JAC Advance Access published online on September 26, 2008
Journal of Antimicrobial Chemotherapy, doi:10.1093/jac/dkn405
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Review |
Methicillin-resistant Staphylococcus aureus and animals: zoonosis or humanosis?
Department of Medical Microbiology, Royal Devon & Exeter Foundation NHS Trust, Church Lane, Exeter, Devon EX2 5AD, UK
* Tel: +44-1392-402-970; Fax: +44-1392-412-835; E-mail: marina.morgan{at}rdeft.nhs.uk
 |
Abstract |
|---|
Top
Abstract
IntroductionMethicillin-resistant Staphylococcus aureus (MRSA) is increasing worldwide. Occasionally, animals are colonized or infected incidentally with human strains. Recently, however, new strains of MRSA emerging from within the animal kingdom, particularly in pigs, are causing human infection. MRSA has been reported in species as diverse as companion animals, horses and pigs, through to chinchillas, bats and parrots. In contrast, whereas strains of community-associated MRSA, the majority of which carry genes encoding Panton–Valentine leucocidin, are spreading rapidly in human populations, only sporadic cases have been reported in animals to date. Although MRSA has been found in some meat products, the implications for human infection through consumption are unclear. This review examines the epidemiology of MRSA in animals and human attendants/owners, the diagnosis and management of MRSA colonization, infection and infection control strategies in animals.
Key Words: MRSA , Panton–Valentine leucocidin , companion animals , horses , pigs
|
Introduction |
|---|
Methicillin-resistant Staphylococcus aureus (MRSA) is no longer primarily a human healthcare-associated problem, but is now a community-associated problem, especially in the USA, where community-associated MRSA (CA-MRSA) is displacing the older ‘hospital-associated’ MRSA (HA-MRSA) strains.
Methicillin resistance is due to a modified penicillin-binding protein PBP2a, encoded by the mecA gene, located on one of six types of staphylococcal chromosomal cassettes (SCCs), which vary greatly in size. With the exception of isolates of sequence type (ST) 22, SCCs in HA-MRSA strains usually contain additional genetic material, including genes encoding resistance to multiple classes of antimicrobials. The smallest cassette containing a mecA gene, SCCmec type IV, is present in clones of CA-MRSA, which are becoming endemic in many parts of the world.1 While many human CA-MRSA strains have additional genetic material including genes encoding production of Panton–Valentine leucocidin (PVL), these strains are comparatively rare in animals.
Generally, companion animal strains of MRSA differ from those in livestock and meat production animals. This is probably because in companion animals, MRSA acquisition is primarily a humanosis, the strains carried by human owners being passed on to their animals. Traditional animal husbandry involved far less close contact between animals (which were often not housed) than today's intensively farmed livestock intended for human consumption. The newly emerging MRSA strains such as ST398 found among pigs present a genuine zoonotic risk, as their attendants may become colonized or infected with new strains of MRSA.2
|
History of MRSA infection in animals |
|---|
In 1972, MRSA was found in milk from Belgian cows with mastitis.3 However, the MRSA status of the dairymen was not investigated. MRSA has since been reported in many diverse species, including dogs,4–19 cats,10,13,15,18–25 sheep,26 chickens,27 horses,20,28–32 rabbits,15,18,33 seals,10 psittacine birds,15,18 and one turtle, bat, guinea pig and chinchilla.18
Historically, MRSA infections in companion animals involved strains resembling human nosocomial strains, including epidemic MRSA (EMRSA).17 When these epidemic HA-MRSA clones were observed in dogs,9,17,21 the assumption was that the direction of spread had been from man to animals—a ‘humanosis’. However, this situation is changing rapidly, with strains of MRSA that are thought to have evolved in animals colonizing and infecting human attendants.2 Particularly notable are the MRSA strains associated with pigs, which were non-typeable by PFGE using SmaI, but were subsequently found to belong to multilocus ST (MLST) ST398. ST398 is associated with a number of different staphylococcal protein A (spa) types, including t011, t034, t108, t567, t899 and t939.34 The t011 strain is primarily associated with SCCmec IV and IVa, whereas t108 is associated with SCCmec V.2 MLST and spa typing of French and Dutch MRSA strains35 show that ST398 and spa type t108 are now also emerging in the human population, accounting for 20% of the MRSA occurring in humans in the Netherlands.36–38
|
Prevalence of MRSA in the animal kingdom |
|---|
MRSA strains differ in their human/animal affiliation and pathogenic potential. Since most reported animal isolates of MRSA are from clinical infections following failure of empirical therapy,17 there are few epidemiological studies of the prevalence of MRSA in animals. Such sampling bias, inadequate culture methodology and identification methods together with geographical and strain differences may obscure the true carriage rate of MRSA in animals. MRSA was not found in any of 102 dogs screened in one Ontario study,39 whereas another Ontario veterinary school study found only 1/193 dogs to be carriers.40
As in humans, poor skin condition in animals favours staphylococcal carriage. Of cats with inflammatory skin disease examined at the University of Pennsylvania, 58% carried MRSA compared with only 7% of healthy cats.41 Another study found only 3/148 healthy cats to be MRSA-positive.42
In the largest equine study to date, involving 3969 swabs from 2283 Canadian horses, the overall MRSA colonization rate was 2.7%, half the affected horses being colonized nasally.29 Ninety-nine percent of 120 horses colonized with CA-MRSA had the Canadian EMRSA-5 strain (ST8),29 whereas the same authors reported the predominant strain in companion animals to be CA-MRSA-2 (ST5).43
The nosocomial equine MRSA infection rate was 1.8/1000 Canadian admissions29 compared with an incidence of 4.8/1000 among equine admissions to a Viennese hospital.31
