Mini Review
Livestock-associated methicillin-resistant Staphylococcus aureus in animals and humans

https://doi.org/10.1016/j.ijmm.2011.09.004Get rights and content

Abstract

Since 2004 MRSA emerged in animals, particularly in pigs and veal calves. This new MRSA variant was since its first appearance referred to as Livestock Associated-MRSA (LA-MRSA). In Europe and Northern America, LA-MRSA belongs predominantly to clonal complex (CC) 398 whereas in Asia ST9 seems to be dominant in pigs. Persons in direct contact with LA-MRSA-positive animals have an increased risk of becoming MRSA positive. The risk of carriage is mainly related with the intensity of animal contact and with MRSA prevalence among animals on the farm. In contrast with its success in animals, it seemed that MRSA CC398 is a poor persistent colonizer in humans. MRSA ST398 can, however, cause serious (invasive) infections and outbreaks, although, only incidentally reported so far. Farm hygiene and antimicrobial use contributed to MRSA occurrence in animals. Therefore these two determinants should in principle be incorporated into MRSA-control programmes in animal production. Like any other microorganism, LA-MRSA is expected to be able to adapt to new hosts and may change over time in the potential to colonize and to produce toxins. Also, the current circulating clone CC398 may be replaced by another clone in Western countries or emerge in countries where this clone is currently low-prevalent. Ongoing MRSA surveillance in humans and animals is needed to detect changes in epidemiology and to implement effective control measures.

Introduction

Staphylococcus aureus (S. aureus) is a Gram-positive bacterium which belongs to the commensal flora of humans and various animal species (Vanderhaeghen et al., 2010b). Multiple body sites can be colonized in humans, but the anterior nares are the most frequent colonized sites (Wertheim et al., 2005). Approximately 20% of healthy human individuals are persistent S. aureus carriers, about 30% are intermittent carriers and around 50% are never colonized with S. aureus (Kluytmans and Struelens, 2009). In humans, S. aureus is regarded the most important cause of nosocomial infections with clinical conditions ranging from minor skin infections to severe, life-threatening infections (Lowy, 1998, Kluytmans and Struelens, 2009).

In animals, S. aureus is one of the three major pathogenic Staphylococcus species, together with S. hyicus and the Staphylococcus intermedius group – SIG (S. pseudintermedius, S. intermedius, and S. delphini) with S. hyicus and SIG more restricted in host species compared to S. aureus. S. aureus can cause intramammary infections in cattle and small ruminants (Vanderhaeghen et al., 2010b). It can also cause joint problems in chickens (Butterworth et al., 2001) and it is increasingly reported in surgical site infections in small companion animals and horses (Catry et al., 2010).

Section snippets

Methicillin-resistant Staphylococcus aureus (MRSA)

Soon after the introduction of penicillin, around 1945, the majority of the S. aureus population had become resistant to penicillin through the production of beta-lactamase, an enzyme that hydrolyzes penicillin. In the late 1950s, the beta-lactamase-resistant methicillin was introduced in human medicine. However, soon after introduction, the first methicillin-resistant isolates of S. aureus were reported (Robinson and Enright, 2003).

Methicillin resistance is caused by the acquisition of the mecA

MRSA control in humans

The large MRSA prevalence differences between countries can partly be explained by differences in level of screening, isolation and treatment of patients and staff in hospitals. For example, in the Netherlands and Scandinavian countries a pro-active system has been applied, called the “search and destroy” policy. This strategy consists of active screening of high-risk patients and exposed healthcare workers for MRSA carriage. Risk patients involved hospitalized patients who are repatriated from

Emergence of LA-MRSA in livestock and other animals

From 1970 to 2000, MRSA was rarely isolated from animals, and if so, these strains were generally supposed to be of human origin, as shown by bio-typing. Therefore, it was thought that until the end of the 20th century, the animal husbandry reservoir was of little relevance to MRSA causing diseases in humans. It was assumed that MRSA was a problem caused by antimicrobial use in human medicine (Catry et al., 2010).

In 1975 the first report on MRSA isolated from cows with mastitis was published (

Molecular aspects of MRSA ST398

MRSA isolates of ST398 possess some typical features. As aforementioned, the strains are non-typeable with standard PFGE using SmaI digestion. This is due to the presence of a restriction/methylation system leading to protection from SmaI digestion (Bens et al., 2006). The strains carry SCCmec element IV or V (Smith and Pearson, 2010). SCCmec cassette types II and III have also been reported but this may be the result of misidentification (Jansen et al., 2009). Many different spa-types have

Public health consequences of LA-MRSA

Persons in direct contact with MRSA-positive animals have an increased risk of becoming MRSA positive. This has been documented for individuals working in companion animal and equine clinics, and livestock production environments (Morgan, 2008). It has been shown that MRSA ST398 has limited host specificity; it is able to colonize and to cause infections in various hosts. So far, the mechanisms of host adaptation are poorly understood (Cuny et al., 2010). However, incidentally reported so far,

Risk factors for animal and human LA-MRSA carriage

Few studies investigated risk factors for the occurrence of ST398 in animals and humans. A high risk of animal to human transmission of ST398 has been reported in pig farming (Lewis et al., 2008, Smith et al., 2009, van den Broek et al., 2009). A direct association between MRSA carriage in animals and MRSA carriage in humans was observed in veal calf farming (Graveland et al., 2010). It was demonstrated that LA-MRSA carriage among veal farmers and their family members and employees was strongly

Human to human transmission of MRSA ST398

Few studies have examined transmissibility, and from these it appears that in hospital settings, ST398 transmits less frequently than most HA-MRSA strains (van Rijen et al., 2008, van Rijen et al., 2009, Wassenberg and Bonten, 2010, Wassenberg et al., 2011). A large Dutch multi-center study in hospital settings has shown that the relative risk on transmission of MRSA ST398, as compared to HA-MRSA, was 0.28 (Wassenberg et al., 2011). Based on these data, the genotype-specific single admission

Conclusions

LA-MRSA seems to be recently introduced into production animals and is predominantly present in pigs and veal calves. However other animals can be MRSA carrier as well due to overflow towards other species.

