REVIEW

Human health risks associated with antimicrobial-resistant enterococci

and Staphylococcus aureus on poultry meat

V. Bortolaia1, C. Espinosa-Gongora1 and L. Guardabassi1,2

1) Department of Veterinary Disease Biology, Faculty of Health and Medical Sciences, University of Copenhagen, Frederiksberg C, Denmark and 2) Department of
Biomedical Sciences, Ross University School of Veterinary Medicine, St Kitts, West Indies

Abstract

Enterococci and staphylococci are frequent contaminants on poultry meat. Enterococcus faecalis, Enterococcus faecium and Staphylococcus aureus
are also well-known aetiological agents of a wide variety of infections resulting in major healthcare costs. This review provides an overview of
the human health risks associated with the occurrence of these opportunistic human pathogens on poultry meat with particular focus on the risk
of food-borne transmission of antimicrobial resistance. In the absence of conclusive evidence of transmission, this risk was inferred using data
from scientic articles and national reports on prevalence, bacterial load, antimicrobial resistance and clonal distribution of these three species
on poultry meat. The risks associated with ingestion of antimicrobial-resistant enterococci of poultry origin comprise horizontal transfer of
resistance genes and transmission of multidrug-resistant E. faecalis lineages such as sequence type ST16. Enterococcus faecium lineages
occurring in poultry meat products are distantly related to those causing hospital-acquired infections but may act as donors of quinupristin/
dalfopristin resistance and other resistance determinants of clinical interest to the human gut microbiota. Ingestion of poultry meat
contaminated with S. aureus may lead to food poisoning. However, antimicrobial resistance in the toxin-producing strains does not have
clinical implications because food poisoning is not managed by antimicrobial therapy. Recently methicillin-resistant S. aureus of livestock
origin has been reported on poultry meat. In theory handling or ingestion of contaminated meat is a potential risk factor for colonization by
methicillin-resistant S. aureus. However, this risk is presently regarded as negligible by public health authorities.
Clinical Microbiology and Infection 2015 European Society of Clinical Microbiology and Infectious Diseases. Published by Elsevier Ltd. All
rights reserved.

Keywords: Broiler, chicken, Enterococcus faecalis, Enterococcus faecium, foodborne transmission, Staphylococcus aureus, turkey
Article published online: 17 December 2015

Taken together, E. faecalis and E. faecium are ranked as the third

Corresponding author: L. Guardabassi, Department of Biomedical
Sciences, Ross University School of Veterinary Medicine, St Kitts,
West Indies
E-mail: LGuardabassi@rossvet.edu.kn
V. Bortolaia and C. Espinosa-Gongora are rst co-authors
Introduction
Enterococci and staphylococci are frequent contaminants on
poultry meat and well-established opportunistic pathogens in
human medicine. Enterococcus faecalis, Enterococcus faecium and
Staphylococcus aureus are leading causes of human infections
that may affect virtually any body site and range in severity from
uncomplicated wound infections to fatal endocarditis [1,2].
cause of bacteraemia in Europe and in America accounting for
approximately 11%13% of all bacteraemia cases [3,4]. Staph-
ylococcus aureus is the most common cause of skin and soft
tissue infections and nosocomial bacteraemia in America and
Europe [2]. All these Gram-positive cocci are also normal
commensals in poultry and other domestic animals. Strains of
animal origin may be transmitted to humans through direct
contact with animals or via exposure to contaminated food. In
industrialized countries, the risk of zoonotic transmission by
direct contact with poultry is limited to farmers, veterinarians
and slaughterhouse workers, who represent a small fraction of
the general human population. Food-borne transmission may
affect a larger part of the population through consumption and
handling of contaminated poultry meat and other food items
that may be cross-contaminated in the kitchen. The

Clin Microbiol Infect 2016; 22: 130140

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http://dx.doi.org/10.1016/j.cmi.2015.12.003
CMI Bortolaia et al. Antimicrobial-resistant enterococci and S. aureus on poultry meat 131

TABLE 1. Prevalence (%) of Enterococcus faecalis and Enterococcus faecium in raw poultry meat as determined by selective
enrichment (SE) and direct plating (DP) on selective media

