Antibiotic use in livestock

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Antibiotic use in livestock is the use of antibiotics for any purpose in the husbandry of livestock, which includes not only the treatment or prophylaxis of infection but also the use of subtherapeutic doses in animal feed and/or water[1] to promote growth and improve feed efficiency in intensive animal farming. Antimicrobials (including antibiotics and antifungals) and other drugs are used by veterinarians and livestock owners to increase the growth rates of livestock, poultry, and other farmed animals, although these pharmaceuticals do not have to be administered by a veterinarian. The use of some drugs is banned in some countries, most notably Denmark, due to food contamination or concern about increasing antibiotic resistance, its link to antibiotic-resistant infections in humans,[2] and what some consider antibiotic misuse. Other drugs may be used only under strict limits, and some organizations and authorities seek to further restrict the use of some or all drugs in animals. Other authorities, such as the World Organization for Animal Health, say that "Without antibiotics there would supply problems of animal protein for the human population".[3]

However, in 2013 the CDC finalized and released a report detailing antibiotic resistance and classified the top 18 resistant bacterium as either being urgent, serious or concerning threats (CDC). Of those organisms, three (CDIFF, CRE and Neisseria gonorrhoeae) have been classified as urgent threats and require more monitoring and prevention (CDC). In the US alone, more than 2 million people are diagnosed with antibiotic resistant infections and over 23,000 die per year due to resistant infections (CDC).[4]

History of the practice

In 1910 in the United States, a meat shortage resulted in protests and boycotts.[5][6] After this and other shortages, the public demanded government research into stabilization of food supplies.[5] Since the 1900s, livestock production on United States farms has had to rear larger quantities of animals over a short period of time to meet new consumer demands. Factory farming or the use of high intensity feedlots originated in the late 19th century when advances in technology and science allowed for mass production of livestock. Global agriculture production doubled four times within 1820 and 1975, feeding one billion in 1800 and up to 6.5 billion in 2002.[7] Along with the new large animal densities came the threat of disease, therefore requiring a greater disease control of these animals. In 1950, a group of United States scientists found that adding antibiotics to animal feed increases the growth rate of livestock.[5][8] American Cyanamid published research establishing the practice.[5]

By 2001 this practice had grown so much that a report by the Union of Concerned Scientists found that nearly 90% of the total use of antimicrobials in the United States was for non-therapeutic purposes in agricultural production.[9]

Antibiotics have an appropriate place in the humane care of illness in livestock, when they reduce the suffering of a sick animal or control the spread of the illness to nearby animals.[10] Thus, ideas that they should never be used in livestock husbandry are misguided.[10] Instead, the goal is to prevent the allowance of preventive use from being distorted into routine use, constituting overuse.[10]

Drugs and growth stimulation

Certain antibiotics, when given in low, sub-therapeutic doses, are known to improve feed conversion efficiency (more output, such as muscle or milk, for a given amount of feed) and/or may promote greater growth, most likely by affecting gut flora.[11]

Antibiotic Growth Promoters used in Livestock Production
drug class effect
Bambermycin increase feed conversion ratio and weight gain in chickens, beef cattle, swine, and turkeys.[12][13]
Lasalocid Ionophore increase feed conversion ratio and weight gain in beef cattle.[12][13]
Monensin Ionophore increase feed conversion ratio and weight gain in beef cattle and sheep; promotes proficient milk production in dairy cows.[12][13]
Salinomycin Ionophore increase feed conversion ratio and weight gain.[13]
Virginiamycin peptide increase feed conversion ratio and weight gain in chickens, swine, turkeys, and beef cattle.[12][13]
Bacitracin peptide increase weight gain and feed conversion ratio in chickens, turkeys, beef cattle, and swine; promotes egg production in chickens.[12][13]
Carbadox increase feed conversion ratio and weight gain in swine.[12]
Laidlomycin increase feed conversion ratio and weight gain in beef cattle.[12]
Lincomycin increase feed conversion ratio and weight gain in chickens and swine.[12]
Neomycin/ oxytetracyclinee increase weight gain and feed conversion ratio in chickens, turkeys, swine, and beef cattle.[12]
Penicillin increase feed conversion ratio and weight gain in chickens, turkeys, and swine.[12]
Roxarsone increase feed conversion ratio and weight gain in chickens and turkeys.[12]
Tylosin increase feed conversion ratio and weight gain in chickens and swine.[12]

