Monday, August 1, 2011

What the USDA Doesn't Want You to Know About Antibiotics and Factory Farms


| Fri Jul. 29, 2011 3:00 AM PDT for Mother Jones

Here is a document the USDA doesn't want you to see. It's what the agency calls a "technical review"—nothing more than a USDA-contracted researcher's simple, blunt summary of recent academic findings on the growing problem of antibiotic-resistant infections and their link with factory animal farms. The topic is a serious one. A single antibiotic-resistant pathogen, MRSA—just one of many now circulating among Americans—now claims more lives each year than AIDS.
Back in June, the USDA put the review up on its National Agricultural Library website. Soon after, a Dow Jones story quoted a USDA official who declared it to be based on "reputed, scientific, peer-reviewed, and scholarly journals." She added that the report should not be seen as a "representation of the official position of USDA." That's fair enough—the review was designed to sum up the state of science on antibiotic resistance and factory farms, not the USDA's position on the matter.
But around the same time, the agency added an odd disclaimer to the top of the document: "This review has not been peer reviewed. The views expressed in this publication do not necessarily reflect the views of the United States Department of Agriculture." And last Friday, the document (original link) vanished without comment from the agency's website. The only way to see the document now is through the above-linked cached version supplied to me by the Union of Concerned Scientists.
What gives? Why is the USDA suppressing a review that assembles research from "reputed, scientific, peer-reviewed, and scholarly journals"?
To understand the USDA's quashing of a report it had earlier commissioned, published, and praised, you first have to understand a key aspect of industrial-scale meat production. You see, keeping animals alive and growing fast under cramped, unsanitary conditions is tricky business. One of the industry's tried-and-true tactics is low-level, daily doses of antibiotics. The practice helps keep infections down, at least in the short term, and, for reasons no one really understands, it pushes animals to fatten to slaughter weight faster.
Altogether, the US meat industry uses 29 million pounds of antibiotics every year. To put that number in perspective, consider that we humans in the United States—in all of our prescription fill-ups and hospital stays combined—use just over 7 million pounds per year. Thus the vast bulk of antibiotics consumed in this country, some 80 percent, goes to factory animal farms.
For years, scientists have worried that the industry's reliance on antibiotics was contributing to the growing problem of antibiotic resistance. The European Union took action to curtail routine antibiotic use on farms in 2006 (taking Sweden's lead, which had banned the practice 20 years before).
But here in the United States, the regulatory approach has been completely laissez-faire—and the meat industry would like to keep it that way. The industry claims that even though antibiotic-resistant bacteria have been found both in confined animals and supermarket meat, there's simply no evidence that livestock strains are jumping to the human population.
Here is where we get back to that now-you-see-it, now-you-don't USDA research summary, which reads like a heavily footnoted rebuttal to the industry line. Assembled by Vaishali Dharmarha, a research assistant at the University of Maryland, the report summarizes research from 63 academic papers and government studies. Here are few of her findings:
• "Use and misuse of antimicrobial drugs in food animal production and human medicine is the main factor accelerating antimicrobial resistance."
• "[F]ood animals, when exposed to antimicrobial agents, may serve as a significant reservoir of resistant bacteria that can transmit to humans through the food supply."
• "Several studies conducted by the Centers for Disease Control and Prevention (CDC) on antimicrobial-resistant Salmonella showed that [antibiotic resistance] in Salmonella strains was most likely due to the antimicrobial use in food animals, and that most infections caused by resistant strains are acquired from the consumption of contaminated food."
• "Farmers and farm workers may get exposed to resistant bacteria by handling animals, feed, and manure. These exposures are of significant concern to public health, as they can transfer the resistant bacteria to family and community members, particularly through person-to-person contacts."
• "Resistant bacteria can also spread from intensive food animal production area to outside boundaries through contact between food animals and animals in the external environment. Insects, flies, houseflies, rodents, and wild birds play an important role in this mode of transmission. They are particularly attracted to animal wastes and feed sources from where they carry the resistant bacteria to several locations outside the animal production facility."
Naturally, such assertions didn't please the meat industry....."

To read the story in its entirety click here.

Below is a copy of the document spoken of in the first line:

This is Google's cache of http://fsrio.nal.usda.gov/nal_web/fsrio/fsheet_pf.php?id=235. It is a snapshot of the page as it appeared on Jun 28, 2011 04:07:20 GMT. Thecurrent page could have changed in the meantime. Learn more

These search terms are highlighted: usda technical review a focus on antimicrobial resistance  
 You are here: Home / Pathogen Biology / A Focus on Antimicrobial Resistance
 Pathogen Biology
 
 Antimicrobial Resistance
 
  A Focus on Antimicrobial Resistance
 
This technical review was written by a university cooperator. This review has not been peer reviewed. The views expressed in this publication do not necessarily reflect the views of the United States Department of Agriculture.
This technical review illustrates the following key points about antimicrobial resistance:
  • Growing public health concern worldwide.
  • Infections caused by antimicrobial-resistant microorganisms increase the risk of morbidity and mortality in serious diseases.
  • Use and misuse of antimicrobial drugs in food animal production and human medicine is the main factor accelerating antimicrobial resistance.
  • Dairy products and beef are the most commonly implicated sources in foodborne disease outbreaks.
  • Research is focused on identifying sources and reservoirs of resistant bacteria, analyzing resistance mechanisms, as well as investigating dissemination routes of resistant bacteria in food animal production.
antibiotics
Antimicrobial resistance (AMR) or antibiotic resistance (ABR), the ability of bacteria or other microorganisms to resist the effects of antimicrobial drugs or antibiotics, is a growing public health concern worldwide.2122447 Infections caused by antimicrobial-resistant microorganisms often fail to respond to standard treatments, thereby reducing the possibilities of effective treatment and increasing the risk of morbidity and mortality in serious diseases. For instance, it is estimated that approximately 440,000 cases of multidrug-resistance tuberculosis (MDR-TB) emerge annually, causing at least 150,000 deaths.351363The increasing rate of AMR has raised the concern that we may enter the “post antibiotic era” where no effective antibiotics for treating several life-threatening infections would be available.
The extensive use and misuse of antimicrobials have resulted in the development of AMR both in human and animal bacterial pathogens.4435 The persistent circulation of resistant bacterial strains in the environment leads to possible contamination of food and water.43 In addition, food animals, when exposed to antimicrobials agents, may serve as a significant reservoir of resistant bacteria that can transmit to humans through the food supply.13 The resistant bacteria, including strains of SalmonellaCampylobacter, and Staphylococcus have been implicated in several foodborne disease outbreaks.16
The economic impact of AMR is significant. Insufficient or failed treatment leading to morbidity and mortality is a huge human cost.27 AMR not only increases the need of more expensive therapies but also prolong hospital stays.9 In 2008, a study of attributable medical costs for antibiotic-resistant infections estimated that infections in 188 patients from a single healthcare institution cost between 13.35 and 18.75 million dollars.23 The National Academies' Institute of Medicine in 1998 estimated that antimicrobial-resistant bacterial infections cost the United States (U.S.) four to five billion dollars annually.38 Prudent use of antimicrobials in food animals and human medicine, as well as effective monitoring and surveillance is required to control the spread of antimicrobial-resistant bacteria, control the risks of AMR to human health, and to reduce the economic burden.13
Natural Reservoirs and Transmission
poultry
AMR has been recognized in several foodborne pathogens, including Salmonella,Campylobacter jejuniStaphylococcus aureusEscherichia coli and Yersinia enterocolitica.6013 Reservoirs of these pathogens include humans as well as several animals. Food animals which may be asymptomatic carrier of these pathogens, when exposed to antimicrobial agents in the animal production environment, may serve as a reservoir of resistant pathogens. Main animal reservoirs include:6013471920
  • Salmonella -- Multiple animal species, including poultry, cattle, pigs, sheep, horses, and wild birds.
