Implications for our Food Supply?

Sources of Methicillin-Resistant Staphylococcus aureus (MRSA) and Other Methicillin-Resistant
Staphylococci: Implications for our Food Supply?

M. Ellin Doyle 1 , Faye A. Hartmann 2 , Amy C. Lee Wong 1,3 ,
Food Research Institute 1 , Clinical Pathology Laboratory, Veterinary Medical Teaching Hospital 2 ,
Department of Bacteriology 3 , University of Wisconsin, Madison

January 2011

Funded in part by the American Meat Institute Foundation with the financial help of Orion Code.

1 Background on Pathogenic Staphylococci

Staphylococcus aureus

Human foodborne intoxication
Staphylococcus aureus is a well-known foodborne pathogen that produces heat-stable
enterotoxins during growth on a variety of foods including meat and poultry products, eggs,
cream-filled pastries, potatoes, and some salads. Vegetables are less commonly cited as vehicles
for S. aureus. However, two outbreaks in restaurants in the U.S. in 2003 and 2005 were traced to
carrots, green peppers, and leeks. In addition, a survey of minimally processed vegetables and
sprouts in Korea found that about 11% were contaminated with S. aureus. (200)
Numerous staphylococcal enterotoxins have been described and it is ingestion of these
enterotoxins and not of S. aureus cells that cause a rapid onset of nausea and vomiting within 1-6
hours. Less than 200 ng toxin is sufficient to cause symptoms (59). Generally S. aureus
concentrations of 100,000 cells/g food are necessary. Although symptoms may be severe, they
usually resolve within a day and serious complications, hospitalization, and death are rare,
afflicting primarily the very young, the elderly, the chronically ill and those who have consumed
a large amount of contaminated food.

In some circumstances, ingestion of staphylococci can cause enteritis. Staphylococcal
enterocolitis occurs occasionally in infants, immunocompromised adults and others receiving
large doses of antibiotics. When normal human intestinal flora is depleted or absent, S. aureus
cells may grow in the intestines and produce enterotoxins that cause profuse diarrhea. (133)
S. aureus has been a food safety concern for meat producers and food processors for
decades because it is widespread in the environment and often detected in air, dust, water, raw
milk, other foods, and on environmental surfaces. It survives desiccation and tolerates high levels
of salt. S. aureus cells are destroyed by heat but if they have already produced enterotoxins in a
food, the toxins will survive approved doses of irradiation and some thermal processes, including
pasteurization. (69;179)

S. aureus has also been a problem for caterers and others involved in food preparation.
According to several studies, S. aureus is present in nasal passages or skin of about 50% of
people and in intestines of about 20% of people in the general population. (4;66) Thus,
asymptomatic food handlers may harbor S. aureus and can contaminate food during preparation.
(211) If contaminated foods, for example salads or some desserts at a picnic, are left out at
ambient temperature for extended periods, S. aureus may multiply and produce enterotoxins.
Staphylococcal food poisoning is believed to be greatly underreported (by about 25 fold)
and underdiagnosed (by about 29 fold). The short duration of illness and infrequent
complications seldom bring it to the attention of health care professionals. Staphylococcal
enterotoxins cause foodborne illness in about 241,000 persons in the U.S. annually. (191)
Twenty-one outbreaks in the U.S. in 2007 (and 14 in 2008)
(http://www.cdc.gov/foodborneoutbreaks/documents/2007/bacterial.pdf) and 291 outbreaks in
Europe in 2008 (56) were attributed to staphylococcal enterotoxin poisoning. Data from Centers
for Disease Control and Prevention (CDC) indicate that nearly half of the 542 outbreaks
occurring in 1998-2008 were associated with some type of meat. (Table 1). Seafood,
potatoes/rice/noodles, vegetables/salads, combination foods, and dairy products were also cited
as food vehicles. Reported annual outbreaks during this 10 year period peaked in 2002 and then
declined. (Figure 1). Approximately 53% of reported outbreaks affected only 2-4 people while
only 6.7% of outbreaks involved more than 50 cases. Table 2 lists some large outbreaks
occurring during this period in the U.S., Argentina, Brazil, India, Japan, and Europe.

Non-foodborne human illness
Nearly all S. aureus isolates are coagulase positive, i. e. they produce an enzyme that
causes clotting of blood plasma. In addition, S. aureus produces many other virulence factors
(besides enterotoxins) such as exfoliative toxins, toxic shock syndrome toxin, and leukocidins
and is responsible for a variety of mild to severe skin and soft tissue infections and numerous
serious infections including endocarditis, endophthalmitis, osteomyelitis, meningitis, bacteremia,
pneumonia, and toxic shock syndrome. (125) Approximately 50% of healthy adults carry S.
aureus in their nasal passages or on skin and about half of those persons are persistent carriers
and the remainder are intermittent carriers. (66) Some data indicate that host genetic factors
(181) and competing microflora (66) may affect persistence of colonization by S. aureus. A
review of published data revealed that, overall, nasal, inguinal or axillary colonization with S.
aureus was associated with a four-fold increase in serious infections. (185) Asymptomatic
carriage or colonization of individuals with S. aureus may be a risk factor for person-to-person
transmission of these bacteria and for contamination of food.
ME Doyle, FA Hartmann, ACL Wong
Food Research Institute, UW–Madison, www.fri.wisc.edu/
January 2011
Funded in part by the American Meat Institute Foundation
4Animal infections
Infections due to S. aureus have been reported in many mammal species as well as for
wild and domestic birds and in some reptiles. Some animals are asymptomatic while others
suffer respiratory, gastrointestinal, or skin and soft tissue infections. S. aureus is a significant
cause of mastitis in cows and small ruminants (230). Whether animals can be persistent carriers
of S. aureus in a manner similar to humans has yet to be determined. However, animals can
intermittently harbor S. aureus. A recent study found that 10% of healthy dogs visiting a clinic
for regular vaccinations harbored S. aureus (180). Molecular analyses of isolates from different
animals have revealed that there are some strains that appear to be host-dapted to a particular
animal species (horses, cattle, pigs, sheep, chickens, or humans) and other strains can colonize
multiple species of animals. (37) S. aureus can be transferred between humans and animals and
frequently infections in companion animals can be traced back to their human caretakers. (184)
Other pathogenic staphylococci
Coagulase-positive staphylococci, other than S. aureus, can cause infections in humans
and animals. Some veterinary isolates of coagulase-positive staphylococci are classified in the S.
intermedius group (SIG). S. intermedius was originally described in 1976 and appeared to be part
of the normal microflora of the skin and mucosal membranes of dogs and cats. It has also been
detected in a variety of other animals, including horses, mink, goats, foxes, raccoons, and
pigeons but is not commonly present in humans. Recent molecular analyses demonstrated that
isolates of S. intermedius detected in a large number of different animals and geographic
locations have some significant differences and the species can best be reclassified into three
clusters: S intermedius, S. pseudintermedius, and S. delphini A and B. These three species
constitute the S. intermedius group (SIG). (190)
S. pseudintermedius is the most frequently encountered pathogen in the SIG and was first
identified as a novel species in 2005 by examination of rRNA gene sequences in clinical
staphylococcal isolates from several animals. (45) The majority of isolates from dogs are now
classified as S. pseudintermedius although earlier research papers identified them as S.
intermedius. S. delphini was originally isolated from a dolphin but some isolates from horses,
pigeons and mink, previously identified as S. intermedius, are now classified as S. delphini. (202)
S. pseudintermedius has been isolated from pet owners and veterinarians (154) and
occasionally causes infections in humans exposed to dogs carrying these bacteria (29;206).
Invasive infections have occurred in persons bitten by dogs (65) and two recent articles reported
S. intermedius as the cause of skin abscesses in an injecting drug user (106) and meningitis in an
infant (48).
S. intermedius group pathogens produce a number of virulence factors (coagulase,
hemolysins, exfoliative toxin and others) similar to those associated with S. aureus. (65;91)
When animals are injured, sick, or otherwise weakened, these bacteria may cause skin, ear, and
wound infections. (240) Some SIG isolates also produce enterotoxins and could potentially cause
foodborne intoxication. (14) One foodborne outbreak in southwestern U.S. in 1991 affecting
over 265 people was traced to S. intermedius producing type A enterotoxin in a butter blend.
