Animal Welfare and Food Safety
By F. Bailey Norwood, Ph.D., and Jayson L. Lusk, Ph.D.
The 2011 movie Contagion tells a fictional story of how globalization and ease of travel can produce fast-spreading pandemics, killing people more quickly than government authorities can respond. The culprit for this Hollywood illness is a new virus of unknown origin, resistant to all known vaccines.
It isn’t until the end of the movie that the origin of the killer is revealed. It all began (spoiler alert) with a bat carrying a piece of banana to a hog farm. The bat manages to fly into an enclosed building where sad-looking hogs are housed in tight quarters. The bat drops the banana on the floor, where it is quickly eaten by a hog. Presumably, the banana or the bat carried a virus, which spread to the pigs. One of the pigs is then slaughtered, and a man carving the meat in China fails to wash his hands before he shakes the hand of a character played by Gwyneth Paltrow, who then travels back to the United States where she dies—but not before sickening many others.
The premise of Contagion is that raising hogs on “factory farms” encourages the emergence of deadly pathogens. How accurate is this caricature? In reality, a bat is more likely to drop food near hogs or chickens raised outdoors. Would the movie have been more realistic if the bat infected a pig raised on an organic farm, a farm where animals roamed “free range,” or a farm owned by a small producer slaughtering his own animals and selling locally? Or would a more accurate film show the bat shedding feces near a field of broccoli, sickening people consuming fruits and vegetables instead of meat? Is it true that animal welfare and food safety are trade-offs, or are they instead complements? When we pay more for humane meat, are we also getting safer food or are we accepting greater risk? These are the questions we investigate in the present article.
Animals versus Plants
Before discussing the relationship between animal welfare and food safety, it is useful to step back and look at the big picture. If asked, many people would probably consider foods derived from animals to be less safe than those derived from plants. Yet, news stories routinely report outbreaks from jalapeños, melons, tomatoes and lettuce. If a vegan is just as likely to suffer from a foodborne illness as a meat eater, then the discussion of animal welfare and food safety takes a different tone.
Which is more dangerous to consume: plant or animal? One recent survey of food safety experts suggests a belief that eating produce is riskier than eating pork, beef, eggs, poultry or dairy. Part of this assessment, however, is due to aggregation. All fruits and vegetables are grouped into one category; different types of meats are counted separately.
More insight can be gained by investigating actual outbreak data. Table 1 reports the results of an analysis utilizing 10 years of U.S. Centers for Disease Control and Prevention outbreak data (from 1999 to 2008) to calculate the number of annual illnesses and deaths attributable to different foods as well as the economic costs of the illnesses (medical costs, productivity losses and estimates of the value of mortality). Even if poultry alone is compared with all produce, poultry results in more illnesses and deaths. Beef causes more illnesses but fewer deaths than pork, and eggs appear safer than any of the meats. Vegan advocates claiming that animal-derived foods are riskier to consume4 apparently have some evidence to support them. Fewer illnesses or deaths result from the consumption of bakery and produce than meats, eggs and dairy. Moreover, many of the illnesses from produce originate from livestock and spread to plants through the wind or poor manure treatment. The Center for Science in the Public Interest calculates that roughly one-third of all foodborne illnesses from a plant source is of animal origin, whether it be livestock or wildlife.[4, 6]
Investigating the sources of foodborne illnesses also helps us understand the link between animal welfare and food safety. If the most humanely produced foods are also the safest, perhaps this correlation suggests causation? The comparisons in Table 1 are in some ways unfair, though. Americans today consume more poultry than any other meat product, so even if a meal containing poultry is safer than beef or pork, more illnesses may result from poultry consumption simply because chicken is consumed on such a large scale. Using the data in Table 1 to claim poultry is risky is a bit like claiming roads in Texas are more dangerous than those in Wyoming simply because more Texans die in car crashes—however, the population size of the two states would seem the more logical culprit. Analogously, the volume and value of the food should be taken into consideration when comparing risks. Consumers might voluntarily accept riskier food if they value it more.
For a better comparison, we took the illness values in Table 1, converted them into percentages and divided the percentages by the amount of money a typical household spends on each food type. What results is an index of food risk accounting for both consumption and value of the foods. As shown in Figure 1, meats remain more than two times riskier than produce. The risks associated with eggs relative to other foods, however, are greatly increased compared with Table 1. Eggs may not cause more illnesses than produce overall, but for each dollar spent, they do. The risk from seafood also rises, and though produce may cause more illnesses than beef overall, each dollar spent on beef is more likely to get you sick than a dollar spent on produce. As in Table 1, poultry remains the riskiest food to consume.