  • Campylobacter jejuni and Campylobacter coli -- Food animals, including cattle, poultry, and swine.
  • Staphylococcus aureus -- Food animals, including poultry, pigs, and cattle, and companion animals, including cats and dogs.
  • Shiga toxin-producing E. coli -- Food animals, including cattle and swine.
  • Yersinia enterocolitica -- Multiple animal species, including pigs, rodents, livestock, and rabbits.
In addition, resistant bacteria have been isolated from the environment, including air, water, soils and animal wastes. Soil microbes provide a large reservoir of resistance genes that can quickly move to other microbial communities, including enteric bacteria and pathogens, upon selection from antibiotic use.36
Four Modes of Transmission
  1. Food Animals -- Antimicrobials are used for therapeutic purposes and growth promotion in food animal production.50 This exerts selection pressure and leads to the potential development of AMR in commensal bacteria in the intestinal tract of food animals. During slaughtering of these animals, carcass contamination may occur that subsequently lead to contamination of meat from these animals.15 The resistant bacteria are then transmitted to humans through the consumption of contaminated meat.604737 These bacteria can then colonize humans and cause antimicrobial-resistant infections. For example, food animals contribute a significant proportion of E. coli in the human gastrointestinal tract through the consumption of contaminated food. Drug-resistant E. coli strains of animal origin (e.g. fluoroquinolone-resistant E. coli from chickens) can cause infections in humans.13 Human infection with Salmonella entericaserovar Typhimurium (e.g. definitive phage type (DT) 104) has been associated with the consumption of chicken, beef, pork, sausages, and meat paste.51 In addition, the resistant bacteria can transfer their resistance genes to other endogenous human bacteria and pathogens, including CampylobacterSalmonella, and pathogenic E. coliO157. 183747
  2. Animal-to-Human Contact -- Resistant bacteria from animals can transmit to humans by direct contact.18 Farmers and farm workers may get exposed to resistant bacteria by handling animals, feed, and manure. These exposures are of significant concern to public health, as they can transfer the resistant bacteria to family and community members, particularly through person-to-person contacts. For instance, a study showed that poultry farmers were at a greater risk of carrying drug-resistant enterococci than the urban residents. Another study reported that poultry house workers were 32 times more susceptible to harbor gentamicin-resistant E. coli as compared with community counterparts.48 In addition, companion animals can also transmit the resistant bacteria to humans. For instance, Salmonella Typhimurium DT104 and methicillin-resistant S. aureus (MRSA) isolates have been reported to spread from companion animals, such as dogs, horses, and cats to humans.19132
  3. Animal-to-Animal Contact -- Resistant bacteria can also spread from intensive food animal production area to outside boundaries through contact between food animals and animals in the external environment. Insects, flies, houseflies, rodents, and wild birds play an important role in this mode of transmission. They are particularly attracted to animal wastes and feed sources from where they carry the resistant bacteria to several locations outside the animal production facility.48
  4. Environment -- Resistant bacteria enter the environment mainly through waste disposal. Resistant bacteria in the environment (soil, water, air) can transmit to humans via food chain and other human exposure pathways. This occurs in the following ways:48
    • Contamination of crops fertilized with animal waste
    • Irrigation of crops contaminated by animal waste
    • Emission of waste aerosols from animal houses or waste storage facilities, field fertilized with untreated manure, or trucks transporting animals for processing
    • Waste runoff into groundwater and surface water
    • Contamination of other food animals
Mechanisms of Acquiring Antimicrobial Resistance
Microbial populations acquire AMR through two main mechanisms. These include:
  1. Mutation -- Exposure of bacteria to sublethal concentrations of antimicrobial agents results in the selection of resistant strains (survivor bacteria) by the process of natural selection. Under continuous antimicrobial pressure, the survivor bacteria, which have low intrinsic resistance to antimicrobials, reproduce, spread, rapidly dominate, or can even displace the antimicrobial-susceptible population.484137 Over time, the survivor bacteria undergo mutations which may further enhance their resistance to antimicrobials. Spontaneous mutations may lead to the development of AMR in bacteria and favor survival under antimicrobial pressure.1448 For example, resistance to fluoroquinolones (FQs) in Campylobacter occurs spontaneously due to mutations, particularly point mutations, in drug target genes. A single point mutation which occurs in the quinolone resistance-determining region (QRDR) of DNA gyrase A (GyrA), substantially develops resistance towards FQs in Campylobacter, while in other enteric organisms (e.g. Salmonella and E. coli), stepwise accumulation of point mutations is required to acquire high-level FQ resistance.3426
  2. Gene Transfer -- The resistance genes may also be acquired by horizontal gene transfer (HGT) which requires a donor of the resistance genes.35 In bacteria, HGT is mediated by three mechanisms:3634
    • Transformation -- Incorporation of foreign (exogenous) DNA from the surroundings into the genome of a bacterial cell. Transformation may be a main mechanism for acquiring chromosomally encoded resistance (e.g. FQ and macrolide resistance in Campylobacter).3634
    • Conjugation -- Transfer of extra-chromosomal DNA segments, known as plasmids, between related or unrelated bacteria through physical contact. Conjugation plays a main role in acquiring plasmid-mediated resistance (e.g. tet (O), tetracycline resistance in Campylobacter).373634 Plasmids also possess mobile DNA elements, known as transposons and integrons. These DNA elements possess multiple antimicrobial-resistant genes and are responsible for rapid spread of these genes among different bacteria. For example, the ABR pattern ofS. Typhimurium DT104 constitutes an integron coding for resistance to sulfonamides, ampicillin, and streptomycin. Resistance can also be transferred from commensal (non-pathogenic) to pathogenic bacteria through conjugation.37,14
    • Transduction -- Injection of bacteriophage (viral) DNA into the bacterial genome. Bacterial DNA, which may contain resistant genes, may get incorporated into the viral DNA and may disperse with new bacteriophages. These new bacteriophages may then inject into new hosts and disseminate resistance genes into a new population.36
It is estimated that mobile genetic elements, including plasmids, transposons, integrons, gene cassettes, and bacteriophages account for more than 95 percent of AMR acquired by gene transfer.48 These mobile elements have been shown to transmit genetic determinants for several different AMR mechanisms and may result in rapid dissemination of resistant genes among different bacteria.37
Factors Accelerating Antimicrobial Resistance
There are two main factors which accelerate AMR. These factors include:
  1. Use and Misuse of Antimicrobials -- Antimicrobials are commonly used to treat infections in humans and animals. However, their use and misuse exerts selection pressure and accelerate selection of resistant bacterial populations. The use and misuse of antimicrobials in animal production and human medicine is summarized below.