(110)
Compared to coagulase-positive staphylococci, coagulase-negative staphylococci are
rarely pathogenic and are often considered to be opportunistic pathogens, such as S. epidermidis
ME Doyle, FA Hartmann, ACL Wong
Food Research Institute, UW–Madison, www.fri.wisc.edu/
January 2011
Funded in part by the American Meat Institute Foundation
5is for humans. (27) However, occasionally coagulase-negative staphylococci produce
enterotoxins and have been associated with foodborne outbreaks. (232) .
Certain coagulase-negative staphylococci are important components of meat starter
cultures. (60) Recent investigations found that genes coding for staphylococcal virulence factors
were rare in coagulase-negative staphylococci isolated from sausage and cheese. Of 129 strains
tested, only one contained a gene coding for an enterotoxin and none were capable of producing
toxic shock syndrome toxin. Some strains did have genetic information coding for hemolysins
and some were capable of producing biogenic amines. Of somewhat greater potential concern
was the presence of antibiotic resistance genes in 71% of isolates with nearly half the strains
resistant to more than one antibiotic (58)
Methicillin Resistance in Staphylococci
Staphylococci are notorious for rapidly evolving resistance to many antibiotics.
Penicillins and other β-lactam antibiotics kill bacterial cells by interfering with cell wall
synthesis. Not long after penicillin was first used to treat human infections, S. aureus strains
producing penicillinase (an enzyme that degrades penicillin) were detected and it is estimated
that now >80% of S. aureus produce penicillinase. Methicillin (meticillin), a β-lactam antibiotic
that is not inactivated by penicillinase, was introduced in the late 1950s. But by 1961, there were
reports of methicillin-resistant staphylococci in a hospital in the United Kingdom. (94) Although
epidemiology of MRSA (methicillin-resistant S. aureus) is currently being intensely studied, it
should be noted that, in most hospitals and geographic areas, MSSA (methicillin-susceptible S.
aureus) are responsible for a greater number of infections and are often also resistant to multiple
classes of antibiotics.
MRSA: Methicillin-resistant Staphylococcus aureus
Methicillin-resistant S. aureus (MRSA) are resistant to all currently available β-lactam
antibiotics, including penicillins, cephalosporins, carbapenems, and their derivatives. Resistance
to methicillin is mediated by the mecA gene which encodes an altered penicillin-binding protein,
located in the cell wall, that has a low affinity for β-lactam antibiotics. Since β-lactam antibiotics
interfere with bacterial cell wall synthesis, this decreased binding of β-lactams renders them
ineffective against MRSA. The mecA gene resides on a large heterogeneous mobile genetic
element called the staphylococcal cassette chromosome (SCCmec). (90;105)
To date, nine SCCmec variations have been described but types I – V are the most
common. SCCmec types I – III are relatively large and are typically found in strains associated
with hospitals and other healthcare facilities. SCCmec types IV and V are smaller in size and are
usually found in MRSA associated with community-acquired infections. Molecular analyses of
numerous MRSA strains indicate that resistance genes have been transferred to various
methicillin-susceptible S. aureus (MSSA) strains on multiple occasions. (177) These resistance
genes have also been transferred to other staphylococcal species. Many MRSA are also resistant
to other classes of antibiotics which makes it a challenge to treat serious infections. Table 3 lists
important events in the emergence of methicillin-resistant staphylococci that infect humans.
MRSA have spread worldwide and are now the most commonly identified antibiotic
resistant bacteria in hospitals in Europe, the Americas, North Africa, and the Middle- and Far-
East. (53) Approximately 478,000 hospitalizations in the U.S. in 2005 were associated with S.
ME Doyle, FA Hartmann, ACL Wong
Food Research Institute, UW–Madison, www.fri.wisc.edu/
January 2011
Funded in part by the American Meat Institute Foundation
6aureus infections and 58% of those (278,000) were caused by MRSA. (114) MRSA is estimated
to cause illness in more than 150,000 persons annually in health care facilities in the European
Union. (124)
Terms used to designate different MRSA strains are sometimes inconsistent or confusing.
Many isolates and clones were originally named according to the geographical areas where they
were first described, for example USA100 (an isolate from U.S. hospitals) and the New
York/Japan clone. In 2002, a proposal was made to identify isolates according to sequence type
(ST), antibiotic resistance, and SCCmec type. ST is determined by multilocus sequence typing
(MLST) of 7 housekeeping genes in an isolate and comparing these to known sequences
published on the MLST website (http://saureus.mlst.net). As of February 2011, this site
contained data on 3665 isolates, representing 1861 STs. Antibiotic resistance is designated as
MRSA or MSSA and the SCCmec type as I to V. For example the New York/Japan clone is
ST5-MRSA-II and USA300 is ST8-MRSA-IV. However, many publications continue to refer to
well known strains by their old names. Sequence types that differ in only a few of the genetic
loci tested, are grouped into clonal complexes (CCs) using BURST (based upon related sequence
types) analysis. The number of the ST that is considered closest to the ancestral type is used as
the CC number. Five major clonal complexes originated in hospitals. (177) Other CCs developed
from S. aureus strains circulating in the community, outside of healthcare facilities. (39) CC398
is a clonal complex that originated in swine. (37;129)
MRSA carriage and infection in humans
According to several studies, approximately 50% of people in the general population are
carriers of S. aureus. (4;66) However, CDC estimates that only about 1.5% of the population are
carriers of MRSA. Screening of 8,446 patients entering a hospital in England for elective day-
surgery indicated that, overall, 0.76% were carriers of MRSA. However, the incidence was 4
times greater for persons >60 years of age than for those < 60 years old. (51) A much higher
prevalence of 7.5% was reported for >29,000 patients admitted to acute care hospitals in
Scotland. Data showed that rates were much greater for patients >65 years of age and for those
admitted from other health care facilities. (174) Nasal carriage of a livestock associated strain of
MRSA was 5.6% among employees of a Dutch pig slaughterhouse. (220) Several studies have
demonstrated that carriers of MRSA are at greater risk for developing serious infections
compared to people who are not carriers.
MRSA, like methicillin-susceptible S. aureus, can cause a range of infections from
relatively mild skin infections to life threatening invasive bloodstream infections, pneumonia,
central nervous system infections, and pericarditis. MRSA has been a chronic problem in
hospitals and long term care facilities for over 40 years causing severe infections, particularly in
patients in surgical wards and intensive care units. Infections acquired in the community
typically affect skin and soft tissues, causing mild to severe symptoms. These infections often
occur in healthy younger people without the usual risk factors for healthcare aquired MRSA and
infections often recur after treatment. Severe, invasive community acquired MRSA infections,
including pneumonia, also occur. There is evidence that these more severe infections are
increasing as the virulent USA300 strain spreads. (39)
Another troubling aspect of MRSA infections and colonizations is the fact that they often
persist for extended periods. Persistence of MRSA was monitored in 403 patients admitted to a
German hospital more than once during a three year period. Overall half-life of persistence was
549 days with duration of persistence dependent on the site(s) colonized or infected. (145)
ME Doyle, FA Hartmann, ACL Wong
Food Research Institute, UW–Madison, www.fri.wisc.edu/
January 2011
Funded in part by the American Meat Institute Foundation
7Hospital-associated MRSA (HA-MRSA)
MRSA was first detected in a UK hospital in 1961 and was detected a few years later in
U.S. hospitals and other health care facilities where the widespread use of antibiotics selected for
bacteria carrying resistance genes. Until the 1990s, MRSA was almost exclusively an issue in
hospitals and long term care facilities, affecting surgical patients, other aged or ill residents, and
some healthcare workers. Some MRSA infections occurred in non-hospitalized persons but these
were traced to close contacts with persons who had been hospitalized. MRSA infections were
classified by CDC as HA if they were detected in patients 48 hours after admission to a hospital
or were detected in patients with a recent history of hospitalization, surgery, dialysis, or an
indwelling catheter. Due to the high rate of antibiotic usage in health care facilities, HA-MRSA
are often resistant to many classes of antibiotics (tetracyclines, sulfa-drugs, gentamicin,
tobramycin, etc.) in addition to the β-lactams. Five major lineages or clonal complexes (CC5,
CC8, CC22, CC30, CC45) originated in hospitals and have spread globally. Most possess one of
the larger SCCmec types I – III which also carry genes for resistance to other antibiotics. Type II
is most common in U.S. HA-MRSA while type III is found more often in other countries.