Country E. faecalis E. faecium No. of samples Meat type Method Reference

Greece 0 0 19 C DP [36]
Greece 9 12 300 C DP [37]
Italy 13 11 238 C/T DP [38]
Tunisia 63 33 51 C/T DPa [39]
Canada >94 4 206 C SE [40]
Canada >94 0 91 T SE [40]
USA 42 44 480 C SE [48]
USA 85 10 478 T SE [48]
USA nd 30 343 C SE [41]
Colombia 81 13 200 C SE [42]
Denmark 48 96 150 Cb SE [50]
Denmark 74 81 167 Cc SE [50]
Sweden 78 10 100 C SE [46]

Abbreviations: nd, not determined; C, chicken; T, turkey; C/T, chicken and turkey.
a
Direct plating preceded by culture in non-selective broth.
b
Broiler meat produced in Denmark.
c
Broiler meat imported to Denmark.

consequences of exposure to contaminated poultry meat differ
between enterococci and S. aureus. Enterococci can colonize
the consumers gut, mainly the colon, where they represent a
small proportion (<1%) of the culturable microbiota [5], and
subsequently may act as opportunistic pathogens and donors of
antimicrobial resistance determinants to the indigenous
microbiota. Ingestion of S. aureus strains may lead to food
poisoning if the strains present on meat have the ability to
produce enterotoxins [6]. In addition, it has been hypothesized
that handling or consumption of poultry meat may result in
colonization of skin and mucosae (e.g. nasal and oral mucosae)
[7,8], which is considered an important risk factor for S. aureus
infections [9]. Food-borne transmission of livestock-associated
methicillin-resistant S. aureus (MRSA) is of particular concern
in view of the recent emergence of these multidrug-resistant
bacteria in meat products, including poultry meat [10,11].
Zoonotic transmission of enterococci and S. aureus from
poultry has been studied almost exclusively in relation to
antimicrobial resistance, primarily vancomycin and methicillin
resistance, respectively. Experimental data on colonization of
the human gut by resistant strains of poultry origin are scarce
and limited to enterococci. Hence frequency and load of these
bacteria on poultry meat and comparative analysis of antimi-
crobial resistance patterns and clonal types among poultry and
human clinical isolates are the only scientic elements available
to assess the risk of food-borne transmission.
The present review provides state-of-the-art knowledge of
the human health risks associated with the occurrence of these
opportunistic pathogens on poultry meat with particular focus
on the contribution of antimicrobial-resistant strains of poultry
origin to human infections. PubMed was searched systematically
for articles published in the last 5 years on prevalence, anti-
microbial resistance and host specicity of enterococci and
S. aureus on poultry meat as well as for older articles doc-
umenting health risks derived from ingestion of strains of
poultry origin. National surveillance reports were used to
complement such information. Epidemiological links between
poultry meat and human infections were inferred based on
similarities in the patterns of antimicrobial resistance and clonal
distribution between poultry and human clinical isolates.
Prevalence and Loads of Enterococci and
S. aureus on Poultry Meat
Poultry meat may become contaminated with E. faecalis,
E. faecium and S. aureus at slaughter or through food handling.
For enterococci, it is assumed that most bacteria present on
meat derive from animals because gut bacteria from food
handlers should not reach food products if good hygiene
standards are followed. It should be noted that enterococci
are normal commensals in the gut of poultry and contamina-
tion of carcasses by faecal bacteria is more common in poultry
than in other food-producing animal species, mainly because
of the lower hygienic standards in poultry slaughtering
compared with pig and cattle slaughtering. Consequently, the
prevalence of poultry meat samples contaminated by entero-
cocci is generally high, even though it varies greatly depending
on the sample types and the isolation methods employed by
different studies as well as on the hygiene conditions of the
slaughterhouse(s) under study (Table 1). Based on the avail-
able scientic literature, the prevalence of raw poultry meat
products contaminated with E. faecalis and E. faecium may
reach 96% (Table 1). The load of enterococci on poultry meat
ranges from 101 to 103 CFU per gram of raw chicken or
turkey meat [12,13].