Use in different livestock

In swine production

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Main article: Subtherapeutic antibiotic use in swine

Lua error in package.lua at line 80: module 'strict' not found. The use of antibiotics to increase the growth of pigs is most studied of all livestock. This use for growth rather than disease prevention is referred to as subtherapeutic antibiotic use. Studies have shown that administering low doses of antibiotics in livestock feed improves growth rate, reduces mortality and morbidity, and improves reproductive performance. It is estimated that over one-half of the antibiotics produced and sold in the United States is used as a feed additive. Although it is still not completely understood why and how antibiotics increase the growth rate of pigs, possibilities include metabolic effects, disease control effects, and nutritional effects.[14] While subtherapeutic use has many benefits for raising swine, there is growing concern that this practice leads to increased antibiotic resistance in bacteria. Antibiotic resistance occurs when bacteria are resistant to one or more microbial agents that are usually used to treat infection. There are three stages in the possible emergence and continuation of antibiotic resistance: genetic change, antibiotic selection, and spread of antibiotic resistance.[15]

In production of other livestock

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File:2789694551 37beafc438 b - Grass Fed Beef - Ryan Thompson - Flickr - USDAgov.jpg
Organic beef comes from cattle who have not been fed antibiotics.

Regulatory context

The use of drugs in food animals is regulated in nearly all countries. Historically, this has been to prevent alteration or contamination of meat, milk, eggs and other products with toxins that are harmful to humans. Treating a sick animal with drugs may lead to some of those drugs remaining in the animal when it is slaughtered or milked. Scientific experiments provide data that shows how long a drug is present in the body of an animal and what the animal's body does to the drug. Of particular concern are drugs that may be passed into milk or eggs. By the use of 'drug withdrawal periods' before slaughter or the use of milk or eggs from treated animals, veterinarians and animal owners ensure that the meat, milk and eggs is free of contamination.

These restrictions include not only poisons or drugs (such as penicillin) which may result in allergic reactions but also contaminants which may cause cancer. It is illegal in the USA to administer drugs or feed substances to animals if they have been shown to cause cancer.

One of the main restrictions is the amount that is administered to animals in the industry. These drugs should be administered to healthy livestock at a low concentration of 200 g per ton of feed. The amount distributed is also altered throughout the lifespan of livestock in order to meet specific growth needs.[16]

Legality of the use of specific drugs in animal medicine varies according to location.

Just as in human medicine, some drugs are available over the counter and others are restricted to use only on the prescription of a veterinary physician. In the USA, the Food and Drug Administration (FDA) requires specific labels on all drugs, giving directions on the use of the drug. For animals, this includes the species, dose, reason for giving the drug (indication) and the required withdrawal period, if any. Federal law requires laypersons to use drugs only in the manner listed. Veterinarians who have examined an animal or a herd of animals may issue a replacement label, giving new directions, based on their medical knowledge. It is illegal in the USA for any layperson to administer any drug to a food animal in a way not specific to the drug label. Over-the-counter drugs which may be used by laypersons include anti-parasite drugs (including fly sprays) and antimicrobials. These drugs can be applied as sprays, creams, injections, oral pills or fluids, or as a feed additive, depending on the drug and the label.

In December 2013, the FDA updated its regulations to try to begin reducing use of antibiotics for growth enhancement.[17] Significant lobbying comes from all directions, from those against tighter regulation to those who complain it doesn't go far enough.[18]

Currently few policies, regulations and laws exist that promote limitation of antibiotic use on factory farms. In addition, few policies are being created that call for this decrease in antibiotic use. However, numerous state senators and members of congress showed support for the Preventing Antibiotic Resistance Act of 2015 (PARA) and the Preservation of Antibiotics for Medical Treatment Act of 2013 (PAMTA). These acts proposed amendments be made to the Federal Food, Drug and Cosmetic Act which would limit and preserve the use of antibiotics for medically necessary situations. Both of these bills died in Congress in 2015.[19]

