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Meat Safety

DANIEL Y. C. FUNG, MAHA N. HAJMEER, CURTIS L. KASTNER,JUSTIN J. KASTNER, JAMES L. MARSDEN, KAREN P. PENNER,RANDALL K. PHEBUS, J. SCOTT SMITH, and MARTHA A. VANIER

Kansas State University, Manhattan, Kansas

I. INTRODUCTIONA. Current Status of Meat SafetyB. Meat IrradiationC. Dietary SupplementsD. Genetic ModificationE. Consumers’ Knowledge and Practices

II. HISTORY OF MEAT INDUSTRY SAFETYA. Current Status of Meat ConsumptionB. Early Developments of Meat SafetyC. Food Safety and Government Regulations

III. MICROBIOLOGICAL HAZARDS ASSOCIATED WITH MEATSA. Meat MicrobiologyB. Microbiological Intervention StrategiesC. Rapid Methods and Automation in Microbiology

IV. CHEMICAL HAZARDS ASSOCIATED WITH MEATSA. Pesticide ResiduesB. Hormone DisruptorsC. Antibiotic ResiduesD. Chemicals from Production or Processing

V. PHYSICAL HAZARDS ASSOCIATED WITH MEATS: IDENTIFICATION ANDCONTROL

VI. CURRENT REGULATORY POLICIES AND INSPECTIONA. Concepts of Hazard Analysis Critical Control Points (HACCP)B. Operational Steps in HACCP

* This material is based upon work supported by the Cooperative State Research, Education, and Extension Ser-vice, United States Department of Agriculture, under Agreement no. 93-34211-8362. Contribution no. 00-193-Bfrom the Kansas-State Agricultural Experiment Station.

Copyright © 2001 by Marcel Dekker, Inc. All Rights Reserved.

C. Potential for Recall of Meat and Poultry ProductsD. USDA Policy on RecallsE. Processes of Conducting a RecallF. Imported Products: State vs. Federal Programs and Agencies InvolvedG. Definitions

VII. MEAT SAFETY IN THE FUTUREA. Food/Meat Safety and Research NeedsB. Domestic and International Meat Safety in the Future and Meat Safety Standards

VIII. SUMMARY

REFERENCES

I. INTRODUCTION

A. Current Status of Meat Safety

The safety of food and meat is of major concern to consumers, processors, retailers, foodservice industry, government agencies, educational institutions, public health profession-als, researchers, and the general public locally, regionally, nationally, and internationally.Meat safety during processing, packaging, transporting, storing, displaying, selling, cook-ing, serving, and eventually consumption ideally should be constantly under tight scrutinyby government officials, food processors, food handlers, food providers, and the consumersthemselves. Although in developed countries food and meat usually are safe for consump-tion after proper preparation, many factors can lead to foodborne disease outbreaks. Someoutbreaks can be mild and affect a small number of people, but others can be large and af-fect hundreds and thousands of people, resulting in serious short- and long-term conse-quences and even death. The purpose of this chapter is to examine some major issues re-lated to meat safety.

Although ascertaining the exact number of foodborne outbreaks in the world is im-possible, the number may be in the hundreds of millions per year. In the United States, es-timates have ranged from 1.4 million to 150 million cases per year (2). Todd (71) estimatedthat 12.6 million foodborne illness cases occurred per year, costing $8.4 billion. Bean andGriffin (9) reported that from 1973 to 1987, a total of 7,458 outbreaks with 237,545 casesoccurred in the United States, of which 327 and 120 outbreaks were attributed to beef andpoultry, respectively. A more recent report by Bean et al. (8) indicated that 2,423 outbreaksoccurred and resulted in 77,373 cases from 1988 to 1992, with bacterial pathogens causingthe largest percentage of outbreaks (79%) and cases (90%). Annual, national, direct and in-direct costs (1993 dollars) were estimated to be $2.9 to $6.7 billion, respectively, for food-borne illnesses caused by Campylobacter jejuni or Campylobacter coli, Clostridium per-fringens, Escherichia coli O157:H7, Listeria monocytogenes, Salmonella (nontyphoid),and Staphylococcus aureus by the Centers for Disease Control and Prevention (15). Themost recent estimates (September 16, 1999) by the CDC were 325,000 serious illnesses re-sulting in hospitalization, 76 million cases of gastrointestinal illnesses, and 5,000 deathseach year in the United States. This number of annual deaths was reduced from the 9,000reported by CDC in previous years.

Estimating the number of outbreaks and cases caused directly by meat products is dif-ficult because sources for a large number of outbreaks were listed as “multiple vehicles”and “unknown”. For example, in 1992 the percentages of outbreaks by vehicle of trans-mission were beef (2.2%), chicken (1.7%); ham (0.5%); unknown meat (0.7%); turkey

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(0.7%), multiple vehicles (13.3%), and unknown vehicle (62.0%). However, there is nodoubt that meat accounts for many foodborne disease outbreaks and cases annually.

The most sensational outbreak related to meat was the Escherichia coli O157:H7 out-break attributed to undercooked hamburger by a fast food chain in the Pacific Northwest inlate 1992 and early 1993, which resulted in 501 cases, 151 hospitalizations, 45 cases ofhemolytic uremic syndrome (HUS), and four deaths (3). This outbreak literally transformedU.S. consumers’ awareness of and concern about food safety issues and directly led tochanges in government policy and regulation that resulted in improvement of safety in allareas of the food industry.

This outbreak directly and indirectly stimulated the formation and active involve-ment in the public policy arena of consumer groups such as Safe Tables Our Priority(S.T.O.P.) and the Lois Joy Galler Foundation for Hemolytic Uremic Syndrome, Inc. KarenPenner, in a lecture entitled “Consumers and Food Safety” at the Excellence in Food Sci-ence X program held at Kansas State University on September 17, 1999, indicated that con-sumers’ fears about the food supply include pesticides, Salmonella, irradiation, biotech-nology, growth hormones, E. coli O157:H7, lead, product tampering, and milk allergies. Asurvey by the Food Market Institute (FMI) (31) of consumers’ attitudes from 1994 to 1998showed that confidence in food safety was lowest in 1994 (73%), peaked at 84% in 1996,and fell to 81% in 1998. The FMI also reported that about 70% to 75% of consumers ratedproduct safety very important during this period. The report indicated where food safetyproblems occur, from highest to lowest: in processing, at restaurants, at home, during trans-portation, in markets, and on farms. The most important source of foodborne illness wasmishandling of food, followed by “germs,” chicken, improper cooking, old food, beef,seafoods, mayonnaise, and fruit and vegetables. Telephone calls to the Kansas Departmentof Health and Education by consumers with questions about food safety issues increasedfrom less than 500 in 1988 to 2000 in 1999 (Paige, S. personal communication, 1999). Cur-rent emerging issues related to consumers’ perceptions of food safety include irradiation,dietary supplements, genetically modified foods, and consumers’ practices.

