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Livestock associated MRSA: Tiger or Pussycat?

Published: February 10, 2014
By: Peter Davies BVSc, PhD (Department of Veterinary Population Medicine, University of Minnesota)
“The larger the island of knowledge, the longer the shoreline of wonder (doubt)”
Ralph Sockman 
The following comments are personal reflections on how the issue of “livestock associated methicillin resistant Staphylococcus aureus” (LA-MRSA) has evolved in the USA and globally. At the Leman conference, my presentation will emphasize details of recent research we have been conducting at the University of Minnesota to understand S. aureus ecology and the potential occupational risks for workers in the US swine industry. The comments below present a broader context of the epidemiology and sociology of LA-MRSA as a foundation for interpreting these recent observations. 
Angst is born ( again)!
It is approaching a decade since July 2004 when the phenomenon of LA-MRSA burst onto the scene in the Netherlands then echoed throughout the swine production world.1 MRSA (deservedly) have high name recognition among the public as the flagship organism of a loosely defined fleet of “Superbugs” (or now more fashionably “nightmare bacteria”). Emergence of apparently novel pathogens rightly furrows the brows of infectious disease clinicians and epidemiologists. Will it be the ‘big one’ that wrecks an unprecedented toll on public and/or animal health and creates massive social and economic disruption? If there is a food animal reservoir, a few nanoseconds might expire before somebody asks what the industry has done wrong to deliver this evil upon society.
As each new ship sails in (BSE; Salmonella Typhimurium DT104; vancomycin resistant enterococci; Nipah virus; Hepatitis E virus, H5N1 and novel H1N1 influenza viruses; SARS and MERS; NDM-1, ESBL E. coli, carbapenem- resistant Klebsiella,…and LA-MRSA…) uncertainty is usually the prevailing sentiment among the medically and epidemiologically literate. It takes time, often many years, to get a reasonable handle on the magnitude of a novel microbial threat, with the public interest arguably best served when guarded consternation drives systematic research that is enhanced by thoughtful inference. Much of this appropriate response has occurred with the LA-MRSA issue, particularly in the Netherlands. The island of knowledge of LA-MRSA is now fairly extensive, predictably bringing new questions and uncertainties, but also some time to gauge the likely public health impact. Unfortunately it is rarely the guarded consternation of the prudent and epidemiologically informed that drives the public conversation. 
Whipping up a frenzy!
While discovery of apparently emerging pathogens rightly troubles most people, these events are the lifeblood of those who make their living by peddling panic to the public. If food animals are implicated, even remotely, as having any role in the threat du jour, the tone from the ‘science journalists’ will usually degenerate towards apocalyptic finger pointing. History tells us that journalistic hyperbole often misses the mark by many orders of magnitude with respect to actual public health impact. BSE (one case where animal feeding practices were responsible for the propagation of the agent) illustrates the discrepancy between predictions of carnage purveyed by journalists (often cherry picking the upper confidence interval from the most pessimistic projection among highly uncertain models), and the actual toll on public health. Estimates aired in the media of predicted human deaths from variant CJD reached hundreds of thousands, but the ultimate (and still tragic) global toll over 16 years is around 230 – equivalent to about 2 days of road fatalities in the USA. SARS and H5N1 influenza are other examples where cumulative human deaths to date (respectively about 800 and 400 globally over about a decade) are of Lilliputian dimensions relative to the doomsday predictions, and are dwarfed by the public health burdens from daily risks like road deaths, and even lightning strike.2 And just to place LA-MRSA in perspective, the global tally of fatal cases currently stands at ONE (more later), and in the USA the number of confirmed cases of clinical infection with LAMRSA currently stands at ZERO. The ritual of ‘crying wolf’ benefits nobody but the scaremongering authors, contributes nothing to addressing any concerns and, like in the fable, is probably counterproductive for that rare future moment when the real wolf appears. I in no way want to trivialize the valid concerns that accompany all events of disease and pathogen emergence, but point out that those who hawk sensation for a living have little interest in the whole truth, or even reasonable perspective. Touting doomsday scenarios is a better business model.
I have written elsewhere of some myths and misinformation about LA-MRSA that was aired earlier in the course of the LA-MRSA ‘panic-demic.3 The romantic narrative of the swashbuckling journalists nobly fighting to inform a gullible public about the evils that are knowingly propagated by unscrupulous and money-grubbing food (and particularly meat) industries who hide their secrets from the hapless consumers has, for me personally, passed from tiresome to nauseating. My dismay about the quality of US journalism about LA-MRSA is not simply fatigue from listening to a ‘broken record’. It is that the same refrain keeps repeating when they should be reading from a very different and more factual score. Recent exhibits of journalistic ineptitude on LA-MRSA rival the stratospheric levels set in 2009, when at least one could offer a defense of greater uncertainty. But as I have stated before, ‘given the level of politicization of discussions about food animal production in general, and intensive livestock production in particular, it is now quaint if not delusional to dream of rational and factual public discourse on these issues.