Administering drugs

Lua error in package.lua at line 80: module 'strict' not found.Drugs can be administered to animals in a variety of means, just as with humans. Among these are topical (on the skin), by injection (including intravenous, subcutaneous, subcutaneous implants, intramuscular and intraperitoneal), and orally.[20] Oral drugs can be in pill or liquid form, or can be given by mixing with feed or drinking water.[20] The appropriate route for treatment depends on the specific case and can vary by: illness, severity of illness, selected drug, age or condition of the animal, species of the animal, type of housing and other factors.[20] For animals that are not regularly fed a concentrated feed or which can be handled repeatedly, a slow-release injection might be the most appropriate. Some drugs are not available or appropriate in this form and should be delivered orally. For animals that are fed regularly (rather than grazing freely) or that can not be easily handled, the most appropriate means of administering the drug may be to include the drug in feed or water. This eliminates the stress of daily (or more frequent) handling of animals, which can make the animals more ill. Poultry are most commonly medicated in this fashion, as they are easily stressed to the point of dying. Administering the drug by feed also prevents injection wounds in animals.[20]

The timely administration of drugs is key to preventing animal suffering and economic loss to the farmer. Animals which are ill can infect other animals, and may become so ill that they can not be sold. A variety of techniques are used to monitor animals for illness so that they can be treated appropriately. Stress reduction, adequate nutrition, shelter, and quarantine of incoming stock are all important factors to promote growth and reduce illness and the need for active treatment.[20] The age and status of an animal is also important in determining correct treatment – a young animal or pregnant animal is at greater risk and are treated more aggressively than an older animal. Specifically in calves, the period in which they begin to separate from their mothers generates stress and makes them more susceptible to catching an infection like pneumonia. Antibiotics are commonly administered in the calves' feed during this time to fight the possibility of stress-induced infections.[20] Feed antibiotics are also used to prevent illnesses in calves caused by liver abscesses that develop during their last stages of growth.[20]

Use by country

European Union

The European Union (EU) in 1999 implemented an antibiotic resistance monitoring program and phase out plan for all antibiotic use by 2006.[21] Although the European Union banned the use of antibiotics as growth agents from 2006,[22] its use has not changed much until recently[citation needed]. In Germany, 1,734 tons of antimicrobial agents were used for animals in 2011 compared with 800 tons for humans. On the other hand, Sweden banned their use in 1986 and Denmark started cutting down drastically in 1994, so that its use is now 60% less.[23] In the Netherlands, the use of antibiotics to treat diseases increased after the ban on its use for growth purposes in 2006.[24] In 2011, the EU voted to ban the prophylactic use of antibiotics, alarmed at signs that the overuse of antibiotics is blunting their use for humans.[25]

United States

In 2011, a total of 13.6 million kilograms of antimicrobials were sold for use in food-producing animals in the United States,[26] which represents 80% of all antibiotics sold in the United States.[27] Of the antibiotics given to animals, 72 percent are "medically-important" drugs that are also used in humans, while the rest are drug classes like ionophores which are not used in human medicine.[26] Due to concerns about the overuse of antibiotics in food-producing animals, the U.S. Food & Drug Administration has implemented new industry guidelines that will restrict the use of medically-important drugs to uses "that are considered necessary for assuring animal health" and will require veterinary oversight.[28]

China

Of all countries, China produces and consumes the most antibiotics.[29]

Antibiotic use has been measured by checking the water near factory farms in China.[30][31] Measurements have also been taken from animal dung.[32]

Half of the antibiotics manufactured in China are used in the production of livestock.[33]

It was calculated that 38.5 million kg (or 84.9 million lbs) of antibiotics were used in China's swine and poultry production in 2012.[34]

India

In 2012 India manufactured about a third of the total amount of antibiotics in the world.[35]

Brazil

Brazil is the world's largest exporter of beef and the government regulates antibiotic use in the cattle production industry.[36]

Concerns about antibiotic resistance

More recently, there has been increased concern about the use of anti-microbials in animals (including pets, livestock, and companion animals) contributing to the rise in antibiotic resistant infections in humans. The use of antimicrobials has been linked to the rise of resistance in every drug and species where it has been studied, including humans and livestock. However, the role of antibiotic use in food animals – in contrast to the use of antibiotics in humans – in the rise of resistant infections in humans is in dispute. The use of antimicrobials in various forms is widespread throughout animal industry, and is presented as key to preventing animal suffering and economic loss. It is linked by some activist groups to animal welfare concern, large scale commercial agriculture, international food trade, agricultural protectionist laws, environmental protection (including climate change) and other topics, which make the aims of some groups on both sides of the debate difficult to untangle.

