrants the need for a One Health approach to fighting the dissemination of antimicrobial resistance.
2 Risk of Transfer of Antimicrobial-Resistant Bacteria
The number of companion animals has significantly increased over the last 50 years (Guardabassi et al. 2004; Pomba et al. 2017). The closer contact between owners and companion animals creates opportunities for pathogen interchange through direct and indirect contact (Guardabassi et al. 2004; Damborg et al. 2016).
The public health risks associated with the transfer of antimicrobial-resistant bacteria from companion animals have been reviewed in the European Medicine Agency and its Antimicrobial Working Party reflection paper (Pomba et al. 2017). Pomba et al. (2017) alerted for existence of several antimicrobial resistance microbiological hazards coming from companion animals to humans (Table 1).
The concerns surrounding the role of companion animals in the dissemination of resistant bacteria to humans are strengthened by numerous studies reporting the colonization and/or infection of companion animals with bacteria harboring clinically relevant antimicrobial resistance mechanisms or bacteria belonging to high-risk clonal lineages to humans (Guardabassi et al. 2004; Damborg et al. 2016; Pomba et al. 2017).
This has been one of the main focus of the research conducted in the Antibiotic Resistance Laboratory in Enterobacteriaceae, non-Enterobacteriaceae, Staphylococci and Enterococci (Féria et al. 2001a; Féria et al. 2001b; Caniça et al. 2004; Delgado et al. 2007; Braga et al. 2011; Couto et al. 2011; Pinho et al. 2013; Catry et al. 2015; Couto et al. 2015a; Razuaskas et al. 2015a; Razuaskas et al. 2015b; Couto et al. 2016a; Couto et al. 2016b; Razuaskas et al. 2016; Pomba et al. 2017; Costa et al. 2018; Marconi et al. 2018; Marques et al. 2018; Rodrigues et al. 2018; Belas et al. 2019; Marques et al. 2019a; Marques et al. 2019b).
3 Antimicrobial Resistance Mechanisms and Bacteria of Concern
3.1 Staphylococci
Portugal is among the European countries with higher frequency of methicillin-resistance in invasive Staphylococcus aureus from humans (ECDC 2009). Methicillin-resistant Staphylococcus aureus (MRSA) have been detected in a wide number of animal species (Catry et al. 2010; Pomba et al. 2017), including in Portugal (Coelho et al. 2011; Couto et al. 2014b; Beça et al. 2015; Couto et al. 2015b; Couto et al. 2016a; Rodrigues et al. 2018).
In companion animals, MRSA has been isolated from skin and soft-tissue infections, post-surgical wound infections, urinary tract infections and pneumonia (Catry et al. 2010; Pomba et al. 2017). In a study from Portugal, conducted in the Antibiotic Resistance Laboratory, several MRSA were detected in companion animals with skin and urinary tract infections (Couto et al. 2016c). Notably the MRSA strains isolated from companion animals belonged to CC5 which is a lineage associated with human infection in Portugal (Couto et al. 2015a; Couto et al. 2016c).
In fact, the similarity of MRSA clonal lineages isolated from companion animals and humans has been reported worldwide (Weese and Duijkeren 2010; Pomba et al. 2017). In another study about the clonal diversity, virulence patterns and antimicrobial and biocide susceptibility among human, animal and environmental MRSA in Portugal, S. aureus clonal lineages from companion animals (CC5 and CC22) were associated with specific sets of virulence genes and often with a lower number of resistance genes than isolates belonging to the livestock associated CC398 (Couto et al. 2015b). Colonization of companion animals with MRSA has been previously reported ranging from 0% to 7% (Leornardo and Markey 2008; Catry et al. 2010; Pomba et al. 2017). In one study from Portugal, 1.4% of cats and 0.7% of dogs were reported to be colonized by MRSA (Couto et al. 2014b).
The risk of transmission of MRSA between companion animals and humans has been demonstrated highlighting the role of both species in this issue (Damborg et al. 2016; Pomba et al. 2017). Interestingly, veterinary staff seems to be at higher risk of being colonized by MRSA (Baptiste et al. 2005; Loeffler et al. 2005; Catry et al. 2010, Pomba et al. 2017). Besides MRSA, companion animal health care providers from Portugal also had a high frequency of colonization by methicillin resistant Staphylococcus epidermidis (MRSE) (Rodrigues et al. 2018). MRSAs colonizing humans from this study belonged to the major human healthcare clone in Portugal (ST22-t032-IV), the livestock-associated MRSA (ST398-t108-V) and to the New York-/Japan-related clone (ST105-t002-II) (Rodrigues et al. 2018). Furthermore, S. epidermidis is an important nosocomial pathogen responsible for life-threatening infections associated with the use of medical devices and in immunocompromised individuals, whose management is hindered by frequent resistance to antimicrobials (Costa et al. 2018).
Most infections in companion animals are caused by Staphylococcus pseudintermedius, especially in dogs (Couto et al. 2016a; Couto et al. 2016b). The detection of multidrug-resistant methicillin-resistant S. pseudintermedius (MRSP) is increasingly being reported leading to significant therapeutic limitation in small animal veterinary medicine (Couto et al. 2014b; Couto et al. 2016a; Couto et al. 2016b; Pomba et al. 2017). A significant increase in the detection of multidrug-resistant MRSP has been recently noted in companion animals from Portugal (Lisbon) (Couto et al. 2016a). Although methicillin-susceptible S. pseudintermedius isolates are genetically diverse, a limited number of MRSP clones have spread worldwide resembling the worldwide dissemination of MRSA (Van Duijkeren et al. 2011; Pomba et al. 2017). Like MRSA, the emergence of MRSP represents a great problem for small animal veterinary medicine since S. pseudintermedius is the primary staphylococcal species colonizing healthy dogs and cats. MRSP colonization is more common in dogs than in cats. Furthermore, MRSP can cause many types of infections in companion animals as skin and ear infections, surgical site infections, gingivitis, hepatitis, urinary tract infections, respiratory infections, arthritis, peritonitis and septicaemia (Van Duijkeren et al. 2011; Pomba et al. 2017). It is important to keep in mind that veterinary hospitals and clinics play an important role in the dissemination control of MRSP (Pomba et al. 2017).