B. Meat Irradiation

Meat irradiation appears to be imminent, especially with the use of electron beam technol-ogy rather than radioactive isotopes. The Titan Corporation Plant in Sioux City, Iowa, is onthe verge of opening. The United States Department of Agriculture (USDA) has approvedan irradiation level of 1.5 to 3.0 kGy for poultry (fresh or frozen), and proposed approvalof maximum levels of 4.5 kGy and 7.0 kGy for fresh and frozen red meat, respectively. In-ternationally, 41 countries have clearances for commercial food irradiation, with meat andpoultry clearances in 23 countries for different categories and different doses. Consumeracceptance of irradiated food is high. A report by the FMI and Grocery Manufacturers ofAmerica (32) showed that 60% of consumers were likely to buy irradiated meat in 1997 and55% in 1998. John A. Fox (personal communication, 1999) reported that 80% of con-sumers surveyed are willing to purchase irradiated versus nonirradiated poultry, if the priceis the same; 30% would pay a 10% premium; and 15% would pay a 20% premium. Thus,meat irradiation is moving in a positive mode with consumers at the present time.

C. Dietary Supplements

The Dietary Supplement and Health Education Act (DSHEA) of 1994 (an amended FoodAdditive Amendments of 1958) permits the use of vitamins, minerals, herbs or other botan-

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icals, amino acids, and other substances in foods. The safety issues involved include over-supplementation, use of botanicals not from plants typically used for food, use of hormoneproducts, and the lack of purity of ingredients. Some of the problems include product re-calls, deaths attributed to supplements containing ephedra, and reports of adverse effects.However, about 50% of the public use dietary supplements, as reported by Camire andKantor (13).

D. Genetic Modification

According to Hoban (44), U.S. consumers’ acceptance of genetically modified food is asfollows: 72% support agriculture biotechnologies, 90% support medical biotechnologies,75% believe biotechnologies will result in personal family benefits, and about 66% wouldbuy produce modified to taste better or remain fresher. Internationally, 61% of Europeansavoid products with modified ingredients. Market tests of cloned beef in Japan showed thatthe low price (50% lower than other beef) outweighed concerns for the new technology.Starting in April 2000 in Japan, tofu, corn snacks, and soy milk with genetically modifiedingredients must have the proper labeling. Labeling of meat is under consideration.

E. Consumers’ Knowledge and Practices

The last hurdle in food safety is the consumer. Zhang et al. (79) identified some risky homeconsumption practices in Kansas: 26% of respondents to a survey canned their vegetables,9% ate undercooked hamburger, 2% drank unpasteurized milk, and 56% consumed raw orundercooked eggs. In a national survey, Gravani et al. (41) reported that 92% of consumerswere concerned about raw meat left out for more than 4 hours, 82% were concerned aboutcooked meat left out for more than 4 hours, 24% believed off-odor or flavor caused illness,28% believed freezing kills harmful bacteria, and 17% did not wash their hands after han-dling raw poultry. Thus, consumers still need great deal more food safety education.

Challenges in such education include recognizing current consumers as key playersin food safety and informing them about emerging pathogens, about new technologies, andbenefits and risks; stressing the need to change behavior as new knowledge is gained; andcommunicating to all that they are food safety educators, wherever they are in the food andnutrition system. Meat safety will be enhanced greatly by appropriate consumer educationin all levels of society.

II. HISTORY OF MEAT INDUSTRY SAFETY

A. Current Status of Meat Consumption

Meat is nutritious for humans and other living entities, such as microorganisms. Growth ofundesirable microorganisms in meat and meat products may result in spoilage and food-borne illnesses. Thus, from ancient times, humans have devised ways to ensure the safetyof meat mainly through religious practices.

Meat is a major part of the human diet. Lupton and Cross (56) reported that U.S. percapita consumption of meat, poultry, and fish in 1990 was 191.5 lb, including 112.3 lb ofred meat, 63.8 lb of poultry, and 15.4 lb of fish. Compared with similar data in 1965, theincreases in consumption were 1113% for chicken, 146% for turkey, and 37% for fish,while consumption of red meat decreased by 10%. More recent data compiled by Weaber(77) in 1999 indicated that per capita consumption was 120.4 lb. for red meat and 96.7 lb.

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for chicken and turkey. Thus, consumption of red meat and poultry combined increased be-tween 1990 and 1999 (176.1 lb. versus 217.1 lb.) Per capita spending on beef, pork, andchicken combined increased from $332.69 in 1986 to $425.57 in 1998; however, spendingon beef decreased from 53.8% of the total in 1986 to 44.1% in 1998.

There is no doubt that meat is the basis of a big industry in the United States and inmany developed countries. For example, the volume of U.S. beef exports increased fromabout 170 million lb. in 1976 (valued at $110 million) to about 2,000 million lb in the late1990s (valued at about $2.5 billion). Cattle sold by the 10 largest US companies in 1998were worth $30 billion (77). With so much at stake, it is necessary to keep meat safe at alllevels of production, processing, and sales.

B. Early Developments of Meat Safety

Upton Sinclair’s 1906 book (66) The Jungle is frequently labeled as the first public call toaddress meat safety in the United States. Although Sinclair’s book certainly did propel thetightening of U.S. food safety policy, public concern and governmental policies dealingwith the safety of American food clearly were born much earlier. In fact, food safety issueswere on the minds of pre-Colonial era pirates; the U.S. Army; President Abraham Lincoln;and, most noticeably, foreign importers of U.S. food products.

During the 17th and early 18th centuries, pirates in the West Indies earned the name“buccaneers” for their characteristic practice of drying—or “boucaning”—beef. This prac-tice enabled them to stock their ships with preserved, safe meat that they both consumedand sold, as reported by Price and Schweigert (65). Other preservation practices, whichhave beginnings dating back to 2000 B.C., have played a significant role in the history ofthe United States. For example, during the War of 1812, the U.S. Army purchased a dis-proportionate amount of its meat from New Englander Sam Wilson. Mr. Wilson, who wasrenowned for applying the basic food safety principles of using clean barrels and low tem-perature storage for his salted beef, stamped the letters “US,” for “United States,” on hisbarrels earmarked for sale to the Army. Interestingly, those in the army interpreted the let-ters to represent “Uncle Sam’s” meat, and over time, the origin of this term became ob-scure. Today, of course, the accepted connotation of “Uncle Sam” is the U.S. governmentitself (65).

