Antimicrobial resistance in bacteria associated with porcine respiratory disease in Australia

doi:10.1016/j.vetmic.2014.03.014

Veterinary Microbiology

Volume 171, Issues 1–2, 25 June 2014, Pages 232-235

https://doi.org/10.1016/j.vetmic.2014.03.014 Get rights and content

Abstract

The porcine respiratory disease complex greatly affects the health and production of pigs. While antimicrobial agents are used to treat the respiratory infections caused by bacterial pathogens, there is no current information on antimicrobial resistance in Australian pig respiratory bacterial isolates. The aim of this study was to determine the antimicrobial resistance profiles, by determining the minimum inhibitory concentration of nine antimicrobial agents for 71 Actinobacillus pleuropneumoniae, 51 Pasteurella multocida and 18 Bordetella bronchiseptica cultured from Australian pigs. The majority of A. pleuropneumoniae isolates were resistant to erythromycin (89%) and tetracycline (75%). Resistance to ampicillin (8.5%), penicillin (8.5%) and tilmicosin (25%) was also identified. The P. multocida isolates exhibited resistance to co-trimoxazole (2%), florfenicol (2%), ampicillin (4%), penicillin (4%), erythromycin (14%) and tetracycline (28%). While all the B. bronchiseptica isolates showed resistance to beta-lactams (ampicillin, ceftiofur and penicillin), some were resistant to erythromycin (94%), florfenicol (6%), tilmicosin (22%) and tetracycline (39%). The incidence of multiple drug resistance (MDR) varied across the species – in B. bronchiseptica, 27.8% of resistant isolates showed MDR, while 9.1% of the resistant isolates in A. pleuropneumoniae, and 4.8% in P. multocida showed MDR. This study illustrated that Australian pig strains of bacterial respiratory pathogens exhibited low levels of resistance to antimicrobial agents commonly used in the pig industry.

Introduction

The porcine respiratory disease complex (PRDC), one of the most significant problems affecting health and production in the pig industry worldwide, is described as a multifactorial pneumonic state resulting from the interaction of bacteria, viruses and stresses caused by management, environment and genetic conditions (Opriessnig et al., 2011). A range of bacterial pathogens is associated with the initiation and progress of PRDC, with Mycoplasma hyopneumoniae, Actinobacillus pleuropneumoniae, Haemophilus parasuis, Pasteurella multocida and Bordetella bronchiseptica having significant roles (Fablet et al., 2011, Opriessnig et al., 2011).

The use of antimicrobial agents, beta-lactams (ampicillin, penicillin and cephalosporins) (except for B. bronchiseptica), co-trimoxazole (sulfonamide and trimethoprim combination), florfenicol, macrolides (erythromycin, tilmicosin and tulathromycin) and tetracyclines remains the best treatment option to control PRDC (Karriker et al., 2013). The usage of antimicrobial agents has the potential to select for antimicrobial resistance (Barton et al., 2003). Resistance to antimicrobials commonly used to treat PRDC have been detected previously in porcine respiratory disease pathogens from many countries (Vicca et al., 2004, de la Fuente et al., 2007, San Millan et al., 2009, Tang et al., 2009, Chander et al., 2011, Kucerova et al., 2011, Nedbalcová and Kucerova, 2013).

In the past, antimicrobial resistance in Australia was reported in A. pleuropneumoniae (Eaves et al., 1989) and P. multocida (Stephens et al., 1995). However, no information exists for B. bronchiseptica. Thus, this study aimed to determine the antimicrobial susceptibility of A. pleuropneumoniae, P. multocida and B. bronchiseptica Australian isolates against antimicrobial agents used for bacterial respiratory pathogens.

Section snippets

Materials and methods

The bacterial isolates tested were obtained from Australian pigs in diagnostic disease investigations and then submitted to the Microbiology Research Group, EcoSciences Precinct, Department of Agriculture Fisheries and Forestry (DAFF), Queensland, Australia for confirmatory identification and/or serotyping. A total of 71 A. pleuropneumoniae, 51 P. multocida and 18 B. bronchiseptica isolates collected between the years 2002 and 2013 were selected from the culture collection of the Microbiology

Results and discussion

The MIC distribution of 71 A. pleuropneumoniae, 51 P. multocida and 18 B. bronchiseptica isolates, the percentage of resistance in each antimicrobial as well as the MIC₅₀ and MIC₉₀ are shown in Table 1.The MICs of the reference strains in each test run were within the CLSI acceptable quality control ranges. All A. pleuropneumoniae were susceptible to ceftiofur, co-trimoxazole, florfenicol and tulathromycin. Overall, 66 of 71 (93%) of the A. pleuropneumoniae isolates were resistant to one or

Acknowledgements

We acknowledge the financial support provided by the Australian Pork Cooperative Research Centre (CRC) project 2A-107 1213 for the operating expenses to complete this work which was part of a PhD degree undertaken by D. Dayao. The PhD study was supported by the Australian Centre for International Agricultural Research (ACIAR) project AH/2009/022 John Allwright Fellowship.