In Portugal, the Antibiotic Resistance Laboratory has conducted extensive studies about the S. pseudintermedius (MRSP and MSSP) colonization and infection in dogs and cats to characterize their clonality, antimicrobial susceptibility, biocide susceptibility and immunogenic properties (Couto et al. 2014a; Couto et al. 2015b; Couto et al. 2016c; Couto et al. 2016b). A worrying finding from these studies was the significant increase in staphylococci resistance, mainly S. pseudintermedius, to a large number of antimicrobials over the last 16 years (Couto et al. 2016a). Importantly, this included an increase in the detection of multidrug-resistant MRSP and the mecA gene (Couto et al. 2016b). The increase of MRSP in Portugal was linked to the dissemination of the S. pseudintermedius clonal lineage ST71-II-III, which is also the most disseminated clonal lineage in dogs and cats from Europe (Kadlec et al. 2010; Perreten et al. 2010).
Colonization of humans with S. pseudintermedius seems to be uncommon and transient, however owners and veterinarians in contact with infected companion animals may have a higher risk of being MRSP positive (Pomba et al. 2017). There are some reports of colonization of veterinarians by MRSP that could suggest an occupational risk (Sasaki et al. 2007; Ishihara et al. 2010; Paul et al. 2011; Soedarmanto et al. 2011; Gómez-Sanz et al. 2013; Chanchaithong et al. 2014; Pomba et al. 2017). Furthermore, in 2014 a cluster of infections in a tertiary hospital due to MRSP clone ST71 was described in humans (Starlander et al. 2014).
While MRSA strains isolated from companion animals are mainly related to different human-associated MRSA clones, the scenario for MRSP is different. Diverse SCCmec elements occur among the different MRSP genetic lineages, suggesting that the mecA gene has been acquired by different S. pseudintermedius strains on multiple occasions. (Pomba et al. 2017). Transfer of SCCmec elements between different staphylococcal species is possible, which is a concern.
3.2 Enterococci
Enterococci are opportunistic pathogens, that have become an important cause of nosocomial and community-acquired infections, such as septicemia, endocarditis, UTI and diarrhea. Moreover, these bacteria are an important key indicator for several human and veterinary resistance surveillance systems (Torres et al. 2018). Enterococcus faecalis and Enterococcus faecium are the most common species isolated from human and companion animal infections. Enterococci are intrinsically resistant to several antimicrobials which have important therapeutic implications (Torres et al. 2018). Therefore, acquired resistance to ampicillin/penicillin and to high-level gentamicin, a classic therapeutic synergetic combination, strongly limits the treatment options against enterococcal infections (Chow, 2000). Such resistance mechanisms have been described in enterococci isolated from companion animals from Portugal (Delgado et al. 2007; Marques et al. 2018b).
Some studies provide that healthy livestock, wildlife, food-producing animals and companion animals can harbour pathogenic Enterococci that can be transferred via food chain or through close contact with humans. Furthermore, some Enterococci species are able to evolve from being simple commensal bacteria to being pathogenic to humans and animals through the acquisition of virulence factors encoded in mobile genetic elements (Bortolaia and Guardabassi 2015; Pillay et al. 2018).
For instance, the E. faecalis ST16 clonal lineage is considered a zoonotic pathogen and food and industries seem to have contributed to its dissemination (Torres et al. 2018). Furthermore, this clonal lineage is frequent among high-level gentamicin resistant strains harboring the bifunctional enzyme (Ruiz-Garbajosa et al. 2006). Other important Enterococci high-risk clonal complexes (CC) associated with nosocomial infections in humans include the E. faecalis CC6 (formerly CC2) and the ampicillin-resistant E. faecium CC17 (Leavis et al. 2006; Kuch et al. 2012).
Due to its clinical relevance, the Antibiotic Resistance Laboratory has contributed with epidemiological studies about the antimicrobial resistance and population structure of enterococci isolated in Portugal (Delgado et al. 2007; Pomba et al. 2010; Braga et al. 2011; Braga et al. 2013; Marques et al. 2018a). In one of these studies, the first report of a biocide resistance mechanism in E. faecalis and its dissemination amongst the genus Enterococcus was reported (Braga et al. 2011).
Ampicillin-resistance and/or high-level gentamicin resistance in enterococci from companion animals with UTI in Portugal (Lisbon) over 16 years was low when compared with the resistance frequencies detected in Enterobacteriaceae (Marques et al. 2019a). However, many of these isolates belonged to E. faecalis ST16, E. faecalis CC6 and to the ampicillin-resistant E. faecium CC17. Interestingly, a previous study has shown that healthy dogs seem to be reservoirs of ampicillin-resistant E. faecium CC17 (Damborg et al. 2009).
The acquired resistance to vancomycin due to van gene carriage is another resistance mechanism of great importance in human medicine (Pomba et al. 2017). Ampicillin-resistance in E. faecium from Europe seams to often predict the increase in the rates of vancomycin-resistant enterococci (VRE) within some years (Werner et al. 1904). Although, the level of ampicillin-resistant E. faecium in companion animals with UTI was low, higher frequencies have been reported in other parts of Europe (Damborg et al. 2009). Therefore, active surveillance is imperative.
Healthy dogs and cats may become colonized by VRE. Furthermore, VRE isolated from companion animals may also belong to clonal lineages associated with hospital-acquired infections (Pomba et al. 2017).
4 Enterobacteriaceae and Non-Enterobacteriaceae
There are a large number of studies reporting the detection of extended spectrum beta- lactamases (ESBLs) - producing bacteria in companion animal infections and in colonized animals (Ewers et al. 2012; Belas et al. 2014; Pomba et al. 2014a; Damborg et al. 2015; Pomba et al. 2017).
Detection of carbapenemase-producing Enterobacteriaceae and non-Enterobacteriaceae are still a rare event; however, reports in healthy and sick animals are increasing by the day, and will likely become a serious problem in the future (Pomba et al. 2014b; Chanchaithong et al. 2014; Gentilini et al. 2018; Grönthal et al. 2015; Köck et al. 2018).