Formal U.S. food safety policy has its historical ties in the USDA. Indeed, if one isto comprehend the development of U.S. food safety policy, a familiarity with the history ofthis federal department is necessary. The USDA began as a sub-cabinet-level agency onMay 15, 1862, when President Abraham Lincoln signed the enabling legislation for the de-partment’s creation. Although President Lincoln had unsuccessfully pushed for cabinet-level status for the department, he was nonetheless pleased that the United States now hada department to help enhance the productivity of the American farmer (45). This purpose—to make farmers more productive—was narrowly adhered to by the department during itsinitial years. Interestingly, however, other emphases, particularly regulation, within the de-partment were hinted at early on in its history. Perhaps the most prophetic glimpse of a fu-ture expansion of the department’s activities came during President Lincoln’s Annual Mes-sage to Congress on December 1, 1862. Only 7 months after the inception of the agriculturedepartment, Lincoln mentions that “some valuable tests in chemical science [are] now inprogress in the laboratory” (4). Although it is certainly debatable for what purposes—to en-hance productivity or food safety—such chemical tests were being conducted, the merepresence of this emphasis provided the groundwork for future food safety investigations in

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the department’s Bureau of Chemistry. In 1883, Harvey W. Wiley, the Bureau’s director,began to address public concerns regarding the widespread practice of selling colored lardas butter and other food adulteration atrocities (5). In addition to the chemical examinationof foods, Wiley’s famous Poison Squad, a team of healthy young men who were fed adul-terated food until their health deteriorated, was effective in arousing the public’s concernabout food safety (5).

One of the strongest influences on the development of U.S. food safety policy wasforeign trade. In the late 1800s, European countries were beginning to voice their legiti-mate concerns about pleuropneumonia, tuberculosis, trichinae, and other animal diseasesin U.S. livestock and meat exports (17). First among the international community to takeaction was England, which in 1879 required that all cattle imported from the UnitedStates be slaughtered within 10 days of importation in order to minimize the spread ofpleuropneumonia. Italy and Hungary followed with trade restrictions on U.S. pork be-cause of trichinae. Later, in 1880, Germany and Spain implemented bans on U.S. meat, asdid France, Turkey, and Romania in 1881. Before the end of the 1880s, Greece andDenmark had joined the list of nations banning U.S. meat on the basis of food safetyconcerns (17).

As a result of the significant shrinkage of willing international buyers, U.S. meat ex-ports fell significantly. The country, having no animal or meat inspection systems in place,found itself with a huge credibility problem with food safety. This problem, felt mostpainfully by the meat packing and livestock industries, forced the U.S. government to in-augurate a service that would certify to foreign governments the healthfulness of Americananimals and the safety of its meat (17).

The U.S. Congress, under great pressure from the meat packers and livestock pro-ducers, passed legislation in August 1890 to create an animal and meat inspection program(69). This piece of legislation actually was only a feeble attempt by the government to sat-isfy the packers and producers, and the country’s credibility problem persisted. Meanwhile,the USDA Bureau of Animal Industry, created in 1884 to conduct research on animal dis-eases, was priming itself for an expanded regulatory role. A marked enlargement of regu-latory power was granted to the Bureau after the unable-to-export meat industry convincedCongress to establish an inspection program of real value. On March 3, 1891, the U.S.Congress added a truly substantive policy for inspecting animals and meat to the 1890 in-spection law. Now the Bureau of Animal Industry clearly had both the power and budgetaryauthority to inspect and certify (to indicate passage of) U.S. animals and meat prior to ex-portation. The inspection and certification system affected offered-for-export salted porkand bacon, cattle, sheep, and swine (5).

The first-ever inspection carried out as a result of the 1891 legislation occurred inNew York City on May 12, 1891. The economic fruits of the legislation soon became ap-parent when, in September of 1891, Germany removed its restriction on U.S. pork. Later,Denmark, France, Italy, and Hungary followed by repealing their own trade bans. It wasclear that the new meat and animal inspection policy had helped resuscitate exports by re-capturing the respect of the international community (17).

The 1890 Meat Inspection Act, after the 1891 modification and other amendments,also required inspection prior to the slaughter of cattle, sheep, and hogs that were bound forinterstate trade. Postmortem inspection was to be implemented as well, but only at the dis-cretion of the U.S. Secretary of Agriculture (17). Although it had helped reestablish inter-national trade stability for meat and animals, the U.S. inspection program was still in its in-fancy and laden with problems. In 1894, Dr. D.E. Salmon, Chief of the Bureau of Animal

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Industry, complained that “The large number of abattoirs (slaughterhouses) which do an in-terstate trade has made it impossible up to the present time to extend the service sufficientlyto include them all,” as recorded by the Department of Agriculture in 1894 (22). Althoughthe USDA hailed the fact that only one in 5,000 cattle carried tuberculosis, it was concernedthat because of meager Congressional appropriations, it was unable to inspect all meat andanimals identified for interstate trade. Because of this lack of funding and the popularity ofa congressionally mandated program to microscopically inspect pork (for export), officialswithin the USDA and the meat industry itself began to debate who should pay for inspec-tion. Dr. Salmon at the Bureau of Animal Industry, writing on behalf of the Secretary ofAgriculture, recommended the following in 1894:

The Secretary of Agriculture recommends that the law providing for the inspection of exportand interstate meat be so amended as to compel the owners of the meat inspected to pay thecost of the microscopic inspection. . . It is only equitable that those pay for the inspection whoare directly pecuniarily benefited thereby. As the law exists today, any slaughtering establish-ment, no matter how insignificant, which declares it has or expects to have foreign trade inmeats, has a legal right to demand governmental inspection and certification. It costs individ-uals nothing (22).

In 1899, the Department unsuccessfully appealed for an emergency appropriation toaddress anticipated needs in inspection (23). By 1905, U.S. meat inspection policy man-dated both antemortem and postmortem inspections, and government and industry officialspraised the program. Millions of dollars of annual foreign trade depended on the success ofthe meat inspection program (24), and this economic motivation fueled the program’sfunding.