    • Antimicrobials in Animal Production -- Antimicrobials are used in animal production systems to treat and control bacterial infections as well as for growth promotion.3714 The prolonged use of antimicrobials, particularly at low levels, promotes the selection of AMR among commensal bacteria in the gastrointestinal tract of food animals. For example, FQ-resistant Campylobacter have emerged as a result of FQ use in chickens.1 When contaminated food is consumed, the resistance genes from commensal bacteria can be transferred to other bacteria, including foodborne pathogens, in the intestinal tract of humans. Several studies conducted by the Centers for Disease Control and Prevention (CDC) on antimicrobial-resistant Salmonella showed that AMR in Salmonella strains was most likely due to the antimicrobial use in food animals, and that most infections caused by resistant strains are acquired from the consumption of contaminated food.2437
    • Antimicrobials in Human Medicine -- Antimicrobials are commonly used in human medicine to treat bacterial infections. They are not meant to be used against viral infections like common cold, most sore throats, and flu.227 Both overuse, such as over-prescribing of antimicrobials for critically ill patients, and underuse, such as taking inadequate dose for an inappropriate length of time, are the main cause of selection of antimicrobial-resistant bacterial populations.629The inappropriate use of antimicrobials in the hospitals and close contact among sick patients creates an environment for the dissemination of antimicrobial-resistant bacteria.41 For example, methicillin-resistant Staphylococccus aureus(MRSA) and vanomycin-resistant enterococci (VRE) are mainly associated with hospital environments or those who have had prolonged stays in the hospital.27
  2. Environmental Stresses -- Several environmental stresses, which are frequently applied in food preservation processes, have been linked to the increase in bacterial resistance towards antimicrobials. For example, a study reported an increase in AMR in foodborne pathogens, including S. aureusE. coli, and S. enterica serovar Typhimurium, under sublethal low pH or high sodium chloride stress. Another study showed that high osmolarity and starvation regulates the expression of bacterial lipocalin, a protein which helps bacterial adaptation to environmental stress and is responsible for the dissemination of AMR genes. Environmental stress can enhance plasmid transfer and plasmid numbers, thereby increasing resistance.39
Detection Methods (Antimicrobial Susceptibility Testing)
antimicrobial susceptibility testing
There are three main purposes of antimicrobial susceptibility testing. These include:303157
  • Detect clinically relevant AMR in common pathogens
  • Confirm susceptibility to chosen antimicrobial agents
  • Administer appropriate antimicrobial therapy
The methods to determine antimicrobial susceptibility are based on the analysis of bacterial growth on solid or liquid medium containing a specified concentration of a single drug.25Several methods are used by clinical laboratories to test antimicrobial susceptibility. These methods are categorized into three main types:
  1. Quantitative Methods -- In these methods, minimum inhibitory concentration (MIC) i.e. the lowest concentration of antibiotic that inhibits bacterial growth is determined. These methods are performed on a liquid medium (broth) or on a solid medium (agar), and take approximately three days to complete. There are four main types of quantitative methods:3161
    • Macrobroth or Tube Dilution Method -- The procedure involves preparing two-fold dilution of antibiotics in test tubes containing a liquid growth medium. Then, these test tubes are inoculated, incubated, and examined for visible bacterial growth as observed by turbidity. The lowest concentration of antibiotic that completely inhibits visual growth of bacteria (no turbidity) is recorded asMIC. This method is tedious and requires large amount of reagents and space.31
    • Microbroth Dilution Method -- The procedure involves inoculation of a standard amount of bacteria into the wells of a microtiter plate containing different dilutions of antibiotic. After incubation, the plates are either examined visually or with an analytical instrument for bacterial growth to determine MIC. This method is fast, convenient, reproducible, and requires less space and reagents.4931
    • Agar Dilution Method -- The procedure involves inoculation of a standard amount of bacteria onto the nutrient agar plates containing different concentrations of antibiotic. After incubation, the plates are examined for bacterial colonies that indicate bacterial growth. The lowest concentration of antibiotic that inhibits colony formation on agar surface is recorded as MIC.61
    • Antimicrobial Gradient Method – The procedure involves the use of commercially available strips containing an exponential gradient of antibiotic. The strips are placed in a radial fashion on the agar plate that has been inoculated with a standard bacterial suspension. After incubation, MIC is read at the point of intersection of an elliptical growth inhibition zone with the strip that has an MIC scale printed on it. The Etest (AB BIODISK) is a commercial version of this method available in the U.S. The test is rapid and easy to use, but is expensive and best suited for MIC determination of one or two drugs.61315
  2. Qualitative Methods -- In these methods, susceptibility or resistance of bacteria to a particular antibiotic is determined. MIC is not determined in these methods. The main qualitative method is disk diffusion method.
    • Disk Diffusion Method -- The procedure involves the use of paper disks that are impregnated with a single concentration of different antibiotics. The disks are placed onto the agar plate that has been the inoculated with standard number of bacteria. After incubation, zone diameter (zone of inhibition around each antibiotic disk) is measured to the nearest millimeter and reference tables published by the Clinical and Laboratory Standards Institute (CLSI) are used to determine if the bacteria are Susceptible (S), Intermediate (I) or Resistant (R). The test is simple, does not require any special equipment, flexible in terms of disk selection, and is least expensive of all susceptibility methods.3149
  3. Rapid Methods -- Several molecular methods that are rapid, and highly sensitive and specific have been developed or are underway research for direct detection of resistance genes. Some of these methods include:3031254219
    • Polymerase Chain Reaction-Restriction Fragment Length Polymorphism (PCR-RFLP)
    • Polymerase Chain Reaction-Single Stranded Conformational Polymorphism (PCR-SSPC)
    • Amplified Fragment Length Polymorphism (AFLP)
    • Pulsed-field Gel Electrophoresis (PFGE)
    • Multilocus Enzyme Electrophoresis
    • DNA Fingerprinting
    Rapid methods have limited application because only a few resistance genes are strongly associated with phenotypic resistance. There are several other mutations and expression mechanisms responsible for AMR which are difficult to detect by current molecular techniques. Therefore, there is considerable need for development of rapid and accurate methods to detect AMRin microorganisms.3031
For additional information on antimicrobial susceptibility testing, please visit CDC -- Laboratory Testing and Training Resources – Antibiotic/Antimicrobial Resistance.
Prevention and Control of Antimicrobial Resistance
Limiting the inappropriate use of antimicrobials both in humans and animals, and controlling the transmission of resistant bacteria is a key to control AMR. This can be achieved through the following ways in human medicine and animal agriculture.4371316
In Human Medicine:
  • Reducing inappropriate prescriptions and informing consumers about the appropriate uses and limitations of antimicrobial drugs.
  • Discouraging the inappropriate use of antimicrobials, such as for viral infections without bacterial complications.
  • Using rapid and accurate diagnostic methods to facilitate appropriate drug prescriptions.
