The poultry microbiome, culture-based ecology continues to mislead us all

Shigella penetrating the intestinal wall. Source: cellimagelibrary.org

If the world was enriched and homogenized, we would actually have a very good idea of what the microbiological community within looks like. Fortunately, the world is much more complex than the miniature environments we culture in the lab, and high throughput sequencing (HTS) is allowing us to fully appreciate micro-biodiversity. As new information becomes available, many of our models for microbial communities continue to be challenged by the actual composition of species in natural environments.

In the world of food safety, we rely on these models to set policy on a regulatory level, and to set critical limits down at the production level. Which tests we run on what products depend directly on what organisms (that cause food borne illness or spoilage) are supposed to be found on that type of food. The authors of this study that came out in PLOS ONE this February examined the microbiome associated with poultry products from farm to fork (meaning from clucking chicken to packaged poultry product) using HTS rather than culture/enrichment methods. The results indicate that there is an unappreciated amount of diversity between different stages of the poultry production process, and that we may not acknowledge the presence of some organisms as much as we should.

In the study, samples were taken from multiple steps in the poultry production process: wet and dry litter, fecal samples, fluid from carcasses collected during the cooling process following slaughter, and fluid from raw retail poultry products (legs, wings, and breasts). Other than the retail portion, all of the samples collected were from the same batch of birds from start to finish. The available RNA from viable cells in each sample was amplified and identified as belonging to specific species using a combination of Illumina sequencing and database referencing (blastn and usearch).

From this pile of data, lists of organisms were compiled to compare the ecosystem profile for each point in production.

The numbers refer the the number of unique taxa found in each group

The authors were very surprised by the amount of diversity between the two litter samples (wet and dry) and the fecal sample. They expected to see very similar profiles, as all of the predicted microbes in those groups would be inoculated from contact with fecal material (young chicks have no inherited microflora, and are coprophagous); however, all of the groups’ microbial communities had very little in common. As shown above, of the hundreds of unique species identified, only 52 were actually found at every stage from farm to fork.

In evaluating food safety, several results are of concern. The first was that the authors found significant amounts of Shigella spp., which have traditionally not been associated with poultry products and may not be a part of many sanitation programs. The second is that in one of their dry litter samples, the authors found a large amount of C. jejuni. It’s presence was interesting as previous studies have found it difficult to cultivate C. jejuni onto dry litter, suggesting that it will not grow in that environment. This discovery further shows that our attempts to cultivate bacteria are not indicative of their behavior in “the wild”. There may be nutrient gradients or a symbiont in play that allows C. jejuni to grow; therefore the possible contamination of dry litter has to be acknowledged in that facility’s Campylobacter monitoring program.

The last point of interest I’ll discuss here is the large amount of unique species that were found in samples following slaughter. This suggests that these species did not come from the farm, but rather were introduced during slaughter and processing. Interestingly, among Campylobacter spp., there was little to no abundance of C. jejuni in the samples, but differing amounts of other Campylobacter spp. This is revealing, as we have been predisposed to expect C. jejuni to be present due to our use of selective media.

Let’s fully appreciate the amount of diversity found within the processing facility, the authors collected two post-processing samples labeled carcass rinse and carcass weep. The rinse was composed of fluid shaken off of the carcass following its removal from the chlorinated chill tanks, and the weep was the drippings from the same carcass 48 hours later. 2/3 of the unique species found the weep samples were not found in the rinse. The authors interpret this as being due to the fact that the sterilization of carcasses is not the goal of poultry processing, and provide the example that viable Salmonella can be recovered from carcasses even after they are sent through the standard antimicrobial processes. The goal is to reduce enumeration, not sterilization.

Finally, in examining the retail samples, we get what we expect. Similar organisms as the weep, with some new faces, presumably because they persisted through processing at undetectable levels, and slowly grew as the product was stored in refrigeration.

The authors conclude by examining some potential symbionts that would allow C. jejuni to persist, but ultimately say that due to the high number of environments C. jejuni can occupy, attempting to exclude it in a universal way will not be very effective.

So all in all, a thorough example of the misdirection we receive from culture bias, and a startling look at how, given enough incubation time, properly processed meat can still support a huge amount of microbial diversity, including many food borne pathogens.

Appreciate this diversity, and make sure you cook your chicken to temperature.

 

ResearchBlogging.org

Oakley BB, Morales CA, Line J, Berrang ME, Meinersmann RJ, Tillman GE, Wise MG, Siragusa GR, Hiett KL, & Seal BS (2013). The Poultry-Associated Microbiome: Network Analysis and Farm-to-Fork Characterizations. PloS one, 8 (2) PMID: 23468931

Do organic animal operations encourage management decisions that negatively impact animal welfare? Part 2

Here’s the second portion of my paper: Do organic animal operations encourage management decisions that negatively impact animal welfare?