Pigs have increasingly been found to be colonized with MRSA in the Netherlands, France and other countries, although not as yet in the UK. In 2005, monthly screening of batches of 10 pigs from each of nine Dutch abattoirs, found 209/540 pigs (38.7%) to be MRSA-positive overall. In 81% of the 54 batches of pigs tested, at least one pig was nasally colonized with MRSA.44 Among pigs in Ontario, the ST5 strain of MRSA predominated. Nasal and rectal swabs of 285 pigs from 20 pig farms resulted in 9/20 farms being identified as having pigs carrying MRSA belonging to spa t539 (the USA100 clone; ST5).45 In another Dutch study, more than 75% of pig-associated strains of MRSA were found on spa sequencing to be t011 and t108, the t011 primarily associated with SCCmec IV and IVa, whereas t108 was associated with SCCmec V.2
|
Risk factors for colonization and infection of animals |
|---|
Risk factors for acquisition of MRSA by animals mirror those for human acquisition, namely living in a household with a colonized human or animal, hospitalization and surgery. Repeated veterinary practice or hospital admissions and usage of antimicrobials such as aminoglycosides29 have all been noted as risk factors. Horizontal spread of MRSA between animals on farms and in veterinary establishments is well recognized,29 particularly larger establishments with more than 20 horses.28
|
MRSA infection in companion animals |
|---|
MRSA infections in animals are predominantly skin and soft tissue infections (especially post-surgical). During 1 year in the UK, 1.5% (95/6519) of the clinical samples from infected animals yielded MRSA. These comprised 69 dogs, 24 cats, 1 horse and 1 rabbit.33 The following year, the same authors reported that of 31 randomly selected MRSA strains, 29 (94%) were indistinguishable from UK EMRSA.17 The incidence of MRSA infection in a small animal hospital in Berlin was 1.85/1000 admissions.18 MRSA-infected rabbits are uncommon,10,30,46 although one rabbit carrying a PVL-producing MRSA strain has been reported.15
In an Irish veterinary hospital, more than half of their 25 MRSA animal isolates were of canine origin, with eight horses, one cat, one rabbit and one seal also infected.10 Whether dogs are more susceptible to carrying certain strains is unclear, but there was a predominance of MRSA infection among dogs. In a UK study, nearly three times as many dogs as cats were actually infected with MRSA.33
Perhaps unsurprisingly, MRSA presence is often associated with veterinary surgery. In one report, four dogs suffered post-operative infections following facture repairs after road traffic accidents and one developed infection after a routine posterior cruciate ligament repair. Four of the five recovered after removal of implants and appropriate antimicrobial therapy,12 suggesting that as with human prosthetic infections, removal of the prosthesis is usually necessary for cure.
|
MRSA infection in horses |
|---|
Skin and soft tissue MRSA infections,20 bacteraemia, septic arthritis,29,31 osteomyelitis,31 implant-related infections, metritis,47 omphalitis,4,28 catheter-related infections and pneumonia29 have all been reported in horses. The first outbreak of MRSA infection in horses was noted in 1993, with 11 horses infected post-operatively in a veterinary teaching hospital in Michigan.20 Subsequent outbreaks occurred in Japan,47 Austria,32 the UK,4 Ireland,10 the USA and Canada.29 This latter outbreak involved 14 clinical infections, including 4 cases of septic arthritis, 3 intravenous (jugular) line infections, 2 pneumonias and a mastitis.29
Some MRSA strains, e.g. CA-MRSA-5 (ST8), appear adapted to equine colonization28 and are often gentamicin- and tetracycline-resistant. The most prevalent global isolate is the USA500 strain, although MRSA ST254 was responsible for infection in four horses in an Austrian veterinary school.31
|
MRSA infection in cattle |
|---|
S. aureus causes mastitis in milking herds, and occasionally purulent dermatitis in their milkers.48 Since the first report of MRSA in cattle in 1972,3 cows with mastitis seem the most likely to harbour MRSA. This may be due to horizontal transfer of MRSA via the wet hands of colonized or infected milkmen, and selection by the use of antibiotics to treat mastitis. Recently, none of the 1043 milk and udder swabs from dairy farms in NW England were positive for MRSA,49 yet 9/12 MRSA samples from mastitic Korean cows were positive in 2002.50 The only report of PVL-positive MRSA in cattle to date is from Korea.11
|
MRSA infection in pigs |
|---|
During an outbreak of ‘exudative epidermitis’ (a disease normally due to Staphylococcus hyicus) afflicting Dutch pigs, following unsuccessful therapy with cephalosporins, tylosin and co-trimoxazole, MRSA was found to be the causative organism. All isolates were spa type t011, ST398. S. hyicus exudative epidermitis disease has a mortality of 20%, but the MRSA-infected piglets were successfully treated with enrofloxacin.51
|
MRSA contamination of meat products |
|---|
Of the 540 pigs sampled in Dutch abattoirs in 2005–06, 209 pigs (39%) were MRSA-positive.44 Whether such MRSA pose a risk to human health is being investigated. The MRSA isolated from 6/717 samples of meat from sheep sampled in Jordan was felt to be due to human contamination.26 Contamination of chicken with MRSA was uncommon. In the Far East, only 2/119 Korean chicken joints were positive50 compared with 2/293 samples (1%) in Japan,27 where in both cases the MRSA attributed to contamination from humans during processing.27 However, a recent survey of foodstuffs by the VWA (Voedsel en Waren Autoiteit) in Holland found many samples contaminated with MRSA. Of the 1300 samples of different meats examined at commercial outlets, 31% of turkey, 27% of chicken, 17% of veal, 10% of pork and beef and 6% of lamb samples were contaminated with MRSA. The majority (84%) of the MRSA isolates were non-typeable MRSA. In view of the low numbers of non-typeable MRSA in patients, the authors concluded ‘foodstuffs play a negligible role, if any, in the spread of MRSA’.52
|
PVL-producing MRSA strains in animals |
|---|
CA-MRSA, containing SCCmec IV, and genes encoding for PVL (a toxin that attacks white blood cells) are increasingly implicated in recurrent skin sepsis and fatal necrotizing pneumonia in humans.53,54 However, CA-MRSA producing PVL are rarely reported in animals8 and then usually in companion animals. PVL-producing CA-MRSA have occurred in cats, dogs, rabbits, birds,15 bats, turtles, pigs18,36 and cattle.11 The majority of the new, rapidly spreading pig-associated strains reported to date are PVL-negative.