  • Developing vaccines and adapting hygienic practices, such as hand washing and safe food handling to reduce the spread of AMR.
For additional information on prevention of antibiotic-resistant infections through appropriate use of antimicrobials, please visit CDC -- How can I Prevent Antibiotic-resistant Infections.
In Animal Agriculture:
  • Understanding the risks and benefits of antimicrobial use in food animals.
  • Development and implementation of principles guiding appropriate antimicrobial use in the food animal production.
  • Improvement in animal husbandry and food production practices to reduce the dissemination of AMR.
  • Development of regulations for prudent use of antimicrobials in food animals.
  • Development of testing and reporting protocols for drug-resistant foodborne pathogens by regulatory agencies.
  • Reduction in the usage of antimicrobials that are “critically important” for human medicine in food animals.
In addition, several surveillance programs, and educational and health campaigns have been initiated by national and international agencies to monitor, control, and prevent AMR. Some examples include:3637822
Foodborne Disease Outbreaks
milk and cheese
Antimicrobial-resistant strains of foodborne pathogens are widespread throughout the world. Most of these resistant pathogens are zoonotic in origin and acquire their resistance in food animal host before they transmit and infect human beings via the consumption of contaminated food.51 Therefore, foods of animal origin are frequently associated with antimicrobial-resistant foodborne disease outbreaks. Some foods that have been associated with antimicrobial-resistant infections and outbreaks include:455116
  • Chicken
  • Beef
  • Pork
  • Dairy products
  • Salad vegetables
There is limited information available on these outbreaks because reporting of AMR in foodborne pathogens, such as Salmonella and E. coli, is not required by the CDC. Between 1973 and 2009, 35 outbreaks resulting in 19,897 illnesses, 3,061 hospitalizations, and 26 deaths have been reported by the Center for Science in the Public Interest. Dairy products (34 percent) and ground beef (26 percent) were most commonly implicated foods in these outbreaks. Salmonella Typhimurium was the main causative microorganism responsible for 14 of 35 outbreaks.16
The lists of national and international outbreaks summarized below, demonstrate that most antimicrobial-resistant outbreaks are associated with Salmonella Typhimurium DT104 which is usually resistant to five drugs – ampicillin, chloramphenicol, streptomycin, sulfonamides, and tetracycline.
Selected Foodborne Outbreaks in North America
The following list of national outbreaks indicates that dairy products are the most frequently implicated foods in antimicrobial-resistant outbreaks.
2011 Multistate Turkey Burger Outbreak10
  • Contaminated turkey burgers
  • Resulted in 12 cases
  • Contamination was possibly due to improper food handling
  • Implicated microorganism was Salmonella Hadar with multidrug resistance
2009 Multistate Beef Outbreak11
  • Contaminated beef and ground beef
  • Resulted in 40 cases
  • Contamination source was not reported
  • Implicated microorganism was Salmonella Newport with multidrug resistance
2006-2007 Illinois Cheese Outbreak6
  • Contaminated Mexican-style aged cheese
  • Resulted in 85 cases
  • Contamination was due to inadequately pasteurized milk used to prepare cheese
  • Implicated microorganism was Salmonella Newport with multidrug resistance
2001 Tennessee Barbeque and Coleslaw Outbreak29
  • Contaminated pork barbeque and coleslaw
  • Resulted in three cases
  • Contamination was due to handling of barbeque and coleslaw by an infected food handler
  • Implicated microorganism was methicillin-resistant Staphylococcus aureus
1997 Northern California Cheese Outbreak12
  • Contaminated Mexican-style cheese
  • Resulted in 31 cases
  • Contamination was due to unpasteurized raw milk used to prepare cheese
  • Implicated microorganism was Salmonella Typhimurium DT104 with 5-drug resistance
1997 Northern California Milk-Cheese Outbreak12
  • Contaminated Mexican-style cheese and raw milk
  • Resulted in 79 cases
  • Contamination was due to unpasteurized raw milk and cheese prepared from it
  • Implicated microorganism was Salmonella Typhimurium DT104b with 5-drug resistance
1997 Washington State Cheese outbreak58
  • Contaminated Mexican-style soft cheese
  • Resulted in 54 cases
  • Contamination was due to unpasteurized raw milk used to prepare cheese
  • Implicated microorganisms were and Salmonella Typhimurium DT104 and SalmonellaTyphimurium DT104b with 5-drug resistance
1985 Illinois Milk Outbreak46
  • Contaminated pasteurized milk
  • Resulted in 16,659 cases
  • Contamination was likely due to mixing of raw milk and pasteurized milk
  • Implicated microorganism was SalmonellaTyphimurium with unusual antimicrobial resistance pattern
For additional information on antimicrobial-resistant bacterial outbreaks in the U.S. , visitOutbreakNet -- Foodborne Outbreak Online Database.
For additional foodborne outbreak information and statistics in the U.S., visit FoodNet -- Foodborne Diseases Active Surveillance Network.
Selected International Foodborne Outbreaks
The following list of international outbreaks indicates that not only meat and dairy products, but also salad vegetables, such as lettuce and potato are also implicated in antimicrobial-resistant outbreaks.
2008 Morocco Chicken Tagine Outbreak3
  • Contaminated chicken tagine
  • Resulted in 45 cases
  • Contamination was due to poorly cooked broiler chicken used to prepare tagine
  • Implicated microorganism was Salmonella Typhimurium with multidrug resistance
2005 Denmark Carpaccio (Beef) Outbreak17
  • Contaminated carpaccio (thinly sliced raw fillet of beef)
  • Resulted in five cases
  • Contamination was due to contaminated imported beef used to prepare Carpaccio
  • Implicated microorganism was Salmonella Typhimurium DT104 with 6-drug resistance
2000 England and Wales Lettuce Outbreak28
  • Contaminated lettuce
  • Resulted in 361 cases
  • Contamination was likely due to inadequate washing of lettuce at food outlets
  • Implicated microorganism was Salmonella Typhimurium DT104 with 6-drug resistance
1998 England Raw Milk Outbreak59
  • Contaminated raw milk
  • Resulted in 86 cases
  • Contamination was due to failure of on-farm pasteurization of milk
  • Implicated microorganism was Salmonella Typhimurium DT104 with multidrug resistance
1998 Denmark Pork Outbreak40
  • Contaminated pork and pork products
  • Resulted in 25 cases, including two deaths
  • Contamination was due to contaminated pork and products prepared from it
  • Implicated microorganism was Salmonella Typhimurium DT104 with 5-drug and quinolone resistance
1995 Netherlands Food Outbreak32
  • Contaminated food
  • Resulted in 41 cases, including five deaths
  • Contamination was due to infected dietary worker who prepared food for patients
  • Implicated microorganism was methicillin-resistant Staphylococcus aureus
1989 Caribbean Potato Salad Outbreak33
  • Contaminated potato salad served at a cruise ship
  • Resulted in 21 cases
  • Contamination was due to infected food handler who prepared and handled salad
  • Implicated microorganism was Shigella flexneri with with multidrug resistance
For additional international foodborne outbreak information, visit the Program for Monitoring Emerging Diseases of the International Society of Infectious Disease.