While the pedestrian standards of science journalism are dismaying, the media do not have a monopoly on hyperbole and overstatement. Science combines two basic processes: observation and inference. I contend that biased (or worse still deliberately hyperbolic) inference afflicts more than a small portion of the peer-reviewed literature published to date on LA-MRSA. Almost no studies refer to the fact that only one fatality in the world has been associated with LA-MRSA over 9 years and that the clinical burden of LA-MRSA to date has been very small. Another prevalent but misleading statement about the human health implications is that LA-MRSA represent a high proportion of ‘cases’ in countries such as the Netherlands, without pointing out that ‘cases’ in those countries include people who are colonized (i.e. culture positive nasal swabs) but do not have infections. A recent and well conducted Danish study concluded ‘we therefore face an infectious occupational exposure of huge quantitative dimensions but of unknown clinical importance.6 The statement per se is true, but the authors fail to point out that based even on their own data, not to mention the accumulated preceding studies, the real unknown is exactly how SMALL is the clinical impact of LA-MRSA. Current data are sufficient to conclude that the clinical importance of LA-MRSA (meaning those organisms now known to occur in livestock in many countries) is ‘non-zero’ but very small. This is a mild example of insufficient context, but there are many more papers in which inferences drawn are questionable or even completely unjustified. The collective bias toward overstatement of the public health impact (real and projected) of LA-MRSA is pervasive, and the gatekeepers of quality (author responsibility and critical thinking, peer review and editorial standards) are inadequate. Two examples discussed below illustrate inferences that were so inappropriate (if not completely unjustified) that myself along with other colleagues submitted letters to the editor to document our concerns.
The first was a tragic report from France of a fatal case of ST398 MSSA (i.e. methicillin sensitive) infection of a girl with no known contact with livestock. The isolate involved had multiple attributes that were uncommon among ST398 MRSA isolates from pigs, yet the authors blithely inferred that ‘spread of S. aureus ST398 among livestock is a matter of increasing concern because strains of this sequence type were able to acquire PVL genes and cause necrotizing pneumonia in a young immunocompetent patient.’ Our response argued that apart from the different attributes of the organism (t571 MSSA) and the absence of any evidence of livestock involvement, there was substantial information supporting the possibility that the organism derived from a human rather than animal reservoir. This has since been strongly endorsed by identification of distinct human and pig clades of that specific spa type (t571) of ST398 S. aureus that are likely epidemiologically independent. Storm in an academic teacup, you say? But for the fact that the original paper immediately spawned considerable media and blogger interest, including a blog titled “News Break: PigMRSA involved in the death of a child” despite the fact that it was not MRSA, and there was no contact with pigs. The post remains alive and well at http:// www. superbugtheblog.com/2010/07/news-break-pig-mrsast398- involved-in.html.
The second study published in late 2012 concluded that risk from LA-MRSA in livestock dense regions extended to the general community and not just to people with livestock contact.10 We contend that this paper had serious flaws both in methodology and inference, and its final conclusion was unwarranted and contradicted by three much larger and methodologically superior studies (see below). Unfortunately, a press statement issued when the paper was published ensured that the unjustified inference was echoed through scaremonger community. After all, the amplifiers merely relay what the credentialed scientists were stating in a ‘peer reviewed journal’. In both cases, I believe that the authors of the papers we not sufficiently diligent (or perhaps just too busy) to consider alternative hypotheses before leaping to very questionable conclusions. Worse still is that the review process of the journal was patently inadequate for ensuring even rudimentary standards of inference. However, the most frustrating issue was the constipated process we encountered in publishing our concerned response to these papers. In both cases, publication of the letters (just 500 words) required almost a year, most of it spent trapped in the bowels of the journal while the babble that had been generated continued to cycle around the Internet. Probably not a functional model for how science can inform public debate! Now that I have vented that frustration, let’s get back to the Tiger and the Pussycat. 
LA-MRSA: Where are the bodies?
I am emboldened to use this arguably tasteless subtitle by recalling an article I read as a graduate student over 30 years ago. During the 1960s when oral contraceptives were unleashed on the western world, there was a little research and much speculation that this might have grave consequences for cardiovascular health and mortality in young women. Unsurprisingly, much of the doomsday predictions were propagated by entities with philosophical objections to contraception. A couple of decades later, ‘where are the bodies’ was a rhetorical question pointing out that the wolf had not appeared. With LA-MRSA, where we confront concerns about an acute infectious process (rather than a chronic and metabolic process), a decade after the emergence of LA-MRSA is not too soon to pose this question.