You can find part 1 here, or read the entire paper here.

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Welfare from an Ecocentric Perspective
Animal welfare has always been and remains to be an important goal in organic operations (Riddle, 2005; IFOAM, 2005); however, organic producers are still questioned on the welfare status of their animals because of their organic certification. Among the many definitions intended to quantify animal welfare, Frasier et al. (1997, p.187) provide three basic animal welfare ideals:

1. The animal should feel well, corresponding to the concepts of experience, feeling, interest, and preference.
2. The animal should function well, corresponding to the concepts of need and clinical health.
3. The animal should lead a natural life through the development and exercise of its natural adaptations, corresponding to the concept of the “innate nature” of the animal.

In general, livestock in conventional settings have their welfare measured using the first two ideals, with the most emphasis placed on the second. Producers are first and foremost concerned with the prevention of disease that could hurt production or cause unnecessary pain; humane slaughter laws are designed to prevent excess excitement and discomfort (National Archives and Records Administration, 2012b), and welfare audits for slaughter facilities are designed to reduce animal stress prior to slaughter (Grandin and Johnson, 2006). Using these criteria, it becomes clear how viewing welfare through the first two of Frasier’s ideals might suggest organically raised animals could have poorer welfare. It has been shown that organic farms have a higher rate of parasite-related disease (Lund and Algers, 2003), and the use of veterinary drugs is strongly suggested to be a last resort after alternative methods have been exhausted (IFOAM, 2005). There is also a financial incentive, as once antibiotics have been given to an animal, that animal cannot return to organic production (Riddle, 2008; National Archives and Records Administration, 2012a).

Through the naturalistic perspective however, welfare for organic producers can depend much less on the first two ideals, and more weight is placed on the third. This viewpoint changes the significance of the risks involved in many organic practices, such as free range housing, as both organic producers and consumers emphasize the third ideal as a priority (Alroe et al., 2001; Lund, 2006). Additionally, the ecocentric perspective further lowers the emphasis on the first two, as disease and parasites are both considered healthy parts of a larger ecosystem, and the health of the ecosystem is crucial to the health of the herd and the sustainability of the farm. This idea of looking past the individual is what causes dispute when quantifying animal welfare on the organic farm. Most producers, veterinarians, USDA inspectors, and animal owners evaluate animal welfare at the level of the individual, whereas the ecocentric organic producers are more likely to evaluate welfare at the level of the flock/herd, within the herd’s role in the overall ecosystem. At this level, a few animals in poor health are acceptable in a natural ecosystem where small amounts of disease are permissible. The ecocentric view disallows an attempt to alter a healthy system determined by nature by eradicating this small population.

Because animal welfare may be determined using more qualitative criteria in an organic operation, how do organic producers react to poor welfare or illnesses of individual animals? Organic producers hold the health of their animals high in their priorities (IFOAM, 2005; Riddle 2005), so they must be able to maintain a standard of herd health not only for the benefit of their animals, but to keep production high. As part of the naturalness or ecocentric ethos, organic producers believe that farmers should not try to take control of the environment, as conventional techniques do, but work hand in hand with nature. Thus, any method used to completely eradicate disease through the use of chemicals or medications does not promote a sustainable ecosystem, as it reveals an attempt to control the environment rather than work to bring the ecosystem back into balance (Verhoog et al., 2003). Therefore, prevention becomes key, and the U.S. organic requirements mandate preventative practices that emphasize working with nature such as selection of species and type of livestock that are appropriate to the site and resistant to prevalent disease, provision of a sufficient organic feed ration, and the use of appropriate housing, pasture management, and sanitation protocol to minimize the occurrence of pathogens (Riddle, 2008).

 

New Research: Do organic animal operations encourage management decisions that negatively impact animal welfare? Part 1

For my senior ethics class, I chose to write about an issue everyone has an opinion on, from granola folks at the co-op telling me to watch Food Inc. to farmers complaining about the outbreak of upper respiratory disease from those untreated organic herds sneezing over the fence. I actually ended up changing my own views quite a bit following the extensive research I did, and I really enjoyed writing the paper. I wanted to evaluate the claims often made to me by professors in my land grant school (Oregon State) about the misleading advertizing and hidden evils of organic production, and I wanted to see if there was anything to back up the fanaticism and devotion sometimes projected by organic devotees. This paper is by NO MEANS an exhaustive review of the literature, and I am not qualified to make any official judgement, and is simply meant to be a personal commentary from a recent graduate.