|
Transmission between companion animals and companion humans/owners |
|---|
Like their companion animals, companion humans are more often colonized than infected, providing a reservoir for reinfection of their loved ones, human and animal.5,6,8 Human skin scales with MRSA are easily shed from leg ulcers, eczematous skin and pressure areas during the activities of daily living. Undetected colonized animals provide a reservoir for continuing relapsing infection in humans.6,16,24,25
Intra-hospital MRSA transmission was reported in a UK care of the elderly ward. Three patients were found to be colonized or infected with MRSA. Screening of staff and the resident cat (which often slept on patients' pillows) revealed five nurses, the physiotherapist and the cat to be carriers. The other animal regularly visiting the ward was the physiotherapist's dog, which was proven to be MRSA-negative.25 The cat, which carried MRSA on paws and back fur, was presumed to have acquired MRSA from skin scales shed from the pressure sore of a heavily colonized patient. MRSA acquisition by staff was assumed to be due to their poor hygiene and lack of hand washing after stroking the cat.25
Although the animal equivalent of a ‘cloud shedder’, a heavily colonized human liberally shedding organisms, has not been reported, the high MRSA loads associated with pyoderma and draining wounds must be a significant risk for acquisition and transmission. American cats with inflammatory skin disease were associated with a far higher incidence of MRSA (58%) than healthy cats (7%) in one study.41
Transmission of PVL-producing S. aureus between humans and dogs was reported in a family where a diabetic lady, her husband, son and dog were all colonized.8
|
Transmission of MRSA between livestock and owners/attendants |
|---|
Close human contact with animals provides more opportunity for transmission between the species. Once acquired, further horizontal transmission of MRSA between animals or humans and their families can occur. Transmission of MRSA was reported between Hungarian cows with sub-clinical mastitis and an agricultural worker who was throat swab-positive.55 In 2004, a Dutch pig farmer's wife developed MRSA mastitis and pleural effusion. Although successfully treated with teicoplanin, eradication therapy failed, and subsequent screening found her husband and daughter to be MRSA carriers. Six months later, with the baby and parents still colonized, wider sampling revealed that 3 co-workers and 10 pigs from the closest holding were carriers of the PFGE non-typeable MRSA, all of which were identical (spa types t108, ST398, SCCmec V).38 With pig strains difficult to type with PFGE, spa typing enabled differentiation of another outbreak involving spa t108, confirming that transmission had occurred between pig farming families, a nurse, a hospital inpatient and between pigs and humans.36
MRSA ST398 particularly seems to be associated with pig farming, reported in Holland and Hanover,2 Singapore,56 Canada57 and France.35 New strains (STs 432–438, ST440 and ST457) have been recognized during the investigation of pig-related outbreaks.35 Currently, MRSA from pig and cattle reservoirs are responsible for 20% of all human MRSA in the Netherlands.37
|
MRSA carriage by veterinary and medical personnel |
|---|
Whereas the nasal carriage rate of MRSA among medical staff attending a conference was 0.3%,58 the baseline nasal carriage rate in vets is much higher. A study of veterinary personnel and students at a livestock conference in the Netherlands found 4.6% to be nasal carriers,59 compared with a rate of 6.5% at an American international conference.60 In the latter study (which sampled 417 attendees), 16% of the nasal carriers (15 of 96) were large animal vets, whereas only 4.4% (12 of 271) of those working with small animals were positive. None of the research personnel carried MRSA.60 A far higher proportion (14/78, 17.9%) of veterinary staff in a small animal referral hospital in the UK carried MRSA,9 most strains indistinguishable from EMRSA-15 (ST22).