(39;146)
Recently, evidence has shown that a substantial minority of HA-MRSA infections are the
result of transmission outside of healthcare facilities and are caused by so-called “feral” strains
that “escaped” from the hospital environment. It has been suggested that the source of these feral
HA-MRSA strains may be persons, who acquired the strains years ago when they received health
care, and who then became long-term carriers in the community. These strains may also have
been disseminated by health care personnel that provide in-home care. (152)
Community-associated MRSA (CA-MRSA)
Cases of MRSA that genuinely originated in the community were originally reported
from a sparsely populated region in western Australia in the early 1990s. MRSA isolates from
these cases were not resistant to multiple antibiotics and genetic analyses revealed that they were
different from other MRSA in Australia. (32;217) More frequent reports of CA-MRSA emerged
in the late 1990s. Patients often suffered skin and soft tissue infections and were otherwise
healthy with no history of recent antibiotic use or residence in health care facilities. Examination
of these CA-MRSA isolates revealed that they were susceptible to more classes of antibiotics
than HA-MRSA and they generally carried smaller, more mobile SCCmec elements, usually
types IV or V. (39) Many CA-MRSA strains produce a toxin that attacks white blood cells called
PVL (Panton-Valentine leukocidin) that is not commonly present in HA-MRSA. Although some
studies suggest that PVL is an important virulence factor, others have shown that strains that do
not produce PVL cause lesions just as severe as those produced by PVL-positive strains. (130)
Several CA-MRSA clones originated in Europe (ST80), North America (ST1 and ST8),
and Australia (ST30) and subsequently spread worldwide with reported cases in countries as
diverse as the Republic of South Africa, Nepal, Argentina, Saudi Arabia, Japan, and Malaysia as
well as most countries in Europe. (214) A particularly virulent clone, USA300 (ST8), first
reported as cause of a prison outbreak in 2000 (36), now causes nearly all CA-MRSA cases in
the U.S. Over a 5 year period at a Baltimore Veterans’ Hospital, skin and soft tissue infections
(SSTIs) caused by USA300 went from 0 in 2001 to 84% of cases in 2005. This was accompanied
by a tripling of the number of hospital visits for SSTIs. (95) Cases of USA300 (Canadian name:
CMRSA10) infection have also been increasing rapidly in Canada. Annual incidence of all
ME Doyle, FA Hartmann, ACL Wong
Food Research Institute, UW–Madison, www.fri.wisc.edu/
January 2011
Funded in part by the American Meat Institute Foundation
8MRSA infections in Alberta doubled from 2005 to 2008 and this was primarily due to the rise of
CMRSA10. (112) USA300 is among the most virulent clones and appears to be more capable of
colonizing human epithelial surfaces and causing skin and soft tissue infections than other CA-
MRSA clones. USA300 contains SCCmec type IV and genes encoding PVL.
Originally USA300 was resistant only to β-lactam antibiotics and erythromycin.
However, in the past 5 years, USA300 has acquired a number of additional antibiotic resistance
genes, apparently from USA100, a common HA-MRSA strain. (147) It has also been
increasingly identified in more serious invasive infections. This strain has spread to Europe,
Asia, Australia and South America, and was the most commonly detected clone in U.S. military
hospitals in Iraq. (39;87;109;209)
CA-MRSA have been reported to cause an increasing proportion of MRSA infections,
including invasive infections, in hospitalized patients (144;219;222;244) and in patients with
end-stage renal disease (96) and cystic fibrosis (208). An analysis of discharge data on 616,375
pediatric cases of skin and soft tissue infections occurring in the U.S. during a ten year period
revealed that hospitalizations for infections caused by CA-MRSA increased dramatically from
<1 case/100,000 in 1996 to 25.5 cases/100,000 in 2006. Rates of CA-MRSA were highest in the
south among white children without health insurance. (67) The emergence of CA-MRSA in
healthcare settings and the appearance of HA-MRSA in the community, along with changes in
virulence and the scope of antibiotic resistance have blurred the distinctions between HA-
MRSA and CA-MRSA.
More extensive information on the evolution, virulence, and epidemiology of CA-MRSA
can be found in two recent comprehensive review articles. (39;164)
MRSA carriage and infection in animals
MRSA infects a variety of animals, including livestock, companion animals and some
wild animals. Table 4 lists some important events in the emergence of methicillin-resistant
staphylococci in animals. The earliest published report of MRSA in farm animals described the
detection of MRSA, in 1972, in Belgian dairy cows with mastitis. (44) Although current methods
for typing MRSA strains were not available then, it is believed that these cases resulted from
human to animal transmission of HA-MRSA. Later reports documented cases and outbreaks in
horses, dogs, and other animals at veterinary clinics and hospitals. (79;198). Some later reports
described animals (dogs, horses and cats) at veterinary hospitals with CA-MRSA infections.
(151)
A new MRSA strain, ST398, first detected in 2003 in swine and swine farmers in the
Netherlands (226;233). ST398 has also been detected in pigs and pig farmers in other countries,
including the U.S. (203), Canada (70;111) , Portugal (170), Belgium (43), and Germany (123).
In the past three years, ST398 has been isolated from humans, horses, chickens, and other
animals, including rats living on pig farms (37;80;221). A different swine-associated MRSA
strain is circulating among pigs and pig farmers in China. (35)
Most livestock-associated MRSA (LA-MRSA) isolates are resistant to tetracyclines and
over 70% of 54 strains tested were resistant to three or more classes of antibiotics, leading some
to suspect that the use of antibiotics in pig farming may have played a role in the evolution of
this strain. All of the strains tested were PVL negative and only four strains had genes coding for
enterotoxins. (101) Pigs, veal calves, and broilers appear to be the main reservoirs for ST398.
(50)
ME Doyle, FA Hartmann, ACL Wong
Food Research Institute, UW–Madison, www.fri.wisc.edu/
January 2011
Funded in part by the American Meat Institute Foundation
9Several studies reported that exposure to horses is a risk factor for human infection with
certain horse-adapted MRSA strains. (26) A majority of horse isolates in Canada belong to a
subtype of the Canadian epidemic strain, MRSA-5, which has a type IV SCCmec. This strain is
also present in horses in other countries and has been reported in numerous people working with
horses. (26;238) Horses can also be infected with ST398 and an outbreak of ST398 affecting 13
horses at a veterinary hospital in Finland resulted in one infected employee. (187)
Table 3 Significant events in emergence of methicillin-resistant staphylococci infecting humans
Year(s)
1961
1965
1968
1981
1988
1991-1992
1992-3
1997
1999-2000
2000
2001
2003
2008
2008-2009
Event
1 st methicillin resistant S. aureus identified in UK hospital
1 st MRSA cases recorded in Australia
1 st hospital outbreak of MRSA in USA
CA-MRSA in injecting drug users
CA-MRSA in hospitalized children, Chicago
1 st CA-MRSA detected in Australia
Foodborne outbreak of HA-MRSA
CA-MRSA in otherwise healthy children in MN and ND
Highly virulent USA300 strain first reported in football players
(PA) and prisoners (MO)
Outbreak caused by USA300 ; prison, Mississippi
Foodborne outbreak of CA-MRSA
LA-MRSA strain ST398 from pigs in Netherlands detected in
humans
Emergence of CA-MRSA strain USA300 in Japan
Multi-drug resistant, dog-related strains of methicillin-resistant
S. intermedius/pseudintermedius (ST71) detected in humans in
U.S., Switzerland
Reference
(94)
(39)
(11)
(188)
(83)
(217)
(118)
(89)
(209)
(36)
(98)
(42;233)
(85)
(108;206)
Swine. Of all livestock, swine appear to most commonly harbor MRSA. In most cases, MRSA
does not appear to seriously affect the health of pigs but there have been reports of MRSA in
pathological lesions in pigs. (149) In 2005, a high prevalence of a new livestock associated
MRSA, ST398, was reported in pigs at Dutch slaughterhouses. This strain was apparently
derived from a methicillin-sensitive S. aureus, known to be associated with pigs and was
designated livestock-associated or LA-MRSA. (42) Data from the EU on MRSA in 4,597 swine
holdings (breeding and production) in 26 countries revealed that overall 14% of breeding and
27% of production herds tested positive for MRSA. However, in some countries, no herds tested
positive while in others, up to 51% of holdings contained MRSA. Highest prevalence of MRSA
was recorded in Spain, Germany, Belgium, and Italy. LA-MRSA (ST398) accounted for 92.5%
of isolates tested. (54)
Other recent surveys report:
• 45% of farms and 25% of pigs in Canada carried MRSA with 59% of isolates identified
as ST398 (111)
• 70% of German pig farms tested positive for MRSA; all were ST398 (123)
ME Doyle, FA Hartmann, ACL Wong
Food Research Institute, UW–Madison, www.fri.wisc.edu/
January 2011
Funded in part by the American Meat Institute Foundation
10•


45% of Italian farms tested positive for MRSA; ST398 was most common strain but
several other types were identified (13)
One U.S. study reported that MRSA was present on 70% of pigs sampled at one
production facility and none of the pigs at another facility. Isolates were ST398. (203)
Another study indicated that MRSA prevalence in pigs at 5 U.S. farms ranged from 0 to
33%. (153) Data is currently available only for a few swine holdings in the U.S.