So rather than sit here blathering, the first portion is below, and you can read the full paper here.

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Few agricultural debates come close to generating the same passionate and heated responses that organic farming seems to elicit. The discussion surpasses the interests of producers with conflicting ideologies to be hotly debated by assertive consumers as well; people who highlight the paradox created by their interest in the safe and responsible production of their food, while avoiding all involvement in its creation. The originally proposed Organic Foods Production Act of 1990 received nearly 300,000 comments on the proposed requirements, more than any other piece of legislation in history (Vos, 2000). Clearly this indicated that the role organic farming played in food production was extremely important to U.S. citizens then, and continues to be a relevant topic as organic operations have grown by 40-50% every five years since 1992 (USDA, 2010).

The general public also has a strong interest in the way animals are managed, especially when management techniques play a role in the health or well-being of the animals prior to their use for meat, milk, or eggs. Humane management is often brought up when discussing the merits or flaws of organic operations, and is extremely important to producers due to the important role animal welfare plays when consumers make purchasing decisions. Prickett et al. (2010) found through the use of a telephone survey that 49% of consumers consider the well-being of farm animals when purchasing meat, and 83% of consumers disagree that lower prices are more important than the well-being of the animals used. These numbers become critical when organic producers need to justify the increased cost of their products and conventional producers are forced to avoid the alternate impression that their animals are treated poorly.
Marketing pressure placed on both groups leads to a vicious back and forth of both valid questions and vague accusations, among which is the suggestion that organic farms can act as reservoirs of disease (Kijlstra and Eijck, 2006). One mechanism for this accusation could be the avoidance of chemical or synthetic intervention for pest control and treatment of disease. This paper seeks to evaluate organic farming ideologies and legal constraints that create ethical dilemmas surrounding animal welfare, and determine whether organic management encourages decisions that are detrimental to the animals involved.

Animal Welfare and the Organic Movement
Early organic movements were created with the goal that a more sustainable and environmentally friendly farming system could be created that would benefit not only farmers and consumers of organic products, but also the animals within this system (Lund, 2006). These ideals have persevered and are a common talking point in promotional materials that market organically raised animals as drug and chemical free, and much closer to a “natural” condition (Riddle, 2005). This concept of “natural” is commonly used to differentiate organically produced animal products from conventional ones.

Utilizing the word “natural” creates an issue of perception; while the public widely accepts “natural” as a product descriptor, the word itself has no legal definition when used in food advertizing or packaging in the U.S. However, consumers have been shown to associate descriptions of “naturalness” not only with animal welfare but sustainability and care for the environment (Verhoog et al., 2003). While this may imply a scheme to sway consumer loyalty, the word is widely accepted by organic producers as an accurate descriptor to differentiate organic methods from conventional. While “natural” can have broad definitions like including the entire universe or everything untouched by man (thus either removing agriculture or providing no distinctions in practice), Verhoog et al. (2004) were able to show that organic producers feel organic can be classified as more natural than conventional agriculture as its aim is to be harmoniously integrated into nature. In this way nature is seen as a teacher or model for sustainable and humane agriculture. This ethos pushes organic farmers into an ecocentric approach when making management decisions. From this perspective, we begin to see how organic farmers may view welfare differently than conventional farmers or veterinarians.

Read the rest of the paper here.

 

ResearchBlogging.org
Vonne Lund, & Bo Algers (2003). Research on animal health and welfare in organic farming—a literature review Livestock Production Science, 80 (1-2), 55-68 : 10.1016/S0301-6226(02)00321-4

Badger culling in the U.K. – step one: cull badgers, step two: …?, step three: profit!

Image from BBC News

A friend of mine thought this would interest me when I last visited him, and I had him send me the links discussing badger culling in the UK to control the spread of bovine tuberculosis (Mycobacterium bovis).  In addition to having an economic impact,  bovine TB also carries a zoonotic concern. I thought I would learn more about the issue, and see what the literature says about the success of the program.

Badger culling has been a part of TB control in the United Kingdom since 1973. Despite this and other programs in place, incidence of TB has only increased during that time. In the thousands of biological and environmental risk factors that have been associated with TB infection risk, Badgers have been identified as an important reservoir and potential vectors for the disease.

The politics surrounding the issue are interesting, and provides a great case example of how public perception can be skewed for certain species. The regular players are all there: the economically invested (in this case, cattle farmers and associated industries), the scientific community, outspoken animal interest groups, a generalized public perception, and the federal government trying to cater to the majority of voters (or campaign contributors, depending on the official and your own opinion). Lets break down these players.

