MRSA in pork products: does the "antibiotic-free" label make a difference?

Back in November, I blogged about one of our studies, examining methicillin-resistant Staphylococcus aureus (MRSA) in Iowa meat products. In that post, I mentioned that it was one of two studies we'd finished on the subject. Well, today the second study is out in PLoS ONE (freely available to all). In this study, we focused only on pork products, and included 395 samples from Iowa, Minnesota, and New Jersey. We also looked at not only conventional meats, but also "alternative" meat products. Most of the latter were products labeled "raised without antibiotics" or "raised without antibiotic growth promotants"--in the markets we tested, very few USDA-certified organic products were available unfrozen, and we were looking for fresh meat products.

In our previous paper, we found MRSA on 1.2% of 165 meat samples. In the current study, we found a higher prevalence--6.6% of 395 samples were contaminated with MRSA. (More about the differences in methods between our two studies later). Interestingly, we didn't find a statistically significant difference in MRSA prevalence on conventional versus alternative pork products--a finding that surprised me, as it contradicts what we've found to date looking at the sources of this meat--conventional versus "alternative" pig farms. Other groups have also found differences on-farm versus on-meat: a 2011 study looking at feedlot cattle didn't find any MRSA in animal samples, though the same group found MRSA in beef products. So, our disparate findings between farms and meat samples are not unheard-of. However, even though our sample size was larger than other U.S. studies to date, it was still fairly small overall--300 conventional and 95 alternative pork samples over a 4-week sampling period from 3 states, so larger multi-state studies are needed to further examine this angle.

It also suggests that we need processing plants and packing companies to work with us to determine where products are being contaminated--because while there may be arguments about the public health importance of MRSA on meats (or lack thereof), it's very likely that if S. aureus are ending up on meat products, other pathogens are as well.

What does the molecular typing tell us, speaking of contamination source? We carried out analyses on all the MRSA and found that the most common type of MRSA was ST398, the "livestock" strain that we previously found on pig farms in the U.S. We also found two "human" types were common: USA300 (a "community-associated" strain) and USA100 (typically considered a "hospital-associated" strain). In the simplest analysis of these findings, these molecular types (a combination of "human" and "pig" strains) suggests that MRSA on raw pork products may be coming both from farms and from food handlers. However, in real life, it's not quite so straightforward. USA100 types have also been found in live pigs. So has USA300. As such, the source of contamination and relative contributions of live pigs versus human meat handlers currently isn't certain.

Within the MRSA strains, we found high levels of antibiotic resistance, similar to what was reported in the recent Waters et al. study. In ours, 76.9% were resistant to two or more antibiotics and 38.5% were resistant to three or more antibiotics tested. (I'll note that we only had funding to test the MRSA--we weren't able to do these tests on all the methiciin-susceptible strains).

Did MRSA prevalence increase in the period between our first study (spring 2009) and this one (late summer/fall 2010)? I doubt it. For this paper, we used a different sampling method, adding the samples to a sterile stomacher bag so that the entire sample was immersed in the culture medium; for the first paper we used external swabbing and so likely didn't capture as many bacteria. This current study more likely represents the "true" MRSA prevalence. But--all isolates were only called as positive/negative, and we didn't measure the number of bacteria on each piece of meat. So, there theoretically could have been just a few colonies of MRSA on the entire piece of meat, and that would have been called a positive sample, while another meat product covered with hundreds of MRSA would have been put in the same category. Therefore, more subtle differences may exist that we didn't pick up in this study, but we will examine in other ongoing studies.

So--what's the take-home here? Don't assume that any meat product is contamination-free, and always use good food handling/cooking practices when dealing with raw meats. As far as the titular question, well, we're still hashing that one out.


Hanson et al. Prevalence of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus (MRSA) on retail meat in Iowa.

Waters et al. Multidrug-Resistant Staphylococcus aureus in US Meat and Poultry.

O'Brien et al. MRSA in conventional and alternative retail pork products.

Lin et al. Evidence of multiple virulence subtypes in nosocomial and community-associated MRSA genotypes in companion animals from the upper midwestern and northeastern United States.

Weese et al. The Prevalence of Methicillin-Resistant Staphylococcus aureus Colonization in Feedlot Cattle.

Weese et al. Detection and quantification of methicillin-resistant Staphylococcus aureus (MRSA) clones in retail meat products.

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Huh. That is interesting, that there's little difference in the sources.

I don't eat much meat, but of course it could still get to me with bad handling practices. I really wish people weren't so opposed to irradiation or other possible non-antibiotic methods of reducing these.

Is there any evidence of MRSA hanging out in the food processing plants nooks and crannies?
I know we're thinking of Listeria as kind of hanging out in the plants in a semi-permanent (i.e. not anything that can be cleaned out) sort of way. But we have no real clue if it's hiding in drains in biofilms or if there are asymptomatic carriers among the workers, or what.

I haven't seen any studies of that and we've not been able to get into any plants, but I find it hard to imagine it *wouldn't* be there. I'd love to check on environmental surfaces, in the air, and in workers' noses.