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Cited by (56)

Characterization of Actinobacillus pleuropneumoniae isolated from pigs in Japan using whole genome sequencing
2023, Comparative Immunology, Microbiology and Infectious Diseases
We conducted whole-genome sequencing to investigate the serotypes, the presence of virulence and antimicrobial resistance genes, and the genetic relationships among isolates of Actinobacillus. pleuropneumoniae derived from diseased pigs. Serotype 2 (71.2%) was the most common, but the prevalence of serotypes 6 (13.6%) and 15 (6.8%) increased. Existing vaccines are considered ineffective on the isolates belonging to serotypes 6 and 15. The phylogenetic tree based on core genome single nucleotide polymorphisms showed that the isolates were clustered by serotype. Of the isolates, 62.5% did not have an antimicrobial resistance gene, including a florfenicol resistance gene, but 32.2% had a tetracycline resistance gene. The antimicrobial resistant phenotype and genotype were almost identical. The plasmid-derived contigs harbored resistance genes of aminoglycosides, tetracyclines, β-lactams, phenicols, or sulfonamides. It has been suggested that isolates with different genetic properties from vaccine strains are circulating; however, antimicrobial resistance may not be widespread.
Whole genome characterization of a multidrug-resistant hypervirulent Pasteurella multocida with a new drug-resistant plasmid
2023, Poultry Science
Pasteurella multocida (P. multocida) is a zoonotic bacterium that can cause diseases in a variety of animals. It was divided into 5 serogroups, and serogroup A is mainly prevalent in avian hosts. We isolated a virulent and multidrug-resistant P. multocida strain from Guangdong duck liver and named it PMWSG-4 (GenBank accession no. CP077723.1). To understand the pathogenicity of this strain, the pathogenicity test was carried out with mice and ducks. The results showed that PMSWG-4 was highly pathogenic to ducks and mice, and the LD50 is 4.5 and 73 CFU, respectively. In order to study its genetic characteristics, pathogenicity, and relationship with the host, we performed a whole genome sequencing. The genome size of the isolated PMWSG-4 was 2.38 Mbp, with a G+C content of 40.3%, and coding 2,313 Coding DNA Sequence (CDS). The genome carries 162 potential virulence-associated genes, 32 different drug resistance phenotypes, 102 genes possibly involved in pathogen–host interaction, 2 gene island groups, and 4 prophages. In addition, we also found a new drug-resistant plasmid from strain PMWSG-4, named pXL001 (GenBank accession no. CP077724.1). After verified, the plasmid is a new plasmid carrying the floR florfenicol resistance gene. The whole genome is of great significance for further studying the pathogenesis and genetic characteristics of duck-derived P. multocida.
Prevalence and time trend analysis of antimicrobial resistance in respiratory bacterial pathogens collected from diseased pigs in USA between 2006–2016
2020, Research in Veterinary Science
Swine respiratory disease complex (SRDC) causes massive economic losses to the swine industry and is a major animal welfare concern. Antimicrobials are mainstay in treatment and control of SRDC. However, there is a lack of data on the prevalence and trends in resistance to antimicrobials in bacterial pathogens associated with SRDC. The objective of this study was to estimate the prevalence and changes in resistance to 13 antimicrobials in swine bacterial pathogens (Streptococcus suis, Pasteurella multocida, Actinobacillus suis and Haemophilus parasuis) in the U.S.A using data collected at University of Minnesota Veterinary Diagnostic Laboratory between 2006 and 2016. For antimicrobials for which breakpoints were available, prevalence of resistance remained below 10% except for tetracycline in S. suis and P. multocida isolates, and these prevalence estimates remained consistently low over the years despite statistical significance (p < .05) in trend analysis. For antimicrobial-bacterial combinations without available breakpoints, the odds of isolates being resistant increased by >10% annually for 7 and 1 antimicrobials in H. parasuis and S. suis isolates respectively, and decreased >10% annually for 4 and 1 antimicrobials in A. suis and H. parasuis isolates, respectively, according to the ordinal regression models. Clinical implications of changes in AMR for A. suis and H. parasuis should be interpreted cautiously due to the lack of interpretive criteria and challenges in antimicrobial susceptibility tests in the case of H. parasuis. Future studies should focus on surveillance of antimicrobial resistance and establishment of standardized susceptibility testing methodologies and interpretive criteria for these animal pathogens of critical importance.
Antimicrobial resistance of Pasteurella multocida isolated from diseased food-producing animals and pets
2019, Veterinary Microbiology
Citation Excerpt :
In Australia, a more recent study on 51 P. multocida isolated from swine reported very low levels of resistance, except for tetracycline (28%) (Dayao et al., 2014). Two studies in swine, one in China on 233 isolates and the other on 454 isolates collected in South Korea also identified high levels of tetracycline resistance (58.0% and 66.5% respectively) (Tang et al., 2009; Oh et al., 2018), higher than those reported in Europe (El Garch et al., 2016), North America (Sweeney, 2017), Australia (Dayao et al., 2014) and in our study (6.7%). Similarly, resistance to florfenicol reached 18.5% in South Korea, whereas it appeared to be very limited in Europe.