The Economically Invested

On this issue, everyone seems to be on board that bovine TB is a problem in the UK. The ones who really care though are cattle producers, meat and dairy processing companies, and the retail ends associated with those products. When oppositional parties want to discredit this group, we see them described as “big corporations” only concerned about the bottom line. These claims are many times true, as even the small farmer has to maintain a decent profit margin to provide for him or herself. This group tends to be less publicly oppositional, preferring to exercise their strength through advertizing, lobbying, and funding research that can help support their position. Within this issue, I wasn’t able to find any ads produced by organizations in the UK, however, I did find some farmer concerns over the issue. One was the difficulty in getting approved for a badger cull in your area, and the other was the fear of response from activist groups if they did choose to participate in the program. The position of the farm interest groups is that the spread of bovine TB is an animal welfare and economic concern, and that badger culling will be critical in suppression of the disease. Local wildlife can often aid transmission of disease; however, we have also seen blame placed incorrectly on wildlife in other situations.

Animal Interest Groups

There are many groups in the UK that advocate for Animal interests, and they’re pretty much unanimous in the opinion that culling badgers is not an effective or ethical way to combat bovine TB prevalence. However, they do have different techniques in approaching opposition. While many of them strictly condemn the practice and advertize to sway public opinion, one group (with the support of many others), Gloucestershire Wildlife Trust, has been independently vaccinating wild badgers for bovine TB. At this time they haven’t investigated the effectiveness of the vaccine itself, but rather the economical viability of the process. Their results so far have shown that it would cost more than twice as much to vaccinate an entire hectare instead of culling. Typically these same groups in other controversial situations are very politically active.

The General Public

Generally the least informed and (arguably) the most powerful, the majority of public opinion represents the majority of voters and consumers. Regarding badger culling however, most of the general public has been shown in polls to oppose the practice. Agricultural controversies are often represented by government and industry actions that don’t necessarily mirror consumer or public preference, but instead are economically viable. Whether it’s often advocated for or not, above all else the majority of the public wants inexpensive food, and that benefit often outweighs other consumer preferences (though not always). An interesting examination of the public perception of badgers is discussed within this controversy, and this argument can also apply to other similar situations we have seen over the years. BBC explored the role of badgers in popular children’s stories, and related them to other species that receive special protection even if they are not endangered. An example from the states would be our attachment to wild horses as an icon of America, and some of the debates we’ve seen surrounding not only control of wild horses, but within discussions on using horses for food. Kevin Pierce from the article sums this feeling up well:

“It’s an image issue. A lot of farmers like badgers but we also want to control the disease. If your vector spreading TB was a rat, I’m sure that there’d be no problem for farmers in securing a license to take action.”

The Government

Tasked with the burden of trying to please everyone, the federal government often responds to the loudest collective voice along with their own advisers, analysts, and ethics. In this case, we do know that the government has moved forward with culling as they have in the past. Evaluating the motivation behind these decisions is an endless discussion, whether it’s a working system or corrupt is beyond the scope of this post. Feel free to express your opinions on the process in the comments below. The best I hope for is that while looking out for my interests, my officials attempt to remain objective, and speaking of objectivity…

The Scientific Community

I’ve left us for last. The example of objectivity and a lens of evidence to weigh a cost-benefit analysis of the issue not directed by personal interests, concepts of morality, or hidden goals. Or so we would hope. As a realistic scientist who has read a lot of peer-reviewed research, I know that we are never truly objective. All funding comes from somewhere, we interpret our own results, and while we try as hard as we can to be objective, there is no perfect experimental design immune to bias. However, as creator of this site, I obviously hold research in high esteem, so lets look at some of the literature regarding the effectiveness of badger culling in curbing the spread of bovine TB.

According to the sources I found, it appears that badger culling does have a positive effect on the rates of bovine tuberculosis, but strictly within the areas the culling occurs. There’s a beneficial cumulative effect after several years of a culling program (in the reduction of detrimental effects in surrounding areas), but it isn’t necessarily lasting, cost-effective, or repeatable in different situations. The consensus amongst several studies is that localized culling actually increases TB rates in the surrounding areas, due to the displacement of normally local badger populations, and additional factors that we don’t fully understand. Given these effects, there seems to be a general consensus in the literature I viewed that at best badger culling is not a cost effective way to reduce TB transmission, and at worst contributes to the spread of disease.

Culling programs always have fierce opposition from many sources, whether it be culling sea lions to protect Columbia river salmon, culling grey wolves to protect livestock, or culling tame geese that are causing damage to city parks. There are serious concerns from conservationists and animal activists about the effectiveness of such programs that can be well founded, and the controversy surrounding badger culling in the United Kingdom is a clear example  of why these decisions would be more effective if they are backed by empirical research and economic analysis before being presented as a moral dilemma.