Around 70% of all antibiotics administered are used for livestock. Most of the drugs that are given to livestock are misused and incorporated into their diets daily for the purpose of weight gain or to treat illnesses. The overuse of the antibiotic in livestock is harmful to humans because it creates an antibiotic resistant bacteria that can be transferred through several different ways such as: raw meats, consumption of meats, or it can also be airborne. Waste from food-producing animals can also contain antibiotic-resistant bacteria and is sometimes stored in lagoons. This waste is often sprayed as fertilizer and can thus contaminate crops and water with the antibiotic-resistant bacteria.[37] Antibiotic resistance is harmful to humans because it makes them resistant to certain types of drugs for different diseases, and makes it harder for them to fight off infections. [38]

The World Health Organization has published a list of Critically Important Antimicrobials for Human Medicine with the intent that it be used "as a reference to help formulate and prioritize risk assessment and risk management strategies for containing antimicrobial resistance due to human and non-human antimicrobial use." [39]

Positions of advocates for restricting antibiotic use

The practice of using antibiotics for growth stimulation is problematic for these reasons:

  • it is the largest use of antimicrobials worldwide[40]
  • subtherapeutic use of antibiotics results in bacterial resistance[40]
  • every important class of antibiotics are being used in this way, making every class less effective[40]
  • the bacteria being changed harm humans[40]

Donald Kennedy, former director of the United States Food and Drug Administration, has said "There's no question that routinely administering non-therapeutic doses of antibiotics to food animals contributes to antibiotic resistance."[41] David Aaron Kessler, another former director of the FDA, said that "We have more than enough scientific evidence to justify curbing the rampant use of antibiotics for livestock, yet the food and drug industries are not only fighting proposed legislation to reduce these practices, they also oppose collecting the data."[42]

In 2013 the United States Centers for Disease Control and Prevention (CDC) published a white paper discussing antibiotic resistance threats in the US and calling for "improved use of antibiotics" among other measures to contain the threat to human health. The CDC asked leaders in agriculture, healthcare, and other disciplines to work together to combat the issue of increasing antibiotic resistance.[2]

Some scientists have said that "all therapeutic antimicrobial agents should be available only by prescription for human and veterinary use."[43]

The Pew Charitable Trusts have stated that "hundreds of scientific studies conducted over four decades demonstrate that feeding low doses of antibiotics to livestock breeds antibiotic-resistant superbugs that can infect people. The FDA, the U.S. Department of Agriculture and the Centers for Disease Control and Prevention all testified before Congress that there is a definitive link between the routine, non-therapeutic use of antibiotics in food animal production and the challenge of antibiotic resistance in humans."[44]

Moderate positions

The World Organisation for Animal Health has acknowledged the need to protect antibiotics but argued against a total ban on antibiotic use in animal production.[45]

Positions of advocates for status quo

In 2011 the National Pork Producers Council, an American trade association, has said "Not only is there no scientific study linking antibiotic use in food animals to antibiotic resistance in humans, as the U.S. pork industry has continually pointed out, but there isn't even adequate data to conduct a study."[46] The statement contradicts scientific consensus,[47] and was issued in response to a United States Government Accountability Office report that asserts "antibiotic use in food animals contributes to the emergence of resistant bacteria that may affect humans".[48]

The National Pork Board, a Government-owned corporation of the United States, has said that "the vast majority of producers use (antibiotics) appropriately."[49]

Effects of restricting antibiotic use

When government regulation restricts use of antibiotics the negative economic impact is not often considered.[50]

