skip to main content


Title: Risk of Antibiotic‐Resistant Staphylococcus aureus Dispersion from Hog Farms: A Critical Review
Abstract

The World Health Organization has declared antibiotic resistance “one of the biggest threats to global health.” Mounting evidence suggests that antibiotic use in industrial‐scale hog farming is contributing to the spread of antibiotic‐resistantStaphylococcus aureus. To capture available evidence on these risks, we searched peer‐reviewed studies published before June 2017 and conducted a meta‐analysis of these studies’ estimates of the prevalence of swine‐associated, antibiotic‐resistantS. aureusin animals, humans, and the environment. The 166 relevant studies revealed consistent evidence of livestock‐associated methicillin‐resistantS. aureus(MRSA) in hog herds (55.3%) raised with antibiotics. MRSA prevalence was also substantial in slaughterhouse pigs (30.4%), industrial hog operation workers (24.4%), and veterinarians (16.8%). The prevalence of swine‐associated, multidrug‐resistantS. aureus(MDRSA)—with resistance to three or more antibiotics—is not as well documented. Nonetheless, sufficient studies were available to estimate MDRSA pooled prevalence in conventional hog operation workers (15.0%), workers’ household members (13.0%), and community members (5.37%). Evidence also suggests that antibiotic‐resistantS. aureuscan be present in air, soil, water, and household surface samples gathered in or near high‐intensity hog operations. An important caveat is that prevalence estimates for humans reflect colonization, not active infection, and the health risks of colonization remain poorly understood. In addition, these pooled results may not represent risks in specific locations, due to wide geographic variation. Nonetheless, these results underscore the need for additional preventive action to stem the spread of antibiotic‐resistant pathogens from livestock operations and a streamlined reporting system to track this risk.

 
more » « less
Award ID(s):
1316318
NSF-PAR ID:
10456200
Author(s) / Creator(s):
 ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Risk Analysis
Volume:
40
Issue:
8
ISSN:
0272-4332
Page Range / eLocation ID:
p. 1645-1665
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Industrial hog operation (IHO) workers are at increased risk of carryingStaphylococcus aureusin their nares, particularly strains that are livestock-associated (LA) and multidrug-resistant. The pathogenicity of LA-S. aureusstrains remains unclear, with some prior studies suggesting reduced transmission and virulence in humans compared to community-associated methicillin-resistant (CA-MRSA)S. aureus. The objective of this study was to determine the degree to which LA-S. aureusstrains contracted by IHO workers cause disease relative to a representative CA-MRSA strain in a mouse model of skin and soft tissue infection (SSTI). Mice infected with CC398 LA-S. aureusstrains (IHW398-1 and IHW398-2) developed larger lesion sizes with higher bacterial burden than mice infected with CA-MRSA (SF8300) (p < 0.05). The greatest lesion size and bacterial burden was seen with a CC398 strain that produced a recurrent SSTI in an IHO worker. The LA-S. aureusinfected mice had decreased IL-1β protein levels compared with CA-MRSA-infected mice (p < 0.05), suggesting a suboptimal host response to LA-S. aureusSSTIs. WGSA revealed heterogeneity in virulence factor and antimicrobial resistance genes carried by LA-S. aureusand CA-MRSA strains. The observed pathogenicity suggest that more attention should be placed on preventing the spread of LA-S. aureusinto human populations.

     
    more » « less
  2. Industrial hog operation (IHO) workers face a range of occupational hazards, including exposure to zoonotic pathogens such as livestock-associated antimicrobial-resistant Staphylococcus aureus and swine-origin influenza viruses with epidemic or pandemic potential. To better understand this population's occupational exposure to zoonotic pathogens, we conducted a community-driven qualitative research study in eastern North Carolina. We completed in-depth interviews with ten IHO workers and used thematic analysis to identify and analyze patterns of responses. Workers described direct and indirect occupational contact with hogs, with accompanying potential for dermal, ingestion, and inhalation exposures to zoonotic pathogens. Workers also described potential take-home pathways, wherein they could transfer livestock-associated pathogens and other contaminants from IHOs to their families and communities. Findings warrant future research, and suggest that more restrictive policies on antimicrobials, stronger health and safety regulations, and better policies and practices across all IHOs could afford greater protection against worker and take-home zoonotic pathogen exposures.