Research at the USDA Agricultural Research Service
antimicrobial research
The USDA Agricultural Research Service (ARS) is actively involved in food safety research related to AMR in foodborne pathogens under the National Food Safety Program 108. This research program provides the means to ensure that the food supply is safe and secure for consumers and that food and feed meet foreign and domestic regulatory requirements. The following ARS research units conduct research on AMR in foodborne pathogens:
Some research projects on AMR being conducted at these ARS units are:
Project Objectives54
  1. Use ABR data obtained from the Collaboration on Animal Health and Food Safety Epidemiology (CAHFSE) and the NARMS programs and poultry studies to identify sources, reservoirs and amplifiers of resistant food borne and commensal bacteria, as well as the path of dissemination of these resistant bacteria in food producing animals and poultry.
  2. Map the spread of antimicrobial resistance throughout the U.S. using molecular epidemiology and population genetic studies of antimicrobial-resistant bacterial isolates, including participation in USDA VetNet.
  3. Analyze and differentiate antimicrobial resistance mechanisms, both phenotypically and genotypically, and rapidly identify resistant strains.
Accomplishments54
  1. Conducted antimicrobial susceptibility testing and speciation of Campylobacter isolates from the Food Safety Inspection Service (FSIS) chicken parts shakedown and baseline studies on raw chicken parts.
  2. Characterized multidrug-resistant E. coli by plasmid replicon typing and Pulsed-Field Gel Electrophoresis. Observed a high degree of genotypic diversity, with 34 different PFGEtypes found among the 35 isolates examined.
  3. Analyzed AMR genes in bacteria co-isolated from swine fecal samples and indicated thatSalmonella and E. coli may have a common source for acquiring AMR genes or may exchange resistance genes in the swine environment.
  4. Suggested that the common genetic elements in different bacteria may serve as a reservoir for resistance in important pathogens such as Salmonella.
  5. Developed microarrays for detection of multi-drug resistant plasmids in Salmonella andE. coli.
  6. Conducted sequence analysis of multidrug-resistant plasmids from Salmonella and E. coli and indicated that plasmids encode metal and sanitizer resistance genes that may give bacteria that possess them a survival advantage in the animal environment or in the meat processing plant environment.
  7. Determined prevalence of ColE1-like plasmids and kanamycin resistance genes inSalmonella enterica serovars.
  8. Determined prevalence of antimicrobial-resistant E. coli from companion animals and indicated that healthy dogs and cats are a source of antimicrobial-resistant E. coli and may act as a reservoir of AMR that can be transferred to the human host.
  9. Characterized MRSA from companion animals and humans and reported that all isolates from companion animals exhibited the same resistance pattern among the 18 antimicrobials tested.
  10. Detected a new multi-locus sequence type (MLST) among the MRSA isolates.
  11. Conducted antimicrobial susceptibility testing of foodborne pathogens by the animal arm of NARMS on SalmonellaCampylobacterE. coli and Enterococcus from animal and environmental sources.
  12. Determined prevalence, species distribution, and antimicrobial resistance of enterococci isolated from U.S. dairy cattle and found that Enterococcus hirae, E. faecalis, and E. faecium were the most prevalent enterococcal species in dairy cattle fecal samples. The highest levels of resistance were to lincomycin, flavomycin, and tetracycline17.
  13. Conducted Pulsed-Field Gel Electrophoresis (PFGE) to evaluate AMR patterns ofSalmonella serotypes isolated from broiler external carcass rinses and found that S. Kentucky isolates exhibited the greatest heterogeneity with six different AMR patterns within 13 different PFGE patterns.
  14. Determined prevalence of antimicrobial-resistant bacteria from dairy cattle in the northeast U.S. and found that Campylobacter isolates recovered from dairy cattle were resistant to tetracycline.
Project Objectives53
  1. Assess resistance among Salmonella and E. coli originating from bovine sources to 4th generation cephalosporins over time.
  2. Assess resistance among Campylobacter jejuni, Campylobacter coli, Enterococcus faecalis and Enterococcus faecium originating from bovine and porcine sources to macrolides over time.
Accomplishments53
  1. Collected Salmonella and generic E. coli isolates originating from cattle as part of the animal arm of NARMS originating from cattle specimens which are being tested on antimicrobials cefquinome sulfate and cefepime. These antimicrobials belong to a class of drugs called cephalosporins.
  2. Planned to perform molecular analysis of isolates to determine which gene may be responsible for any decreased susceptibilities which are observed as well as detection of extended spectrum Beta-lactamases, enzymes which confer resistance to cephalosporin antimicrobials.
Project Objectives56
  1. Determine the AMR of E. coli from cattle reared with various antibiotic usage regimens.
Accomplishments56
  1. Developed new information on the genetic aspects of how E. coli develops resistance to a member (ceftiofur) of an important class of antibiotics used both in agriculture and in human medicine.
  2. Developed new insights on the bacterial/chemical interactions as related to practical antibiotic treatment protocols.
Project Objectives55
  1. Investigate the molecular mechanisms that coordinate virulence and ABR in Salmonellaobtained from cattle (DT104 and S. dublin) and swine (DT104 and S. choleraesuis).
  2. Investigate the molecular basis for swine resistance to Salmonella colonization by characterizing the immunological aspects of infection.
Accomplishments55
  1. Searched sequence databases for genetic variations in greater than 3,000 porcine genes identified by the research team as differentially-expressed during exposure toSalmonella.
  2. Identified thirty DNA sequence variations in the pig genome, referred to as single nucleotide polymorphisms (SNPs).
  3. Showed that three of the SNPs associated with fecal shedding or tissue colonization ofSalmonella in pigs by genotype analysis of four independent pig populations.
Project Objectives52
  1. Conduct on-farm surveys in organic and all natural poultry production practices to determine the prevalence and diversity of Salmonella serovars in these production systems as compared to more intensive commercial systems.
  2. Develop and evaluate intervention strategies targeting control of Salmonella during the feed withdrawal and transportation processes prior to slaughter of broiler chickens to minimize cross contamination during transport and slaughter.
  3. Evaluate post-harvest interventions to control Salmonella using novel antimicrobials in pre- and post-chiller applications, for both water and air chilling, and for finished raw products.
  4. Develop risk assessment models that can be adapted to organic and all natural production and processing systems.
Accomplishments52
  1. Completed on-farm surveys.
  2. Isolated large collection of Salmonella with serovar Kentucky being the most commonly recovered.
  3. Conducted studies on addition of prebiotics to diets as a means to mitigate Salmonellacolonization.
For additional USDA Antimicrobial Resistance Projects, please visit the FSRIO Research Projects Database.
For additional antimicrobial resistance research projects conducted by other U.S. government and International agencies, please search the FSRIO Research Projects Database.
References
1. Asai, T., K. Harada, K. Ishihara, A. Kojima, T. Sameshima, Y. Tamura and T. Takahashi. 2007. Association of Antimicrobial Resistance in Campylobacter Isolated from Food-Producing Animals with Antimicrobial Use on Farms. Jpn. J. Infect. Dis. 60:290-294. Retrieved May 15, 2011, from http://www.nih.go.jp/JJID/60/290.pdf.