What does Figure 1 tell us about the relationship between animal welfare and food safety? The actions of animal advocacy organizations suggest that they believe animal suffering to be especially profound on egg and pork farms, and for welfare to be relatively higher on beef and dairy farms. Clearly, food safety is not determined solely by animal welfare, as beef is less risky than eggs but about the same as pork. Poultry is much riskier than pork or eggs, yet we believe welfare to be considerably higher for broilers than hogs or layers. It is clear from Figure 1 that food safety must be influenced by many other factors in addition to animal welfare.
Still, there are many reasons to believe a welfare-safety link exists. This means that when we debate how animals should be treated, we are also debating the safety of our food. In the next section, we explore the ways in which animal well-being can be improved and the concomitant change in food safety we should expect.
Natural Animal Behaviors and Safe Food
Animal scientists and consumers often have different notions about what makes for a happy animal. According to many animal scientists in the U.S., high welfare primarily requires a clean, healthy environment where animals are provided with all their physiological needs, are provided adequate shelter and are protected from predators. According to this perspective, there are synergies between animal welfare and food safety, as both can be provided in the same environment.
According to our survey work, roughly 40 percent of Americans agree with this perspective (another 11 percent say they care little about the well-being of farm animals). This leaves 48 percent of Americans who disagree with our depiction of the animal scientists’ view, and believe animals must also be allowed to exhibit natural behaviors if they are to experience high levels of well-being. These behaviors include the ability to move around freely, access to the outdoors and the opportunity to socialize with animals of their species.
Allowing free expression of natural animal behaviors should reduce stress in the animal, and as a consequence may (but may not) reduce the shedding of pathogens. These improvements, however, often come at a cost. Layers raised in a cage-free setting can suffer from injury by other hens, creating stress and even death. Sows moved from a gestation stall into a group pen can now turn around freely, but may turn to encounter an aggressive sow—again, creating stress. We once visited a free-range egg farm where the birds had access to pasture but were continually preyed upon by hawks—this fear would certainly create stress. While there is no guarantee that these improvements are good for animal welfare or food safety, most published research contends that replacing battery cages with cage-free systems (or enhanced cages) and converting gestation stalls to group pens improve animal welfare. And if animal welfare is improved, it is reasonable to believe stress and the shedding of pathogens are lowered—but there are no guarantees. We once talked to an egg farmer raising both caged and cage-free eggs, and his employees would not eat the eggs from the cage-free system, believing the difficulty of identifying and culling sick hens in a cage-free system makes the average egg more risky to eat.
The relationship between animal well-being and food safety becomes more complex when a farm uses a free-range system, where animals have access to both comfortable shelter and the outdoors. Hogs love mud, and mud is rarely sterile. Hogs eagerly root and engage in continuous social interactions. While such a “natural” setting is likely to increase animal well-being in one dimension, it may also make a hog sick, as hogs can more easily come into contact with the feces of other hogs and wildlife, as well as a broad array of worms and other parasites not normally found on a concrete floor. Increased prospects for disease, infection and parasites can turn a happy hog into a sick hog.
One of the original motivations for confining hogs to concrete floors inside buildings (i.e., today’s conventional hog farm) was to separate hogs from parasites and pathogens. Lungworms were once found in at least one-half of hogs in the 1940s, but today the parasite is a rarity. The same can be said for kidney worms. Pork was once thought dangerous to eat if undercooked. The threat was trichinosis—another threat that is today almost nonexistent.[15, 16] Farmers once deliberately raised hogs in the same pastures as cows, knowing hogs would eat undigested grain from cow feces. Chickens would do the same. An egg study found greater Salmonella contamination in free-range eggs, probably due to the easy access rodents have to the chicken feed. Not only do the rodents defecate in the chicken feed, but “mice droppings can be actively sought out by birds when mixed in the feed and or bedding because of their seed-like size and appearance.” However pleasant the small, diversified farm seems, most consumers don’t like to eat animals that ate the feces of other animals. Farmers did not confine animals to cramped cages on hard floors out of malevolence but to reduce parasites and disease. Animal welfare may be compromised by confinement, but animal health is improved, and with it food safety.
Comparing hog health today with 70 years ago isn’t an entirely fair comparison. Given the scientific advancements in animal production since the 1940s, it might be possible to allow hogs outdoor access without the concomitant pathogens and parasites experienced by the 1940 farmer. Yet even today, research finds that hogs given outdoor access experience higher rates of Salmonella, Toxoplasma and Trichinella than hogs on conventional farms.[19, 20] In outdoor systems, Salmonella is spread through sows’ wallowing in the same mudhole, presenting a dilemma for farmers who want to produce safe pork in an outdoor environment.