In 2011, with support from the National Pork Board, I reviewed published studies of ST398 S. aureus to catalogue reports of human clinical disease. The charge was to identify all published information related to clinical infections with ST398 organisms [both MRSA and MSSA (i.e. susceptible to methicillin)]. Eighty three papers or reports were identified to contain information on ST398 associated with clinical cases in humans. Where available, information was recorded on country; numbers of isolates that were from screening swabs; numbers of isolates that were from clinical infections; clinical presentations (e.g., bacteremia; pneumonia; skin or soft tissue infection…); invasiveness (number of cases with invasive infections, i.e. not skin or soft tissue infections); history of animal contact; and number of fatalities. Using conservative criteria of invasiveness (i.e., likely overstating invasiveness by including sputum and urine cultures) there were 2,213 events of positive screening (isolates not linked to infection) and 495 isolates from humans with clinical infections. More than half of the specified presentations were skin or soft tissue infections, or infected wounds. There were 89 cases deemed invasive, and 5 fatalities (note 4 of these were MSSA and without association with livestock) documented globally over several years. Approximately 30% of the 89 invasive cases involved the t571 spa type that is relatively uncommon in pigs. For context, in the USA alone, in 2005 the CDC estimated 94,600 invasive MRSA infections and 18,650 deaths every year.12 That is, if all the invasive and fatal cases of ST398 reported in the world from 2004 to 2011 had occurred in the USA in 2005, they would have represented 0.09% and 0.03% of those cases respectively.
As noted above, some European studies do not distinguish between events of colonization and clinical infection, and thus there is a lack of quantitative information about the actual clinical risks associated with livestock exposures and colonization with ST398 MRSA. The small number of reports of severe or fatal systemic infections with ST398 S. aureus have led to inferences that organisms of this lineage can be serious human pathogens. However, analysis of two years of data for a laboratory serving an estimated population of 800,000 people in a pig dense area in Holland identified 30 ‘clinical’ ST398 isolates, of which 6 were pneumonia or systemic infection (1 blood, 3 sputum, 2 urine). These data suggest an annual risk of approximately 2 clinical infections (and 0.38 invasive infections) per 100,000 people. A more recent report from the hog dense region of Jutland in Denmark (where all MRSA infections are reportable) recorded 3 clinical infections with ST398MRSA (all pig farmers) over 2 years in a population of around 580,000 people. This implies an annual incidence around 0.25 clinical infections per 100,000 people per year. The infections were two cases of impetigo (superficial skin infection) and one case of tonsillitis (where isolation of the organism alone does not prove causation). For context, widely cited estimates for MRSA infection in the USA are 31.8 invasive cases and 6.3 fatalities per 100,000 people per year.
To date, there have been 5 reported fatalities associated with ST398 S. aureus. In 4 of these cases, the organisms were t571 MSSA with no known livestock contact, and therefore are more likely related to the human than the pig clade of t571. The other case was t011 ST398 MRSA (unlike t571, common in pigs in Europe) and the patient had indirect contact with pigs. This 85 year old man suffered from lung carcinoma and chronic obstructive pulmonary disease, and the organism was isolated from pleural fluid. Other than infected bite wounds, reports of medically significant ST398 MRSA infections in healthy livestock workers are remarkably scarce and livestock contact is a notably inconsistent feature of invasive ST398 infections. Some authors default to the assumption that lack of livestock contact constitutes evidence of indirect spread (e.g. via food and the ‘environment) putting the wider public at risk. However, this is a very questionable assumption unless the organisms are known not be belong to the t571 human clade, which itself may prove not to be unique (i.e., other spa-types deemed LA-MRSA may be found to have distinct human-adapted counterparts).
Information on human disease associated with ST398 MRSA is sparse in North America than Europe. A retrospective assessment of 3,687 MRSA clinical isolates in Canada identified only 5 cases with ST398 MRSA, 4 of which presented with skin or soft tissue infections. The CDC has examined over 12,000 US isolates and is yet to identify ST398 among human clinical isolates (Dr. Brandi Limbago, personal communication). Similarly, in the hog dense state of Minnesota, the MN Department of Health has tested over 7,000 clinical isolates of MRSA with sma1 PFGE (inability to type isolates with sma1 is a characteristic of ST398 lineage) and is yet to identify an ‘untypable’ isolate (Dr. Kirk Smith, personal communication). Given the known presence of ST398 in the North American swine industry, and the sporadic reports of clinical infections in swine workers in Europe, it is likely that some clinical infections may have occurred in occupationally exposed individuals in the USA. The absence of reported cases until now in the USA is likely attributable to both a low incidence and low severity of ST398 infections. On the other hand, t571 ST398 MSSA of the human clade has recently been identified as a relatively important source of human MSSA infection in New York, being identified in 5% of non-invasive MSSA cases and 2.5% of MSSA bacteremias. That is, the only documented cases of clinical ST398 infections in the USA to date involve the human clade of t571 that is considered ‘animal independent’. 