This meat inspection program had more flaws, however. Because the policy appliedonly to products bound for interstate trade, a huge intrastate market of beef, pork, and lambwas not inspected. Similarly, condemned meat, although not permitted by the federal gov-ernment for interstate trade, was subject only to state and municipal governance. Unfortu-nately, these local units of government usually were plagued by graft, corruption, and anincreasingly powerful “Beef Trust” (66).

At the end of the 19th century, this Beef Trust, or group of meat industry and gov-ernment leaders that exploited the flaws of U.S. meat inspection policy while providingbrutal labor conditions in order to achieve economic gains, was under scrutiny by the pub-lic. During the Spanish-American War, the U.S. Army had been supplied with rotten meat.Quickly, charges of graft in connection with this event were brought against members ofindustry and government by Theodore Roosevelt (40).

The exposure of graft by the Beef Trust was best accomplished by Upton Sinclair,who, in 1904, wrote The Jungle. Although history books often label this work as a focusedattack on food safety atrocities, it actually was fueled by a more broad motivation: social-ism. Sinclair was hired by the socialist weekly The Appeal to Reason to investigate laborconditions in the Chicago Stockyards and provide a report. Sinclair, after spending 7 weeksamidst the brutalities of “Packingtown,” serially composed The Jungle week-by-week inThe Appeal to Reason during 1904. He was unable to publish the book in its entirety until1906.

Although the primary purpose of The Jungle was to advocate socialism, Sinclair’svivid descriptions of formaldehyde in milk, diseased meat, adulterated butter, tubercularpork, borax-coated and glycerine-filled sausage, and other public health atrocities gainedthe attention of the American public. Although President Theodore Roosevelt mocked Sin-

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clair for his socialist convictions, he used Sinclair’s work to push long-stalled legislationfor meat inspection and pure food through Congress. These two 1906 measures, the Bev-eridge Amendment (now referred to as the Federal Meat Inspection Act or FMIA) and theFood and Drug Act, brought a new level of food safety assurance to the American public.

In addition to this legislation, the United States was making major leaps in foodsafety technologies. In 1890, commercial pasteurization of milk was begun in the UnitedStates. In the same year, mechanical refrigeration for fruit storage was begun in Chicago(47). In 1910, the New York City Board of Health issued an order requiring the pasteur-ization of milk; this governmental mandate marked a significant moment in U.S. foodsafety policy. In 1939, the new Food, Drug, and Cosmetic Act became law, ushering in anew era of consumer-protection measures, while at the same time causing the Food andDrug Administration (FDA) to be removed from the Department of Agriculture despite ob-jections from Secretary of Agriculture Henry Wallace (5). In 1958, the Food AdditivesAmendment was added to the Food, Drug, and Cosmetics Act.

After World War II, poultry became a popular commodity, and in 1957, the federalPoultry Products Inspection Act (PPIA) was passed. This measure, like the FMIA, requiresfederal inspection for interstate commerce. In 1968, the FMIA and PPIA were broadenedto mandate states to adopt inspection systems for their intrastate products that were “equalto” the federal inspection system. This mandate upset some states, but a provision was soonadded to provide federal inspection to those states that did not have an adequate inspectionprogram (5).

The 1906 FMIA, the 1957 PPIA, and the 1958 Food, Drug, and Cosmetics Act stillserve as the principal authorities for food safety policy in the United States. However, theface of the U.S. food supply has changed considerably over the past century, and new food-borne disease trends are developing. A food supply that is highly processed, shipped acrossthe country, and imported from other countries has presented and will continue to presentchallenges to U.S. policy makers (33). A shift from a purely sight-smell-touch method ofinspection to a prevention-based philosophy is being made in the USDA Food Safety andInspection Service (FSIS) to address the microscopic pathogens that are causing 4,000deaths and nine million cases of foodborne disease each year. The incorporation of HazardAnalysis Critical Control Point (HACCP) and other prevention-based policies is being im-plemented at present within both the USDA and the FDA. Consumers, scientists, and a sig-nificantly large portion of the food industry are embracing these new philosophies.

Food safety policy in the United States continues to develop. Throughout its dynamichistory, U.S. food safety policy has influenced, or been influenced by, our nation’s economicsystem, the voices of authors, and foreign governments. If history is any indication, futureU.S. food safety policy issues will continue to be both intriguing and challenging (51).

C. Food Safety and Government Regulations

Consumer reaction to the 1993 outbreak of Escherichia coli O157:H7 forced a reassess-ment of our nation’s meat inspection system. In 1994, USDA Undersecretary for FoodSafety, Michael Taylor, declared E. coli O157:H7 an adulterant in ground beef. The Amer-ican Meat Institute and other trade organizations sued to block the implementation of thispolicy in federal court. A federal court judge upheld USDA policy, and a monitoring pro-gram for E. coli O157:H7 was instituted in 1995. Under this program, the USDA monitorssamples of raw ground beef at retail stores and at grinding plants. Every positive sample re-sults in a product recall.

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A recall at Hudson Foods in 1998 was the largest in U.S. history—25 millionpounds—and resulted in dissolution of the company. After that incident, the USDA at-tempted to shift the responsibility for control of E. coli O157:H7 to the slaughter segmentof the industry through Directive 10.010.1. Under this directive, grinding plants are ex-empted from USDA monitoring if their slaughter supplier employs a validated interventiontechnology and verifies its effectiveness through a routine microbiological testing program.In 1999, the four largest U.S. meat packers announced that they were in compliance withthis directive. The focus of HACCP-based critical control points (CCPs) is to prevent, elim-inate, or reduce hazards to an acceptable level. Steam pasteurization was introduced as apotential CCP for beef carcasses in 1995. In the same year, steam vacuuming was approvedby the USDA for removal of physical defects from carcasses. A rule allowing for the irra-diation pasteurization of ground beef and other meat products were implemented in Febru-ary of 2000 by the USDA.

The term pasteurization is defined by The American Heritage Dictionary as “The actor process of destroying most disease-producing microorganisms.” Technologies are underdevelopment to reduce bioload and allow for the pasteurization of meat and poultry prod-ucts. Pasteurization can be achieved by chemical treatments (i.e., peracetic acid), heat (i.e.,post-process pasteurization of processed meat), and irradiation with either gamma rays oran electron beam. By minimizing contamination, the irradiation pasteurization of raw meatand poultry products may be achieved at very low doses, thereby preventing undesirablequality changes.