Free-range systems for layers and broilers face similar problems. Some of these systems confine the birds at night in large cages on wheels, taking the birds to different locations where they may forage naturally. This more “natural” existence, however, brings the birds in contact with the feces of deer, rodents and feral hogs, and because these wild animals can contaminate vegetables with Salmonella, then free-range poultry can be contaminated also. Free-range poultry often share the pasture with cattle, sheep or goats, allowing cross-contamination between species.
Scientists have measured Salmonella prevalence in poultry meat derived from pasture and organic systems, and tend to find the rates are comparable or higher than in conventionally produced poultry meat. Another study tested broiler chickens for Salmonella and found that 60 percent from an organic-free range producer tested positive, leading them to conclude, “Consumers should not assume that free-range or organic conditions will have anything to do with the Salmonella status of the chicken.” While organic meats are generally more contaminated with pathogens, those pathogens are less likely to be resistant to antibiotics, so it is difficult to say whether organic meats are riskier to eat. The point is that one cannot assume organics are safer.
Other articles on the welfare-safety link considered animal treatment before slaughter, so we concentrate on other production stages in this paper. Contrary to other discussions on this issue, we also ignore antibiotic resistance in livestock. There is a widely held notion that animals can be raised in cramped confinement only if they are routinely fed antibiotics to prevent the spread of disease. This does not seem to be the case. Our European contacts testify that the ban on antibiotics in Sweden, Denmark, the United Kingdom and other nations has not altered the production systems used.
Perceptions of food safety are just as important as actual safety, insofar as driving consumer choice and retail sales. Food producers face a daunting challenge. Not only must they raise live animals that are naturally covered with bacteria, viruses and prions, and then transform the animal products into safe foods, producers must convince the public that the food is safe. Their success is already astonishing if not publicly acknowledged—for every 39 million Americans, only 1 will die of a food-related illness, and he or she is typically very old, very young or has a compromised immune system. However, food activists will go to great lengths to convince the public their food is unsafe, so livestock industries must not only battle bacteria and germs but sensationalized information as well.
Despite developments in traceability systems, it is often impossible to precisely determine what actually causes a food to become contaminated. The technology exists to trace meat back to the farm using meat’s DNA, but even then it is difficult to determine exactly what caused the contamination in the first place, or how the pathogen evaded the myriad precautions employed at modern slaughtering facilities. This, however, does not let the farmer off the hook.
When Food, Inc. told the true story of a young boy who died from infection with Escherichia coli O157:H7, the documentarians blamed the illness on the poor conditions in which the cattle were raised and on the feeding of corn instead of grass. The filmmakers knew viewers would disapprove of the cattle being “ankle-deep in their manure, all day,” and thus the film gave the impression that cattle in feedlots are sad, and that sadness translates to human death. Other people have died from E. coli infection, but their deaths were not sensationalized by documentaries. Three people died from contaminated organic spinach in 2006. The bacterium could have been carried by the wind or water from a nearby farm to where the spinach was growing, but it could also have been the cattle manure used as fertilizer.
There was no documentary exploiting the three deaths in an effort to “expose” the dangers of organic farming. Nor do food activists criticize those who oppose irradiation—perhaps the most effective method of killing pathogens. Why the double standard? We believe much of it has to do with activist and consumer perceptions. Because livestock industries use large-scale, factory-like methods of production, and because the processing and distribution stage are dominated by large corporations, food activists believe these corporations are motivated largely by greed for immediate profits, even at the expensive of consumer health.
While many readers of this article will rightly balk at this caricature of meat production industries, it must be recognized that this is the view subtly expressed by food documentaries such as Food, Inc., Fresh or Forks Over Knives. As a result, in this sensationalistic atmosphere, the livestock industry is likely to be deemed guilty in every outbreak of foodborne illness until proven innocent. The apparent anti-industry bias also means that illness traceable to organic or local food producers will probably be chalked up to an innocent mistake.
The cattle industry’s past mistake in feeding rendered carcasses to cattle continues to haunt it, allowing documentaries like Fresh to use this example as proof that “factory farmers” will cut every corner and do anything to animals that increases short-run profits. Many “so-called” experts once thought this feeding practice to be scientifically sound. It wasn’t. The result was mad cow disease, and subsequent scientific “experts” since then have been understandably viewed with greater skepticism. If farmers had abstained from using a feed that they knew most people would find repugnant—and about which there was still some scientific doubt—the reputation of livestock industries might not have been tarnished.