The Antibiotic Resistance Laboratory has made the first description of an OXA-23-producing ST2 MDR Acinetobacter baumannii in a cat with urinary tract infection (UTI) (Pomba et al. 2014a). Just recently, the transmission of a canine clinical NDM-5 Escherichia coli between an infected dogs and humans was confirmed for the first time (Grönthal et al. 2015) giving additional scientific support to the concerns surrounding the close contact of companion animals with humans (Pomba et al. 2017).
Although less studied than other Gram-Negative bacteria, Pseudomonas aeruginosa is an important pathogen causing otitis and pyoderma in companion animals (Pomba et al. 2017). Notably, carbapenem-producing strains have already been detected in dogs (Hyun et al. 2018). Also, some infections caused by these bacteria are in association with other pathogens, such as MRSP (Lupo et al. 2017).
In an ongoing study conducted in the Antibiotic Resistance laboratory, P. aeruginosa causing external otitis in companion animals from Portugal (Lisbon) showed high resistance levels towards fluoroquinolones and aminoglycosides, which are frequently used topically. Furthermore, resistance to imipenem and doripenem was also noted (Marconi et al. 2018).
Companion animals have been found to be colonized by E. coli and Klebsiella. pneumoniae belonging to important clonal lineages to humans (Pomba et al. 2014b; Johnson et al. 2016; Pomba et al. 2017; Marques et al. 2018; Belas et al. 2019; Marques et al. 2019a). Since many pathogenic bacteria, are thought to make part of the normal gut flora (Podschun and Ullmann 1998; Drzewiecka 2016; Johnson et al. 2016; Martin et al. 2016), gut colonization of companion animals may also represent an important hazard. Interestingly, pet ownership (dogs, cats and other companion animals) was suggested to be a risk factor for human gut colonization by ESBL-producing E. coli (Meyer et al. 2012).
Regarding Enterobacteriaceae, companion animals from the same household may be colonized and share the uropathogenic E. coli O25B: H4: B2-ST131 clonal lineage (Johnson et al. 2009; Johnson et al. 2016). More importantly, humans and dogs with UTI have been shown to share the index uropathogenic E. coli with household members including the family dogs and cats (Murray et al. 2004; Johnson and Clabots 2016). Just recently, in a study conducted by the Antibiotic Resistance Laboratory, companion animals and humans living in close contact were screened for colonization by K. pneumoniae and Proteus mirabilis (Marques et al. 2018a; Marques et al. 2019a). Interestingly, some dogs and humans were shown to be colonized in the gut by undistinguishable (by PFGE and MLST) K. pneumoniae strains, suggesting the possibility of transmission between dogs and humans (Marques et al. 2018a).
Besides beta-lactams, the dissemination of colistin resistance plasmids mcr-1 to 7 has been recently on the spotlight (Yang et al. 2018). The dissemination of MDR carbapenemase-producing bacteria in human medicine has led to the need to return to old antimicrobials such as colistin. The recent identification of the colistin resistance gene mcr-1 in food-production animals and companion animals in multiple countries is a concern (Liu et al. 2016; Perreten et al. 2010; Schwarz et al. 2016). In Portugal, mcr-producing Enterobacteriaceae have been identified in retail meat (Figueiredo et al. 2016); clinical strains (Campos et al. 2011; Mendes et al. 2018) and food producing animals (Kieffer et al. 2017; Freitas-Silva et al. 2018). Moreover, a recent report of a mcr-1-containing E. coli in a person and in multiple dogs and cats heightens these concerns (Zhang et al. 2016).
5 The Future
The current scientific knowledge seems to support the suspicion that companion animals may act in the dissemination of resistant and pathogenic bacterial clones to humans and vice versa.
However, several questions still remain answered. Skin (including ear) and urinary tract infections are the most frequent infection in companion animals. Previously published data, including from the Antibiotic Resistance Laboratory (Féria et al. 2001a; Féria et al. 2001b; Caniça et al. 2004; Delgado et al. 2007; Braga et al. 2011; Couto et al. 2011; Pinho et al. 1099; Catry et al. 2015; Couto et al. 2015a; Razuaskas et al. 2015a; Razuaskas et al. 2015b; Couto et al. 2016a; Couto et al. 2016b; Razuaskas et al. 2016; Pomba et al. 2017; Costa et al. 2018; Marques et al. 2018a; Rodrigues et al. 2018; Belas et al. 2019; Marques et al. 2019a; Marques et al. 2019b), have shown that bacteria causing skin infections and UTIs in companion animals are sometimes associated with major resistance mechanisms and bacterial clonal lineages. Furthermore, several studies support the sharing/transmission of important bacterial clonal lineages between companion animals and humans (Johnson and Clabots 2016; Murray et al. 2004; Johnson et al. 2009; Johnson et al. 2016; Marques et al. 2018a; Marques et al. 2019b). However, the extent to which such transfer occur is still poorly studied. The main goal of the JPI-EC-AMR JTC 2016 Pet-Risk Consortium (Portugal, Germany, Switzerland, UK, Canada) JPIAMR/0002/2016 under CIISA Antibiotic Lab Team Leader Coordination is to clarify the extent of transmission and whether different types of infections may convey additional risk to humans or vice-versa. This project will stand on edge using Next Generation Sequencing technologies to unequivocally evaluate the transmission of clinically relevant antimicrobial mechanisms and pathogenic bacteria.
As a laboratory devoted to the study of antimicrobial resistance in veterinary medicine, it is its mission to reach out to the society (clinicians and owners) in the pursuit of better antimicrobial use practices. The development of antimicrobial stewardship programs as long started in human medicine and are urgently needed in veterinary medicine (Loyd and Page 2017). Antimicrobial stewardship programs are complex and require the interaction of multidisciplinary teams. Such programs aim at creating strategies to promote the rational use of antimicrobials, improve infection control measures and consequently decrease the spread of pathogenic and resistant bacteria (Loyd and Page 2017).
Evidence based learning is the key to fight antimicrobial resistance in a One health approach and pursuing the 5Rs of antimicrobial stewardship: Responsibility, Reduction, Refinement, Replacement and Review (Weese et al. 2013; Loyd and Page 2017). Recently, the European Society of Clinical Microbiology and Infection Diseases Study Group on Veterinary Microbiology started regular post-graduate courses of antimicrobial stewardship in veterinary medicine representing a landmark towards a better future and in which the Antibiotic Resistance Laboratory team leader collaborates as a regular speaker.