Measures to achieve bioload reduction in the live animal may include vaccines and/orthe use of competitive exclusion. The objective of both the USDA and the meat industry isthe elimination of pathogens from meat and poultry products. In 1995, the USDA proposedto make HACCP mandatory in all meat and poultry plants. Under this regulation, largeplants were required to implement HACCP in January 1998 and small plants in January1999. The final stages of HACCP implementation were complete in January 2000 with theinclusion of very small plants under USDA’s HACCP rule.

The years following the 1993 Jack-in-the-Box outbreak will be remembered as aturning point in inspection and food safety, with the most significant achievements beingthe implementation of HACCP across the entire meat and poultry industry and the adventof pasteurization for raw meat and poultry products.

III. MICROBIOLOGICAL HAZARDS ASSOCIATED WITH MEATS

A. Meat Microbiology

All living things interact with the environment that they inhabit. Therefore, the microbeson and in food animals are influenced by the surroundings in which they are reared orhoused. A dirty environment with soil, mud, fecal materials, urine, stale water, insects, ro-dents, flies, and other animals will influence the microbial loads of the hair, hide, udder,skin, and exposed areas of the animal. Good sanitation of the environment will help reducethe microbes on the surface of the animal before transportation to slaughter facilities. Theanimal itself has an inherent microbial population in the gastrointestinal tract and organs.A healthy animal will have fewer pathogenic organisms, and a diseased animal will carrypathogens into the processing areas. During transportation, stress on the animals also willinfluence shedding of organisms into the transportation environment, for example, a truckor holding pen. In the processing area, the cleanliness of the facilities also influences the

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microbial load of the meat after slaughter and fabrication. Sticking, bleeding, and scaldingoperations will spread microorganisms onto and into various tissues. Fecal material fromthe surface of the animal or from the evisceration process will spread potential pathogensto the meat during fabrication. Contaminated water used to clean the processing facilitiesor wash the carcasses also can contribute to microbial contamination of the meat. Chilling,storing, aging, cutting, packing, transporting, distributing, handling, displaying, and sellingof meat and meat products all can contribute to further contamination of the meat. The en-vironment used for the preparations of raw meat for sale such as cutting, slicing, ground-ing, wrapping, and final presentation of the product to consumers also may add to the con-tamination level. Finally, at the cooking stage, improper time and temperature of foodpreparation may not render the meat safe for consumption. The entire “farm to table” chaincan add to contamination of meat by microorganisms. Therefore food scientists, govern-ment agencies, and food processors all have responsibilities to design ways and means tominimize and eliminate these hazards and provide consumers with a safe product as de-tailed by Bourgeois et al. (10), ICMSF (46), Doyle et al. (26), Davies and Board (21).

The contamination of carcasses and various meat cuts in terms of numbers and kindsof various spoilage bacteria, yeast, molds, pathogens, and emerging pathogens has beenstudied and reported extensively (48). The list of microorganisms found on meat and poul-try is extensive. Frequently encountered genera include Pseudomonas, Bacillus, Bro-chothrix, Campylobacter, Clostridium, Escherichia, Enterobacter, Enterococcus, Strepto-coccus, Lactococcus, Lactobacillus, Listeria, Micrococcus, Staphylococcus, Pediococcus,Salmonella, Serratia, Yersinia, and other members of the family Enterobacteriaceae.Yeasts and molds found in meat products include Candida, Torulopsis, Saccharomyces,Rhodotorula, Mucor, Rhizopus, Penicillium, Geotrichum, and Aspergillus. The number ofmicroorganisms on the surface of meat also varies greatly. Fung (35) developed a micro-bial scale to indicate spoilage potential of meat. A bacterial count on meat of 0 log to 2 logcolony-forming units (CFU)/g is considered low. When the count reaches 3 log to 4 logCFU/g, it is considered intermediate. A count of 5 log to 6 log CFU/g is considered high.A count of 7 log CFU/g is considered the “Index of Spoilage,” because when the numberreaches higher than 8 log CFU/g, the meat will have an odor, and at 9 log CFU/g, slime willappear. Most ground beef in supermarkets has 1 million bacteria per gram and will spoilwithin a week in home refrigerators. Excellent reviews on the subject were provided by So-fos (67) and Milner (57), who discussed the sources of contamination of red meat, poultry,and seafoods; types of contamination of red meat, poultry, seafoods and processed prod-ucts; microbial effects on muscle foods; and control of microbial growth in muscle foods.A detailed presentation of important microbial groups in meats is provided by DouglasMarshall in the chapter on “Microbiology of Meats” in the volume.

B. Microbiological Intervention Strategies

A variety of intervention strategies have been used to reduce spoilage and pathogenic or-ganisms on meat surfaces and meat products. Nutsch (61) reviewed these strategies in de-tail in a PhD. dissertation. The following are synopses of major intervention strategies:

1. Handling of Carcasses

Hides and viscera were cited as significant sources of bacterial contamination duringslaughter and processing. The slaughter environment such as walls, floors, air, and handsand garments of workers also were noted as potential sources of cross-contamination. Cor-

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rective measures include chilling carcasses as soon as possible, sanitizing knives betweenanimals, minimizing contact between hide and skinned carcass surfaces, and general goodenvironmental sanitation in the slaughter area.

2. Water Washing

Many washing procedures have been tested with various combinations of temperature ofwater (35°C to 80°C), pressure (10 psi to 400 psi), contact time (4 sec to 36 sec), types ofinstruments, distance from the carcasses, and volume of water (e.g., 1.5 gallon, 1.5 L). Re-ductions of bacteria ranged from almost none to several logs, depending on the combina-tion. The conclusion is that water washing has value in removing extraneous materials andreducing some microorganisms on the carcasses.

3. Hot Water Washing

Here again, many combinations have been tested using various high temperatures such as80°C, 85°C, or 96°C. Care must be taken to avoid discoloration of meat when using high-temperature washing. Reductions of bacteria again ranged from almost none to a 1 to 2 logCFU/cm2 reduction, depending on the time, temperature, pressure, and combinationsthereof. On balance, hot water washing is more effective than cold water washing in re-ducing bacteria from carcasses.

4. Decontamination by Chlorine

Incorporation of chlorine into water to wash carcasses has been investigated by many re-searchers. Chlorine levels used ranged from 20 ppm to 400 ppm, and the effectiveness isinfluenced by the temperature and pH of water. Reductions of microorganisms ranged fromnegligible to 2 log CFU/cm2.