2. Baptiste, K.E. 2005. Methicillin-resistant Staphylococci in Companion Animals. Emer. Infect. Dis. 11:1942-1944. Retrieved April 25, 2011, fromhttp://www.cdc.gov/ncidod/eid/vol11no12/pdfs/05-0241.pdf.
3. Bouchrif, B., S. L. Hello, M. Pardos, B. Karraouan, J-D Perrier-Gros-Claude. 2009. Ceftazidime-resistant Salmonella enterica, Morocco. Emer. Infect. Dis. 15:1693-1695. Retrieved April 25, 2011, from http://www.cdc.gov/eid/content/15/10/pdfs/1693b.pdf.
4. Centers for Disease Control and Prevention. 2000. A Public Health Action Plan to Combat Antimicrobial Resistance. Part 1: Domestic Issues. Interagency Task Force on Antimicrobial Resistance. Retrieved May 10, 2011, fromhttp://www.cdc.gov/drugresistance/actionplan/aractionplan.pdf.
5. Centers for Disease Control and Prevention. 2008. National Antimicrobial Resistance Monitoring System: Enteric Bacteria. Human Isolates Final Report. Retrieved May 9, 2011, fromhttp://www.cdc.gov/narms/annual/2008/NARMS_2008_Annual_Report.pdf.
6. Centers for Disease Control and Prevention. 2008. Outbreak of Multidrug-ResistantSalmonella enterica serotype Newport Infections Associated with Consumption of Unpasteurized Mexican-Style Aged Cheese -- Illinois, March 2006-April 2007. Retrieved May 15, 2011, fromhttp://www.cdc.gov/mmwr/preview/mmwrhtml/mm5716a4.htm.
7. Centers for Disease Control and Prevention. 2010. Antibiotic Resistance Questions and Answers. Retrieved April 7, 2011, from http://www.cdc.gov/getsmart/antibiotic-use/anitbiotic-resistance-faqs.html.
8. Centers for Disease Control and Prevention. 2010. Antibiotic/ Antimicrobial Resistance – Education Campaigns. Retrieved May 12, 2011, fromhttp://www.cdc.gov/drugresistance/campaigns.html.
9. Centers for Disease Control and Prevention. 2011. Antimicrobial Resistance. Retrieved April 16, 2011, from http://www.cdc.gov/ncidod/aip/research/ar.html.
10. Centers for Disease Control and Prevention. 2011. Investigation Announcement: Multistate Outbreak of Salmonella Hadar Infections Associated with Turkey Burgers. Retrieved May 19, 2011, from http://www.cdc.gov/salmonella/hadar0411/040411/index.html
11. Clark, M. Foodborne Illness Outbreak Database. Beef Packers, Inc., Cargill, Ground Beef June, 2009 . Retrieved May 21, 2011, from http://www.outbreakdatabase.com/details/beef-packers-inc.-cargill-ground-beef-june-2009/?or ganism=Salmonella&year=2009&state=10
12. Cody, S.H., S.L. Abbott, A.A. Marfin, B.Schulz, P. Wagner et al. 1999. Two Outbreaks of Multidrug-Resistant Salmonella Serotype Typhimurium DT104 Infections Linked to Raw-Milk Cheese in Northern California. JAMA. 281:1805-1810. Retrieved May 18, 2011, fromhttp://jama.ama-assn.org/content/281/19/1805.full.pdf.
13. Collignon, P., J.H. Powers; T.M. Chiller, A. Aidara-Kane and F.M. Aarestrup. 2009. World Health Organization Ranking of Antimicrobials According to Their Importance in Human Medicine: A Critical Step for Developing Risk Management Strategies for the Use of Antimicrobials in Food Production Animals. Clin. Infect. Dis. 49:132-141. Retrieved April 8, 2011, from http://cid.oxfordjournals.org/content/49/1/132.full.pdf+html.
14. Conter M., D. Paludi, E. Zanardi, S. Ghidni, A. Vergara and A. Ianieri. 2009. Characterization of Antimicrobial Resistance of Foodborne Listeria monocytogenesInt. J. Food Microbiol. 128:497-500. Abstract Retrieved April 23, 2011, fromhttp://www.ncbi.nlm.nih.gov/pubmed/19012982.
15. De Boer, E., J.T.M. Zwartkruis-Nahuis, B. Wit, X.W. Huijsdens, A.J. de Neeling et al. 2009. Prevalence of Methicillin-resistant Staphylococcus aureus in Meat. Int. J. Food Microbiol. 134:52-56. Abstract Retrieved April 27, 2011, from http://www.ncbi.nlm.nih.gov/pubmed/19144432.
16. DeWaal, C.S., C. Roberts and C. Catella. Antibiotic Resistance in Foodborne Pathogens: Evidence for the Need for a Risk Management Strategy. Center for Science in the Public Interest. Retrieved April 14, 2011, fromhttp://cspinet.org/new/pdf/abrfoodbornepathogenswhitepaper.pdf.
17. Ethelberg, S., G. Sorensen, B. Kristensen, K. Christensen, L. Krusell et al. 2007. Outbreak with Multi-resistant Salmonella Typhimurium DT104 Linked to Carpaccio, Denmark, 2005.Epidemiol. Infect. 135:900-907. Retrieved May 21, 2011, fromhttp://www.ncbi.nlm.nih.gov/pmc/articles/PMC2870661/pdf/S0950268807008047a.pdf.
18. Fábrega, A., J. Sánchez-Céspedes, S. Soto and J. Vila. 2008. Quinolone Resistance in the Food Chain. Int. J. Antimicrobial Agents. 31:307-315. Abstract Retrieved April 22, 2011, fromhttp://www.ncbi.nlm.nih.gov/pubmed/18308515 .
19. Farzan, A., R.M. Friendship, C. Poppe, L. Martin, C.E. Dewey. 2008. Molecular Epidemiology and Antimicrobial Resistance of Salmonella Typhimurium DT104 on Ontario Swine Farms. The Canadian Journal of Veterinary Research. 72:188-194. Retrieved April 20, 2011, fromhttp://www.ncbi.nlm.nih.gov/pmc/articles/PMC2276905/pdf/cjvr72_pg188.pdf.
20. Finnish Food Safety Authority Evira. 2011. FINRES-Vet 2007/2009. Finnish Veterinary Antimicrobial Resistance Monitoring and Consumption of Antimicrobial Agents. Evira Publications. Retrieved April 25, 2011, fromhttp://www.evira.fi/files/products/1302157879317_finres_vet_2007_2009.pdf.
21. Food and Drug Administration. 2010. Antimicrobial Resistance. Retrieved April 5, 2011, from http://www.fda.gov/animalveterinary/safetyhealth/antimicrobialresistance/default.htm.
22. Food and Drug Administration. 2010. Combating Antibiotic Resistance. FDA Consumer Health Information. Retrieved April 5, 2011, fromhttp://www.fda.gov/downloads/ForConsumers/ConsumerUpdates/UCM143470.pdf.
23. Frieden, T.R. Antibiotic Resistance and the Threat to Public Health. 2010. Centers for Disease Control and Prevention. U.S. Department of Health and Human Services. Retrieved April 9, 2011, from http://www.cdc.gov/drugresistance/pdf/FriedenTestimony42810.pdf.