Regulation of antibiotics in livestock production would affect the business models of corporations including Tyson Foods, Cargill, and Hormel.[51]

Difficulties with determining relevant facts

It is difficult to set up a comprehensive surveillance system for measuring rates of change in antibiotic resistance.[52] The US Government Accountability Office published a report in 2011 stating that government and commercial agencies had not been collecting sufficient data to make a decision about best practices.[53]

Currently there is no regulatory agency in the United States that systematically collects detailed data on antibiotic use in humans and animals. It is not clear which antibiotics are prescribed for which purpose and at what time. Furthermore, the world has no surveillance infrastructure to monitor emerging antibiotic resistance threats. Because of these issues, it is difficult to quantify antibiotic resistance, to regulate antibiotic prescribing practices, and to detect and respond to rising threats.[2]

Specific resistance that has been identified and human impact

There have been many studies that document antibiotic resistant bacteria in livestock, though the impact of the different bacteria in humans is still undergoing research. At this time, the most well-documented impact on humans is foodborne gastrointestinal illness. In most cases, these illnesses are mild and do not require antibiotics; though if the infectious bacteria is drug-resistant, research has shown that these bacteria have increased virulence (ability to cause disease), leading to prolonged illness. Furthermore, in approximately 10% of cases, the disease becomes severe, requiring more advanced treatments. These treatments can take the form of intravenous antibiotics, supportive care for blood infections, and hospital stays, leading to higher costs and greater morbidity with a trend toward higher mortality. Severe disease with this outcome is more common with drug-resistant bacteria.[2][54] Though all people are susceptible, populations shown to be at higher risk for severe disease include children, the elderly, and those with chronic disease.[2][55][56]

Over the past 20 years, the most common drug-resistant foodborne bacteria in industrialized countries have been non-typhoidal salmonella and campylobacter. Research has consistently shown the main contributing factors are bacteria sourced in livestock.[54] One example of this was a 1998 outbreak of multidrug-resistant salmonella in Denmark linked back to two Danish swine herds.[55] Coupled with the discovery of this link, there have been improved monitoring systems that have helped to quantify the impact. In the United States, it is estimated that there are approximately 400,000 cases and over 35,000 hospitalizations per year attributable to increasing resistant strains of salmonella and campylobacter. In terms of financial impact in the US, the treatment of non-typhoidal salmonella infections alone is now estimated to cost $365 million per year.[2][57] In light of this, in its inaugural 2013 report on antibiotic resistance threats in the United States, the CDC identified resistant non-typhoidal salmonella and campylobacter as "serious threats" and called for improved surveillance and intervention in food production moving forward.[2]

There are other bacteria as well, where research is evolving and revealing that bacterial resistance acquired through use in livestock may be contributing to disease in humans. Examples of these include Enterococcus, E. coli 0157 and Staphylococcus Aureus. In the case of foodborne illness from E.coli, though it is still not typically treated with antibiotics because of associated risk of renal failure, increasing rates of antibiotic resistant infections have been correlated with increasing virulence of the bacteria.[57][58] In the case of enterococcus and staphylococcus aureus, resistant forms of both of these bacteria have resulted in greatly increasing morbidity and mortality in the US.[2] At this point, there have been studies, though a limited number, that definitively link antibiotic use in food production to these resistance patterns in humans and further research will help to further characterize this relationship.[56][59][60]

Mechanisms for transfer to humans

Humans can be exposed to antibiotic-resistant bacteria by ingesting them through the food supply. Dairy products, ground beef and poultry are the most common foods harboring these pathogens.[61] There is evidence that a large proportion of resistant E. coli isolates causing blood stream infections in people are from livestock produced as food.[62]

When manure from antibiotic-fed swine is used as fertilizer elsewhere, the manure may be contaminated with bacteria which can infect humans.[63]

Studies have also shown that direct contact with livestock can lead to the spread of antibiotic-resistant bacteria from animals to humans.,[64][65]

Action and advocacy by country

Legislation and activism worldwide have aimed at restricting antibiotic use in livestock.