5. Decontamination by Organic Acid Treatment

A large body of research has been devoted to this form of decontamination. Acetic acid(1%, 2%, 4%, 5%) spray has been studied extensively. Reduction of bacteria seemed to beorganism dependent. For example, in one study using 1% acetic acid, E. coli was reducedfrom 5 log CFU/cm2 to 2.2 log CFU/cm2, whereas Salmonella wentworth was reduced to1.5 log CFU/cm2. Lactic acid at 2% or 3% also has been studied. Reduction was generallyabout 1 to 2 log CFU/cm2 after treatment. Some studies also combined acetic acid, lacticacid, and even propionic acid in the solution. In general, acid washes can reduce bacterialpopulations by about 2 log CFU/cm2 in optimum combinations.

6. Decontamination by Trimming

Trimming has been used in commercial processing of meat to remove visible contaminants.Many trimming procedures for various types of tissues have been reported. Trimming isvery effective in removing bacteria, because the organisms are removed physically fromthe area, and counts after trimming become very low. Reductions of 2 to 3 log CFU/cm2

have been reported for this procedure. Some studies also have combined washing and trim-ming.

7. Decontamination by Steam Pasteurization™

A commercial antimicrobial carcass intervention process called Steam Pasteurization(SPS™; Frigoscandia Food Process Systems, Bellevue, WA) is being used widely in thebeef slaughter industry. This unit is a stainless steel tunnel encompassing the facility’s

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overhead rail system and is situated immediately prior to the point where carcasses enterthe holding cooler (“hot box”). Carcasses enter the tunnel at normal line speeds and are ex-posed uniformly to saturated steam for 8–10 seconds, bringing the surface temperature upto 85–90°C. The second section of the unit applies a chilled water spray to quickly lowerthe surface temperature of carcasses and reduce adverse color effects. Nutsch et al. (62,63)found the system capable of reducing total aerobic bacterial counts on carcasses by ap-proximately 1.5 log cycles from initial levels of approximately 2.5 log CFU/cm2. Coliform-type populations on carcasses were virtually eliminated. The SPS™ unit, as the last step inthe slaughter phase, serves as a CCP in beef slaughter HACCP programs and is capable ofcontinuously and automatically logging steam chamber temperature for all carcassesprocessed.

8. Decontamination by Steam Vacuuming

Small, localized areas of visible contamination must be removed from carcasses prior towashing. These physical defects can be removed throughout the slaughter process by knifetrimming and/or use of steam vacuuming. Steam vacuuming has become a standard prac-tice in most slaughterhouses and uses a hand-held vacuum nozzle that is sanitized continu-ously by a steam spray. Visible contamination less than one inch in any dimension can bevacuumed from the carcass, thereby reducing yield loss from extensive trimming. Labora-tory validation studies using artificially contaminated meat tissues have shown steam vac-uuming to be effective in reducing microbial contamination on carcasses as reported byDorsa et al. (25) and Phebus et al. (64).

9. Decontamination by Miscellaneous Methods

Other forms of decontamination, including trisodium phosphate, ultraviolet radiation, post-exsanguination dehairing, dry heat, ozone, and bacteriocins, have been used with variousdegrees of success.

B. Rapid Methods and Automation in Microbiology

Rapid methods and automation in microbiology are dynamic fields of study that address theutilization of microbiological, chemical, biochemical, biophysical, immunological, andserological methods for the study of improving isolation, early detection, characterization,and enumeration of microorganisms and their products in clinical, food, industrial, and en-vironmental samples. In the past 15 years, food microbiologists have started to adapt rapidand automated methods in their laboratories. Fung (36–38) has provided detailed reviewson this topic.

1. Improvements in Sampling and Sample Preparation

The Stomacher instrument developed by Tony Sharpe about 20 years ago has become astandard method for homogenizing food samples internationally. It involves putting foodsample and diluents in a sterile bag and placing the bag in the Stomacher, which massagesthe food and dislodges the microbes into the diluent. Viable cell counts then can be madefrom the massaged sample. More recently, Tony Sharpe invented a new instrument namedthe Pulsifier, which can dislodge bacteria from food by pulsification in a bag. Fung et al.(39) evaluated the Pulsifier and found that it provided essentially the same bacterial countsas the Stomacher but with less food debris, which makes the sample better for subsequentmicrobiological manipulations such as ELISA tests or PRC tests.

182 Fung et al.


2. Alternative Methods for Viable Cell Count Procedure

The conventional viable cell count method is time-consuming both in terms of operationand collection of data. Alternative methods that have been well tested in the past 10 yearsare the Spiral Plating, ISOGRID, 3M Petrifilm, and Redigel. All these methods have beenshown to be acceptable in obtaining viable cell counts of foods and are less expensive whenused routinely compared with the conventional method.

3. Instruments for Estimation of Microbial Population and Biomass

The Bactometer, Malthus, and RABIT systems are used to measure impedance and/or con-ductance changes in food due to the growth of total microbes as well as target pathogens.

Monitoring of adenosine triphosphate (ATP) to estimate microbial population andbiomass has gained popularity in recent years. All living things have ATP; thus it can beused to estimate total counts in food and contamination in the environment. Currently, thetrend is to monitor total ATP in the environment regardless of sources (e.g., from bacteria,yeast, mold, blood, or food particles) to ascertain cleanliness of the surfaces (i.e., hygienemonitoring). In this procedure, any amount of ATP beyond the background level will indi-cate contamination of the food preparation surfaces. Cleaning the surfaces properly will re-duce the ATP level.

4. Miniaturized Microbiological Techniques

Identification of microorganisms is an important part of quality assurance and control pro-grams in the food industry. Miniaturized microbiological methods described by Fung (36)as well as API, Enterotube, Minitek, MicroID, IDS, and others are rapid and convenient foridentifying large numbers of pathogens in clinical, food, and industrial samples. Vitek andBiolog are automated miniaturized systems that can identify clinical and environment iso-lates effectively.

5. Immunological Technologies

Enzyme-linked immunoabsorbent assay (ELISA) tests have been very useful in the past 10to 15 years in screening and diagnostic systems. Completely automated systems of ELISAtests such as the VIDAS system, Opus systems, Bio-tek, Detex, and others are now avail-able. Another development is the rapid lateral migration of antigen-antibody complexes intest units for screening target organisms such as E. coli O157:H7, Salmonella, and Listeria,by kits such as VIP and Reveal. These kits provide negative or positive screening results inabout 10 minutes after pre-enrichment of about 18 hr.

Another exciting development in relation to immunology is immunomagnetic cap-ture technology first developed by VICAM for Listeria and now popularized by Dynal fornot only antibody-antigen reactions but also capturing of other target molecules on mag-netic beads. After the capture, a powerful magnet is applied to the side of the test tube toseparate these beads from the rest of the liquid matrix, thus greatly concentrating the targetcells or molecules for further analysis. These methods can eliminate at least one day of de-tection time in many microbiological protocols.