The larger island of knowledge – do we know what LA-MRSA are?
In my experience around zoonotic pathogens over 20 years, simple phenomena rarely stay that way. The initial discovery of ST398 in Netherlands provided a fairly clear and simple narrative. A novel lineage of MRSA had been discovered in livestock (particularly pigs) and constituted a new threat to public health. Possession is nine-tenths of the law and the term ‘livestock associated MRSA’ or ‘livestock associated S. aureus’ understandably became synonymous with ST398-MRSA/S. aureus. However, this once reasonable terminology now causes more confusion than enlightenment. Firstly, we now know that at least one clade of ST398 is in not associated with livestock. Secondly, ST398 S. aureus are not uniquely associated with pigs, a fact that is unsurprising both on the grounds of basic biology (assuming S. aureus is part of the normal flora of pigs) and from research conducted on isolates obtained before,16 and after, the Dutch revelation. There is now accumulating evidence that S. aureus belonging to several MLST lineages (particularly ST9 and ST5, but also others included ST97 and ST1) may be equally ‘pig associated’. MRSA isolates belonging to these lineages (particularly ST9 in Asia) are being increasingly documented in swine. As research continues, a better understanding of the diversity of S. aureus in swine populations will be achieved, and it is clearly much broader than ST398.
‘ST398’ should no longer be seen as synonymous with ‘livestock associated’. Its use as such should be eliminated henceforth, particularly in titles of peer reviewed literature. Though once having some utility, this terminology has been rendered inappropriate by recent research and contributes to misleading inferences that can be carelessly cited as evidence of community spread of S. aureus from livestock sources, without any evidence that this was the case. The use of the term ‘livestock associated’ with MSSA or MRSA should be reserved for isolates that have been directly obtained from or closely linked to livestock environments. Authors drawing inferences indirectly about livestock involvement in the epidemiology of human MRSA cases should be held to a higher level of accountability than has been the case to date. 
Who are at risk of LA-MRSA exposure?
To date there are insufficient data to make any judgments about swine associated MRSA other than ST398. There has yet to be a community based outbreak of ST398 MRSA infection reported from any country, and two reports of hospital associated “outbreaks” were of small scale and predominantly involved asymptomatic carriage and contamination of superficial wounds. Evidence to date indicates the health risks associated with ST398 organisms of livestock origin are overwhelmingly restricted to people with direct animal contact and their immediate families. Across these 3 studies, LA-MRSA prevalence (44%) was > 180 times higher in 352 occupationally exposed persons than in 2,094 rural residents without farm exposure (0.24%). Prevalence in family members of livestock workers was intermediate (5.2%). The studies collectively confirm that in livestock dense regions where exposure to ST398 MRSA is a common occupational risk for livestock workers, it is a lesser risk to their family members, and a negligible risk to persons without livestock or farm contact. 
MRSA myopia- what’s in a gene?
MRSA are differentiated from MSSA based on the presence of a single gene (mecA). MRSA paranoia in the media creates the impression that MSSA have no importance as human pathogens, whereas MSSA contribute significantly to the burden of human S. aureus disease including fatalities across the world. It is remarkable that given the volume of research conducted on ‘LA-MRSA’, the biology and ecology of the parent organism (S. aureus) remains largely overlooked. Much of this focus was justified initially by the effort to understand the extent of the ‘problem’ in the early period of great uncertainty. However, as the conversation in some sectors drifts towards ‘control and interventions’ (albeit unwarranted and probably ineffective), it is essential to understand the basic ecology of S. aureus in pigs. Some very recent studies in pigs and veterinarians have broken this barrier, and more are required if we are to obtain any comprehensive understanding of the basic biology. At the University of Minnesota, we currently have ongoing studies of S. aureus epidemiology in pigs (funded by the National Pork Board) and swine veterinarians (funded by NIOSH through the Upper Midwest Agricultural Safety Center) in the USA, and some results will be presented at the Leman conference. This will include growing evidence that the prevalence of ‘LA-MRSA’ is lower in the USA than in many European countries, and that MSSA variants of most lineages of MRSA associated with pigs around the world are prevalent in the USA. Given that these organisms have likely been associated with pigs since well before the modern era of intensive swine production, the apparent lack of any incremental risk of S. aureus infections recognized swine farmers suggests that their pathogenic potential in humans is probably negligible. Further research into the virulence of livestock associated lineages will be required to explain the apparently minor risk of occupational S. aureus infections of swine farmers despite ‘occupational exposure of huge quantitative dimensions’. 
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This paper was presented at the Allen D. Leman Swine Conference 2013. Engormix thanks the organizing committee for letting us reproduce this paper and the author for granting permission.
Authors:
Peter Davies
University of Minnesota
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Allan Schinckel
Purdue University (USA)
24 de febrero de 2014
very good article - need more like it
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