It has been shown that persons in direct (occupational) contact to LA-MRSA-positive animals have an increased risk for LA-MRSA carriage. The risk for LA-MRSA carriage in humans is mainly related to exposure to MRSA-positive animals. However, the positive association between MRSA carrier

References (55)

  • J.A. Wagenaar et al.

    Unexpected sequence types in livestock associated methicillin-resistant Staphylococcus aureus (MRSA): MRSA ST9 and a single locus variant of ST9 in pig farming in china

    Vet. Microbiol.

    (2009)
  • M.W. Wassenberg et al.

    Transmissibility of livestock-associated methicillin-resistant Staphylococcus aureus (ST398) in Dutch hospitals

    Clin. Microbiol. Infect.

    (2011)
  • H.F. Wertheim et al.

    The role of nasal carriage in Staphylococcus aureus infections

    Lancet Infect. Dis.

    (2005)
  • M. Wulf et al.

    MRSA in livestock animals—an epidemic waiting to happen?

    Clin. Microbiol. Infect.

    (2008)
  • M.W. Wulf et al.

    Prevalence of methicillin-resistant Staphylococcus aureus among veterinarians: an international study

    Clin. Microbiol. Infect.

    (2008)
  • M.A. Argudín et al.

    The emerging methicillin-resistant Staphylococcus aureus ST398 clone can easily be typed using the Cfr9I SmaI-neoschizomer

    Lett. Appl. Microbiol.

    (2010)
  • C.C. Bens et al.

    Presence of a novel DNA methylation enzyme in methicillin-resistant Staphylococcus aureus isolates associated with pig farming leads to uninterpretable results in standard pulsed-field gel electrophoresis analysis

    J. Clin. Microbiol.

    (2006)
  • M.C. Bootsma et al.

    The nosocomial transmission rate of animal-associated ST398 meticillin-resistant Staphylococcus aureus

    J. R. Soc. Interface

    (2011)
  • B. Catry et al.

    Reflection paper on MRSA in food-producing and companion animals: epidemiology and control options for human and animal health

    Epidemiol. Infect.

    (2010)
  • S. Coenen et al.

    European surveillance of antimicrobial consumption (ESAC): outpatient parenteral antibiotic treatment in Europe

    J. Antimicrob. Chemother.

    (2009)
  • S. Cui et al.

    Isolation and characterization of methicillin-resistant Staphylococcus aureus from swine and workers in china

    J. Antimicrob. Chemother.

    (2009)
  • C. Cuny et al.

    Clusters of infections in horses with MRSA ST1 ST254, and ST398 in a veterinary hospital

    Microb. Drug Resist.

    (2008)
  • European Food Safety Authority

    Analysis of the baseline survey on the prevalence of methicillin-resistant Staphylococcus aureus (MRSA) in holdings with breeding pigs, in the EU, 2008 [1]—Part A: MRSA prevalence estimates

    EFSA J.

    (2009)
  • M.B. Ekkelenkamp et al.

    Endocarditis due to meticillin-resistant Staphylococcus aureus originating from pigs

    Ned. Tijdschr. Geneeskd.

    (2006)
  • H. Graveland et al.

    Persistence of livestock associated MRSA CC398 in humans is dependent on intensity of animal contact

    PLoS One

    (2011)
  • H. Graveland et al.

    Methicillin resistant Staphylococcus aureus ST398 in veal calf farming: Human MRSA carriage related with animal antimicrobial usage and farm hygiene

    PLoS One

    (2010)
  • L. Guardabassi et al.

    Novel lineage of methicillin-resistant Staphylococcus aureus, Hong Kong

    Emerg. Infect. Dis.

    (2009)
  • Cited by (243)

    • Usefulness of molecular typing methods for epidemiological and evolutionary studies of Staphylococcus aureus isolated from bovine intramammary infections

      2022, Saudi Journal of Biological Sciences
      Citation Excerpt :

      MRSA isolates have also been found in a wide range of animal species, including various livestock species (Aires-de-Sousa, 2017; Alzohairy, 2011). These MRSA strains have evolved into three types: healthcare-associated MRSA (HA-MRSA) since the 1960 s; community-acquired MRSA (CA-MRSA) since the 1990 s; and new strains that have been associated with livestock since the 2000 s, so-called live-stock-associated MRSA (LA-MRSA) (Graveland et al., 2011; Li et al., 2017). The emergence of the latest MRSA strains in cattle is of great concern for livestock and public health (Haran et al., 2012; Wang et al., 2015; Weese, 2010).

    View all citing articles on Scopus
    View full text