6. Genetic-based Rapid Tests

DNA and/or RNA probes have been used for more than 15 years in rapid detection of tar-get pathogens such as Salmonella and Listeria. Polymerase chain reaction (PCR) for rapidamplification of target DNA has gained much attention recently as a rapid method for de-

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tecting target pathogens. Qualicon markets a BAX system for PCR reaction and also a Ri-boprinting system for characterizing subspecies of target pathogens such as E. coliO157:H7 and Salmonella. These types of genetic techniques certainly will become moreimportant in the future.

IV. CHEMICAL HAZARDS ASSOCIATED WITH MEATS

A. Pesticide Residues

Of all the food contaminants, pesticides probably have received the most interest world-wide. Most pesticides are acutely toxic to humans and animals; even ingestion of low lev-els over a long period of time can have adverse effects. Overall, very few, if any, foods arecontaminated in the United States when pesticides are used according to the prescribed ap-plication guidelines.

The regulation of pesticide use is handled differently by each country throughout theworld, though there is a tendency toward a more unified approach. With the passage of theGATT treaty (General Agreement on Tariffs and Trade), we can expect to see a muchbroader approach to pesticide regulatory activities. The World Health Organization and theUnited Nations Environment Programme play major roles in evaluating and disseminatinginformation on pesticide use and toxicity, as well as other types of toxic compounds.

In the United States, pesticide regulation is under the auspices of three governmentagencies; the Environmental Protection Agency (EPA), the FDA, and the USDA-FSIS. TheEPA is responsible for determining which pesticides are allowed in a particular food andwhat residue levels (if any) are acceptable. Pesticide residues for all foods are covered inParts 150 to 189 of Title 40 of the Code of Federal Regulations (19). Title 40 has an al-phabetical listing of approved chemicals (pesticides), a listing of approved food usages foreach individual pesticide, and residual levels allowed in approved foods. In addition, it con-tains a listing of each commodity/food and pesticides allowed for that food.

Both the FDA and USDA-FSIS (73) are responsible for monitoring pesticideresidues in foods based on levels set by the EPA. The FSIS is responsible for meat and poul-try products, and the FDA covers all other types of raw commodities and processed foodproducts. Since 1995, the FDA has published on their Web site the results from yearly sur-veys of pesticide and chemical residues found in various food items, and that study shouldbe consulted for specific details (30). For years, the USDA has published survey results ofvarious chemical resides in animal products in what is known as the “Red Book.” Both theRed Book and the residue-sampling plan, known as the “Blue Book,” are available in hardcopies and Web versions (74). Unfortunately, there is a lag of about 5 years between thesampling period and the date of publication, which limits its usefulness.

In 1996, the Food Quality Protection Act (FQPA) became law and dramatically al-tered how pesticides are evaluated for human toxicity (76). The FQPA directed the US EPAto further evaluate pesticide risk for children, consider the cumulative effects of exposureto the pesticide and substances having a common mode of action, and consider the poten-tial for endocrine-disrupting effects. In addition, the FQPA removed what has been calledthe “Delaney Paradox.” This was the situation in which the EPA could consider the bene-fit of a pesticide when approving it for use on raw food commodities, even if it was a weakcarcinogen. However, if the food commodity was processed so that the levels were con-centrated above the approved amounts for the original product, then the pesticide residuebecame a “food additive” and was governed by a different law, The Federal Food, Drug,

184 Fung et al.


and Cosmetic Act of 1954 (section 409). Under section 409, the Delaney clause prohibitsthe approval of any food additive that causes cancer in humans or animals.

This section will discuss various pesticides, based on the organism that is to be elim-inated or controlled. Particular attention will be focused on pesticide residues that continueto be associated with potential contamination of meat products.

1. Insecticides

These are by far the most common chemicals used for pest control on both crops and ani-mals. This group can be subdivided into categories based on chemical structure and modeof action.

a. Carbamates. These pesticides can be either insecticides, herbicides, or fungi-cides and have in common a carbamic group in their structures. A variety of substitutionscan occur around the carbamic group, which often will determine both the degree of toxi-city and potential use. In recent years, carbamate residue has not been considered a prob-lem in meat products.

b. Organohalides (halogenated hydrocarbons). Strictly speaking, many classesof pesticides contain halogens, especially chlorine, and can be grouped in this category.The organohalide pesticides have a vast array of different structures but usually have atleast one ring substituent, contain chlorine, and are extremely stable. Examples of this classinclude aldrin, chlordane, dieldrin, endrin, heptachlor, and DDT.

This class of pesticides emerged around the time of World War II. The discovery washeralded as a major breakthrough in the control of various types of insects worldwide (20).The now-infamous DDT was introduced about that time and was critical in the control ofmalaria-bearing mosquitoes. It is probably the least toxic of the organohalides and was rou-tinely applied directly to people, their living quarters, and water supplies. In the 1970s, it andsimilar pesticides were banned in the United States and most countries because of its bioac-cumulation through the food chain, especially in predatory birds such as the bald eagle.

The United Nations Environment Programme at its meeting held in Geneva inSeptember 1999 addressed the worldwide control and production of these type of persis-tent organic pollutants (POPs) (72). Use of almost all of the POPs will be phased out witha few exceptions. There are still concerns that no current substitutes exist for DDT, whichcurrently is produced only in China, India, Mexico, and Russia. It remains the most effec-tive pesticide for use in the control of malaria-bearing mosquitoes and is considered essen-tial in Africa and other tropical regions.

The organohalides are neurotoxins and are noted especially for their persistence inthe environment. Although many have been banned for years, they are still detected read-ily in the environment and fatty tissue of many animals, including humans. The major con-cerns with these pesticides are their potential teratogenicity (toxicity to fetuses), endocrinedisruption, and carcinogenicity.

c. Organophosphates (OPs). These represent a large class of organic compoundswith a variety of uses as herbicides, fungicides, acaricides, and most notably insecticides.They were synthesized first in the 1800s, but the insecticidal properties were not discov-ered until the early 1900s. The German scientist Gerhard Schroder, who synthesized manyof the early OPs, was instrumental in the practical synthesis steps for parathion, which isstill in use today.

The OPs can be divided into about 15 subgroups depending on the types of elementsbound to the core phosphorus atom (16). True organophosphates contain the phosphategroup with various ester linkages to organic substituents.