A survey of swine in Japan found a low prevalence of MRSA (0.9%) in nasal samples
and did not detect ST398. (10)
Factors positively associated with prevalence of MRSA in swine include larger herd sizes
and greater numbers of imported pigs. (55) “Open” versus “closed” farms also have more
colonized pigs, perhaps because of importation of pigs by open farms from MRSA-containing
herds. (57). In a German study, conventionally raised pigs were found to have a higher frequency
of MRSA colonization than organically raised pigs. (148) Hygiene practices on farms also
appear to affect prevalence rates. (157)
Cattle. S. aureus is a significant cause of mastitis in cows and small ruminants (230). However,
the prevalence of methicillin-resistant strains in European cows appears to be low, although there
is intercountry variation. (6;82) MRSA (probably of human origin) was first detected in Belgian
cows in 1972 (44). Recent studies have demonstrated that ST398 is present in German cows
(64), Dutch veal calves (73), and Belgian cows (229). CA-, HA-, and LA-MRSA were all
recently detected in bulk tank milk from cows in Minnesota. (78) Human-associated MRSA
strains have also been detected in mastitic cows in Hungary (100) and Turkey (215)
Poultry. Little information is available on the occurrence of MRSA in chickens and no reports
were found on MRSA in turkeys. Methicillin resistance was first observed in S. aureus isolates
from chickens in Korea in 2001-2003. (126) MRSA was later detected in broiler chickens in
Belgium (160;168) and in broilers but not in breeder chickens in the Netherlands (156). These
isolates were identified as the livestock associated strain, ST398.
Horses. MRSA was first reported in a horse with a surgical wound in 1996 (79). Eleven horses
were infected with MRSA at another veterinary hospital with a strain that appeared to be
identical to those isolated from staff members. (198) Surveys of horses on farms during the past
five years usually report a low prevalence of MRSA of 0 – 4.7%. A higher prevalence (up to
12%) has been observed in horses admitted to veterinary hospitals. (212;240) (236) Transmission
of MRSA from humans appeared to cause the early infections in horses. The most common
MRSA strain now identified in horses, Canadian CMRSA-5 or USA500, is a member of the ST8
or CC8 clone. Although this clone appears to be of human origin, it seldom causes illness in
humans and now appears to be horse-adapted. It is the most prevalent MRSA strain detected in
horses globally. Unlike other farm animals that are primarily transported only for slaughter,
horses are transported internationally for breeding, racing and show-jumping and these
movements have contributed to the spread of this clone. (2) Recently there have been reports of
the livestock-associated strain ST398 in horses (136;223), including a veterinary hospital
outbreak affecting 13 horses in Finland (187).
Table 4 Significant events in emergence of methicillin resistant staphylococci infecting animals
ME Doyle, FA Hartmann, ACL Wong
Food Research Institute, UW–Madison, www.fri.wisc.edu/
January 2011
Funded in part by the American Meat Institute Foundation
11Year(s)
1972
1972
1988
1993-1994
1996
1997
1999
1999-2001
2001-2003
2003
2004
2004-2005
2005
2006-2007
2005-2006
2007
2007
2009
2009
Event
MRSA identified in dairy cows with mastitis
MRSA detected in dogs in Nigeria
MRSA identified in the ward cat of a geriatric unit in
England
MRSA outbreak among horses at veterinary hospital
Methicillin-resistant S. intermedius from European
animals first described
MRSA isolated from leg wound in horse in U.S.
MRSA detected in 11 dogs with wounds, pyoderma, or
surgical procedures (U.S.)
Methicillin-resistant S. intermedius and S. schleiferi
detected in U.S, dogs
MRSA detected in chickens in Korea
LA-MRSA strain, ST398, described in pigs and humans in
Netherlands
MRSA identified in ovine cases of mastitis in Spain
MRSA detected in rabbit and seal in Ireland and rabbit and
avian and rodent companion animals in England
Horse-adapted MRSA strain described from Canadian
horses
MRSA strain ST398 detected in healthy poultry in
Belgium
Multi-drug resistant strain of methicillin-resistant S.
pseudintermedius/intermedius (ST71) reported in animals
(dogs, cats, horses) in Europe and Japan
MRSA strain ST398 reported in a dog in Germany
MRSA strain ST398 reported in veal calves and workers
in Netherlands
MRSA strain ST398 detected in swine and workers in U.S.
MRSA strain ST398 reported in horses in the UK
Reference
(46)
(136)
(197)
(198)
(169)
(79)
(213)
(71;97;104)
(126)
(233)
(72)
(161;176)
(238)
(160;168)
(102;135;18
2;189)
(242)
(73)
(203)
(134)
Dogs and cats. MRSA was first detected in companion animals in Nigeria in 1972. This strain
was similar to human isolates. (136) In 1988, a ward cat in a geriatric rehabilitation unit in
England apparently became colonized after contact with a resident and then served as a reservoir
spreading MRSA to other human residents. (197) MRSA was later detected in dogs with surgical
wounds or skin infections in 1998 (71;213) Surveys generally indicate that prevalence of MRSA
in companion animals is low (<2%) (1;129) and MRSA in companion animals are primarily HA-
MRSA. Epidemiology of MRSA in companion animals was recently reviewed. (136)
Cases of MRSA infection in dogs and cats usually involve lesions in the skin or ears but
invasive infections sometimes occur. Healthy dogs and cats can also carry MRSA
asymptomatically. However, it is suspected that carriage is only transient or intermittent and that
carriage is lost with time and the lack of selective pressure. (237) The use of veterinary drugs and
IV catheters were identified as risk factors for MRSA infections in dogs. (63;143) Many early
ME Doyle, FA Hartmann, ACL Wong
Food Research Institute, UW–Madison, www.fri.wisc.edu/
January 2011
Funded in part by the American Meat Institute Foundation
12reports of companion animals infected with MRSA implicated HA-MRSA originating from
humans but both CA-MRSA (224) and LA-MRSA (242) have caused infections in dogs.
Pets can acquire MRSA from humans and also be a potential reservoir for human MRSA
infection. Similar MRSA strains have been detected in dogs and their owners but surveys of dogs
or humans colonized with MRSA have demonstrated that only a small number of human-dog
pairs are infected with the same MRSA strain. (17;62) HA-MRSA strains have been detected in
therapy dogs and cats visiting human long term care facilities. (33;128) MRSA does not appear
to spread easily from dog to dog. (137)
Other animals. In addition to the companion animals and livestock described above, MRSA has
been detected in a avian pets, including a parrot (178) (176), goats (6), sheep (72), farmed fish
(9), wild rats living on a farm (221), a zoo elephant (92), seals, dolphins and walrus from marine
parks/sanctuaries (61;161), and guinea pig, rabbit, bat, and turtle in a veterinary hospital (234).