The public knows little about livestock agriculture and so will infer the integrity of an industry from a farm’s appearance, in addition to what they read on Grist or see on Real Time with Bill Maher. If a farmer prevents a sow from turning around because it saves money, will the farmer also cut corners on food safety to save money? If a farmer crams a hen into a small cage with four other hens to boost production, would he be unwilling to lower output by removing sick hens from the food production channel? If organic farmers are not held accountable for the foodborne illness they cause simply because they are trying to raise ethical food, livestock producers will be held accountable for the illness they do and do not cause because, in the public’s perception, they seem to be acting unethically toward hens and hogs.
In a telephone survey we conducted with the American Farm Bureau Federation, 78 percent of Americans agreed with the statement, “Animals raised under higher standards of care will produce safer and better tasting meat.”7 There is no separation between perceived animal welfare and perceived food safety. While the first priority of producers of meat, eggs and dairy products is ensuring food is safe, in reality, safe food only has value if it is also perceived to be safe. Let there be no doubt, regardless of whether higher animal welfare creates safer food, food from happy animals will be considered safer.
In general, production systems that provide animals outdoor access have the potential to expose animals to pathogens, viruses and other parasites. In some cases, it appears that this potential is realized. However, in other cases, perhaps due to effects of lower stocking densities or better managerial competence, the risks can be alleviated or even reversed. In short, animal housing conditions are but one factor, and a far from deciding factor, affecting food safety.
However, consumers don’t always see it that way. Consumers conflate perceptions of safety with perceptions of animal welfare. They are not necessarily irrational in doing so, as care and managerial competence in one domain are likely to be correlated with meticulousness in another. Food safety is hard to observe on the farm, especially for the average consumer who doesn’t know Salmonella from Campylobacter. However, through pictures and videos, consumers can readily observe tidiness and stocking density, and the ability of animals to exhibit natural behaviors. Although these do not necessarily relate to food safety, it is not wholly unreasonable for consumers to presume that someone who cares about the one cares about the other. If we are really concerned about the volume of pathogens people actually consume, then we must also be aware of their perceptions—which drive what they put in their mouths.
F. Bailey Norwood, Ph.D., (right) is an associate professor in the Department of Agricultural Economics at Oklahoma State University, where he researches farm animal welfare issues, survey methods and teaching effectiveness.
Jayson L. Lusk, Ph.D., (left) currently serves as professor and Willard Sparks Endowed Chair in the Department of Agricultural Economics at Oklahoma State University. After earning a B.S. in food technology from Texas Tech University in 1997, he received a Ph.D. in agricultural economics from Kansas State University in 2000.
1. Shamberg, S.S. and G. Jacobs [producers]. Soderbergh, S. [director]. Burns, S.Z. [writer] 2011. Contagion [film]. Warner Brothers Pictures [distributor].
2. Hoffman, S. 2009. Knowing which foods are making us sick. Choices 2nd Quarter. 24(2).
3. Batz, M.B., S. Hoffmann and J.G. Morris Jr. 2012. Ranking the disease burden of 14 pathogens in food sources in the United States using attribution data from outbreak investigations and expert elicitation. J Food Prot 75(7):1278–1291.
4. Jacobson, M.F. and Staff of the Center for Science in the Public Interest (CSPI). 2006. Six arguments for a greener diet. Center for Science in the Public Interest.
5. Matthews, K.R. 2009. The produce contamination problem: Causes and solutions, eds. G.M. Sapers, E.B. Solomon and K.R. Matthews. Burlington, MA: Elsevier Inc.
6. We contacted the CSPI to discuss this calculation and believe their assumption of one-third is reasonable.
7. Norwood, F.B. and J.L. Lusk. 2011. Compassion, by the Pound. New York: Oxford Press.
8. Expenditures on beef, pork, poultry and other meats (as a single group) are $842 per year. The numbers for dairy, fruits and vegetables, eggs, and fish and seafood are $481, $842, $60 and $120, respectively. Numbers for beef, pork and poultry are $300, $180 and $180, respectively. These numbers are taken from www.bls.gov/cex/home.htm#publications.
9. Prickett, R.W., F.B. Norwood and J.L. Lusk. 2010. Consumer preferences for farm animal welfare: results from a telephone survey of U.S. households. Animal Welfare 19:335–347.
10. Gallaway, T.R., J.L. Morrow, T.S. Edrington, K.J. Genovese, S. Dowd, J. Carroll, J.W. Dailey, R.B. Harvey, T.L. Poole, R.C. Anderson and D.J. Nisbet. 2006. Social stress increases fecal shedding of Salmonella Typhimurium by early weaned piglets. Current Issues Intest Microbiol 7:65–72.