ResearchBlogging.org
Donnelly CA, Woodroffe R, Cox DR, Bourne J, Gettinby G, Le Fevre AM, McInerney JP, & Morrison WI (2003). Impact of localized badger culling on tuberculosis incidence in British cattle. Nature, 426 (6968), 834-7 PMID: 14634671
Donnelly CA, Wei G, Johnston WT, Cox DR, Woodroffe R, Bourne FJ, Cheeseman CL, Clifton-Hadley RS, Gettinby G, Gilks P, Jenkins HE, Le Fevre AM, McInerney JP, & Morrison WI (2007). Impacts of widespread badger culling on cattle tuberculosis: concluding analyses from a large-scale field trial. International journal of infectious diseases : IJID : official publication of the International Society for Infectious Diseases, 11 (4), 300-8 PMID: 17566777
Donnelly CA, Woodroffe R, Cox DR, Bourne FJ, Cheeseman CL, Clifton-Hadley RS, Wei G, Gettinby G, Gilks P, Jenkins H, Johnston WT, Le Fevre AM, McInerney JP, & Morrison WI (2006). Positive and negative effects of widespread badger culling on tuberculosis in cattle. Nature, 439 (7078), 843-6 PMID: 16357869

What your intoor/outdoor cat could be sharing with the local pumas

Image from Pet-peeves.org

Generally not small talk, though I imagine they might be interested in the projections for this year’s salmon run (pause for polite awkward laughter). A new article from PLoS ONE has been discussed, implying that, while direct contact may not be routine, exchange of disease between domesticated and wild cats may be fairly common.

The group of scientists involved were examining the occurrence of Toxoplasmosis, Bartonellosis, and FIV. They went out to rural Colorado and California and trapped 260 bobcats and 200 pumas to take blood samples. They also collected blood from 275 domestic cats that lived in the areas investigated, most of whom were feral and free ranging. They tested the serum of these animals for antigens that indicated infection, and ran a statistical analysis that looked at the prevalence of each disease compared to factors such as age, location, sex, and species. The data was collected over a ten year period.

I’m not going to discuss much of the wild species data, but there are some important trends for those interested in pet health, though it’s not very surprising. The researchers revealed that the prevalence of disease was much higher in domestic animals near urban areas than in those rural. This indicates that even though there is a larger number of hosts and vectors (fleas and ticks primarily) in rural areas, clearly the higher concentration of animals in urban areas and increased interactions between domestic cats and wild species (created by human expansion into undeveloped areas) plays a much larger role in the transmission of infectious diseases.

There are also some cool snippets about FIV here as well. The discussion mentions that male cats were slightly more likely to be carrying FIV, which is to be expected due to the higher rate of sex hormone driven behaviors such as roaming and fighting. The FIV strains found in the wild felids also had greater genetic diversity, suggesting that the FIV we know and vaccinate for may be a relatively new disease (at least in comparison to wild FIV serovars). The data shows that the highest combination of pathogens that the domestic cats tested positive for were FIV and Bartonellosis, and the authors mention that because Bartonellosis and FeLV infection have also been correlated in other studies, this data implies that there may be a relationship between the three. However, that relationship may be as simple as having similar risk factors.

The take home message of the study is that wild populations can serve as an important reservoir for multiple zoonotic diseases, and that exposure to this reservoir is mediated by the domestic cats we frequently come into contact with. Just one more reason to think about convincing your kitten that the outside world is scary, and that they don’t necessarily have to go check out what the big cats are doing. Feel free to check out the paper yourself, its light on jargon and easy to read. I’m actually a little disappointed to see that they collected this data over a ten year span, but chose not to do any comparison of the rates of disease from year to year. It would have been interesting to see how climate differences and population growth may have affected the number of vectors and associated risk. Additionally, because all of the samples were collected opportunistically when wild animals were trapped for other non-related studies, there was no way to ensure sampling without replacement, which may have skewed the data.

ResearchBlogging.org
Sarah N. Bevins1*, Scott Carver2, Erin E. Boydston, Lisa M. Lyren, Mat Alldredge, Kenneth A. Logan, Seth P. D. Riley, Robert N. Fisher, T. Winston Vickers, Walter Boyce, Mo Salman, Michael R. Lappin, Kevin R. Crooks, & Sue VandeWoude (2012). Three Pathogens in Sympatric Populations of Pumas, Bobcats, and Domestic Cats: Implications for Infectious Disease Transmission PLoS ONE