Are the animals on whom you find MRSA sick? If you are finding the bugs on the meat, this means they have breached the skin barrier and are not commensal per se. DO you find more MRSA on hides and hair?

Are titers ever determined for these studies, or is it a PCR yes/no?

Susan, MRSA rarely causes actual disease in pigs--it's typically commensal. Finding it on the meat doesn't mean it's necessarily *in* the muscle--many ways it can become contaminated during processing, and with ground products, obviously anything that was external means it can go anywhere. When we do animal MRSA sampling, we usually check the nose as that's the main reservoir, though it can also be found on skin.

hibob, these are using pure cultures, and no blood/serology. So we isolate first, and then use PCR for the variety of molecular genetic testing we carry out.

Or are you asking for quantitation of microbial counts on the meat products? As mentioned, that wasn't done for this particular study.

Even if you bought a pig, and feed it yourself, with vegetables that you buy in your local grocery.. it still wouldn't be really 'clear' meat. Nowadays literally everything is polluted.

Lately I've been seeing more articles talking about MRSA contamination of meat, and other than as a marker for the prevalence of antibiotic overuse, I'm not sure this is a real problem. Maybe it's my constant exposure to MRSA in the hospital that has led to me to be less worried about it, because so many people are carriers, but it's really not that big a deal outside the ICU. Further, with meat, staph contamination in general will be inevitable with time. I see it as less of a slaughterhouse problem and more of an issue for the local health department checking the fridge temperatures in restaurants, and being sure to sear the outsides of your steak. I think we have to just accept that our general pattern of antibiotic overuse has made this a ubiquitous bacterium, and we just have to get used to it now. In terms of food contaminants I'd be much more bothered by campylobacter, enterotoxigenic e. coli, etc.

Mark, I guess we differ on "not that big of a deal." As far as death, I agree with you that the ICU will be the worst cases, but we still see and hear stories from many people with recurrent infections that really impact their quality of life.

For food, I differ with you that I don't see it as much of a cooking issue (searing the outsides of your steak), but an environmental contamination issue (eg Grandma handling meat products and then touching her nose, or not wiping everything down carefully after having meat packages on the countertops, etc.) I agree that campy etc. cause more nasty disease directly attributable to food contamination, but we're really just starting to scratch the surface as far as understanding what, if any, role that meat products play in the ecology and transmission of S. aureus.

RE: Post #11 "...but we're really just starting to scratch the surface as far as understanding what, if any, role that meat products play in the ecology and transmission of S. aureus." In your line of research, I'd be careful what surfaces you're scratching :-)

I was reading an article in Science about finding MRSA in non-farm soil samples. I assume that these are totally different strains. (Around here, there are pigs rooting around in the fields, but I gather most pigs are born and die indoors.)

For food, I differ with you that I don't see it as much of a cooking issue (searing the outsides of your steak), but an environmental contamination issue (eg Grandma handling

Trioxidane is the key in fighting infection and superbugs. A new technology is tackling just that with the use of ozone and hydrogen peroxide.

I buy "raised without antibiotics" or "raised without antibiotic growth promotants" meats because it's a better way to raise animals and for the health of various critters living in and around the pig farms and the in waterways effected by run-off, not for my own health.

And then I eat at Taco Bell and have beef that was probably raised by Zombies and then processed by even more evil Zombies using hacksaws with blades dipped in Hep C.

Does this count as middle ground?

What three states did you perform the study?

Tara, you said in a comment, "we've not been able to get into any plants" Have you not been able to because the plants won't let you or you just decided not to?

Re #17, we haven't found any that will let us in. The 3 states were mentioned in the first paragraph--Minnesota, Iowa and New Jersey.

Thanks for answering the second question and sorry about the first question. I'm surprised at myself that I missed it in the first paragraph.

There is little evidence that LA-MRSA strains are being able to colonize either the slaughterhouse environment (each slaughterhouse tends to have it's own established "flora" or humans. Hospital associated strains are by far, the isolates mostly associated with Human infections of MRSA.
In terms of food safety, MRSA behaves pretty much in the same way as MSSA when ingested by the gastro-intestinal route, and, like MSSA is rarelly treated. Even because foodborne outbreaks with S. Aureus are not really ususally associated with the organism it self but rather the toxins it produces, it really tends much more to be a foodborn intoxication rather than a foodborne infection.
That said, what mostly concerns me are the latest findings of hospital associated strains colonizing pets.
Happy to discuss.

By Lowlander (not verified) on 31 Aug 2012 #permalink

There has been very little examination of MRSA in slaughterhouses here in the US--and note that the meat was found to be contaminated with a mix of LA, CA, and even HA strains. You note that "Hospital associated strains are by far, the isolates mostly associated with Human infections of MRSA"--but this is a bit misleading. Certainly for invasive infections, absolutely. But for skin and soft tissue infections, CA seem to be more important--and remember that MRSA are only the tip of the iceberg, as MSSA are out there causing infections as well but don't get any respect.