24. Gilchrist, M.J., C. Greko, D.B. Wallinga, G.W. Beran, D.G. Riley et al. 2007. The Potential Role of Concentrated Animal Feeding Operations in Infectious Disease Epidemics and Antibiotic Resistance. Environ. Health Pers. 115:313-316. Retrieved April 10, 2011, fromhttp://www.ncbi.nlm.nih.gov/pmc/articles/PMC1817683/pdf/ehp0115-000313.pdf.
25. Gillespie, S.H. (ed). 2001. Antibiotic Resistance: Methods and Protocols. Book ReviewInt. Microbiol. 4:53-54. Retrieved May 6, 2011, fromhttp://www.im.microbios.org/13march01/BR2%20Gillespie-Berlanga.pdf.
26. Han, J., O. Sahin, Y-W Barton and Q. Zhang. 2008. Key Role of Mfd in the Development of Fluoroquinolone Resistance in Campylobacter jejuniPLoS Pathogens. 4:1-12. Retrieved April 24, 2011, from http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2390758/pdf/ppat.1000083.pdf.
27. Hawkey, P.M. The Growing Burden of Antimicrobial Resistance. J. Anti. Chemo. 62 (Suppl. 1): i1-i9. Retrieved April 14, 2011, fromhttp://jac.oxfordjournals.org/content/62/suppl_1/i1.full.pdf+html.
28. Horby, P.W. , S.J. O’Brien, G.K. Adak, C. Graham, J.I. Hawker et al. A National Outbreak of Multi-resistant Salmonella enterica serovar Typhimurium Definitive Phage Type (DT) 104 Associated with Consumption of Lettuce. Epidemiol. Infect. 130:169-178. Retrieved May 21, 2011, from http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2869951/pdf/12729184.pdf.
29. Jones, T.F., M.E. Kellum, S.S. Porter, M. Bell and W. Schaffner. 2002. An Outbreak of Community-Acquired Foodborne Illness Caused by Methicillin-Resistant Staphylococcus aureus.Emerg. Infect. Dis. 8:82-84. Retrieved May 16, 2011, fromhttp://www.cdc.gov/ncidod/eid/vol8no1/pdf/01-0174%20jones.pdf.
30. Jorgensen, J.H. 1993. Selection Criteria for an Antimicrobial Susceptibility Testing System.J. Clin. Microbiol. 31:2841-2844. Retrieved May 3, 2011, fromhttp://www.ncbi.nlm.nih.gov/pmc/articles/PMC266141/pdf/jcm00023-0015.pdf.
31. Jorgensen, J.H. and M.J. Ferraro. 2009. Antimicrobial Susceptibility Testing: A Review of General Principles and Contemporary Practices. Clin. Infect. Dis. 49:1749-1755. Retrieved May 4, 2011, from http://cid.oxfordjournals.org/content/49/11/1749.full.pdf+html.
32. Kluytmans, J., van Leeuwen W., W. Goessens, R. Hollis, S. Messer, L. Herwaldt et al. 1995. Food-Initiated Outbreak of Methicillin-Resistant Staphylococcus aureus Analyzed by Pheno- and Genotyping. J. Clin. Microbiol. 33:1121-1128. Retrieved May 24, 2011, fromhttp://www.ncbi.nlm.nih.gov/pmc/articles/PMC228116/pdf/331121.pdf.
33. Lew, J.F., D.L. Swerdlow, M.E. Dance, P.M. Griffin, C.A. Bopp et al. 1991. An Outbreak of Shigellosis aboard a Cruise Ship Caused by Multiple-antibiotic-resistant Strain of Shigella flexneriAm. J. Epidemiol. 134:413-420. Abstract Retrieved May 24, 2011, fromhttp://aje.oxfordjournals.org/content/134/4/413.abstract.
34. Luangtongkum, T., B. Jeon, J. Han, P. Plummer, C.M. Logue and Q. Zhang. 2009. Antibiotic Resistance in Campylobacter: Emergence, Transmission, and Persistence. Future Microbiol. 4:189-200. Author manuscript Retrieved April 24, 2011, fromhttp://www.ncbi.nlm.nih.gov/pmc/articles/PMC2691575/pdf/nihms114727.pdf.
35. Martinez, J.L. 2009. The Role of Natural Environments in the Evolution of Resistance Traits in Pathogenic Bacteria. Proc. R. Soc. B. 276:2521-2530. Retrieved April 7, 2011, fromhttp://www.ncbi.nlm.nih.gov/pmc/articles/PMC2684669/pdf/rspb20090320.pdf.
36. Mathew, A.G. Antibiotic Resistance in Bacteria Associated with Food Animals: A United States Perspective of Livestock Production. 2007. Foodborne Pathogens and Disease. 4:115-133. Abstract Retrieved April 21, 2011, from http://www.ncbi.nlm.nih.gov/pubmed/17600481.
37. McDermott, P.F., S. Zhao, D.D. Wagner, S. Simjee, R.D. Walker and D.G. White. 2002. The Food Safety Perspective of Antibiotic Resistance. Anim. Biotechnol. 13:71-84. Abstract Retrieved April 21, 2011, from http://www.ncbi.nlm.nih.gov/pubmed/12212946.
38. McGowan, J.E. 2001. Economic Impact of Antimicrobial Resistance. Emerg. Infect. Dis. 7:286-292. Retrieved April 18, 2011, fromhttp://www.cdc.gov/ncidod/eid/vol7no2/pdfs/mcgowan.pdf.
39. McMahon, M.A.S., J. Xu, J.E. Moore, I.S. Blair and D.A. McDowell. 2007. Environmental Stress and Antibiotic Resistance in Food-Related Pathogens. Appl. Environ. Microbiol. 73:211-217. Retrieved May 14, 2011, fromhttp://www.ncbi.nlm.nih.gov/pmc/articles/PMC1797128/pdf/0578-06.pdf.
40. Molbak, K., D.L. Baggesen, F.M. Aarestrup, J.M. Ebbesen, J. Engberg. 1999. An Outbreak of MultiDrug-Resistant, Quinolone-Resistant Salmonella enetrica Serotype Typhimurium DT104. N. Engl. J. Med. 341:1420-1425. Retrieved May 23, 2011, fromhttp://www.nejm.org/doi/pdf/10.1056/NEJM199911043411902.
41. National Institute of Allergy and Infectious Diseases. National Institutes of Health. 2009. Antimicrobial (Drug) Resistance. Retrieved April 21, 2011, fromhttp://www.niaid.nih.gov/topics/antimicrobialResistance/Understanding/Pages/causes.aspx .
42. Nielsen, E.M., M. Torpdahl, S. Ethelberg, and A.M. Hammerum. 2009. Variation in Antimicrobial Resistance in Sporadic and Outbreak-related Salmonella enterica Serovar Typhimurium. Emerg. Infect. Dis. 15:101-103. Retrieved May 8, 2011, fromhttp://www.ncbi.nlm.nih.gov/pmc/articles/PMC2660706/pdf/08-0853_finalD.pdf.