     
    more » « less
  3. Staphylococcus aureus (S. aureus) is an asymptomatic colonizer of 30% of all human beings. While generally benign, antibiotic resistance contributes to the success of S. aureus as a human pathogen. Resistance is rapidly evolved through a wide portfolio of mechanisms including horizontal gene transfer and chromosomal mutation. In addition to traditional resistance mechanisms, a special feature of S. aureus pathogenesis is its ability to survive on both biotic and abiotic surfaces in the biofilm state. Due to this characteristic, S. aureus is a leading cause of human infection. Methicillin-resistant S. aureus (MRSA) in particular has emerged as a widespread cause of both community- and hospital-acquired infections. Currently, MRSA is responsible for 10-fold more infections than all multi-drug resistant (MDR) Gram-negative pathogens combined. Recently, MRSA was classified by the World Health Organization (WHO) as one of twelve priority pathogens that threaten human health. In this targeted mini-review, we discuss MRSA biofilm production, the relationship of biofilm production to antibiotic resistance, and front-line techniques to defeat the biofilm-resistance system. 
    more » « less
  4. Abstract

    Confronted with the rapid evolution and dissemination of antibiotic resistance, there is an urgent need to develop alternative treatment strategies for drug‐resistant pathogens. Here, an unconventional approach is presented to restore the susceptibility of methicillin‐resistantS. aureus(MRSA) to a broad spectrum of conventional antibiotics via photo‐disassembly of functional membrane microdomains. The photo‐disassembly of microdomains is based on effective photolysis of staphyloxanthin, the golden carotenoid pigment that gives its name. Upon pulsed laser treatment, cell membranes are found severely disorganized and malfunctioned to defense antibiotics, as unveiled by membrane permeabilization, membrane fluidification, and detachment of membrane protein, PBP2a. Consequently, the photolysis approach increases susceptibility and inhibits development of resistance to a broad spectrum of antibiotics including penicillins, quinolones, tetracyclines, aminoglycosides, lipopeptides, and oxazolidinones. The synergistic therapy, without phototoxicity to the host, is effective in combating MRSA both in vitro and in vivo in a mice skin infection model. Collectively, this endogenous chromophore‐targeted phototherapy concept paves a novel platform to revive conventional antibiotics to combat drug‐resistantS. aureusinfections as well as to screen new lead compounds.

     
    more » « less
  5. The role of the environment in the emergence and spread of antimicrobial resistance (AMR) is being increasingly recognized, raising questions about the public health risks associated with environmental AMR. Yet, little is known about pathogenicity among resistant bacteria in environmental systems. Existing studies on the association between AMR and virulence are contradictory, as fitness costs and genetic co-occurrence can be opposing influences. Using Escherichia coli isolated from surface waters in eastern North Carolina, we compared virulence gene prevalence between isolates resistant and susceptible to antibiotics. We also compared the prevalence of isolates from sub-watersheds with or without commercial hog operations (CHOs). Isolates that had previously been evaluated for phenotypic AMR were paired by matching isolates resistant to any tested antibiotic with fully susceptible isolates from the same sample date and site, forming 87 pairs. These 174 isolates were evaluated by conventional PCR for seven virulence genes (bfp, fimH, cnf-1, STa (estA), EAST-1 (astA), eae, and hlyA). One gene, fimH, was found in 93.1% of isolates. Excluding fimH, at least one virulence gene was detected in 24.7% of isolates. Significant negative associations were found between resistance to at least one antibiotic and presence of at least one virulence gene, tetracycline resistance and presence of a virulence gene, resistance and STa presence, and tetracycline resistance and STa presence. No significant associations were found between CHO presence and virulence, though some sub-significant associations merit further study. This work builds our understanding of factors controlling AMR dissemination through the environment and potential health risks.

     
    more » « less