First Emergence of Resistance to Macrolides and Tetracycline Identified in Mannheimia haemolytica and Pasteurella multocida Isolates from Beef Feedlots in Australia

Tamara Alhamami,Mandi Carr,Piklu Chowdhury,Darren Trott,Tania Veltman,Joanne Mollinger,Henrietta Venter,Layla Mahdi,Sam Abraham,Ania Deutscher,Steven Djordjevic,Nancy Gomes,Manouchehr Khazandi,Conny Turni

doi:10.3390/microorganisms9061322

Abstract

Bovine respiratory disease (BRD) causes high morbidity and mortality in beef cattle worldwide. Antimicrobial resistance (AMR) monitoring of BRD pathogens is critical to promote appropriate antimicrobial stewardship in veterinary medicine for optimal treatment and control. Here, the susceptibility of Mannheimia haemolytica and Pasteurella multicoda isolates obtained from BRD clinical cases (deep lung swabs at post-mortem) among feedlots in four Australian states (2014–2019) was determined for 19 antimicrobial agents. The M. haemolytica isolates were pan-susceptible to all tested agents apart from a single macrolide-resistant isolate (1/88; 1.1%) from New South Wales (NSW). Much higher frequencies of P. multocida isolates were resistant to tetracycline (18/140; 12.9%), tilmicosin (19/140; 13.6%), tulathromycin/gamithromycin (17/140; 12.1%), and ampicillin/penicillin (6/140; 4.6%). Five P. multocida isolates (3.6%), all obtained from NSW in 2019, exhibited dual resistance to macrolides and tetracycline, and a further two Queensland isolates from 2019 (1.4%) exhibited a multidrug-resistant phenotype to ampicillin/penicillin, tetracycline, and tilmicosin. Random-amplified polymorphic DNA (RAPD) typing identified a high degree of genetic homogeneity among the M. haemolytica isolates, whereas P. multocida isolates were more heterogeneous. Illumina whole genome sequencing identified the genes msr(E) and mph(E)encoding macrolide resistance, tet(R)-tet(H) or tet(Y) encoding tetracycline resistance, and blaROB-1 encoding ampicillin/penicillin resistance in all isolates exhibiting a corresponding resistant phenotype. The exception was the tilmicosin-resistant, tulathromycin/gamithromycin-susceptible phenotype identified in two Queensland isolates, the genetic basis of which could not be determined. These results confirm the first emergence of AMR in M. haemolytica and P. multocida from BRD cases in Australia, which should be closely monitored.

Highlights

Bovine respiratory disease (BRD) is an infectious disease that causes a significant economic loss for the beef industry, accounting for 70–80% morbidity and 40–50% mortality
The current study evaluated the Antimicrobial resistance (AMR) profiles of M. haemolytica and P. multocida isolates obtained from the lungs of necropsied cattle at feedlots in four Australian states over a five-year period (2014–2019)
This study reports the first identification of resistance among Australian isolates of M. haemolytica and P. multocida associated with fatal cases of BRD in Australian feedlot cattle

Summary

Introduction

Bovine respiratory disease (BRD) is an infectious disease that causes a significant economic loss for the beef industry, accounting for 70–80% morbidity and 40–50% mortality. Other risk factors include stress from weaning, transport, and marketing, which predisposes calves to infectious agents that cause BRD [4]. The bacteria most often associated with BRD are Mannheimia haemolytica and Pasteurella multocida [5,6]. In USA and Canada, M. haemolytica was once recognised as the most commonly isolated and economically significant BRD pathogen, responsible for widespread morbidity and mortality [8]. P. multocida has become a more significant BRD pathogen. In one recent Canadian feedlot study, the prevalence of P. multocida as a cause of BRD cases was 54.8%, compared to 30.5% for M. haemolytica [9]

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