The nasal carriage rates of MRSA among veterinary personnel working with pigs are high.58,60 Of the 272 attendees at an international pig conference in Denmark, 34 (12.5%) participants from nine countries were carriers, 31 isolates belonging to spa t011, t108, t571, t567 or t899 corresponding to ST398.60 A questionnaire survey of attendees showed that contact with cattle, country of origin and wearing masks did not influence the rate of colonization.61
In an investigation in Northern England, where 11 of 67 horses (16%) were MRSA-positive, including 3 clinical infections, no veterinary staff screened positive.4 However, prolonged close contact with a heavily colonized foal in intensive care led to three students being infected, and a further 10% (10/103) of the associated personnel colonized with CA-MRSA (ST8).32 In Ireland, following identification of MRSA in animals (47/133 S. aureus isolates), MRSA was isolated from 10 attendant veterinary personnel from four different practices and the veterinary hospital.10 In Michigan, during an outbreak investigation where only 5 of 20 personnel consented to MRSA screening, 3 were positive.20
|
MRSA carriage among agricultural personnel |
|---|
In a study comparing carriage rates of staphylococci among 113 farmers and 113 non-pig farmers, 10% (5/50) of the farmers carrying staphylococci were carrying MRSA. However, with such small numbers, the results were not felt to be statistically significant.62 In a French study of nasal swabs from 44 farmers and 21 controls, 19 strains of S. aureus were present. These included six isolates of ST398 of which only one was methicillin-resistant.35 AFLP analysis of 20 ST398 strains from the nares of slaughterhouse pigs plus 18 strains from hospital inpatient farmer screens and 8 isolates from a veterinary diagnostic centre revealed the highly clonal nature of these pig related strains.3
Agricultural workers and their families involved with pig, and (to a far lesser extent) cattle, farming have a high likelihood of MRSA colonization, with up to 23% Dutch pig farmers being nasal carriers of MRSA;36 hence, with the incidence of MRSA carriage in pig farmers estimated at 760 times that of the normal population,36 all individuals working with pigs in the Netherlands are now routinely isolated and MRSA screened on entering hospital.
|
Pitfalls in detection of MRSA in animals |
|---|
Lack of standardization regarding culture methodology, susceptibility testing, genetic profiling and sampling methods often make meaningful comparisons of reported studies difficult. Mass animal screening is logistically difficult and expensive, and hitherto felt to be largely impracticable. Where screening has been done, combinations of nasal, perineal and throat or wound swabs were taken.19
It can be physically difficult to screen animals properly. In an MRSA outbreak involving a hospital cat, ‘nose swabs were not possible without suitable restraint’, so only paw and fur swabs were taken.25
Direct culture of dry swabs of skin or hair may yield less staphylococci than enrichment cultures of pre-moistened swabs. Cutting the animal hair and then culturing the scalpel blades after gently scraping the skin have been advocated as a method for culturing MRSA carriage in cats.42
The conventional typing methodology for newer animal strains has had to be adapted, since some pig-associated MRSA are not typeable by PFGE. When spa typing, involving the X region of the protein A gene, is used, the majority of such ‘non-typeable’ pig strains are spa t011 or t108, ST398.2
Animals may be only transiently colonized with MRSA7 or harbour several types of coagulase-positive staphylococci. Animal-associated species of staphylococci that may be confused with MRSA include Staphylococcus intermedius, which has been particularly associated with canine pyoderma, Staphylococcus schlieferi, S. hyicus, Staphylococcus delphini and Staphylococcus pseudointermedius.63 S. intermedius derived its name from possessing phenotypic properties of both. S. aureus and Staphylococcus epidermidis.64 S. intermedius has been reportedly isolated from dogs, cats, mink, pigeons and foxes and is estimated to cause >90% of coagulase-positive staphylococcal animal infections.16 Interestingly, owners of infected dogs are reportedly seven times more likely to carry S. intermedius than non-dog owners.65
An additional complicating factor is the emergence of S. pseudointermedius, which phenotypically resembles S. intermedius and S. delphini. S. pseudointermedius cannot be distinguished from S. intermedius using commercial identification kits and colonizes veterinary staff.64 Early reports of S. intermedius and canine pyoderma should be interpreted with caution, as there is some confusion regarding the terminology and differentiation of S. intermedius and S. pseudointermedius. It has been suggested that many of the S. intermedius isolates reported from dogs and cats may have actually been S. pseudointermedius66 and that true S. intermedius is more likely to be found in wild pigeons.67 One investigation of methicillin-resistant staphylococci isolated from dogs found methicillin-resistant S. pseudointermedius in four dogs and MRSA only in one.40
|
Management of MRSA in animals |
|---|
Infection control and prevention of acquisition of MRSA
Common sense, good hygiene and education are key, especially in veterinary practices. Environmental contamination with MRSA acts as a reservoir for infection. Ten percent of the environmental swabs in a veterinary hospital yielded MRSA, including doorknobs and a board marker—all ‘touch sites’ where hand contact would be expected.9
Ninety-seven percent of the Canadian hospitals allowed dogs to visit patients, some animals having unrestricted access to all wards. Thirty-two (36%) owners were lamentably ignorant of infection control practices and possible zoonotic infections with 20% not practising hand hygiene and 40% unable to name one zoonotic disease.39
Known MRSA-positive animals should be nursed apart from other animals, with strict hand washing and gloves and gowns if in close contact. It seems sensible to adopt the human infection control precautions of seeing known MRSA-positive patients last in the clinic, then cleaning the room thoroughly and thus avoiding any unnecessary exposure of the animal to other animals in the waiting room.
The importance of applying infection control precautions as routine was highlighted in an outbreak relating to students nursing a sick foal in intensive care. After the foal was found to be MRSA-positive, despite introduction of barrier precautions, three personnel developed skin sepsis, impetigo or folliculitis.33 One of the students suffered with pre-existing eczema. All humans were treated successfully.