The future of antibiotic resistance and pathogenic bacteria is still uncertain, but the Antibiotic Resistance laboratory will continue to focus its efforts in obtaining useful epidemiological data, guide antimicrobial use through the establishment of antimicrobial stewardship programs, and reaching the society to increase awareness and help to improve this worldwide problem.
References
Baptiste, K.E., Williams, K., Willams, N.J., Wattret, A., Clegg, P.D., Dawson, S., Corkill, J.E., O’Neill, T., Hart, C.A.: Methicillin-resistant staphylococci in companion animals. Emerg. Infect. Dis. 11, 1942–1944 (2005)
Barza, M., Travers, K.: Excess infections due to antimicrobial resistance: the attributable fraction. Clin. Infect. Dis. 34, 126–130 (2002)
Beça, N., Bessa, L.J., Mendes, Â., Santos, J., Leite-Martins, L., Matos, A.J., da Costa, P.M.: Coagulase-positive staphylococcus: prevalence and antimicrobial resistance. J. Am. Anim. Hosp. Assoc. 51, 365–371 (2015)
Belas, A., Marques, C., Aboim, C., Pomba, C.: Emergence of Escherichia coli ST131 H30/H30-Rx subclones in companion animals. J. Antimicrob. Chemother. 74, 266–269 (2019). https://doi.org/10.1093/jac/dky381
Belas, A., Salazar, A.S., Telo da Gama, L., Couto, N., Pomba, C.: Risk factors for faecal colonisation with Escherichia coli producing extended-spectrum and plasmid-mediated AmpC β-lactamases in dogs. Vet. Rec. 175(8), 202 (2014)
Braga, T.M., Marujo, P.E., Pomba, C., Lopes, M.F.: Involvement, and dissemination, of the enterococcal small multidrug resistance transporter QacZ in resistance to quaternary ammonium compounds. J. Antimicrob. Chemother. 66(2), 283–286 (2011). https://doi.org/10.1093/jac/dkq460
Braga, T.M., Pomba, C., Lopes, M.F.: High-level vancomycin resistant Enterococcus faecium related to humans and pigs found in dust from pig breeding facilities. Vet. Microbiol. 161(3–4), 344–349 (2013). https://doi.org/10.1016/j.vetmic.2012.07.034
Bortolaia, V., Guardabassi, L.: Zoonotic transmission of antimicrobial resistant enterococci a threat to public health or an overemphasized risk?. In: Zoonoses infection Affecting Humans and animals. Focus on Public Health Aspects, pp. 407–431. Springer, New York (2015)
Campos, J., Cristino, L., Peixe, L., Antunes, P.: MCR-1 in multidrug-resistant and copper-tolerant clinically relevant Salmonella 1,4,[5],12:i:- and S. Rissen clones in Portugal, 2011 to 2015. Euro Surveill. 21(26) (2016). https://doi.org/10.2807/1560-7917.es.2016.21.26.30270
Caniça, M., Dias, R., Correia, J.D., Pomba, C.: Genetic relatedness between human and animal polymorphic blaTEM genes strengthens zoonotic potential among uropathogenic Escherichia coli strains. J. Antimicrob. Chemother. 54(1), 284–286 (2004). https://doi.org/10.1093/jac/dkh307
Catry, B., Cavaleri, M., Baptiste, K., Grave, K., Grein, K., Holm, A., Jukes, H., Liebana, E., Lopez Navas, A., Macka, D., Magiorakos, A.P., Moreno Romo, M.A., Moulin, G., Muñoz Madero, C., Matias Ferreira Pomba, M.C., Powell, M., Pyörälä, S., Rantala, M., Ružauskas, M., Sanders, P., Teale, C., Threlfall, E.J., Törneke, K., van Duijkeren, E., Torren, E.J.: Use of colistin-containing products within the European Union and European Economic Area (EU/EEA): development of resistance in animals and possible impact on human and animal health. Int. J. Antimicrob. Agents 46(3), 297–306 (2015). https://doi.org/10.1016/j.ijantimicag.2015.06.005
Catry, B., Van Duijkeren, E., Pomba, M.C., Greko, C., Moreno, M.A., Pyörälä, S., Ružauskas, M., Sanders, P., Threlfall, E.J., Ungemach, F., Törneke, K., Munoz-Madero, C., Torren-Edo, J.: Scientific Advisory Group on Antimicrobials (SAGAM) (2010). Reflection paper on MRSA in food -producing and companion animals: epidemiology and control options for human and animal health Epidemiology and Infection 138(5):626–44
Chanchaithong, P., Perreten, V., Schwendener, S., Tribuddharat, C., Chongthaleong, A., Niyomtham, W., Prapasarakul, N.: Strain typing and antimicrobial susceptibility of methicillin-resistant coagulase-positive staphylococcal species in dogs and people associated with dogs in Thailand. J. Appl. Microbiol. 117, 572–586 (2014)
Chow, J.W.: Aminoglycoside resistance in enterococci. Clin. Infect. Dis. 31, 586–589 (2000)
Coelho, C., Torres, C., Radhouani, H., Pinto, L., Lozano, C., Gómez-Sanz, E., Zaragoza, M., Igrejas, G., Poeta, P.: Molecular detection and characterization of methicillin-resistant Staphylococcus aureus (MRSA) isolates from dogs in Portugal. Microb. Drug Resist. 17, 333–337 (2011)
Costa, S.S., Viveiros, M., Pomba, C., Couto, I.: Active antimicrobial efflux in Staphylococcus epidermidis: building up of resistance to fluoroquinolones and biocides in a major opportunistic pathogen. J. Antimicrob. Chemother. 73(2), 320–324 (2018)
Couto, N., Belas, A., Centeno, M., van Duijkeren, E., Pomba, C.: First description of fexA-positive methicillin-resistant Staphylococcus aureus ST398 from calves in Portugal. J. Global Antimicrob. Resist. 2(4), 342–343 (2014a)