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132 Clinical Microbiology and Infection, Volume 22 Number 2, February 2016 CMI

TABLE 2. Prevalence (%) of Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) in raw poultry meat as determined by
selective enrichment (SE) and direct plating (DP) on selective media

Country S. aureus MRSA Meat type No. of isolates Method Reference

Canada 1 C 250 SE [28]

USA 0 C 222 DP [29]
USA 18 0 C 45 SE [22]
USA 19 0 T 36 SE [22]
USA 25 2 T 57 nd [23]
USA 25 4 C 76 nd [23]
USA 41 0 C 46 SE [21]
USA 77 4 T 26 SE [21]
The Netherlands 16 Ca 520 SE [10]
The Netherlands 35 Ta 116 SE [10]
Germany 24 C 443 SE [30]
Germany 25 Ca 24 SE [24]
Germany 32 T 460 SE [20]
Germany 50 Ta 22 SE [24]
Denmark 0 Cb 121 SE [11]
Denmark 18 Cc 193 SE [11]
Poland 68 1 C 125 SE [17]
China 41 2 C 264 SE [27]
Pakistan 18 1 C 209 SE [14]
Hong Kong 7 Ca 255 SE [26]
Korea 43 0.5 C 913 nd [25]

Abbreviations: nd, not determined; C, chicken; T, turkey.

a
Including imported meat.
b
Broiler meat produced in Denmark.
c
Broiler meat imported to Denmark.

Staphylococcus aureus in retail poultry meat products can
have either animal or human origin as a consequence of
possible contamination by meat handlers. Both S. aureus and
MRSA have been shown to be more frequent in turkey meat
(19.4%77% and 32%50%, respectively) than in chicken meat
(17.8%68% and 0.3%25%, respectively) (Table 2)
[10,11,1430]. This reects the higher prevalence in turkey at
the farm level [16,19]. The frequency of S. aureus/MRSA isola-
tion from poultry meat is generally similar to that from pork but
higher than that from beef [10,2123,26]. Based on the few
data available in the scientic literature, the load of S. aureus in
poultry raw meat is generally below 102 CFU/g [3133] with
the exception of minced meat, where S. aureus concentrations
as high as 104 CFU/g have been reported in one study [33].
With regard to the load of MRSA, a Canadian study estimated
very low level of contamination (1030 CFU/g) on raw chicken
meat [28]. Experimental infection of healthy and traumatized
skin was successfully reproduced in 50% of skin sites (ID50)
using an inoculum of 103 and 102 CFU/cm2, respectively,
although occlusion was always necessary [34]. Based on these
data MRSA loads on raw chicken meat appear to be too low to
cause infection by contact with healthy intact skin.
Antimicrobial Resistance in Enterococci and
S. aureus Isolated from Poultry Meat
Enterococci are intrinsically resistant to various antimicrobial
classes and there are remarkable differences in the patterns and
to a lesser extent in the genetic bases of acquired resistance
between E. faecium and E. faecalis [1]. A wide variety of resis-
tance genes has been detected in S. aureus of animal origin
conferring resistance to virtually all antimicrobial classes used in
veterinary medicine [35]. Data on antimicrobial resistance in
enterococci isolated from meat products are provided by
numerous studies [3645] and surveillance programmes
[30,4650] that have employed these microorganisms as in-
dicators of antimicrobial resistance. On the contrary, data on
antimicrobial resistance in S. aureus of meat origin are scarce
and largely biased to MRSA. Prevalence of antimicrobial resis-
tance changes over time and varies depending on host species
and country of origin (Fig. 1) [51], most likely as a consequence
of differences in antimicrobial usage.
At present, the resistance phenotypes of clinical relevance
that may be linked to poultry meat comprise resistance to
ampicillin, gentamicin, quinupristin-dalfopristin and vancomycin
in E. faecium and resistance to gentamicin in E. faecalis. Resis-
tance to ampicillin and vancomycin in E. faecalis and resistance
to other clinically relevant drugs such as linezolid, daptomycin
and tigecycline in both species are rare or even not detected
among poultry isolates [51]. In contrast, enterococci of poultry
origin often exhibit resistance to tetracyclines but such a
phenotype has limited importance from a human clinical
perspective [51]. Methicillin resistance is by far the most
important resistance phenotype in S. aureus isolated from
poultry meat because of the importance of -lactams in the
therapy of staphylococcal infections and of the emergence of
livestock-associated MRSA in poultry farming [2,16,20]. Other