Treatment of MRSA infection in animals
Treatment options may be limited for the more resistant human EMRSA strains. Equine strains are likely to be gentamicin-resistant.4,29 High-level mupirocin resistance43 and variable levels of erythromycin, fluoroquinolone and inducible clindamycin resistance have been reported. It is essential to ensure that apparently clindamycin-susceptible strains are tested for inducible clindamycin resistance since nearly 72% of the strains proved clindamycin-resistant on D testing.68
Occasionally, antimicrobials less commonly used in human medicine may be useful. A horse in Wisconsin with an osteitis and draining sinus due to mixed organisms, including MRSA, was discharged only after 2 weeks of oral chloramphenicol, although the long-term outcome was not reported.30
MRSA decolonization of animals and owners
The natural history of MRSA colonization in the different animal species is largely unknown. Close liaison between vets and physicians is essential to coordinate swabbing and decolonization, particularly if simultaneous animal and human decolonization is to be attempted. No controlled trials have been performed, but case reports suggest that decolonization of animals is possible.5,6,16 Clinically infected animals are often treated with co-trimoxazole and may be decolonized with topical decolonization lotions similar to those used in humans.
Failure to eradicate MRSA carriage from humans may be due to reacquisition of the strains from close human or animal contacts. Hence, the possibility of an animal reservoir should be considered, and if proven, decolonization of all carriers was considered.
Decolonization of a husband and wife team of intensive care nurses and their dog with triclosan and nasal mupirocin finally resulted in clearance.5 A 48 year old male diabetic, responding to intravenous vancomycin for an MRSA stump cellulitis, remained MRSA-positive after decolonization. When his wife, a renal transplantee, developed MRSA cellulitis, further screening revealed the dog to be colonized with MRSA too. Both wife and the dog were decolonized, and the couple was advised to avoid intimate contact with the dog. However, having failed to decolonize the dog, a second bout of decolonization of the trio was undertaken. Despite this, the husband developed another stump infection, necessitating a third and successful bout of decolonization of the whole family.6 Interestingly, this study reported the use of topical vancomycin cream intra-nasally as the isolate was mupirocin-resistant. Worries about encouraging resistance have led the Scandinavians to ban mupirocin in animals, and nowadays, topical antibiotics are usually recommended only as a last resort.
MRSA clearance of patients and their animals was successfully carried out using oral antimicrobials in two different settings, in the first family using rifampicin and ciprofloxacin,16 and in the second family group, using rifampicin and clarithromycin.8
Decolonization of people colonized with pig-associated strains can be difficult, and repeatedly unsuccessful.36 Repeated efforts at eradication of a PVL-associated strain of MRSA from a husband, wife, son and dog necessitated resorting to the usage of ciprofloxacin and rifampicin.8 When a 31 year old nurse with MRSA and psoriasis failed decolonization, she was treated with oral doxycycline and rifampicin, and repeated topical decolonization. Her dog and daughter proved to be reservoirs, although interestingly, the grandmother—also a psoriatic—remained free of MRSA, despite considerable childcare exposure. Finally, only after both mother and dog received oral rifampicin and clarithromycin was the strain eradicated.16
Decolonization of companion animals
For transient MRSA carriage, such as that resulting from hospital visits of pet therapy dogs, washing the dogs' paws with chlorhexidine may suffice.7 Topical decolonization of furry felines is especially difficult, and ingestion of disinfectants may be harmful to them. Hence, if attempted, animals should be rinsed thoroughly afterwards. In the geriatric ward outbreak, and with the offending cat reluctant even to be swabbed, no attempt at decolonization was made. The cat was simply removed.25
Official detailed guidance for management of MRSA in animals and the potential for decolonization is available from the British Small Animals Veterinary Association (BSAVA) web site.69 Guidelines advocate decolonization only ‘if the human companion is immunosuppressed or otherwise vulnerable’ but suggested that regimens include antibacterial shampoos and 2% fusidic acid or 2% mupirocin intranasal cream two to three times daily.69
Decolonization of large animals
Topical chlorhexidine/1% acetic acid has been used to decolonize horses with systemic and incisional infections. However, overall, the efficacy of topical antimicrobials for decolonization is unclear,28 as sometimes instigating screening and good infection control standards alone may result in disappearance of carriage.70 The efficacy of any decolonization is more effective when re-exposure to MRSA is prevented.28,70
|
Discussion |
|---|
MRSA is now increasingly recognized in the animal world. New types of MRSA appear to be evolving in animals. These pose a potential threat to human health through occupational exposure and ease of spread during the increased international movement of livestock and agricultural personnel. Asymptomatic colonization and shedding of MRSA by veterinary and agricultural personnel, together with selection pressures due to antimicrobial feed additives and injudicious usage of antibiotics may contribute to the establishment of MRSA in the food chain and domestic animals. The true scale of the problem is unknown, and more surveillance studies, particularly of animal products in the food chain, are in progress. However, there is no substitute for good hygiene practices, both in the household and in human and animal healthcare environments. A history of contact with animal or human MRSA, and early culture of wounds not responding to first-line therapy would enable earlier recognition of MRSA and appropriate management. When faced with repeated and inexplicable failures of decolonization in humans, a history of close exposure to animals and birds should be sought. Where sharing of MRSA between species is suspected, a combined diagnostic and therapeutic approach with veterinary colleagues is advised.
|
Transparency declarations |
|---|
I declare that I have no financial conflicts of interest, and I have not been funded in any way to prepare this article.
|
References |
|---|
1 . Kollef MH, Micek ST. Methicillin-resistant Staphylococcus aureus: a new community-acquired pathogen? Curr Opin Infect Dis (2006) 19:61–8.