Couto, N., Belas, A., Couto, I., Perreten, V., Pomba, C.: Genetic relatedness, antimicrobial and biocide susceptibility comparative analysis of methicillin-resistant and -susceptible Staphylococcus pseudintermedius from Portugal. Microb. Drug Resist. 20(4), 364–371 (2014b)
Couto, N., Belas, A., Kadlec, K., Schwarz, S., Pomba, C.: Clonal diversity, virulence patterns and antimicrobial and biocide susceptibility among human, animal and environmental MRSA in Portugal. J. Antimicrob. Chemother. 70(9), 2483–2487 (2015a)
Couto, N., Belas, A., Oliveira, M., Almeida, P., Clemente, C., Pomba, C.: Comparative RNA-seq-based transcriptome analysis of the virulence characteristics of methicillin-resistant and -susceptible Staphylococcus pseudintermedius strains isolated from small animals. Antimicrob. Agents Chemother. 60(2), 962–967 (2015b)
Couto, N., Belas, A., Rodrigues, C., Schwarz, S., Pomba, C.: Acquisition of the fexA and cfr genes in Staphylococcus pseudintermedius during florfenicol treatment of canine pyoderma. J. Glob. Antimicrob. Resist. 7, 126–127 (2016a)
Couto, N., Martins, J., Lourenço, A.M., Pomba, C., Varela, C.A.: Identification of vaccine candidate antigens of Staphylococcus pseudintermedius by whole proteome characterization and serological proteomic analyses. J. Proteomics 133, 113–124 (2016b)
Couto, N., Monchique, C., Belas, A., Marques, C., Gama, L.T., Pomba, C.: Trends and molecular mechanisms of antimicrobial resistance in clinical staphylococci isolated from companion animals over a 16-year period. J. Antimicrob. Chemother. 71(6), 1479–1487 (2016c)
Couto, N., Pomba, C., Moodley, A., Guardabassi, L.: Prevalence of methicillin-resistant staphylococci among dogs and cats at a veterinary teaching hospital in Portugal. Vet. Rec. 169(3), 72 (2011)
Leavis, H.L., Bonten, M.J., Willems, R.J.: Identification of high-risk enterococcal clonal complexes: global dispersion and antibiotic resistance. Curr. Opin. Microbiol. 9, 454–460 (2006)
Damborg, P., Broens, E.M., Chomel, B.B., Guenther, S., Pasmans, F., Wagenaar, J.A., Weese, J.S., Wieler, L.H., Windahl, U., Vanrompay, D., Guardabassi, L.: Bacterial zoonoses transmitted by household pets: state-of-the-art and future perspectives for targeted research and policy actions. J. Comp. Pathol. 155, S27–S40 (2016)
Damborg, P., Morsing, M.K., Petersen, T., Bortolaia, V., Guardabassi, L.: CTX-M-1 and CTX-M-15-producing Escherichia coli in dog faeces from public gardens. Acta Vet. Scand. 57, 83 (2015)
Damborg, P., Top, J., Hendrickx, A.P., Dawson, S., Willems, R.J., Guardabassi, L.: Dogs are a reservoir of ampicillin-resistant Enterococcus faecium lineages associated with human infections. Appl. Environ. Microbiol. 75, 2360–2365 (2009)
Delgado, M., Neto, I., Correia, J.H., Pomba, C.: Antimicrobial resistance and evaluation of susceptibility testing among pathogenic enterococci isolated from dogs and cats. Int. J. Antimicrob. Agents 30(1), 98–100 (2007)
Drzewiecka, D.: Significance and roles of Proteus spp. bacteria in natural environments. Microb. Ecol. 72, 741–758 (2016)
ECDC: Surveillance of antimicrobial resistance in Europe 2016. Annual Report of the European Antimicrobial Resistance Surveillance Network (EARS-Net). ECDC, Stockholm (2017)
ECDC, EFSA, EMEA.: Joint scientific report of ECDC, EFSA and EMEA on methicillin-resistant Staphylococcus aureus (MRSA) in livestock, companion animals and food. Summary of the scientific Opinion of the Panel on Biological Hazards (EFSA/BIOHAZ) on “Assessment of the Public Health significance of methicillin-resistant Staphylococcus aureus (MRSA) in animals and foods” and the Reflection paper of the Committee for Medicinal Products for Veterinary Use (EMEA/CVMP) on “MRSA in food producing (2009)
EMA: Sales of veterinary antimicrobial agents in 30 European countries in 2015 (2017b). http://www.ema.europa.eu/docs/en_GB/document_library/Report/2017/10/WC500236750.pdf. Accessed Mar 2018
Ewers, C., Bethe, A., Semmler, T., Guenther, S., Wieler, L.H.: Extended-spectrum β-lactamase-producing and AmpC-producing Escherichia coli from livestock and companion animals, and their putative impact on public health: a global perspective. Clin. Microbiol. Infect. 18, 646–655 (2012)
Féria, C., Machado, J., Duarte Correia, J., Gonçalves, J., Gaastra, W.: Virulence genes and P fimbriae PapA subunit diversity in canine and feline uropathogenic Escherichia coli. Vet. Microbiol. 82(1), 81–89 (2001a)
Féria, C., Machado, J., Duarte Correia, J., Gonçalves, J., Gaastra, W.: Distribution of papG alleles among uropathogenic Escherichia coli isolated from different species. FEMS Microbiol. Lett. 202, 205–208 (2001b)
Figueiredo, R., Card, R.M., Nunez, J., Pomba, C., Mendonça, N., Anjum, M.F., Da Silva, G.J.: Detection of an mcr-1-encoding plasmid mediating colistin resistance in Salmonella enterica from retail meat in Portugal. J. Antimicrob. Chemother. 8, 2338–2340 (2016)
Freitas-Silva, J., Inácio, S., Mourão, J., Antunes, P., Mendes, A., de Carvalho, A.P., Vasconcelos, V., Peixe, L., da Costa, P.M.: Occurrence of mcr-1 in Escherichia coli from rabbits of intensive farming. Vet. Microbiol. 227, 78–81 (2018)