Origins of the MRSA were unknown in some cases but appeared to be from human caretakers
for the birds, seal, and elephant calf and from pigs for the farm rats.
MRSA in Foods
MRSA hase been detected in a variety of foods from countries in North America, Europe
and Asia. Foods may be contaminated by human strains of MRSA present in meat processors
and other food handlers. Meat may also be contaminated by MRSA carried in animals as
demonstrated by a study following pigs from lairage through slaughter to commercial pork
products. (153) Another study investigating MRSA on German pigs at slaughter and at several
steps during processing found that 65% of pigs were positive at stunning. However, only 6% of
carcasses on the slaughter line, 4.2% of meat samples during processing and 3% of finished meat
products tested positive. (16)
Some studies detected primarily HA-MRSA strains in foods indicating that humans were
the probable source (81;171;216;239) and others detected primarily LA-MRSA (15;40;229). An
Australian study found that S. aureus isolates (not MRSA) on beef carcasses at an abattoir were
indistinguishable from strains on workers’ hands. It appeared that the workers contaminated the
carcasses during evisceration and processing. (231) However, in the Netherlands, a more recent
study reported that meat handlers were not colonized with MRSA and that the MRSA detected
on meat were LA-MRSA. (41)
Table 5 summarizes results from surveys in several countries for MRSA in raw meats.
There are also reports of low levels of MRSA in chicken meat in Japan and Jordan. (113;172)
Most of this research was aimed at detecting the presence of MRSA and contamination levels
were not quantified. A recent Canadian study found that most positive meat samples contained
<100 cfu/g (239) and a recent Dutch study reported that MPN (most probable numbers) of
MRSA in meat ranged from 0.06 (veal) to >10 (pork) bacteria/g. (41) It should be noted that
sampling and culture methods differed among the studies so that results are not strictly
comparable. Within most studies, incidence of MRSA was less common in poultry than in beef
and pork. (132;139;239)
Since S. aureus is a known cause of mastitis in ruminants, several studies analyzed milk
from cows with mastitis and detected MRSA. (Table 5) Some of these strains also produced
enterotoxins. Pasteurization kills S. aureus so this would be a potential problem only for raw
milk and raw milk products.
ME Doyle, FA Hartmann, ACL Wong
Food Research Institute, UW–Madison, www.fri.wisc.edu/
January 2011
Funded in part by the American Meat Institute Foundation
13MRSA has also been detected in other foods not included in Table 5, for example, goat
milk (49), lamb and mutton (40;172), rabbit and wild boar meat (139), minimally processed
vegetables (200), and fresh fish (175).
Table 5. Reported incidence of MRSA in pork, beef, chicken (c), turkey (t), and raw milk
% positive
Location
Beef
Pork
USA
3.3
5.6
Canada
5.6
9.6
Netherlands 10.6 (beef); 10.7
15.2 (veal)
Netherlands 0
3.1
Germany 33.3%
10.5%
Germany
Spain
Poland
Taiwan
Korea
Korea
9.6*
2.2 (veal)
1.8
0
3.9
4.3-11.3
1
0.3
5
0
* beef and pork
Poultry
Ref.
(171)
1.2
(239)
16.0 (c), 35.3 (t) (40)
20.5 (c)
31.6 (t)
0.7 (c), 0 (t)
0 (t)
0.3-7.8 (c)
0.3 (c)
0
Milk
Location % positive Ref.
Belgium
9.3
(229)
Italy
12.9 (15)
India
1.2
(121)
(227)
(119) Japan
Turkey
1.1
17.2
(192)
(139)
(23)
(132)
(131)
(175) Poland
1.1
U.S. (MN) 5.3
(81)
(216)
(23)
(78)
Methicillin resistance in other species of Staphylococcus
Methicillin resistance in canine S. intermedius isolates was first reported in the mid-late
1990s. (71;169) For several years, these strains appeared to constitute a small proportion of S.
intermedius isolates from animals and, although they exhibited some resistance to other drugs,
there were other antibiotics effective against these bacteria. Early reports of methicillin-resistant
S. intermedius from companion animals were probably isolates of methicillin-resistant S.
pseudintermedius based on the recent changes to Staphylococcus intermedius group taxonomy.
(190)
Starting in 2006, there were more frequent reports of methicillin-resistant S.
pseudintermedius (MRSP) and methicillin-resistant S. intermedius group (MRSIG) strains that
were resistant to multiple classes of antibiotics, in addition to the β-lactam group.
(102;135;183;189) S. pseudintermedius ST71 became established as the most common multidrug
resistant strain in Europe during this time. (182) Increasing prevalence of multidrug resistant
strains was also documented in an examination of clinical samples from dogs in Tennessee
during the period from 2001 to 2005. Methicillin-resistance frequencies in S. intermedius and S.
schleiferi isolates in 2005 were 15.6% and 46.6%, respectively. (97)
Published reports generally indicate a low prevalence of MRSP in dogs and cats. (240)
However, a survey of healthy dogs in Hong Kong indicated a 17% prevalence of methicillin-
resistant S. intermedius (52) and a study at a veterinary hospital reported that 30% of S.
pseudintermedius isolates were methicillin resistant. (189) A recent study of 103 canine
ME Doyle, FA Hartmann, ACL Wong
Food Research Institute, UW–Madison, www.fri.wisc.edu/
January 2011
Funded in part by the American Meat Institute Foundation
14methicillin-resistant S. pseudintermedius isolates from Europe and North America revealed that
there were two major clonal lineages: ST71 in Europe and ST68 in North America. Nearly all
strains were resistant to nine classes of important veterinary antimicrobials. Over 70% of these
isolates contained the SCCmec element II-III. Types III, IV, V, and VII were present in other
strains. (167)
Methicillin resistance has been detected in other staphylococci including S. schleiferi and
S. epidermidis from dogs (104), a human clinical isolate of coagulase-negative S. lugdunensis
(116) and several staphylococcal species on freshwater fish in Greece (3).
MRSP/MRSIG strains are seldom isolated from human food but there is one report of
MRSIG in camel meat in Jordan. (5) Methicillin-susceptible S. intermedius in a butter blend
caused a foodborne outbreak in 1991 (110) indicating that MRSIG is a potential cause of
foodborne staphylococcal intoxication.
Epidemiology of MRSA and MRSP/MRSIG in People
Infections acquired in healthcare facilities
Methicillin-resistant staphylococci first emerged in 1961 in response to the use of
methicillin in hospitals. For most of the next 30 years, many strains of HA-MRSA evolved in
healthcare facilities and certain strains became increasingly prevalent endemic pathogens in
hospitals in Europe and North America as infected or colonized patients shed MRSA into the
surrounding environment and the bacteria were then spread by contaminated equipment and the
hands of healthcare workers. MRSA continued to evolve in, and spread to, healthcare facilities
around the world. By 1991, MRSA accounted for 29% of all clinical bacterial isolates in U.S.
hospitals (166). In the U.S., about 2% of S. aureus infections in intensive care units were MRSA
in 1974. This increased to 22% in 1995 and to 64% in 2004. (117) Data collected by CDC from
463 hospitals in the U.S. in 2006-2007 revealed that S. aureus caused 15% of healthcare-
associated infections, particularly surgical site infections and ventilator-associated pneumonia.
Methicillin-resistance was detected in 56.2% of the S. aureus strains responsible for these
infections. (84) Recently, concentrated efforts to prevent nosocomial transmission of MRSA in
some hospitals appear to be reducing the proportion of S. aureus infections caused by MRSA, for
example, from 52% to 39% over 4 years in one hospital system. (75) Incidence of serious MRSA
infections are also decreasing in U.S. hospitals. (19;103)
MRSA can be transmitted in hospitals by person-to-person contact or, in one outbreak, by
food. But MRSA infections acquired in hospitals are often invasive with serious effects because
the bacteria bypass protective layers of skin and are introduced directly into the body through
needles, tubes, or surgical procedures. Surgical site infections (SSIs) are estimated by CDC to
complicate about 5% of surgeries performed in the U.S. each year, costing the healthcare system
approximately $10 billion. MRSA is increasingly identified as the cause of SSIs and one study
demonstrated that each SSI caused by MRSA results in an average of 23 additional days in the
hospital and costs as much as $60,000. (7;241) Other studies of neonates in intensive care units
(204) and patients with nosocomial pneumonia (162) demonstrated that MRSA infections
increase mortality as well as causing longer hospital stays and much higher costs for care.
