MRSA colonization and infection among persons with occupational livestock exposure in Europe: Prevalence, preventive options and evidence

Highlights

• Livestock-associated MRSA of clonal lineage CC398 cause multiple human infections.

• Twelve case reports of infections among livestock-exposed persons are published.

• The incidence of occupation-related MRSA CC398 infections is unknown.

• Specific guidance towards prevention of MRSA CC398 infections is lacking.

Abstract

Colonization with livestock-associated Methicillin-resistant Staphylococcusaureus (LA-MRSA) among persons occupationally exposed to pigs, cattle or poultry is very frequent. In Europe, LA-MRSA mostly belong to the clonal lineage CC398. Since colonized persons have an increased risk of developing MRSA infections, defining the burden of work-related infection caused by LA-MRSA CC398 is of interest to exposed personnel, insurance companies and infection control staff. This review summarizes data on the types of occupation-related infections caused by LA-MRSA CC398, the incidence of such infections as well as potential preventive strategies.

We identified twelve case reports on infections among livestock-exposed persons. Overall, there is a lack of data describing the incidence of occupation-related infections due to MRSA CC398. Currently, no specific guidance towards the prevention of LA-MRSA CC398 colonization of persons with routine exposure exists. In vitro, MRSA CC398 strains are susceptible (>95%) to mupirocin. Single reports have described effective decolonization of persons carrying LA-MRSA CC398, but long-term success rates are low in case of continuous livestock contact.

Overall, the occupational health risk due to LA-MRSA CC398 is not well understood. Currently, prevention of human LA-MRSA CC398 infection is mostly based on the recommendation to perform screening and decolonization therapies prior to elective medical interventions in order to avoid nosocomial infections, but there is no conclusive evidence to perform specific measures aiming to forestall community-acquired infections.

Introduction

Methicillin-resistant Staphylococcus aureus (MRSA) is a pathogen which causes a variety of human infections such as abscesses, pneumonia, endocarditis or sepsis. MRSA infections are usually endogenously acquired, i.e. infection follows asymptomatic carriage of MRSA, when the bacterium is able to penetrate the skin or mucous membranes (e.g. after surgical interventions). This has been shown by studies demonstrating that genetic fingerprints of S. aureus strains, which are detected in patients’ nasal vestibules (the major sites of human S. aureus colonization), are usually identical with those of isolates subsequently causing nosocomial infections in the respective patients (Corne et al., 2005, Kaspar et al., 2015, von Eiff et al., 2001). Hence, nasal carriers of MRSA have a significantly higher risk to develop MRSA infection compared with non-carriers (Kluytmans et al., 1997).

Following investigations which indicated that healthcare personnel is more frequently colonized with MRSA compared to the general population, it has been asked to what extent nurses or doctors are rather “vectors” or “victims” of MRSA and whether work-related acquisition of MRSA has an impact for occupational health (Albrich and Harbarth, 2008).

However, besides the healthcare sector, the community, pets and horses, it is known since about a decade that MRSA are widely distributed among livestock and affect >40% of German pig-, 20% of cattle- and 20–90% of turkey farms, respectively (Idelevich et al., 2015, Köck et al., 2014a). In European countries, livestock-associated (LA-) –MRSA are predominantly associated with clonal complex (CC) 398. This is different in other parts of the world (e.g. Asia), where LA-MRSA more frequently exhibit other clonal lineages such as CC9. MRSA CC398 is normally rarely found among humans (Köck et al., 2014a), but can cause cytotoxic effects on human epithelial cells similar to that of primarily “human” MRSA clones, form biofilms and cause severe human infections (Ballhausen et al., 2014, Nicholson et al., 2013, Witte et al., 2007).

Following the upsurge of MRSA CC398 on European farms, numerous investigations have proven that persons in contact with livestock are at high risk to become colonized with LA-MRSA. Table 1 summarizes studies showing that MRSA CC398 colonization involves 24–86% of pig-, 31–37% of cattle-, and 9–37% of poultry-farmers, as well as 44–45% of pig-care veterinarians in European countries (Antoci et al., 2013, Bisdorff et al., 2012, Cuny et al., 2009, Dahms et al., 2014, Garcia-Graells et al., 2012, Geenen et al., 2013, Gilbert et al., 2012, Graveland et al., 2011, Graveland et al., 2010, Köck et al., 2012, Morcillo et al., 2011, Mulders et al., 2010, Paterson et al., 2013, Richter et al., 2012, Van Cleef et al., 2010a, Van Cleef et al., 2014, Van Cleef et al., 2010b, Van Den Broek et al., 2009, Vandendriessche et al., 2013, Verkade et al., 2013, Wulf et al., 2006, Wulf et al., 2008b).

Although MRSA CC398 colonization of occupationally exposed persons may mostly remain without symptoms, it poses a risk to farmers, veterinarians, butchers and other exposed personnel as well as their household contacts with respect to causing endogenous community-acquired or nosocomial infections (Smith and Wardyn, 2015). Due to the extremely high nasal colonization rates in this group of persons, the occupational health risk is likely to be much higher than that caused by hospital-associated MRSA strains, which colonize healthcare personnel (Albrich and Harbarth, 2008).

However, there are only limited data describing the quality and quantity of this occupational risk.

Therefore, this review aims to summarize data about two questions:

• How frequent are LA-MRSA infections among persons with livestock contact?

• Which measures potentially prevent either MRSA CC398 colonization or infection among persons with direct livestock contact or their household members?