Surveillance of Pasteurella multocida resistance in food-producing animals is essential to guide the first-line treatment of respiratory diseases and to limit economic losses. Since Pasteurella are the most common bacteria isolated from dog and cat bites, this surveillance is also needed to guide treatment in humans in case of bites. The aim of this study was to characterize the phenotypic resistance of P. multocida strains isolated from respiratory infections in animals, including both food-producing animals and pets. Data collected between 2012 and 2017 by the French national surveillance network for antimicrobial resistance referred to as RESAPATH were analyzed. The proportions of resistance to antimicrobials of relevance in veterinary and human medicines were estimated for each animal species. For cattle, resistance trends over the period were investigated using non-linear analysis applied to time-series. In total, 5356 P. multocida isolates were analyzed. Proportions of resistance of P. multocida were almost all below 20% over the period, and, more precisely, all resistance proportions were below 10% for rabbits, sheep and dogs. The highest resistance proportions to enrofloxacin were identified for cattle (4.5%) and dogs (5.2%). Despite its frequent use in livestock, resistance to florfenicol was less than 1% in P. multocida strains, regardless of the animal species considered. Time series analyses revealed continuous increases in resistance to tetracycline, tilmicosin, flumequine and fluoroquinolones in P. multocida strains isolated from cattle. These trends contrast with the decrease in use of antibiotics in cattle in France and with the decrease in resistance observed in E. coli isolated from diseased cattle.
3Antimicrobial resistance of Pasteurella multocida isolates recovered from swine pneumonia in Spain throughout 2017 and 2018
2019, Veterinary and Animal Science
Citation Excerpt :
Similar results were obtained for 36 isolated previously (Sellyei et al., 2009; Tang et al., 2009). Other safer phenicol, florfenicol, that is used exclusively in veterinary patients for the therapy of pneumonia caused by P. multocida (Kehrenberg, Wallmann, & Schwarz, 2008), was equally highly effective against clinical isolates (Dayao et al., 2014; de Jong et al., 2014). Nevertheless, resistance to florfenicol in two German isolates, being associated to plasmid pCCK381 and florR gene, was described ten years ago (Kehrenberg et al., 2008).
A total of 32 Pasteurella multocida isolates were obtained from 60 cases of swine pneumonic lungs collected in “Castilla y León” (northwestern Spain) between November 2017 and April 2018. Capsular type A isolates were isolated from 96.9% cases and capsular type D from the remaining 3.1%. All isolates were characterized for their susceptibilities to eight antimicrobial agents and the presence of eight resistance genes. The frequency of susceptibility was lower than 60% in four of the drugs, 84.4% of the isolates showed resistance to at least two compounds, and 46.9% to a combination of three drugs. The resistance patterns suggested that enrofloxacin, chloramphenicol, tetracycline and cefotaxime were the compounds most likely active to P. multocida. The usage of PCR revealed that ermC, bla_ROB1, tetB and msrE genes occurred in more than 37.0% isolates, that suggested its putative accountability in the resistance of the strains harbor them. However, most were detected in susceptible strains and only a genetic explanation for the resistance could be linked to erythromycin. Therefore, the resistances to clyndamicin, cotrimoxazol, β-lactams and tetracyclin observed by phenotypic testing remains genetically unexplained and further investigations are required.
Characterization of Pasteurella multocida strains isolated from human infections
2019, Comparative Immunology, Microbiology and Infectious Diseases
Isolates of Pasteurella multocida recovered from infected humans (n = 15) were characterized by traditional and molecular microbiological methods and were compared with cat-derived strains (n = 5). The most prevalent subspecies among strains from human infections was P. multocida subsp. septica (80%), and nearly all isolates showed a similar combination of virulence-associated genes. MLST analysis classified the 20 P. multocida strains into 16 different sequence types, and we assigned 11 new sequence types (ST), however, only one of those (ST 334) was shared by two human and one cat isolates. P. multocida subsp. septica strains formed a distinct phylogenetic group within the species. The strains showed resistance to erythromycin, clindamycin and sulfamethoxazole, and with two exceptions, resistance to tilmicosin was also detected. Each strain was susceptible to ampicillin, streptomycin, gentamycin, tetracycline, doxycycline, cefazolin, cefpodoxime, chloramphenicol, florfenicol and enrofloxacin. Common characteristics (virulence profile and antibiotic sensitivity pattern) shared by strains isolated from humans and cats support the view that domestic cats may serve as a potential reservoir for P. multocida.