Some countries, other than the U.S., conduct nationwide surveys of hospitals to
determine prevalence of MRSA. Results from the 2008 Canadian Ward Surveillance study
(CANWARD) demonstrated that about 27% of S. aureus strains tested were MRSA and 68.8%
ME Doyle, FA Hartmann, ACL Wong
Food Research Institute, UW–Madison, www.fri.wisc.edu/
January 2011
Funded in part by the American Meat Institute Foundation
15of the MRSA isolates were HA-MRSA. (244) A national hospital survey in 2007 in Australia
reported that nearly 33% of S. aureus infections were due to MRSA and, of these, 76% were
HA-MRSA strains and 24% were CA-MRSA strains. (http://www.agargroup.org/surveys)
National data are not available for many other countries and information from individual
hospitals demonstrate a range in the prevalence of MRSA, for example, a 69% prevalence rate in
a tertiary hospital in Nepal (210) and a 45.5% prevalence rate in a community hospital in Japan
(122). It should be noted that data from individual hospitals and different countries are not
always comparable because in some cases all S. aureus infections in all patients are reported
while other studies are restricted to reports on patients in intensive care or surgical wards.
Some European countries, including Denmark, Finland, the Netherlands, Norway and
Sweden, now have a very low prevalence of MRSA infections and less than 3% of clinical S.
aureus isolates are MRSA. These countries have implemented intensive national “search and
destroy” programs that reduce the incidence and transmission of MRSA in hospitals. (24;228)
According to data from 28 European countries compiled by EARS-NET (European
Antimicrobial Resistance Surveillance Network), the proportion of MRSA among total S.
aureus isolates has stabilized or declined in most countries. However the proportion of MRSA
remains >25% in 10 countries. (53)
Although efforts to control MRSA in healthcare settings appear to be achieving success,
some countries with a low prevalence of MRSA, including Iceland and Denmark have seen
recent increases in numbers of MRSA infections as the epidemiology of MRSA changes.
(86;201) Newer LA- and CA-MRSA strains, that originally evolved in human or livestock
outside of healthcare institutions, are increasingly being identified as the cause of infections
acquired in hospitals. (115;123) The CANWARD surveillance studies showed that the
proportions of CA-MRSA among all MRSA isolated in Canadian hospitals increased from 9.1%
in 2005-06 to 19.5% in 2007 and 27.6% in 2008. (244)
Infections acquired in the community
Prior to the 1990s, most cases of MRSA that were acquired outside of healthcare
institutions could be traced to long-term treatment with antibiotics or contact with someone who
had been in a healthcare facility. Strains causing these infections were typical HA-MRSA strains
resistant to multiple classes of antibiotics. With the evolution of CA-MRSA strains and animal-
associated MRSA strains, infections acquired outside of healthcare institutions, in the
community, were caused by a more diverse array of strains of MRSA. A recent comprehensive
review of CA-MRSA describes the emergence of CA-MRSA strains and their virulence,
epidemiology, treatment, and prevention. (39) Only a brief summary of the important aspects of
MRSA epidemiology will be presented here.
Community acquired infections often occur in young, healthy people and cause skin and
soft tissue infections (SSTIs) or pneumonia rather than invasive disease. Data from the 2008
Australian survey noted that the median age of people infected with community associated
strains of MRSA was 35, while the median age for hospital associated cases was 74. Similar age
associations were reported for MRSA infections in Alberta, Canada. (112) Groups of people
living in close quarters, such as children at day care centers, military trainees, family members,
prisoners, and athletes and also persons at a low socio-economic status, such as inner city
residents, Native Americans and other indigenous populations are at higher risk for acquiring
MRSA infections in the community.
ME Doyle, FA Hartmann, ACL Wong
Food Research Institute, UW–Madison, www.fri.wisc.edu/
January 2011
Funded in part by the American Meat Institute Foundation
16There are no national surveillance programs for collecting data on MRSA infections and
colonization in the general population but CDC estimates that, although nearly 50% of people
carry S. aureus in their nasal passages, a much smaller number, approximately 1.5% of the
general population are asymptomatic carriers of MRSA. Nasal colonization with MRSA has
been shown to increase risk for infections by fourfold. (185)
Examples of clusters and outbreaks of MRSA acquired in the community include the
following:
• Over a 5 year period, 3,531 cases of MRSA occurred in service members and recruits
(without recent surgery or hospitalization) at a large army training installation. Over 80% of
infections were caused by CA-MRSA strains. (155)
• An outbreak of MRSA occurred among players on a high school football team who were
living in a school gymnasium during a training camp. Sharing towels, skin injuries, and
higher BMI (body mass index) levels were identified as risk factors. (107)
• Food is not a common vehicle of infection for MRSA. Only one foodborne community
outbreak has been described in Tennessee in 2000. Food involved was contaminated by a
colonized food handler.(98)
In the U.S., CA-MRSA strain USA300 causes the great majority of community acquired
infections while CA-MRSA strains in Europe and Australia are more diverse with multiple
important clones described. Rates of CA-MRSA are also much lower in Europe as compared to
the U.S. (163) USA300 appears to be spreading to other countries, in Asia, Europe, and South
America and to Australia and there is concern that this virulent strain may greatly expand its
range and increase the burden of community acquired MRSA infections worldwide.
Community-acquired MRSA infections have been increasing in developed countries but
they are not as commonly reported in less developed countries which may be a result of fewer
laboratories with the capability of typing MRSA strains. A recent investigation of skin and soft
tissue infections in Cambodian children identified numerous CA-MRSA infections. (28) In
Beijing China, CA-MRSA was found to cause about 4% of SSTIs. (243)
Infections acquired in the community can also come from animals. Animals may be a
reservoir for human infection by MRSA since many different species can carry or have
infections due to MRSA. Recently recognized at-risk human groups include veterinarians,
livestock handlers and pet owners. (39) For example, due to the increased prevalence of MRSA
in some horse populations, horses may serve as a reservoir for acquisition of MRSA by people.
{#57}Typing of isolates of MRSA from veterinary personnel and animals in Ireland detected a
horse-adapted CC8 strain in 23 horses and 12 humans, including 7 people who worked closely
with MRSA-positive horses. (2) In addition, persons in contact with pigs are more susceptible to
acquiring infections due to LA-MRSA. A high prevalence of nasal carriage of LA-MRSA strain,
CC398, was detected in pig slaughterhouse workers in the Netherlands. Working with live pigs
was the most important risk factor but exact transmission routes from animals to humans have
yet to be determined. (220) MRSA can also be transmitted between cows and humans. {#41}
There are also reports of MRSP infections in humans believed to be the result of contact
with pets that were carrying or infected with MRSP. {#684} It may be possible for commensal
methicillin-resistant staphylococci in dogs to serve as a reservoir for transmission of
antimicrobial resistance determinants to susceptible strains of staphylococci in people. {#684}
ME Doyle, FA Hartmann, ACL Wong
Food Research Institute, UW–Madison, www.fri.wisc.edu/
January 2011
Funded in part by the American Meat Institute Foundation
17Routes of infection
Staphylococci are spread among humans and animals and bwtween species either by
direct physical contact or indirectly through clothing, towels, equipment, food, air, or surfaces
contaminated by infected or colonized persons or animals.