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CMI Bortolaia et al.
antimicrobial classes used in the management of S. aureus in-
fections in clinical practice and to which resistance is observed
among poultry isolates include uoroquinolones, aminoglyco-
sides and lincosamides. Even though tetracyclines, macrolides
and trimethoprim-sulfamethoxazole are rarely used for man-
agement of staphylococcal infections, these antimicrobial agents
are used in poultry production and resistance can be used as a
marker to track zoonotic transmission [51,52].
Poultry reservoirs of antimicrobial-resistant enterococci and
S. aureus may be identied by comparing patterns of antimi-
crobial resistance in isolates from poultry meat and diseased
humans within dened geographical regions. National surveil-
lance programmes represent an optimal source of data repre-
sentative of large populations and comparable across countries
and over time. This explains why the data on occurrence of
antimicrobial resistance in enterococci presented in this review
are largely based on national surveillance reports including data
for both human and poultry isolates (Fig. 1). Ampicillin resis-
tance is relatively common in E. faecium compared with
E. faecalis. The prevalence of ampicillin-resistant E. faecium in
poultry meat products varies signicantly depending on
geographical region and poultry species (Fig. 1a). For example,
in Denmark ampicillin-resistant E. faecium accounts for 3% and
16% of E. faecium isolates from domestic and imported broiler
meat, respectively [50], whereas in the USA it represents 10%
and 54% of the isolates from chicken and turkey meat,
respectively [48].
Ampicillin resistance occurs at high levels (>90%) in human
clinical isolates independent of geographical origin (Fig. 1a),
which is an indirect indication that poultry meat does not
contribute signicantly to occurrence of ampicillin resistance in
human pathogenic E. faecium. This is further supported by the
population genetics of human pathogenic ampicillin-resistant
E. faecium, which are to a certain degree distinct from those
of poultry strains (see the next section and references therein)
and by the fact that ampicillin resistance mainly spreads in
E. faecium by vertical transmission of chromosomal mutations
whereas conjugative transfer of ampicillin resistance has been
reported sporadically [53,54]. Hence, the risk that ampicillin-
resistant E. faecium possibly ingested through food may trans-
fer ampicillin resistance determinants horizontally to human
pathogenic E. faecium is very limited based on current knowl-
edge [1].
The patterns of gentamicin resistance in E. faecium also vary
signicantly between countries. In Denmark, high-level genta-
micin resistance is absent in poultry meat isolates despite being
high (72%) among clinical isolates (Fig. 1a(i)), whereas in the
USA high-level gentamicin resistance occurs less frequently
(13%) among clinical isolates but more frequently among
poultry meat isolates (7% and 8% in broiler and turkey meat,
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Antimicrobial-resistant enterococci and S. aureus on poultry meat 133
respectively) (Fig. 1a(v)). Similar patterns are also observed for
high-level gentamicin resistance in E. faecalis (Fig. 1b). These
data suggest that the potential risk of transfer of high-level
gentamicin resistance from poultry to human enterococci is
higher in the USA than in Denmark, although comparative
studies of the mobile genetic elements encoding gentamicin
resistance in poultry and clinical strains are needed to assess
this zoonotic risk.
Similarly, the patterns of vancomycin-resistant E. faecium
(VREF) appear to be unconnected between humans and poultry
within dened geographical areas. In Denmark, prevalence of
VREF has never been >4.5% among clinical isolates, whereas it
ranged from 80% in 1995 to undetectable levels in 2013 in
E. faecium isolated from poultry and poultry meat [50]. In
contrast, VREF is widespread in hospitals in the USA (up to 76%
of clinical isolates), whereas it is virtually absent among isolates
from poultry [48] (Fig. 1a(v)). These prevalence data clearly
mirror the patterns of glycopeptide use in human medicine in
the two countries as vancomycin is rarely used in Denmark but
has been extensively used for two decades in the USA [1,50].
Transfer of vancomycin resistance from poultry to clinical
enterococci has been hypothesized mainly for the vanA type
because other resistance determinants such as vanB and vanN
have been detected in poultry meat isolates only sporadically
[44,55]. This hypothesis was supported by the discovery of a
poultry-specic nucleotide polymorphism in the vanX allele (G
at position 8234) in the vanA-carrying transposable element
(Tn1546) in clinical isolates [56,57]. However, this zoonotic
risk has diminished considerably after the ban of avoparcin use
and the consequent decrease of VREF in poultry ocks [58],
even though a high frequency (50%) of VREF-positive broiler
ocks at slaughter has been reported in Denmark 15 years after
the ban of avoparcin [59].
Quinupristin/dalfopristin resistance occurs at variable fre-
quency (28%73%) among E. faecium isolates from poultry
meat both in Europe and in the USA (Fig. 1a), suggesting that it
is not directly linked to use of the quinupristin/dalfopristin
analogue virginiamycin, which was discontinued in European
poultry production in 1999 but is still used in the USA. Co-
selection of quinupristin/dalfopristin-resistant strains in
poultry may be enhanced by genetic linkages to genes confer-
ring resistance to other antimicrobial classes (e.g. macrolides)
[60]. Information on occurrence of quinupristin/dalfopristin
resistance in human isolates is limited. Different authors sug-
gested that poultry may represent a reservoir of this resistance,
but the hypothesis has not been corroborated by molecular
epidemiology data on strains of poultry and clinical origin
[61,62].
Also, tetracycline resistance occurs at variable frequency in
enterococci isolates from poultry meat of different geographical
134 Clinical Microbiology and Infection, Volume 22 Number 2, February 2016 CMI