43. Normanno, G., G. La Salandra, A. Dambrosio, N.C. Quaglia, M. Corrente. 2007. Occurrence, Characterization and Antimicrobial Resistance of Enterotoxigenic Staphylococcus aureus Isolated from Meat and Dairy Products. Int. J. Food Microbiol. 115:290-296. Abstract Retrieved April 12, 2011, from http://www.ncbi.nlm.nih.gov/pubmed/17321621.
44. Normanno, G., M. Corrente, G. La Salandra, A. Dambrosio, N.C. Quaglia et al. 2007. Methicillin-Resistant Staphylococcus aureus (MRSA) in Foods of Animal Origin Product in Italy.Int. J. Food Microbiol. 117:219-222. Abstract Retrieved April 6, 2011, fromhttp://www.ncbi.nlm.nih.gov/pubmed/17533002.
45. Pu Shuaihua, F. Han and B. Ge. 2009. Isolation and Characterization of Methicillin-ResistantStaphylococcus aureus Strains from Louisiana Retail Meats. Appl. Environ Microbiol. 75:265-267. Retrieved May 15, 2011, from http://aem.asm.org/cgi/reprint/75/1/265.pdf.
46. Ryan, C.A. , M.K. Nickels, N.T. Hargett-Bean, M.E. Potter, T. Endo et al. 1987. Massive Outbreak of Antimicrobial-Resistant Salmonellosis Traced to Pasteurized Milk. JAMA. 258:3269-3274. Retrieved May 20, 2011, from http://jeffosadec.files.wordpress.com/2011/01/massive-outbreak-of-antimicrobial-resistant-s almonellosis-traced-to-pasteurized-milk.pdf.
47. Schroeder, C.M., C. Zhao, C. DebRoy, J. Torcolini, S. Zhao, D.G. White et al. 2002. Antimicrobial Resistance of Escherichia coli O157 Isolated from Humans, Cattle, Swine, and Food. Appl. Environ. Microbiol. 68:576-581. Retrieved April 20, 2011, fromhttp://aem.asm.org/cgi/reprint/68/2/576.
48. Silbergeld, E.K., J. Graham and L.B. Price. 2008. Industrial Food Animal Production, Antimicrobial Resistance, and Human Health. Annu. Rev. Public Health. 29:151-169. Abstract Retrieved April 24, 2011, from http://www.ncbi.nlm.nih.gov/pubmed/18348709.
49. Sockett, D.C. 2006. Antimicrobial Susceptibility Testing. Wisconsin Veterinary Diagnostic Laboratory. Retrieved May 8, 2011, fromhttp://www.wvdl.wisc.edu/PDF/WVDL.Info.Antimicrobial_Susceptibility_Testing_at_WVDL.pdf .
50. Teale, C.J. 2002. Antimicrobial Resistance and the Food Chain. J Appl. Microbiol. Symp. Suppl. 92:85S-89S. Retrieved April 22, 2011, fromhttp://onlinelibrary.wiley.com/doi/10.1046/j.1365-2672.92.5s1.20.x/pdf.
51. Threlfall, E.J. 2002. Antimicrobial Drug Resistance in Salmonella: Problems and Perspectives in Food- and Water-borne Infections. FEMS Microbiol. Rev. 26:141-148. Retrieved April 24, 2011, from http://onlinelibrary.wiley.com/doi/10.1111/j.1574-6976.2002.tb00606.x/pdf.
52. USDA Agricultural Research Service. 2011. Annual Report 2010. An Integrated Systems Approach to Reduce Salmonella in Organic and All Natural Poultry Handling. Retrieved May 25, 2011, from http://ars.usda.gov/research/projects/projects.htm?ACCN_NO=413129&showpars=true&fy=2010 .
53. USDA Agricultural Research Service. 2011. Annual Report 2010. Development of Resistance to 4th Generation Cephalosporin. Retrieved May 26, 2011, fromhttp://ars.usda.gov/research/projects/projects.htm?ACCN_NO=411533&showpars=true&fy=2010 .
54. USDA Agricultural Research Service. 2011. Annual Report 2010. Epidemiology, Ecology, and Molecular Genetics of Antimicrobial Resistance in Pathogenic and Commensal Bacteria from Food Animals. Retrieved May 23, 2011, fromhttp://ars.usda.gov/research/projects/projects.htm?ACCN_NO=410525&showpars=true&fy=2010 .
55. USDA Agricultural Research Service. 2011. Annual Report 2010. Molecular Analysis ofSalmonella Virulence, Antibiotic Resistance, and Host Response. Retrieved May 26, 2011, fromhttp://www.ars.usda.gov/research/projects/projects.htm?ACCN_NO=409771&showpars=true&fy=2010 .
56. USDA Agricultural Research Service. 2011. Annual Report 2010. Novel Pre-Harvest Intervention to Protect Antimicrobials of Critical Importance in Human and Veterinary Medicine. Retrieved May 24, 2011, from http://ars.usda.gov/research/projects/projects.htm?ACCN_NO=416861&showpars=true&fy=2010 .
57. Utah Department of Health. Office of Epidemiology. 2005. Public Health Issues in Antimicrobial Susceptibility Testing. Retrieved May 5, 2011, fromhttp://health.utah.gov/epi/fact_sheets/antibiotics/antibio_st_print.pdf.
58. Villar, G.R., M.D. Macek, S. Simons, P.S. Hayes, M.J. Goldoft et al. 1999. Investigation of Multidrug-Resistant Salmonella Serotype Typhimurium DT 104 Infections Linked to Raw-Milk Cheese in Washington State. JAMA. 281: 1811-1816. Retrieved May 18, 2011, fromhttp://jama.ama-assn.org/content/281/19/1811.full.pdf.
59. Walker, R. A., A.J. Lawson, E.A. Lindsay, L.R. Ward, P.A. Wright et al. 2000. Decreased Susceptibility to Ciprofloxacin in Outbreak-Associated Multiresistant Salmonella typhimuriumDT104. Vet. Record. 147:395-386. Abstract Retrieved May 22, 2011, fromhttp://www.cabdirect.org/abstracts/20003001268.html.
60. White, D.G., S. Zhao, S. Simjee, D.D. Wagner, and P.F. McDermott. 2002. Antimicrobial Resistance of Foodborne Pathogens. Microbes and Infection. Abstract Retrieved April 9, 2011, from http://www.ncbi.nlm.nih.gov/pubmed/11932191.
61. Wiegand, I., K. Hilpert and R.E.W. Hancock. 2008. Agar and Broth Dilution Methods to Determine the Minimal Inhibitory Concentration (MIC) of Antimicrobial Substances. Nature Protocols. 3:163-175. Retrieved May 7, 2011, fromhttp://www.cmdr.ubc.ca/bobh/rjpdocs/353_2008_NatureProtocols_3_p163.pdf.
62. World Health Organization. 2011. Antimicrobial Resistance. Frequently Asked Questions. Retrieved May 14, 2011, from http://www.who.int/drugresistance/amr_q&a.pdf.
63. World Health Organization. 2011. Antimicrobial Resistance. Retrieved April 6, 2011, fromttp://www.who.int/mediacentre/factsheets/fs194/en/.
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