European Union

On 1 January 2006 the European Union banned the non-medicinal use of antibiotics in livestock production.[66]

United States

Some grocery stores have policies about voluntarily not selling meat produced by using antibiotics to stimulate growth. In 2012 in the United States advocacy organization Consumers Union organized a petition asking the store Trader Joe's to discontinue the sale of meat produced with antibiotics.[67]

The U.S. Animal Drug User Fee Act was passed by Congress in 2008 and requires that drug manufacturers report all sales of antibiotics into the food animal production industry.[68][69]

Some proposed legislation in the US has failed to be adopted.[70] The Animal Drug and Animal Generic Drug User Fee Reauthorization Act of 2013 proposes other regulation.

In the United States the danger of emergence of antibiotic-resistant bacterial strains due to wide use of antibiotics to promote weight gain in livestock was determined by the United States Food and Drug Administration in 1977, but nothing effective was done to prevent the practice. In March, 2012 the United States District Court for the Southern District of New York, ruling in an action brought by the Natural Resources Defense Council and others, ordered the FDA to revoke approvals for the use of antibiotics in livestock which violated FDA regulations.[71] On 11 April 2012 the FDA announced a program to phase out unsupervised use of drugs as feed additives and, on a voluntary basis, convert approved uses for antibiotics to therapeutic use only, requiring veterinarian supervision of their use and a prescription.[72][73]

In response to consumer concerns about the use of antibiotics in poultry, in 2007, Perdue removed all human antibiotics from its feed and launched the Harvestland brand, under which it sold products that met the requirements for an "antibiotic-free" label. By 2014, Perdue had also phased out ionophores (antibiotics used in animals to lower production costs by promoting growth, and preventing disease) from its hatchery and began using the "antibiotic free" labels on its Harvestland, Simply Smart and Perfect Portions products.[74] By 2015, 52% of the company's chickens were raised without the use of any type of antibiotics.[75]

In 1970 the FDA started recommending that antibiotic use in livestock be limited but set no actual regulations governing this recommendation.[1] Further, in 2004 the Government Accountability Office (GAO) heavily critiqued the FDA for not collecting enough information and data on antibiotic use in factory farms. From this the GAO concluded that the FDA does not have enough information to create effective policy changes regarding antibiotic use. In response to this the FDA insisted that more research was being conducted and voluntary efforts within the industry would solve the problem of antibiotic resistance.[76]

China

In 2012 an American newspaper described the Chinese government's regulation of antibiotics in livestock production as "weak".[77]

India

In 2011 the Indian government proposed a "National policy for containment of antimicrobial resistance".[78] Other policies set schedules for requiring that food producing animals not be given antibiotics for a certain amount of time before their food goes to market.[79][80] A study released by Centre for Science and Environment (CSE) on 30 July 2014 found antibiotic residues in chicken. This study claims that Indians are developing resistance to antibiotics — and hence falling prey to a host of otherwise curable ailments. Some of this resistance might be due to large-scale unregulated use of antibiotics in the poultry industry. CSE finds that India has not set any limits for antibiotic residues in chicken and says that India will have to implement a comprehensive set of regulations including banning of antibiotic use as growth promoters in the poultry industry. Not doing this will put lives of people at risk.[81]

Brazil

Antibiotic resistant bacteria have been found in Brazilian cattle.[82]

South Korea

In 1998 some researchers reported use in livestock production was a factor in the high prevalence of antibiotic resistant bacteria in Korea.[83] In 2007 The Korea Times noted that Korea has relatively high usage of antibiotics in livestock production.[84] In 2011 the Korean government banned the use of antibiotics as growth promoters in livestock.[85]

New Zealand

In 1999 the New Zealand government issued a statement that they would not then ban the use of antibiotics in livestock production.[86] In 2007 ABC Online reported on antibiotic use in chicken production in New Zealand.[87]

Research into alternatives

Increasing concern due to the emergence of antibiotic resistant bacteria has led researchers to look for alternatives to using antibiotics in livestock.[88]

Probiotics, cultures of a single bacteria strain or mixture of different strains, are being studied in livestock as a production enhancer.[89]