Person-person
Hospital outbreaks of MRSA have been traced to lax hygiene practices among health care
workers and MRSA outbreaks in the community often occur in groups of people living in close
quarters where they may transmit MRSA through direct physical contact. MRSA transmission in
a UK hospital was audited by swabbing patients’ skin and their environment and also the hands
of healthcare workers. MRSA was transmitted from a source, most commonly a patient’s skin, to
other patient skin areas, furniture, or note pads by the hands of healthcare workers in 22 of 24
cases. In one case a doctor entering an intensive care unit with MRSA on his/her hands
contaminated a notes trolley near a patient. (140) Another study found that the frequency of
transfer of MRSA from the skin of a colonized patient to a gloved hand was 40%. (207)
A cluster of CA-MRSA cases (strain USA300) in the Netherlands occurred in a
beautician, her customers, family members, and contacts. Skin treatments (waxing) performed by
the beautician were identified as the likely mode of transmission. (88)
Airborne transmission
MRSA is present in the nose and on the skin and is shed into the environment by infected
or colonized people and animals, indicating that airborne transmission is a possible route for
infection. MRSA strains, identical to clinical isolates from patients, were detected in the air of
hospital rooms (68) MRSA was detected in all of 57 samples taken of the air in pig fattening
facilities. MRSA constituted about 0.1% of mesophilic bacteria detected in the air samples. (195)
Animal Contact
LA-MRSA ST398 was first described in pigs in the Netherlands in 2003. (42;233)
Subsequent studies reported detection of this strain among farmers and a survey indicated that
human carriers of ST398 were 12.2-19.7 times more likely to be pig or cattle farmers than to
work at other jobs. (226) While the overall number of MRSA infections in the Netherlands
appears to have stabilized, an increasing percentage of MRSA infections in the country are
caused by this livestock associated strain, even among people without known exposure to pigs or
veal calves. Total MRSA isolates submitted to the national laboratory in the Netherlands in 2008
numbered 2693. Of these 42% were identified as the LA-MRSA ST398 strain as compared to
30% in 2007 and 14% in 2006. Only 29% of people surveyed indicated contact with live pigs or
veal calves. (76) A recent study in Germany found that 86% of farmers and 45% of veterinarians
exposed to pigs with ST398 also carried this strain. However, it was not readily transmitted from
the workers to others as only 4-9% of family members and other close contacts tested positive
for ST398. (38)
Horses may be colonized or infected with an uncommon horse-adapted MRSA strain,
CMRSA-5, and several studies have reported this strain in horse farmers and veterinarians.
(2;238)
Companion animals may also be carriers of MRSA. MRSA was first detected in a
companion animal in a ward cat in a geriatric rehabilitation unit in England. The cat was
ME Doyle, FA Hartmann, ACL Wong
Food Research Institute, UW–Madison, www.fri.wisc.edu/
January 2011
Funded in part by the American Meat Institute Foundation
18apparently infected by a resident and then served as a reservoir spreading the infection to other
human residents. (197) HA-MRSA strains have been detected in therapy dogs and cats visiting
human long term care facilities and may be a souce of infection to residents. (33;128)
Similar MRSA strains have been detected in dogs and their owners but surveys of dogs or
humans colonized with MRSA have demonstrated that only a small number of human-dog pairs
are infected with the same MRSA strain. (17;62) Evidence indicates that pets can acquire MRSA
from humans and that the reverse is also true.
Contaminated equipment and surfaces
Surfaces in both homes (196) and healthcare facilities may harbor MRSA. For example,
MRSA was detected on surfaces in 7 of 25 ambulances tested. (199) Transmission of MRSA in
healthcare facilities can occur by touching contaminated surfaces. Experiments have shown that
gloved hands can pick up MRSA from bedrails, call buttons, tables, and phones at a frequency of
45%. (207) Community-associated MRSA strains on contaminated needles have been
transmitted among illicit drug users. A recent study of persons with MRSA in veterans’ hospitals
revealed that illicit drug users were more likely to be infected with USA300 (CA-MRSA) than
non-drug users. (120) Non-sterile equipment was cited as the cause of CA-MRSA infections in
tattoo recipients in several states. (138)
Numerous reports have also detailed outbreaks in high school and collegiate athletes
where MRSA was detected on equipment and surfaces in athletic facilities as well as on towels
and clothing.(18;21;34;173)
Patients with end stage renal disease (ESRD) are particularly vulnerable to invasive S.
aureus infections because their blood must be treated using dialysis machines at least three times
per week to remove toxins. These patients are frequently hospitalized, receive long courses of
antibiotic treatment, and 14% die annually as a result of infections. Incidence of invasive MRSA
was estimated at 45.2 cases/1000 population among dialysis patients, the highest for any patient
population and about 100 times greater than incidence in the general population. (30)An
increasing proportion of MRSA infections in ESRD patients is due to community-associated
MRSA strains. (96)
Contaminated food
MRSA strains have been detected in meat and may also be present in a variety of other
foods. The origin of these contaminants has been traced to infected/colonized food handlers in
some outbreaks. (98;118) Studies have demonstrated that meat can also become contaminated
during slaughter and processing of animals carrying MRSA. (16;153) In some surveys, MRSA
detected on meat was identified as the livestock-associated strain, ST398. (41)
Significance of MRSA contamination of foods remains uncertain. If meat and other foods
are cooked properly, MRSA cells will be killed. However, as with enterotoxigenic MSSA
strains, under conditions of temperature abuse, MRSA cells could grow in foods, produce heat-
stable enterotoxins, and cause foodborne intoxication. In some individuals whose normal flora
has been depleted by antibiotic treatment, MRSA cells on ready-to-eat foods, including
processed meats, cheeses, and fresh produce, could cause staphylococcal enterocolitis. Finally,
MRSA present on foods could potentially cause skin infections in food handlers. The difficulty
in treating infections caused by pathogens resistant to multiple antibiotics should motivate efforts
to prevent contamination of food with MRSA.
ME Doyle, FA Hartmann, ACL Wong
Food Research Institute, UW–Madison, www.fri.wisc.edu/
January 2011
Funded in part by the American Meat Institute Foundation
19To date, there have been only two reported outbreaks associated with MRSA-
contaminated food. A community outbreak of foodborne illness caused by CA-MRSA occurred
in Tennessee in 2000. (98) Identical MRSA isolates were recovered from 3 ill persons, the
coleslaw they purchased from a convenience store deli, and the nose of a food handler at the
convenience store. This strain produced enterotoxin C. The second reported outbreak of MRSA
occurred in a Dutch hospital and affected 27 patients and 14 health care workers from 1992 to
1993, resulting in five deaths. Epidemiological investigations indicated that a colonized food
handler apparently contaminated food (a peeled banana tested positive for MRSA) served to
hospital patients and some nurses may have inadvertently spread the bacteria to different wards.
(118)
MRSA does not appear to be transferred readily from meat to meat handlers. It was not
detected on hands or in noses of 89 persons working in cold meat processing facilities or
institutional kitchens in the Netherlands even though 14% of samples of meat (veal, pork,
chicken) that they worked with did contain MRSA. Most of the MRSA isolates were identified
as ST398, livestock-associated MRSA. (41)
Other methicillin-resistant staphylococci could potentially cause foodborne intoxication
but no cases have been reported yet. One outbreak in southwestern U.S. in 1991 was traced to
methicillin-susceptible S. intermedius producing type A enterotoxin in a butter blend. (110)
Methicillin-resistant S. intermedius was detected in camel meat in Jordan. (5) MRSIG strains
have been detected in horses but are not usually present in livestock. (240)
The advent of antibiotic-resistant staphylococci poses additional potential food safety
and occupational health concerns. MRSA and MRSIG have been detected in livestock,
companion animals, and wild animals and pose a potential risk to people working with animals.
In addition, the presence of MRSA in food-producing animals and the detection of MRSA in a
small percentage of retail meat samples raises concerns about the potential food-borne
transmission of MRSA.
Control and Prevention
Prevention of staphylococcal infections/intoxication requires strategies to interrupt
various modes of transmission. Essentially these control programs include improvements in
personal hygiene practices among health care workers and food handlers, decontamination of
equipment, surfaces, and clothing, judicious use of antibiotics, proper cooking and storage of
foods, and screening programs
.
Hospital and healthcare programs
Increased morbidity and mortality among hospital patients infected with MRSA has led
to development of some effective control procedures and strict enforcement of MRSA control
policies has been found to decrease rates of MRSA infection in hospitals in 10 European
countries. (77) An important feature of these MRSA-control programs is screening of patients at
admission to ascertain which patients are carriers of MRSA so they can be isolated and treated to
prevent transmission to other patients.