(a)
(i) (ii)

(iii) (iv)

(v)

(b)
(i) (ii)

(iii) (iv)

FIG. 1. Prevalence of antimicrobial resistance in Entero-

(v) (vi)
coccus faecium (a), Enterococcus faecalis (b) and Staphylo-
coccus aureus (c) isolated from poultry meat and human
invasive infections within dened geographical areas. (a,b)
Data were retrieved from surveillance reports [4648,50]
if available; otherwise data from EFSA (for meat samples)
[30] and EARS-net/ResistanceMap (for invasive infections)
(c) [49,65] were used. (c) Data were retrieved from refer-
ences [2123,29,64,65]. AMP, ampicillin; BSB, -lacta-
mase-susceptible -lactam; BRB, -lactamase-resistant
-lactam; DAP, daptomycin; FQ, uoroquinolones; GEN,
gentamicin; KAN, kanamycin; LZD, linezolid; MLS, mac-
rolide/lincosamide/streptogramin; Q/D, quinupristin/dal-
fopristin; RIF, rifampin; TET, tetracycline; TMP/SMX,
trimethoprim-sulfamethoxazole; VAN, vancomycin.
Numbers in brackets represent the total number of iso-
lates tested. *Prevalence of quinupristin/dalfopristin resis-
tance in Danish E. faecium isolates is 54% according to the
EFSA report in which a cut-off value of >1 g/mL is used.