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Veterinary Microbiology

Abstract

Introduction

Section snippets

Materials and methods

Results and discussion

Acknowledgements

References (24)

Characterisation of ceftiofur resistance in swine bacterial pathogens

Vet. J.

Antimicrobial susceptibility patterns of Haemophilus parasuis from pigs in the United Kingdom and Spain

Vet. Microbiol.

Longitudinal study of respiratory infection patterns of breeding sows in five farrow-to-finish herds

Vet. Microbiol.

Antimicrobial susceptibility of Actinobacillus pleuropneumoniae isolates from clinical outbreaks of porcine respiratory diseases

Vet. Microbiol.

Antimicrobial susceptibilities and resistance genes of Canadian isolates of Actinobacillus pleuropneumoniae

Microbiol. Drug Resist. (Larchmont, N.Y.)

Antibiotic resistance in animals

Commun. Dis. Intell. Q. Rep.

Characterisation of a novel Mannheimia sp from Australian feedlot cattle

Aust. Vet. J.

Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals. Approved Standard, CLSI Document VET01-A4

Antimicrobial susceptibility monitoring of respiratory tract pathogens isolated from diseased cattle and pigs across Europe

Characterisation and antimicrobial sensitivity of haemophili isolated from pigs

Aust. Vet. J.

Improved diagnostic PCR assay for Actinobacillus pleuropneumoniae based on the nucleotide sequence of an outer membrane lipoprotein

J. Clin. Microbiol.

Antimicrobial susceptibility of Bordetella bronchiseptica isolates from porcine respiratory tract infections

Antimicrob. Agents Chemother.

Cited by (56)

Characterization of Actinobacillus pleuropneumoniae isolated from pigs in Japan using whole genome sequencing

Whole genome characterization of a multidrug-resistant hypervirulent Pasteurella multocida with a new drug-resistant plasmid

Prevalence and time trend analysis of antimicrobial resistance in respiratory bacterial pathogens collected from diseased pigs in USA between 2006–2016

Antimicrobial resistance of Pasteurella multocida isolated from diseased food-producing animals and pets

3Antimicrobial resistance of Pasteurella multocida isolates recovered from swine pneumonia in Spain throughout 2017 and 2018

Characterization of Pasteurella multocida strains isolated from human infections

Short CommunicationAntimicrobial resistance in bacteria associated with porcine respiratory disease in Australia

Abstract

Introduction

Section snippets

Materials and methods

Results and discussion

Acknowledgements

Vet. J.

Vet. Microbiol.

Vet. Microbiol.

Vet. Microbiol.

Antimicrobial susceptibilities and resistance genes of Canadian isolates of Actinobacillus pleuropneumoniae

Microbiol. Drug Resist. (Larchmont, N.Y.)

Antibiotic resistance in animals

Commun. Dis. Intell. Q. Rep.

Characterisation of a novel Mannheimia sp from Australian feedlot cattle

Aust. Vet. J.

Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals. Approved Standard, CLSI Document VET01-A4

Antimicrobial susceptibility monitoring of respiratory tract pathogens isolated from diseased cattle and pigs across Europe

Characterisation and antimicrobial sensitivity of haemophili isolated from pigs

Aust. Vet. J.

Improved diagnostic PCR assay for Actinobacillus pleuropneumoniae based on the nucleotide sequence of an outer membrane lipoprotein

J. Clin. Microbiol.

Antimicrobial susceptibility of Bordetella bronchiseptica isolates from porcine respiratory tract infections

Antimicrob. Agents Chemother.

Short Communication
Antimicrobial resistance in bacteria associated with porcine respiratory disease in Australia