Prebiotics are non-digestible carbohydrates. The carbohydrates are mainly made up of oligosaccharides which are short chains of monosaccharides. The two most commonly studied prebiotics are fructooligosaccharides (FOS) and mannanoligosaccharides (MOS). FOS has been studied for use in chicken feed. MOS works as a competitive binding site, as bacteria bind to it rather than the intestine and are carried out.[90]

Bacteriophages are able to infect most bacteria and are easily found in most environments colonized by bacteria, and have been studied as well.[88]

In another study it was found that using probiotics, competitive exclusion, enzymes, immunomodulators and organic acids prevents the spread of bacteria and can all be used in place of antibiotics.[91] Another research team was able to use bacteriocins, antimicrobial peptides and bacteriophages in the control of bacterial infections.[92] While further research is needed in this field, alternative methods have been identified in effectively controlling bacterial infections in animals. All of the alternative methods listed pose no known threat to human health and all can lead the elimination of antibiotics in factory farms. With further research it is highly likely that a cost effective and health effective alternative could and will be found.

References

  1. ↑ 1.0 1.1 FDA CVM. 2012: Guidance for Industry #209: The Judicious Use of Medically Important Antimicrobial Drugs in Food-Producing Animals.
  2. ↑ 2.0 2.1 2.2 2.3 2.4 2.5 2.6 2.7 Centers for Disease Control and Prevention. (2013). Antibiotic resistance threats in the United States. Retrieved from http://www.cdc.gov/drugresistance/threat-report-213/pdf/ar-threats-2013-508.pdf. Accessed 3.19.16.
  3. ↑ Hamaide, Sybille de la (11 January 2012) Antibiotics for livestock vital to feed world: OIE. Reuters. Paris. Retrieved 20 April 2015.
  4. ↑ Centers for Disease Control and Prevention. (2016). Antibiotic/Antimicrobial Resistance. Retrieved from http://www.cdc.gov/drugresistance/ (accessed 5.5.16).
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  6. ↑ Reported locally in these:
    • "To Become Vegetarians", Mansfield (O.) News, January 17, 1910, p2
    • "150,000 at Cleveland Stop the Use of Meat" Syracuse Herald-Journal, January 25, 1910, p1
    • "Boycott on Meat is Rapidly Spreading; Men Who Are Blamed For High Price", Atlanta Constitution, January 25, 1910, p1
  7. ↑ Scully, M. (2002). Dominion: the power of man, the suffering of animals, and the call to mercy. St. Martins Griffin, New York (Book).
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  58. ↑ Swartz M. Human Diseases Caused by Foodborne Pathogens of Animal Origin. Clinical Infectious Diseases. 2002. 34:S111-22.
  59. ↑ Bortolaia V, et al. Human health risks associated with antimicrobial-resistant enterococci and Staphylococcus aureus on poultry meat. Clinical Microbiology and Infection. 2016 Feb;22(2):130-40.
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  61. ↑ DeWaal C, Vaughn Grooters S. Antibiotic Resistance in Foodborne Pathogens. Center for Science in the Public Health Interest. May 2013.
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  64. ↑ Casey JA, et al. (2013). High-Density Livestock Operations, Crop Field Application of Manure, and Risk of Community-Associated Methicillin-Resistant Staphylococcus aureus Infection in Pennsylvania. JAMA Internal Medicine. 173(21):1980-1990.
  65. ↑ Chang Q, et al. (2014). Antibiotics in agriculture and the risk to human health: how worried should we be? Evolutionary Applications. 8(3): 240-247.
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  89. ↑ Hume, M. E. (2011). Historic perspective: Prebiotics, probiotics, and other alternatives to antibiotics. Poultry Science 90 (11): 2663-9. PMID 22010256
  90. ↑ Griggs, J. P., Jacob, J. P. (2005) Alternatives to Antibiotics for Organic Poultry Production Poultry Science 14: 750-756.
  91. ↑ Doyle, M.E. 2001: Alternatives to Antibiotic Use for Growth Promotion in Animal Husbandry. Food Research Institute, University of Wisconsin-Madison.
  92. ↑ Joerger, R.D. 2003: Alternatives to antibiotics: bacteriocins, antimicrobial peptides and bacteriophages. Poultry Science 82(4), 640-647.

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