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CMI Bortolaia et al.
origin (10%75% in E. faecium and 35%87% in E. faecalis) but
in this case there is a plausible link between the occurrence of
tetracycline resistance and the widespread use of tetracyclines
in poultry production [30,4650]. Information on tetracycline
resistance in clinical isolates is generally unavailable because it is
not relevant from a clinical perspective. Nevertheless, occur-
rence of tetracycline resistance genes may play a role in co-
selection of genes conferring resistance to clinically relevant
antimicrobials as hypothesized for glycopeptides [63].
The few data available on antimicrobial resistance in S. aureus
isolates from poultry originate from research articles with
limited numbers of isolates and the antimicrobials tested often
do not correspond with those tested for human clinical isolates.
An extensive data set including S. aureus isolates from poultry
meat and human infections in the USA indicates signicantly
higher prevalence of resistance to aminoglycosides, uo-
roquinolones, macrolides, quinupristin-dalfopristin and
trimethoprim-sulfamethoxazole among human clinical isolates
and higher prevalence of tetracycline resistance among poultry
meat isolates (Fig. 1c) [2123,29,64,65]. High prevalence of
tetracycline resistance (as high as 100%) has also been reported
in poultry meat isolates in Germany [66], Poland [17], Hong
Kong [26] and Korea [25]. Overall these data suggest that
poultry isolates are less often resistant to antimicrobials with
the exception of tetracyclines, an antimicrobial class that is
widely used in the production of poultry and other livestock
but that has limited importance in the management of human
S. aureus infections. The recent emergence of MRSA in poultry
meat is a reason for concern because of the importance of
methicillin resistance in clinical settings [67]. However, there is
no evidence that poultry meat can act as a source of MRSA
colonization or invasive infection in humans [7]. Furthermore,
methicillin resistance and other resistance phenotypes of clin-
ical relevance have no implications for S. aureus food poisoning
because this gastrointestinal illness is not managed by antimi-
crobial therapy [67]. Altogether the human health risks asso-
ciated with the presence of antimicrobial-resistant S. aureus on
poultry meat appear to be limited on the basis of the current
scientic literature.
Host-specicity of Enterococcal and S. aureus
Lineages on Poultry Meat
Antimicrobial-resistant enterococci of poultry origin ingested
with food have been shown both to colonize the digestive tract
of healthy humans for a variable time up to 14 days after
ingestion and to exchange antimicrobial resistance genes with
the indigenous microbiota [68,69]. It is unknown to what
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Antimicrobial-resistant enterococci and S. aureus on poultry meat 135
extent these events happen in non-experimental conditions and
contribute to human infections. Recent studies on the popula-
tion structure of E. faecalis and E. faecium of human and animal
origins provide useful information to limit this knowledge gap.
Specic E. faecalis lineages such as clonal complexes CC2,
CC16 and CC87 (as dened by multilocus sequence typing) are
enriched among hospital-derived strains, which is largely
attributable to acquisition of virulence factors and antimicrobial
resistance genes through horizontal gene transfer [70]. How-
ever, in the E. faecalis population structure there is no cate-
gorical evolutionary distinction between clinical, commensal
and animal strains, as shown by Bayesian-based modelling of
population structure [71]. This implies that E. faecalis occurring
on poultry meat, and especially multidrug-resistant strains
belonging to sequence type ST16, may retain a zoonotic po-
tential mainly linked to the lack of host specicity. This gener-
alist lifestyle may allow food-borne strains to colonize the
human gut after ingestion of contaminated food and cause
infection if pathogenic conditions arise.
In contrast with E. faecalis, the majority of E. faecium in-
fections in humans are caused by strains clustering in clade A1,
as dened by single nucleotide polymorphism-based phyloge-
netic analysis of whole-genome sequence data from strains
collected across Europe and the USA. Clade A1 strains, which
include strains belonging to the hospital-associated lineages 17
(comprising, among others, ST16 and ST17), 18 (ST18) and 78
(ST78 and ST192) differ considerably from human commensal
isolates and, to a lesser extent, from animal isolates [72]. In
particular, ST78 isolates have putative evolutionary origins in
common with pets (dogs and cats) and poultry isolates, and
diversied mainly through recombination and acquisition or
loss of mobile genetic elements, which eventually led to adap-
tation to different ecological niches [7175]. Although this
ecological distinction is not absolute, it appears that the main
zoonotic risk linked to E. faecium isolates is represented by
transfer of mobile genetic elements harbouring antimicrobial
resistance genes.
Whereas living poultry is colonized by typically poultry-
associated S. aureus (e.g. ST5, spa types t002, t306 and
t13620) [17,18,76] or livestock-associated MRSA lineages (e.g.
ST9 and ST398) [15,1820], strains isolated from poultry meat
comprise a combination of animal- and human-associated lin-
eages [11,17,20,23,27,77] (Fig. 2). These data suggest persis-
tence of poultry lineages through the meat production chain
[20] but most importantly, provide a strong indication that
slaughtering and meat handling represent critical points for
meat contamination with strains of human origin [17,21,28].
Frequent S. aureus and MRSA lineages in poultry such as ST5
(CC5) and ST398 (CC398) are also common among human
clinical isolates (Fig. 2) [78,79]. It has been proposed that the
136 Clinical Microbiology and Infection, Volume 22 Number 2, February 2016
S. aureus ST5 sub-lineage associated with poultry has evolved
by a single human-to-poultry host jump [80], as previously