2 . Van Belkum A, Melles DC, Peeters JK, et al. Methicillin-resistant and -susceptible Staphylococcus aureus sequence type 398 in pigs and humans. Emerg Infect Dis (2008) 14:479–83.[Web of Science][Medline]
3 . Devriese LA, Homes J. Epidemiology of methicillin-resistant Staphylococcus aureus (MRSA) in dairy herds. Res Vet Sci (1975) 19:23–7.[Web of Science][Medline]
4 . Baptiste KE, Williams K, Williams NJ, et al. Methicillin-resistant staphylococci in companion animals. Emerg Infect Dis (2005) 11:1942–4.[Web of Science][Medline]
5 . Cefai C, Ashurst AS, Owens C. Human carriage of methicillin-resistant Staphylococcus aureus linked with a pet dog. Lancet (1994) 344:539–40.[Web of Science][Medline]
6 . Manian FA. Asymptomatic nasal carriage of mupirocin resistant methicillin-resistant Staphylococcus aureus (MRSA) in a pet dog associated with MRSA infection in household contacts. Clin Infect Dis (2003) 36:e26–e28.[CrossRef][Web of Science][Medline]
7 . Enoch DA, Karas JA, Slater JD, et al. MRSA carriage in a pet therapy dog. J Hosp Infect (2004) 60:186–8.[Web of Science]
8
.
Van Duijkeren E, Wolfhagen MJ, Heck MEOC, et al. Transmission of a Panton–Valentine leucocidin positive methicillin-resistant Staphylococcus aureus strain between humans and a dog. J Clin Microbiol (2005) 43:6209–11.
9
.
Loeffler A, Boag AK, Sung J, et al. Prevalence of methicillin-resistant Staphylococcus aureus among staff and pets in a small animal referral hospital in the UK. J Antimicrob Chemother (2005) 56:692–7.
10 . O'Mahony R, Abbott Y, Leonard FC, et al. Methicillin-resistant Staphylococcus aureus (MRSA) isolated from animals and veterinary personnel in Ireland. Vet Microbiol (2005) 109:285–96.[CrossRef][Web of Science][Medline]
11
.
Kwon NH, Park KT, Moon JS, et al. Staphylococcal cassette chromosome mec (SCCmec) characterization and molecular analysis for methicillin-resistant Staphylococcus aureus and novel SCCmec subtype IVg isolated from bovine milk in Korea. J Antimicrob Chemother (2005) 56:624–32.
12 . Leonard FC, Abbott T, Rossney A, et al. Methicillin-resistant Staphylococcus aureus isolated from a veterinary surgeon and five dogs in one practice. Vet Rec (2005) 158:155–9.[Web of Science]
13
.
Moodley A, Stegger M, Bagcigil AF, et al. spa typing of methicillin-resistant Staphylococcus aureus isolated from domestic animals and veterinary staff in the UK and Ireland. J Antimicrob Chemother (2006) 58:1118–23.
14 . Pak SI, Han HR, Shimizu A. Characterisation of methicillin-resistant Staphylococcus aureus isolated from dogs in Korea. J Vet Med Sci (1999) 61:1013–8.[CrossRef][Web of Science][Medline]
15 . Rankin S, Roberts S, O'Shea K, et al. Panton–Valentine leukocidin (PVL) toxin positive MRSA strains isolated from companion animals. Vet Microbiol (2005) 108:145–8.[CrossRef][Web of Science][Medline]
16 . Van Duijkeren E, Box ETA, Heck ME, et al. Methicillin-resistant staphylococci isolated from animals. Vet Microbiol (2004) 103:91–7.[CrossRef][Web of Science][Medline]
17 . Rich M, Roberts L, Kearns AM. Methicillin-resistant Staphylococcus aureus isolates from companion animals. Vet Microbiol (2005) 105:313–4.[CrossRef][Web of Science][Medline]
18 . Walther B, Wieler LH, Friedrich AW, et al. Methicillin-resistant Staphylococcus aureus (MRSA) isolated from small and exotic animals at a university hospital during routine microbiological examinations. Vet Microbiol (2008) 127:171–8.[CrossRef][Web of Science][Medline]
19
.
Weese JS. Methicillin-resistant Staphylococcus aureus; an emerging pathogen in small animals. J Am Anim Hosp Assoc (2005) 41:150–7.
20
.
Seguin JC, Walker RD, Caron JP, et al. Methicillin-resistant Staphylococcus aureus outbreak in a veterinary teaching hospital: potential human-to-animal transmission. J Clin Microbiol (1999) 37:1459–63.
21 . Morris D, Rook KS, Shofer FS, et al. Screening of Staphylococcus aureus, Staphylococcus intermedius and Staphylococcus schlieferi isolates obtained from small companion animals for antimicrobial resistance: a retrospective review of 749 isolates (2003–4). Vet Derm (2006) 5:332–7.
22
.
Strommenger BC, Kehrenberg C, Kettlitz C, et al. Molecular characterisation of methicillin-resistant Staphylococcus aureus from pet animals and their relationship to human isolates. J Antimicrob Chemother (2006) 57:461–5.
23 . Vitale CB, Gross TL, Weese JS. Methicillin-resistant Staphylococcus aureus in cat and owner. Emerg Infect Dis (2006) 12:1998–2000.[Web of Science][Medline]
24
.
Sing A, Tuschak C, Hormansdorfer S. Methicillin resistant Staphylococcus aureus in a family and its pet cat. New Eng J Med (2008) 358:1200–1.
25 . Scott GM, Thomson R, Malone J, et al. Cross-infection between animals and man: possible feline transmission of Staphylococcus aureus infection in humans? J Hosp Infect (1998) 12:29–34.
26 . Qudduomi SS, Bdour SM, Mahasneh SM. Isolation and characterisation of methicillin-resistant Staphylococcus aureus from livestock and poultry meat. Ann Microbiol (2006) 56:155–61.