Gentilini, F., Turba, M.E., Pasquali, F., Mion, D., Romagnoli, N., Zambon, E., Terni, D., Peirano, G., Pitout, J.D.D., Parisi, A., Sambri, V., Zanoni, R.G.: Hospitalized pets as a source of Carbapenem-resistance. Front. Microbiol. 6(9), 2872 (2018)
Gómez-Sanz, E., Torres, C., Lozano, C., Zarazaga, M.: High diversity of Staphylococcus aureus and Staphylococcus pseudintermedius lineages and toxigenic traits in healthy pet-owning household members. Underestimating normal household contact? Comp. Immunol. Microbiol. Infect. Dis. 36, 83–94 (2013)
Greko, C., Badiola, J.I., Catry, B., van Duijkeren, E., Moreno, M.A., Pomba, M.C.: Scientific advisory group on antimicrobials of the committee for medicinal products for veterinary use, European Medicines Agency (EMEA) (2009). Reflection paper on the use of third and fourth generation cephalosporins in food producing animals in the European Union: development of resistance and impact on human and animal health. J. Vet. Pharmacol. Ther. 32, 515–533
Grönthal, T., Österblad, M., Eklund, M., Jalava, J., Nykäsenoja, S., Pekkanen, K., Rantala, M.: Sharing more than friendship - transmission of NDM-5 ST167 and CTX-M-9 ST69 Escherichia coli between dogs and humans in a family, Finland, 2015. Euro Surveill. 23(27), 1700497 (2018)
Guardabassi, L., Schwarz, S., Lloyd, D.H.: Pet animals as reservoirs of antimicrobial-resistant bacteria. J. Antimicrob. Chemother. 54(2), 321–332 (2004)
Ishihara, K., Shimokubo, N., Sakagami, A., Ueno, H., Muramatsu, Y., Kadosawa, T., Yanagisawa, C., Hanaki, H., Nakajima, C., Suzuki, Y., Tamura, Y.: Occurrence and molecular characteristics of methicillin-resistant Staphylococcus aureus and methicillin-resistant Staphylococcus pseudintermedius in an academic veterinary hospital. Appl. Environ. Microbiol. 76, 5165–5174 (2010)
Hyun, J.E., Chung, T.H., Hwang, C.Y.: Identification of VIM-2 metallo-β-lactamase-producing Pseudomonas aeruginosa isolated from dogs with pyoderma and otitis in Korea. Vet. Dermatol. 29(186), e68 (2018)
Johnson, J.R., Menard, M., Johnston, B., Kuskowski, M.A., Nichol, K., Zhanel, G.G.: Epidemic clonal groups of Escherichia coli as a cause of antimicrobial-resistant urinary tract infections in Canada, 2002 to 2004. Antimicrob. Agents Chemother. 53, 2733–2739 (2009)
Johnson, J.R., Davis, G., Clabots, C., Johnston, B.D., Porter, S., DebRoy, C., Pomputius, W., Ender, P.T., Cooperstock, M., Slater, B.S., Banerjee, R., Miller, S., Kisiela, D., Sokurenko, E.V., Aziz, M., Price, L.B.: Household clustering of Escherichia coli sequence type 131 clinical and fecal isolates according to whole genome sequence analysis. Open Forum Infect. Dis. 3(3), 16 (2016). ofw129. eCollection
Johnson, J.R., Owens, K., Gajewski, A., Clabots, C.: Escherichia coli colonization patterns among human household members and pets, with attention to acute urinary tract infection. J. Infect. Dis. 197, 218–224 (2008)
Kadlec, K., Schwarz, S., Perreten, V., Andersson, U.G., Finn, M., Greko, C., Moodley, A., Kania, S.A., Frank, L.A., Bemis, D.A., Franco, A., Iurescia, M., Battisti, A., Duim, B., Wagenaar, J.A., van Duijkeren, E., Weese, J.S., Fitzgerald, J.R., Rossano, A., Guardabassi, L.: Molecular analysis of methicillin-resistant Staphylococcus pseudintermedius of feline origin from different European countries and North America. J. Antimicrob. Chemother. 65, 1826–1828 (2010)
Kieffer, N., Aires-de-Sousa, M., Nordmann, P., Poirel, L.: High Rate of MCR-1-Producing Escherichia coli and Klebsiella pneumoniae among Pigs, Portugal. Emerg. Infect. Dis. 12, 2023–2029 (2017)
Köck, R., Daniels-Haardt, I., Becker, K., Mellmann, A., Friedrich, A.W., Mevius, D., Schwarz, S., Jurke, A.: Carbapenem-resistant Enterobacteriaceae in wildlife, food-producing, and companion animals: a systematic review. Clin. Microbiol. Infect. 24, 1241–1250 (2018)
Leonard, F.C., Markey, B.K.: Methicillin-resistant Staphylococcus aureus in animals: a review. Vet. J. 175, 27–36 (2008)
Kuch, A., Willems, R.J., Werner, G., Coque, T.M., Hammerum, A.M., Sundsfjord, A., Klare, I., Ruiz-Garbajosa, P., Simonsen, G.S., van Luit-Asbroek, M., Hryniewicz, W., Sadowy, E.: Insight into antimicrobial susceptibility and population structure of contemporary human Enterococcus faecalis isolates from Europe. J. Antimicrob. Chemother. 67, 551–558 (2012)
Loyd, D.H., Page, S.W.: Antimicrobial stewardship in veterinary medicine. Microbiol. Spectr. 6(3), ARBA-0023-2017 (2018)
Loeffler, A., Boag, A.K., Sung, J., Lindsay, J.A., Guardabassi, L., Dalsgaard, A., Smith, H., Stevens, K.B., Lloyd, D.H.: Prevalence of methicillin-resistant Staphylococcus aureus among staff and pets in a small animal referral hospital in the UK. J. Antimicrob. Chemother. 56, 692–697 (2005)
Lupo, A., Haenni, M., Madec, J.Y.: Antimicrobial resistance in Acinetobacter spp and Pseudomonas spp. Microb. Spect. 6(3), ARBA-0007-2017 (2018)
Marconi, C., Belas, A., Pomba, C.: Emergence of carbapenemase-resistant Pseudomonas aeruginosa isolates from otitis externa in companion animals. In: 30th European Veterinary Dermatology Congress (ESVD-ECVD), 27–29 September, Dubrovnik Croatia (2018)