11. Brown-Brandl, T.M., E.D. Berry, J.E. Wells, T.M. Arthur and J.A. Nienaber. 2009. Impacts of individual animal response to heat and handling stresses on Escherichia coli and E. coli O157:H7 fecal shedding by feedlot cattle. Foodborne Pathog Dis 6(7):855–864.
12. Rostagno, M. 2009. Can stress in farm animals increase food safety risk? Foodborne Pathog Dis 6(7):767–776.
13. De Mol, R.M., W.G.P. Schouten, E. Evers, H. Drost, H.W.J. Houwers and A.C. Smits. 2006. A computer model for welfare assessment of poultry production systems for laying hens. Netherlands J Ag Sci 54:157–168.
14. Bracke, M.B.M., B.M. Spruijt, J.H.M. Metz and W.G.P. Schouten. 2002. Decision support system for overall welfare assessment in pregnant sows: A model structure and weighting procedure. J Animal Sci 80:1819–1834.
15. Welshans, K. 2011. Modern hog production results in safer pork. Feedstuffs 14.
16. Davies, P.R. 2011. Intensive swine production and pork safety. Foodborne Pathog Dis 8(2), DOI:10.1089/fpd.2010.0717.
17. Davis et al. 1928. Livestock enterprises. Chicago: J.B. Lippincott Company, pp. 284 and 391.
18. Kinde, H., D.H. Read, R.P. Chin, A.A. Bickford, R.L. Walker, A. Ardans, R.E. Breitmeyer, D. Willoughby, H.E. Little, D. Kerr and I.A. Gardner. 1996. Sewage effluent: Likely source of Salmonella enteritidis, phage type 4 infection in a commercial chicken layer flock in southern California: Bacteriologic and epidemiologic findings. Avian Dis 40(3):665–671.
19. It should be noted these outdoor systems also did not receive regular supplements of antibiotics at the subtherapeutic level. Most outdoor production systems do not administer growth hormones or antibiotics to healthy hogs, as being able to label pork “antibiotic-free” and “hormone-free” allows retailers to charge higher premiums.
20. Gebreyes, W.A., P.B. Bahnson, J.A. Funk, J. McKean and P. Patchanee. 2008. Seroprevalence of Trichinella, Toxoplasma and Salmonella in antimicrobial-free and conventional swine production systems. Foodborne Pathog Dis 5(2):199–203, DOI: 10.1089/fpd.2007.0071.
21. Callaway, T.R., J.L. Morrow, A.K. Johnson, J.W. Dailey, F.M. Wallace, E.A. Wagstrom, J.J. Mcglone, A.R. Lewis, S.E. Dowd, T.L. Poole, T.S. Edrington, R.C. Anderson, K.J. Genovese, J.A. Byrd, R.B. Harvey and D.J. Nisbet. 2005. Environmental prevalence and persistence of Salmonella spp. in outdoor swine wallows. Foodborne Pathog Dis 2(3):264–273.
22. Hanning, I.B., J.D. Nutt and S.C. Ricke. 2009. Salmonellosis outbreaks in the United States due to fresh produce: Sources and potential intervention measures. Foodborne Pathog Dis 6(6), DOI:10.1089/fpd.2008.0232.
23. Melendez, S.N., I. Hanning, J. Han, R. Nayak, A.R. Clement, A. Wooming, P. Hererra, F.T. Jones, S.L. Foley and S.C. Ricke. 2010. Salmonella enterica isolates from pasture-raised poultry exhibit antimicrobial resistance from class I integrons. J Appl Microbiol, DOI:10.1111/j.1365-2672.2010.04825.x.
24. Bailey, J.S. and D.E. Cosby. 2005. Salmonella prevalence in free-range and certified organic chickens. J Food Prot 68(11):2451–2453.
25. Van Loo, E.J., W. Alali and S.C. Ricke. 2012. Food safety and organic meats. Ann Rev Food Sci Technol 3:203–225.
26. Voogd, E. 2009. Does animal welfare affect food safety? Food Safety Magazine February/March 42–53.
27. This information is based on an e-mail exchange with Frank Aarestrup, whom we consider the most informed European on antibiotic use in agriculture.
28. Coclanis, P.A. 2011. Food is much safer than you think. The Wall Street Journal. June 14, A13.
29. Felberbaum, M. 2011. New frontier in food safety: meat traceable by DNA. The Commercial Appeal May 31.
30. Chew, W.-P. 2008. Correlation of in-field survival of Escherichia coli O157:H7 with rainfall, relative humidity and soil moisture. Master’s thesis. Department of Food Science. Oklahoma State University.