27 . Kitai S, Shimuzu A, Kawano KJ. Characterisation of methicillin-resistant Staphylococcus aureus isolated from retail raw chicken meat in Japan. J Vet Med Sci (2005) 67:107–10.[CrossRef][Web of Science][Medline]
28 . Weese JS, Rousseau J, Traub-Dargatz JL, et al. Community-associated methicillin-resistant Staphylococcus aureus in horses and humans who work with horses. J Am Vet Med Assoc (2005) 226:580–3.[CrossRef][Web of Science][Medline]
29 . Weese JS, Rousseau J, Willey BM, et al. Methicillin-resistant Staphylococcus aureus in horses at a veterinary teaching hospital: frequency, characterisation and association with clinical disease. J Vet Intern Med (2006) 20:182–6.[CrossRef][Web of Science][Medline]
30 . Hartmann MS, Trostle SS, Klohnen AA. Isolation of methicillin-resistant Staphylococcus aureus from a post-operative wound infection in a horse. J Am Vet Assoc (1997) 211:590–2.
31 . Cuny C, Kuermmerle J, Stanek C, et al. Emergence of MRSA infections in horses in a veterinary hospital: strain characterisation and comparison with MRSA from humans. Euro Surveill (2006) 11:44–7.[Medline]
32 . Weese JS, Caldwell F, Willey BM, et al. An outbreak of methicillin-resistant Staphylococcus aureus skin infections resulting from horse to human transmission in a veterinary hospital. Vet Microbiol (2006) 114:160–4.[CrossRef][Web of Science][Medline]
33 . Rich M, Roberts L. Methicillin-resistant Staphylococcus aureus isolates from companion animals. Vet Rec (2004) 154:310.[Web of Science][Medline]
34 . Van Duijkeren E, Ikawaty R, Broekhuizen-Stins MJ, et al. Transmission of methicillin-resistant Staphylococcus aureus strains between different kinds of pig farms. Vet Microbiol (2007) 126:383–9.[CrossRef][Web of Science][Medline]
35 . Armand-Lefevre L, Ruimy R, Andremont A. Clonal comparison of Staphylococcus aureus isolates from healthy pig farmers, human controls and pigs. Emerg Infect Dis (2005) 11:711–4.[Web of Science][Medline]
36 . Voss A, Loeffen F, Bakker C, et al. Methicillin-resistant Staphylococcus aureus in pig farming. Emerg Infect Dis (2005) 11:1965–6.[Web of Science][Medline]
37 . Van Loo IHM, Huijsdens X, Tiemersma E, et al. Emergence of methicillin-resistant Staphylococcus aureus of animal origin in humans. Emerg Infect Dis (2007) 13:1834–8.[Web of Science][Medline]
38 . Huijsdens XW, van Dijke BJ, Spalburg E, et al. Community acquired MRSA and pig-farming. Ann Clin Microbiol Antimicrob (2006) 5:26.[CrossRef][Medline]
39 . Lefebre SL, Waltner-Toews D, Peregrine A, et al. Characteristics of programs involving canine visitation of hospitalised people in Ontario. Infect Control Epidemiol (2006) 27:754–8.[CrossRef]
40 . Hanselman BA, Kruth SA, Weese J. Methicillin-resistant staphylococcal colonization in dogs entering a veterinary hospital. Vet Microbiol (2007) 126:277–81.[Web of Science][Medline]
41 . Abraham JL, Morris DO, Griffeth GC, et al. Surveillance of healthy cat and cats with inflammatory skin disease for colonization of the skin by methicillin-resistant coagulase-positive staphylococci and Staphylococcus schlieferi ssp. schlieferi. Vet Dermatol (2007) 18:252–9.[CrossRef][Web of Science][Medline]
42 . Lilenbaum W, Nunes EL, Azeredo MAI. Prevalence and antimicrobial susceptibility of staphylococci isolated from the skin surface of clinically normal cats. Lett Appl Microbiol (1998) 27:224–8.[CrossRef][Web of Science][Medline]
43 . Weese JS, Dick H, Willey BM, et al. Suspected transmission of methicillin-resistant Staphylococcus aureus between domestic pets and humans in veterinary clinics and in the household. Vet Microbiol (2006) 115:148–55.[CrossRef][Web of Science][Medline]
44 . De Neeling AJ, van den Broek MJM, Spalurg ED, et al. High percentage of methicillin-resistant Staphylococcus aureus in pigs. Vet Microbiol (2007) 122:366–72.[CrossRef][Web of Science][Medline]
45 . Khanna T, Friendship R, Dewey C, et al. Methicillin-resistant Staphylococcus aureus colonisation in pigs and pig farmers. Vet Microbiol (2008) 128:298–303.[Web of Science][Medline]
46 . Rodriguez-Calleja JM, Garcia-Lopez I, Santos J, et al. Molecular and phenotypic isolates of Staphylococcus aureus from rabbit meat. Res Microbiol (2006) 157:496–502.[Medline]
47 . Anzai T, Kamada M, Kanemaru T, et al. Isolation of methicillin-resistant Staphylococcus aureus (MRSA) from mares with metritis and its zooepidemiology. J Equine Sci (1996) 7:7–11.[CrossRef]
48 . Grinberg A, Hittman A, Leyland M, et al. Epidemiological and molecular evidence of a monophyletic infection with Staphylococcus aureus causing a purulent dermatitis in a dairy farmer and multiple cases of mastitis in his cows. Epidemiol Infect (2004) 132:507–13.[CrossRef][Medline]
49 . Kemp R, O'Connor R, Cabell EJ, et al. Dairy cows—a possible source of methicillin-resistant staphylococcus spp? In: Programme and Abstracts of the First international Conference on MRSA in Animals, Liverpool, University of Liverpool, 2006. 35. Poster 16.