Marques, C., Menezes, J., Belas, A., Aboim, C., Cavaco-Silva, P., Trigueiro, G., Gama, L.T., Pomba, C.: Klebsiella pneumoniae causing urinary tract infection n companion animals and humans: population structure, antimicrobial resistance and virulence genes. J. Antimicrob. Chemother. 74, 594–602 (2019a)
Marques, C., Belas, A., Aboim, C., Trigueiro, G., Cavaco-Silva, P., Gama, L.T., Pomba, C.: Clonal relatedness of Proteus mirabilis strains causing urinary tract infection in companion animals and humans. Vet. Microbiol. 228, 77–82 (2019b)
Marques, C., Belas, A., Menezes, J., Aboim, C., Cavaco-Silva, P., Trigueiro G, Telo Gama, L, Pomba, C.: Companion animals as reservoirs of Klebsiella pneumoniae. [oral communication]. CIISA Congress 2018, 16–17 November 2018, Lisbon, Portugal, p. 70 (2018a)
Marques, C., Belas, A., Franco, A., Aboim, C., Gama, L.T., Pomba, C.: Increase in antimicrobial resistance and emergence of major international high-risk clonal lineages in dogs and cats with urinary tract infection: 16-year retrospective study. J. Antimicrob. Chemother. 73, 377–384 (2018)
Martin, R.M., Cao, J., Brisse, S., Passet, V., Wu, W., Zhao, L., Malani, P.N., Rao, K., Bachman, M.A.: Molecular epidemiology of colonizing and infecting isolates of Klebsiella pneumoniae. mSphere 1, e00261–16 (2016)
Mendes, A.C., Novais, A., Campos, J., Rodrigues, C., Santos, C., Antunes, P., Ramos, H., Peixe, L.: mcr-1 in Carbapenemase-producing Klebsiella pneumoniae with hospitalized patients, Portugal, 2016-2017. Emerg. Infect. Dis. 4, 762–766 (2018)
Meyer, E., Gastmeier, P., Kola, A., Schwab, F.: Pet animals and foreign travel are risk factors for colonisation with extended-spectrum β-lactamase-producing Escherichia coli. Infection 40, 685–687 (2012)
Paul, N.C., Moodley, A., Ghibaudo, G., Guardabassi, L.: Carriage of methicillin-resistant Staphylococcus pseudintermedius in small animal veterinarians: indirect evidence of zoonotic transmission. Zoonoses Public Health 58, 533–539 (2011)
Perreten, V., Kadlec, K., Schwarz, S., Grönlund Andersson, U., Finn, M., Greko, C., Moodley, A., Kania, S.A., Frank, L.A., Bemis, D.A., Franco, A., Iurescia, M., Battisti, A., Duim, B., Wagenaar, J.A., van Duijkeren, E., Weese, J.S., Fitzgerald, J.R., Rossano, A., Guardabassi, L.: Clonal spread of methicillin-resistant Staphylococcus pseudintermedius in Europe and North America: an international multicentre study. J. Antimicrob. Chemother. 65, 1145–1154 (2010)
Pillay, S., Zishiri, O.T., Adeleke, M.A.: Prevalence of virulence genes in Enterococcus species isolated from companion animals and livestock. Onderstepoort J. Vet. Res. 85, e1–e8 (2018)
Pinho, M.D., Matos, S.C., Pomba, C., Lübke-Becker, A., Wieler, L.H., Preziuso, S., Melo-Cristino, J., Ramirez, M.:Multilocus sequence analysis of Streptococcus canis confirms the zoonotic origin of human infections and reveals genetic exchange with Streptococcus dysgalactiae subsp. equisimilis. J. Clin. Microbiol. 51(4), 1099–1109 (2013)
Podschun, R., Ullmann, U.: Klebsiella spp. as nosocomial pathogens: epidemiology, taxonomy, typing methods, and pathogenicity factors. Clin. Microbiol. Rev. 11, 589–603 (1998)
Pomba, C., Couto, N., Moodley, A.: Treatment of a lower urinary tract infection in a cat caused by a multi-drug methicillin-resistant Staphylococcus pseudintermedius and Enterococcus faecalis. J. Feline Med. Surg. 12, 802–806 (2010)
Pomba, C., Endimiani, A., Rossano, A., Saial, D., Couto, N., Perreten, V.: First report of OXA-23-mediated carbapenem resistance in sequence type 2 multidrug-resistant Acinetobacter baumannii associated with urinary tract infection in a cat. Antimicrob. Agents Chemother. 58(2), 1267–1268 (2014a)
Pomba, C., López-Cerero, L., Bellido, M., Serrano, L., Belas, A., Couto, N., Cavaco-Silva, P., Rodríguez-Baño, J., Pascual, A.: Within-lineage variability of ST131 Escherichia coli isolates from humans and companion animals in the south of Europe. J.l Antimicrob. Chemother. 69, 271–273 (2014b)
Pomba, C., Rantala, M., Greko, C., Baptiste, K.E., Catry, B., van Duijkeren, E., Mateus, A., Moreno, M.A., Pyörälä, S., Ružauskas, M., Sanders, P., Teale, C., Threlfall, E.J., Kunsagi, Z., Torren-Edo, J., Jukes, H., Törneke, K.: Public health risk of antimicrobial resistance transfer from companion animals. J.l Antimicrob. Chemother. 72(4), 957–968 (2017)
Rodrigues, A.C., Belas, A., Marques, C., Cruz, L., Gama, L.T., Pomba, C.: Risk factors for nasal colonization by methicillin-resistant Staphylococci in healthy humans in professional daily contact with companion animals in Portugal. Microb. Drug Resist. 24(4), 434–446 (2018)
Ruiz-Garbajosa, P., Bonten, M.J., Robinson, D.A., Top, J., Nallapareddy, S.R., Torres, C., Coque, T.M., Cantón, R., Baquero, F., Murray, B.E., del Campo, R., Willems, R.J.: Multilocus sequence typing scheme for Enterococcus faecalis reveals hospital-adapted genetic complexes in a background of high rates of recombination. J. Clin. Microbiol. 44, 2220–2228 (2006)