ME Doyle, FA Hartmann, ACL Wong
Food Research Institute, UW–Madison, www.fri.wisc.edu/
January 2011
Funded in part by the American Meat Institute Foundation
20For example, incidence of MRSA in the Netherlands is extremely low (0.7% in 2008) and
this is attributed to effective implementation of the national MRSA guidelines in every
healthcare setting for more than 20 years. These guidelines recommend prudent and restrictive
use of antibiotics and an infection prevention program called “search and destroy.” All patients
and healthcare workers are screened for MRSA and if tests are positive they are isolated and
treated to eliminate MRSA. Policies for cleaning and disinfection are also strictly followed.
(225) A cost-benefit analysis in a Dutch hospital concluded that this program prevented 36 cases
of bacteremia annually and 10 deaths and saved >200,000 euros/yr. (228)
Similar programs have been implemented in other European countries with similar
success in preventing hospital-associated infections. However, there has been discussion
recently regarding the merits of adopting such a strict control program. The “search and destroy”
programs require a lot of resources in testing all patients, keeping them in isolation until test
results come back, and continuing to isolate them if tests are positive. (22) Patients infected with
or carrying MRSA must then be treated to eliminate MRSA. Some have questioned the cost
effectiveness of testing all incoming patients and instead recommend testing only certain patient
populations, such as those entering intensive care units or those scheduled for surgery. Others
recommend strengthening general infection control procedures throughout health care facilities
to reduce all nosocomial infections. Still others point out that because increasing numbers of
MRSA infections are acquired outside of health care settings, an effective MRSA control
program will need to address prevention of infections arising in the community as well methods
to control infections in hospitals.
Another strategy to reduce MRSA in healthcare facilities is the reduction of antibiotic use
to lower selection pressure for MRSA. This may be a useful procedure as a decrease in antibiotic
use in a Taiwanese hospital from 2004 to 2009 was significantly correlated with fewer MRSA
infections in patients. (127)
Sanitizers and surface treatments
Several sanitizers can be used to control methicillin-resistant staphylococci. Use of
alcohol hand rubs has been significantly correlated with decreasing rates of MRSA infections.
(186;205) Chlorhexidine is also an effective antiseptic but some strains of MRSA have
developed resistance to it. (12) Mist application of a mixture of chlorine dioxide and a quaternary
ammonium compound was found to inactivate MRSA on several environmental surfaces. (25)
Nonthermal plasmas were shown to be effective in inactivating both planktonic and biofilm
associated MRSA. (20;99) Swimming pools containing chlorinated water, biguanide-treated
water, or salt water did not permit survival of MRSA. (74)
Certain chemicals added to surface materials exert toxic effects on bacteria. Copper is a
known bacteriocide and copper-based biocide solutions (141) and copper incorporated into
surfaces (235) both effectively killed MRSA. Silver is also bactericidal and a TiO 2 -Ag composite
completely inactivated MRSA within 24 hours. (158) Data comparing bactericidal effects of Cu-
and Ag –containing materials, under different conditions of temperature and humididity, indicate
that Cu may be more effective in indoor environments. (150) A nanocomposite film
incorporating a cell wall degrading enzyme has been developed and found to be effective in
killing MRSA. This may prove useful in hospitals and other areas where infection control is
critical. (165)
ME Doyle, FA Hartmann, ACL Wong
Food Research Institute, UW–Madison, www.fri.wisc.edu/
January 2011
Funded in part by the American Meat Institute Foundation
21Prevention of foodborne intoxication
Preventing staphylococcal intoxication by MRSA strains requires the same precautions as
for MSSA strains. Efforts should be made to prevent contamination throughout the food
production, processing and preparation chain. Workers have been implicated in many outbreaks
of foodborne disease. They may shed bacteria and viruses, even when asymptomatic and several
weeks after they have recovered from an illness. Improved hygiene precautions, consistently
practiced by persons in food preparation and processing would significantly improve safety of
foods. (211) Foods also must be cooked properly and refrigerated or kept hot until consumption.
A recent analysis of growth requirements noted that S. aureus can grow at a water activity of
0.867 and at temperatures as low as 8°C. (218)
Data gaps and research needed
• Characteristics of different methicillin-resistant staphylococci should be compared to common
methicillin-sensitive strains to determine any differences in growth in different foods and
sensitivity to heat, sanitizers and other control methods and why/how certain strains are
adapted for colonization of particular animal species
• More data are needed on prevalence and concentration of MRSA in meats and the MRSA
strains present to determine sources of contamination – human or livestock. Since the ecology
of MRSA is changing, MRSA levels in foods should be monitored over time.
• Studies should determine whether food handlers can acquire MRSA from preparing meat and
other foods containming MRSA.
• Risk factors associated with MRSA and MRSIG infections in animals need to be better
characterized so that animal infections and potential transmission to humans can be better
controlled.
• Animal husbandry practices and slaughtering methods vary in different countries. Research
should determine whether some methods result in greater contamination of meat.
• Some studies in the U.S. and other countries reported that there is e relatively high prevalence
of MRSA on some farms and a lo prevalence or absence or MRSA on other farms. The
reasons for this should be investigated.
• Important transmission pathways are not completely understood, including from animals to
humans, among people in the community, and potential aerosolization and airborne spread.
• Genetic studies of the different SCC and MLST types would provide more information on
important virulence and resistance factors.
• Potential for horizontal transfer of SCCmec among staphylococci is not well understood but
may be an important factor in increasing prevalence of antibiotic resistance.
Summary and Perspective
S. aureus is commonly found in humans with approximately 50% of the population
colonized in the nasal passages or on the skin. A much smaller percentage, about 1.5% of people,
are colonized with MRSA. While many people harboring S. aureus are asymptomatic, they may
ME Doyle, FA Hartmann, ACL Wong
Food Research Institute, UW–Madison, www.fri.wisc.edu/
January 2011
Funded in part by the American Meat Institute Foundation
22pass these bacteria to others directly or contaminate food, clothing, towels, and other surfaces.
Carriage of MRSA increases risk for serious infections that are difficult and more expensive to
treat. Methicillin resistance also occurs in other staphylococci, including S. intermedius and S.
pseudintermedius that colonize and infect pets and other animals.
Enterotoxigenic staphylococci (including MRSA) that grow in foods can cause foodborne
intoxication. Occasionally these staphylococci, when ingested, produce enterotoxins in the
intestines causing enterocolitis in people whose normal flora has been depleted. In hospitals, S.
aureus, including MRSA, cause a large proportion of invasive infections when they enter the
body through surgical wounds, catheters, or other medical devices or procedures. In the
community, staphylococci primarily cause pneumonia and skin and soft tissue infections. Some
MRSA strains are highly virulent and MRSA infections cause significant morbidity and
mortality.
Methicillin resistance was originally reported in hospitals and HA-MRSA strains are
usually resistant to many other antimicrobials besides penicillin-related compounds. CA-MRSA
strains evolved outside of health care facilities and are usually sensitive to most other antibiotics.
Many of these strains have spread globally. Methicillin resistance has also emerged in other
environments where antibiotics are used including veterinary hospitals (MRSP and MRSIG) and
livestock operations (LA-MRSA). Methicillin resistance genes are carried on a mobile genetic
element that can be transferred to other staphylococcal species.
Sources of methicillin resistant staphylococci for human infections include colonized or
infected people, companion animals, and livestock and objects and surfaces contaminated by
them. Staphylococci have been detected in the air indicating that aerosolization of staphylococci
occurs and is potentially a transmission pathway in healthcare facilities and farms with large
numbers of colonized animals. Since MRSA has been detected in retail foods and on animal
carcasses at slaughter, food may also be a source of infection to food handlers or of foodborne
intoxication to consumers. Surveys to date indicate that the prevalence of MRSA in meat is low
and the concentration of bacteria in food samples is also low. In some cases MRSA
contamination of foods appears to result from MRSA present in dairy cows or in animals before
slaughter and in other cases, from human food handlers.
Although MRSA and MRSIG contamination of foods is not currently a significant
problem, these bacteria continue to evolve and spread in the environment. MRSA was originally
isolated in a UK hospital in 1961, community-associated MRSA strains appeared in the early
1990s as did methicillin-resistant S. intermedius (pseudintermedius) in companion animals, and
livestock associated MRSA strains were first described in 2003. Ongoing monitoring of
methicillin-resistant staphylococci in foods and the environment would be prudent.
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