50
.
Lee JH. Methicillin (oxacillin)-resistant Staphylococcus aureus strains isolated from major food animals and their potential transmission to humans. Appl Environ Microbiol (2003) 69:6489–94.
51 . Van Duijkeren E, Jansen MD, Flemming SC, et al. Methicillin-resistant Staphylococcus aureus in pigs with exudative epidermitis. Emerg Infect Dis (2007) 13:1408–10.[Web of Science][Medline]
52 . MRSA bacteria on meat. 05 Maart 2008 – nieuwsbericht. http://www.vwa.nl/portal/page?_dad=portal&pageid=119,1639824&_schema=PORTAL&p_news_item_id=23121(11 September 2008, date last accessed).
53
.
Issartel B, Tristan A, Lechevallier S, et al. Frequent carriage of Panton–Valentine leucocidin genes by Staphylococcus aureus isolates from surgically drained abscesses. J Clin Microbiol (2005) 43:3203–7.
54 . Gillet Y, Issartel B, Vanhems P, et al. Association between Staphylococcus aureus strains carrying gene for Panton–Valentine leukocidin and highly lethal necrotising pneumonia in young immunocompetent patients. Lancet (2002) 359:753–9.[CrossRef][Web of Science][Medline]
55 . Juhasz-Kaszanyitzky E, Janosi S, Somogyi P, et al. MRSA transmission between cows and humans. Emerg Infect Dis (2007) 13:630–1.[Web of Science][Medline]
56 . Witte W, Strommenger B, Stanek C, et al. Methicillin-resistant Staphylococcus aureus ST398 in humans and animals, central Europe. Emerg Infect Dis (2007) 13:255–8.[Web of Science][Medline]
57 . Wulf M, Voss A. MRSA in livestock animals—an epidemic waiting to happen? Clin Microbiol Infect (2008) 14:519–21.[CrossRef][Web of Science][Medline]
58 . Nulens E, Gould I, Mackenzie F, et al. Staphylococcus aureus carriage among participants at the 13th European congress of Clinical microbiology and Infectious diseases. Eur J Clin Microbiol Infect Dis (2005) 24:145–8.[CrossRef][Web of Science][Medline]
59 . Wulf M, van Nes A, Eikelenboom-Boskamp A, et al. Methicillin-resistant Staphylococcus aureus in veterinary doctors and students in the Netherlands. Emerg Infect Dis (2006) 12:1939–41.[Web of Science][Medline]
60 . Hanselman BA, Kuth SA, Rousseau J, et al. Methicillin-resistant Staphylococcus aureus colonisation in veterinary personnel. Emerg Infect Dis (2006) 12:1933–8.[Web of Science][Medline]
61 . Wulf M, van Serum M, van Nes A, et al. Prevalence of methicillin-resistant Staphylococcus aureus among veterinarians: an international study. Clin Microbiol Infect (2008) 14:29–34.[CrossRef][Web of Science][Medline]
62 . Aubry-Damon H, Grenet K, Nidaye-Sall P, et al. Antimicrobial resistance in commensal flora of pig farmers. Emerg Infect Dis (2004) 10:873–9.[Web of Science][Medline]
63 . Gortel K, Campbell KL, Kamoma I, et al. Methicillin resistance among staphylococci isolated from dogs. Am J Vet Res (1999) 60:1526–30.[Web of Science][Medline]
64
.
Hajek V. Staphylococcus intermedius, a new species isolated from animals. Int J Syst Bacteriol (1976) 26:401–8.
65 . Guardabassi L, Loeber ME, Jacobson A. Transmission of multiple antimicrobial-resistant Staphylococcus intermedius between dogs affected by deep pyoderma and their owners. Vet Microbiol (2004) 98:23–7.[CrossRef][Web of Science][Medline]
66
.
Sasaki T, Kikuchi K, Tanaka Y, et al. Methicillin-resistant Staphylococcus pseudointermedius in a veterinary teaching hospital. J Clin Microbiol (2007) 45:1118–25.
67
.
Bannoehr J, Ben Zakour NL, Waller AS, et al. Population genetic structure of the Staphylococcus intermedius group: insights into agr diversification and the emergence of methicillin-resistant strains. J Bacteriol (2007) 189:8685–92.
68 . Rich M, Roberts L, Deighton L. Clindamycin resistance in methicillin-resistant Staphylococcus aureus isolated from animals. Vet Rec (2005) 156:220.[Web of Science][Medline]
69 . MRSA guidelines. http://www.bsava.com/resource/mrsa/mraguidelines/mrsaguidelines.htm (28 May 2008, date last accessed).
70 . Weese JS, Rousseau J. Attempted eradication of methicillin-resistant Staphylococcus aureus colonisation in horses on two farms. Equine Vet J (2005) 36:510–4.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  A. Pantosti and M. Venditti What is MRSA? Eur. Respir. J., November 1, 2009; 34(5): 1190 - 1196. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. Chen, J. R. Mediavilla, D. C. Oliveira, B. M. Willey, H. de Lencastre, and B. N. Kreiswirth Multiplex Real-Time PCR for Rapid Staphylococcal Cassette Chromosome mec Typing J. Clin. Microbiol., November 1, 2009; 47(11): 3692 - 3706. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||