Ružauskas, M., Couto, N., Kerziene, S., Siugzdiniene, R., Klimiene, I., Virgailis, M., Pomba, C.: Prevalence, species distribution and antimicrobial resistance patterns of methicillin-resistant staphylococci in Lithuanian pet animals. Acta Vet. Scand. 57, 27 (2015)
Ružauskas, M., Couto, N., Pavilonis, A., Klimiene, I., Siugzdiniene, R., Virgailis, M., Vaskeviciute, L., Anskiene, P.C.: Characterization of Staphylococcus pseudintermedius isolated from diseased dogs in Lithuania. Pol. J. Vet. Sci. 19(1), 7–14 (2016)
Ružauskas, M., Couto, N., Siugzdiniene, R., Klimiene, I., Virgailis, M., Vaskeviciute, L., Mockeliunas, R., Pomba, C.: Methicillin-resistant coagulase-negative Staphylococcus spp. prevalence in Lithuanian dogs: a cross-sectional study. Veterinarski Aarhiv 85(2), 175–187 (2015b)
Sasaki, T., Kikuchi, K., Tanaka, Y., Takahashi, N., Kamata, S., Hiramatsu, K.: Methicillin-resistant Staphylococcus pseudintermedius in a veterinary teaching hospital. J. Clin. Microbiol. 45, 1118–1125 (2007)
Soedarmanto, I., Kanbar, T., Ülbegi-Mohyla, H., Hijazin, M., Alber, J., Lämmler, C., Akineden, Ö., Weiss, R., Moritz, A., Zschöck, M.: Genetic relatedness of methicillin-resistant Staphylococcus pseudintermedius (MRSP) isolated from a dog and the dog owner. Res. Vet. Sci. 91, e25–e27 (2011)
Starlander, G., Börjesson, S., Grönlund-Andersson, U., Tellgren-Roth, C., Melhus, A.: Cluster of infections caused by methicillin-resistant Staphylococcus pseudintermedius in humans in a tertiary hospital. J. Clin. Microbiol. 52, 3118–3120 (2014)
Torres, C., Alonso, C.A., Ruiz-ripa, L., Léon-Sampedror, R., del Campo, R., Coque, T.M.: Antimicrobial resistance in Enterococcus spp. of animal origem. Microbiol. Spectr. 6(4), ARBA-0032-2018 (2018)
van Duijkeren, E., Catry, B., Greko, C., Moreno, M.A., Pomba, M.C., Pyörälä, S., Ružauskas, M., Sanders, P., Threlfall, E.J., Torren-Edo, J., Törneke, K.: Scientific advisory group on antimicrobials (SAGAM) (2011). Review on methicillin-resistant Staphylococcus pseudintermedius. J. Antimicrob. Chemother. 66, 2705–2714
van Duijkeren, E., Greko, C., Pringle, M., Baptiste, K.E., Catry, B., Jukes, H., Moreno, M.A., Pomba, M.C., Pyörälä, S., Rantala, M., Ružauskas, M., Sanders, P., Teale, C., Threlfall, E.J., Torren-Edo, J., Törneke, K.: Pleuromutilins: use in food-producing animals in the European Union, development of resistance and impact on human and animal health. J. Antimicrob. Chemother. 69(78), 2022–2031 (2014)
Weese, J.S., van Duijkeren, E.: Methicillin-resistant Staphylococcus aureus and Staphylococcus pseudintermedius in veterinary medicine. Vet. Microbiol. 140, 418–429 (2010)
Weese, J.S., Page, S.W., Prescott, J.F.: Antimicrobial stewardship in animals. In: Giguere, S., Prescott, J.F., Dowling, P.M. (eds.) Antimicrobial Therapy in Veterinary Medicine, pp. 117–132. John Wiley and Sons (2013)
Werner, G., Coque, T.M., Hammerum, A.M., Hope, R., Hryniewicz, W., Johnson, A., Klare, I., Kristinsson, K.G., Leclercq, R., Lester, C.H., Lillie, M., Novais, C., Olsson-Liljequist, B., Peixe, L.V., Sadowy, E., Simonsen, G.S., Top, J., Vuopio-Varkila, J., Willems, R.J., Witte, W., Woodford, N.: Emergence and spread of vancomycin resistance among enterococci in Europe. Euro. Surveill. 13, 19046 (2008)
World Health Organization: Global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics (2017a). http://www.who.int/medicines/publications/WHO-PPL-Short_Summary_25Feb-ET_NM_WHO.pdf. Accessed Mar 2018
World Health Organization: Critically important antimicrobials for human medicine. 5th Revision 2016 (2017b). http://apps.who.int/iris/bitstream/10665/255027/1/9789241512220-eng.pdf. Accessed Mar 2018
Yang, Y.Q., Li, Y.X., Lei, C.W., Zhang, A.Y., Wang, H.N.: Novel plasmid-mediated colistin resistance gene mcr-7.1 in Klebsiella pneumonia. The Journal of Antimicrobial Chemotherapy 73(7), 1791–1795 (2018)
Zhang, X.F., Doi, Y., Huang, X., Li, H.Y., Zhong, L.L., Zeng, K.J., Zhang, Y.F., Patil, S., Tian, G.B.: Possible transmission of mcr-1-Harboring Escherichia coli between companion animals and human. Emerg. Infect. Dis. 9, 1679–1681 (2016)
Acknowledgements
This work was supported by Fundo Europeu de Desenvolvimento Regional (FEDER) funds through the Programa Operacional Factores de Competitividade (COMPETE) and by National funds through the Fundação para a Ciência e Tecnologia (FCT) [CIISA Project UIDP/CVT/00276/2020; project CIISA CONT 7/2016 and PET-Risk Consortium Project Joint Programming Initiative on Antimicrobial Resistance (JPIAMR/0002/2016)]. Adriana Belas (SFRH/BD/113142/2015) and Cátia Marques (SFRH/BD/77886/2011) hold FCT PhD grants. Juliana Menezes holds a research grant from the JPIAMR/0002/2016 Project.
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Pomba, C., Belas, A., Menezes, J., Marques, C. (2020). The Public Health Risk of Companion Animal to Human Transmission of Antimicrobial Resistance During Different Types of Animal Infection. In: Freitas Duarte, A., Lopes da Costa, L. (eds) Advances in Animal Health, Medicine and Production . Springer, Cham. https://doi.org/10.1007/978-3-030-61981-7_14
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