hypothesized for livestock-associated MRSA ST398 in pigs [81].
However, poultry ST5 isolates can be discerned from human
clinical isolates by highly discriminatory typing methods such as
single nucleotide polymorphysm, revealing a high degree of
adaptation [80]. The role of poultry as a source of MRSA
CC398 human infections cannot be assessed because it is not
possible to discern between strains originating from poultry
and other animal species. However, the overall impact of this
livestock-associated lineage appears to be limited, especially in
countries with high MRSA prevalence in the human population
[82]. Other MRSA lineages that are possibly epidemiologically
linked to poultry include ST239 (CC8), which has been re-
ported among healthy chickens in Belgium [16] and is a
worldwide disseminated hospital-acquired MRSA [79] but to
the best of our knowledge has never been reported on poultry
meat. MRSA lineages that have been reported sporadically on
poultry meat products but not in live poultry such as Pan-
tonValentine leukocidin-positive ST8 (USA300) and ST45 are
well-known human-adapted lineages and their occurrence on
chicken meat [11,20,23] is most likely attributable to
contamination.
Transmission of S. aureus from livestock is strongly associated
with direct contact to living animals [15] and secondary human-
to-human propagation from farm settings to the community has
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CMI
FIG. 2. Proportions of S. aureus lin-
eages in live poultry and poultry raw
meat (modied from refs
[10,11,1528,77]).
been considered limited until recently, when proportions of 11
and 38% of MRSA CC398 colonized people report no contact
with pigs, veal calves or broilers [50,83]. The majority of these
cases with unknown CC398 origin are reported in areas of high
livestock production [84]. It has been suggested that MRSA
ST398 cases in people without contact with livestock could be
due to meat handling [85] and consumption of poultry has been
identied as a risk factor for MRSA carriage [86]. However, the
risk of MRSA colonization through exposure to contaminated
meat was estimated to be low for professional meat handlers in
Europe and even lower for the general population [87], although
the risk appears higher in other parts of the world [88]. In
countries like Denmark and the Netherlands, where the popu-
lation is highly concentrated in a few urban areas, the vast ma-
jority of MRSA ST398 cases occur in rural areas with high pig
population densities [89,90]. The low frequency of infections in
urban areas provides indirect evidence that food is not an
important source for transmission of livestock-associated MRSA.
As concluded by Wendlandt et al. [67], the occurrence of MRSA
in meat products does not equate to MRSA being considered a
food-borne pathogen. Even though colonization by ingestion
cannot be neglected [28], considering the low loads of both
S. aureus and MRSA on contaminated poultry meat, the risk is
probably extremely low if meat is consumed after proper
cooking. Accordingly, the European Food Safety Authority
reached the conclusion that the risk of infection to
CMI Bortolaia et al.
slaughterhouse workers and persons handling meat appears to
be low based on the published literature [91].
Conclusions
Although chicken and to a greater extent turkey meat are often
contaminated with E. faecalis, E. faecium and S. aureus, the
bacterial loads are generally low and the risk that humans may
become colonized after ingestion or handling of contaminated
poultry meat can be prevented by proper cooking and kitchen
hygiene. Food-borne colonization of the human gut is more
plausible for enterococci than for S. aureus but the risk that
multidrug-resistant enterococci of poultry origin may cause
infections concerns mainly E. faecalis. The magnitude of this risk
remains unknown and appears to be limited to specic lineages
such as ST16. Colonization by MRSA and other multidrug-
resistant S. aureus after ingestion of contaminated meat is not
supported by scientic evidence. Even though in theory meat
handling is a possible transmission route and there is still a
substantial uncertainty with respect to the prevalence of in-
fections caused by MRSA outside the hospital, epidemiological
data from countries where MRSA is notiable and more in-
formation is available on the MRSA types causing community-
acquired infections indicate that this risk is low for the gen-
eral population [92].
Transmission of antimicrobial resistance by horizontal gene
transfer represents the main risk posed by resistant entero-
cocci on poultry meat. Transfer of gentamicin resistance in
E. faecium and E. faecalis and of quinupristin/dalfopristin resis-
tance in E. faecium are the major potential risks with remark-
able differences between geographical regions. Antimicrobial
resistance is of limited importance in S. aureus strains causing
food poisoning because treatment does not involve antimicro-
bials. Moreover, there is no evidence supporting a ow of
resistance genes of clinical relevance from poultry to human
S. aureus.
Current knowledge on the impact of food-borne E. faecium,
E. faecalis and S. aureus on poultry meat is limited and often
based on indirect evidence. Data on the minimum dose of
resistant strains of poultry origin required to colonize the hu-
man gut and a deeper insight into strain and host factors that
mitigate for or against colonization and transfer of antimicrobial
resistance to the commensal microbiota are needed to assess
the actual health risks to consumers.
Transparency Declaration
The authors declare no conict of interest.
Clinical Microbiology and Infection 2015 European Society of Clinical Microbiology and Infectious Diseases. Published by Elsevier Ltd. All rights reserved, CMI, 22, 130140
Antimicrobial-resistant enterococci and S. aureus on poultry meat 137
Authorship/contribution
VB and CEG collected relevant literature on enterococci and
S. aureus, respectively. LG coordinated the study. All authors
contributed to critical discussion of the available literature and
writing of the manuscript.
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