Finally, as noted we're not looking at it as a food-borne illness, per se, but another vehicle for introducing S. aureus into homes and colonizing their inhabitants.

Thank you for your stimulating reply.
You are not looking at it as food-borne illness, correct. However you mention in this blog entry you have found it in pork without qualifying the finding, therefore misleading the reader. In my opinion which is why I made the note.
Worse than that in my opinion is the omission that current consensus is that MRSA transmission and colonization is thought to occur mostly from living host to living host. Not through animal products. Fomites in general may play a smaller part.
In Europe, environmental sampling of slaughterhouse environment has not revealed colonization of the slaughterhouse environment. In fact carcasse sampling at slaughterhouse level indicates that MRSA strains seem unable to pass beyond the lairage. Why this happens is unclear. Could be the way carcasses are dressed, could be C&D procedures or simple competition with pre-existing slaughterhouse flora.
Your results are interesting, however, from the entry in the blog I infer that samples were taken of pork in shelf at retailer - correct? If so, there are plenty of steps in the supply chain from slaughterhouse to cutting plant, transport and final retailer where humans could have contaminated your samples with CA and HA strains. The LA strains however are harder to explain.
Finally, my note about Hospital associated strains is certainly not misleading, at least in the European context..
The focus in MRSA rather than MSSA is most justified. One is very resilient to our tools combat it, while the other still has quite a bit still to go.
Happy to discuss.

By Lowlander (not verified) on 31 Aug 2012 #permalink

I do discuss those issues both in the post I linked to from my previous MRSA/food post, as well as in the paper, which is open access and freely available to anyone with an internet connection. I'm not sure what you expect in a blog post--I'm certainly not going to repeat every finding and caveat from the paper verbatim--hence the linking.

You keep suggesting the European studies and that I'm misleading, but from research in my lab and others, the situation with swine-associated S. aureus here in the US is quite different from that in Europe. As such, you can't directly extrapolate from their findings to our issues here in the US--meaning we still have a lot of unanswered questions. The strains we see even in live animals in the US are much more diverse than those seen in Europe--we see HA and CA even in our live pigs, so it's unclear whether when we see those in meat samples if it's coming from people or animals (again, as we discuss in the paper). And I disagree that it's a settled matter that meat isn't a risk--so does the USDA, who has funded me to investigate that very question. In this case, meats are acting as essentially a moving fomite, which can possibly contaminate kitchens and meat handlers. There are some interesting environmental sampling papers which show lots of SA associated with kitchen sinks, wastebaskets, etc., and meat products are one (of several) places those could come from.

I have not read the paper nor followed the links, just the post and the comment section from readers. The comments from some readers appear to show this misunderstanding of nature of the hazards between invasive MRSA and general foodborne toxinfection from MRSA/MSSA. I do apologise if the comment about that topic is unfair.
By the way, I have just discovered this blog and am just now going through the older entries. Very interesting, stimulating and very good information to the public. So please do not take my comments as criticism for the sake of it but rather as true discussion and debate of ideas.
I am mentioning European studies and the European context simply because it is the one I know better. I am not suggesting that your study is misleading, I am suggesting that while interesting it does not really fundamentally challenge EFSA's opinion on risk of Human infection with MRSA. being:
1 - HA strains are the largest contributors to human infections
2 - Human colonization with MRSA in a determined geographical area tends to follow the strains in the local hospital
3 - CA is a recognized issue in the US but much much less so in Europe.
4 - LA strains tend to circulate amongst livestock and colonize specific groups of people, constituting an occupational hazard
5 - Within LA's equine LA's appear to be expanding and horses are starting to show the same pattern as Human, i.e. MRSA strains in horses tend to be regionally clustered and related with equine veterinary hospitals

Regarding your disagreement. First I did not say that pork or fomites in general are not a risk, just that epidemiologically, it is not as significant as live host to live host transmission. Second your postulated route contamination of kitchens is, in my opinion, unnecessary to explain what we observe, I am not discarding it, do not take me wrong, I just find it a weaker, less probable explanation. SA likes moist warm mucosas to live and multiply. It survives in fomites and can even multiply given certain right conditions but it mostly survives, not thrives in fomites, I think that your most obvious source of SA in a determined environment has to be a living host the majority of times, so in a kitchen I would look at the inhabitants first: habitants, people visiting, pets and only then pork products.

Of much more importance, I think, are findings of HA and CA strains colonizing living livestock and, I stress again pets. Because they can serve as secondary sources for further re-infection in a community, in the particular case of livestock, where on top of it you apply extra selective pressure due to a different range of antibiotics being used on those strains you can end up with a brand new strain (in fact given enough time that is an inevitability!) or transfer of resistance genes between LA and CA and HA strains which later find their way back to a hospital.
In the case of pets it is extremely worrying because they tend to have a much more intimate contact with people and secondly because you also risk that they go on to contaminate small animal veterinary hospitals where selective pressure will just compound your problem.
Very happy with this debate.

By Lowlander (not verified) on 31 Aug 2012 #permalink