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The OPs are used on a wide variety of crops, grains, and food animals, such as poul-try and cattle. As with carbamates, their toxicity and mode of action are associated with theirreversible inhibition of acetylcholinesterase. Because of fairly rapid breakdown, the OPsdo not accumulate in fatty tissues or the environment (unlike organohalides). Many of thechlorinated OPs are strictly regulated, and, thus, many meat products are monitored byUSDA-FSIS.

d. Synthetic pyrethroids. The pyrethroids are synthetic insecticides modeled afterpyrethrins, which are natural constituents of the flowers of certain chrysanthemums (60).Pyrethrins are the oldest known insecticides, with their use dating back to ancient Chinaand the Middle Ages in the Persia region. Because the natural pyrethrins are not very sta-ble when exposed to air and sunlight, most commercial pyrethrin-type insecticides are syn-thetic derivatives containing halogens, primarily chlorine and fluorine.

The pyrethroids, like most other insecticides, are neurotoxic to insects. The major ad-vantages of this group of insecticides are their low toxicity to humans and animals and theiraction against a wide variety of insects. However, they do cause a “burning” type of skinirritation, which may explain the origin of the name. The pyrethroids are approved for awide variety of crops, including many fruits and vegetables (14). They also are used for pestcontrol on pets and farm food animals. Pyrethroids have replaced many of theorganohalides and organophosphates and are now found commonly in household insectici-dal products.

B. Hormone Disruptors

1. Polychlorinated Biphenyls (PCBs)

The PCBs constitute a group of industrial chemicals that have good stability to chemicaland thermal breakdown and are nonflammable. As with many of the organohalogen pesti-cides, they are considered POPs, and an effort is under way to bring about a worldwide ban.All PCBs typically contain two to nine chlorine atoms and two phenyl groups. Many dif-ferent isomers exist because of the possible arrangement of the chlorine atoms around thephenyl rings.

Prior to their production being halted in most countries in 1974, PCBs were used inelectrical transformers, in electronic parts, and as flame retardants. Production was limitedwhen toxicity was discovered. Until then, little effort was made to control disposal of wastecontaining PCBs. As a consequence, trace amounts are found in soil, water, and animals invarious parts of the world.

Other than a severe skin rash termed chloracne, exposure to high levels of PCBs hasnot caused any problems in adults. However, in two major epidemics in Japan in 1968 andTaiwan in 1978, people ingested rice cooking oils containing high levels of PCBs (1,000ppm or greater) and developed a variety of conditions such as chloracne, liver disorders, fa-tigue, and nausea. Some smaller children exposed to the contaminated oils had delayedneurological and cognitive functioning (20). Based on this and other studies, the FDA des-ignated PCBs as unavoidable environmental contaminants and set tolerances at 0.2 to 2.0ppm for residues in many food products.

2. Polychlorinated Dibenzo-p-dioxins (PCDDs)

Dioxins and dioxin-like compounds are environmental contaminants that are fat solubleand chemically stable. Dioxins originate from combustion of chlorine-containing organiccompounds. Sources of exposure include industrial and municipal incinerators and com-

186 Fung et al.


bustion of leaded gasoline, diesel fuel, and wood. Dioxins also are by-products of chlorinebleaching of paper and pulp and are known to be present in the leachates from certain haz-ardous waste sites. They exhibit high toxicity and carcinogenicity in animal models andthus merit a considerable amount of concern for human public health. The dioxins aresomewhat related to the PCBs and have been grouped with them by some research work-ers because of their hormone-mimicking properties. This group of chemicals contains twomain categories of structurally similar, yet distinct, compounds: the polychlorinateddibenzo-dioxins and furans. The compounds can contain anywhere from 2 to 8 chlorine (orbromine) halogens, which give over 200 possible isomers or congeners. The compound2,3,7,8 tetrachlorodibenzodioxin (abbreviated 2,3,7,8-TCDD or just TCDD) often is re-ferred to in the lay press as dioxin. This is a misnomer, because many different types ofdioxins exist.

Although dioxins are present in the environment in very small amounts (parts per tril-lion), their known carcinogenicity and estrogen-like action are causes for concern. The es-trogen-like activity is of special interest, because the potential to target many differentgenes can disrupt cell functions. Possible effects include disruption of the reproductive sys-tem in the developing fetus, immune system malfunction, and neurological disorders.

Until recently, no major cases of food contamination with dioxins have occurred.That changed in the spring of 1999, when significant contamination was found in dairyproducts, eggs, chickens, baked goods, and some pork and beef products produced in Bel-gium. The contamination was so extensive that by June essentially all of these product werebanned from worldwide trade including in the United States (see “Chemical Contaminants”at the U.S. FDA’s Web site (29). The original source of contamination appears to have beenthe addition of a technical mixture of PCB containing dioxins (formerly used as transformeroil) with an 80,000 kg batch of animal fat. The contaminated fat then was used to formu-late 1.4 million kg of animal feed mix, which was distributed throughout Belgium and, insome cases, France and the Netherlands. Thus, many of the animals fed the feed producedin early 1999 showed levels of contamination 100 to 700 times higher than the U.S. legallimit of 1 ppt. Regulatory officials were able to identify the contaminated food items/prod-ucts, and they were destroyed, but at great financial loss.

The passage of the Food Quality Protection Act and amendments to the Safe Drink-ing Water Act in 1996 required the EPA to develop a screening and testing program for en-docrine disruptors and to implement testing by August 1999. The agency has collected dataand public comments on dioxin environmental contamination and appropriate testing pro-cedures. It is important to note that dioxins are not the only endocrine disruptor–type com-pounds. Most of the restricted chlorinated hydrocarbons (chlordane, DDT, aldrin, hep-tachlor, and endrin) and PCBs also posses endocrine activity. Even though thesecompounds are no longer used (at least in Europe, the United States, and Canada), they stillpersist in the environment.

The final report of the Endocrine Disruptor Screening and Testing Advisory Com-mittee was made available on the EPA’s Web site in August 1998 (75). Estimates indicatethat 50% to 90% of daily exposure to dioxins originates from food, primarily fish, meat,and dairy products, so efforts are directed at minimizing contamination from these sources.

C. Antibiotic Residues

A considerable number of drugs, including antibiotics, are regulated closely by the FDA(20). Antibiotics have a wide variety of toxic affects, including potential teratogenicity and

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mutagenicity. Some of them, especially in the penicillin family, can cause hypersensitivityreactions, which may be life-threatening in susceptible individuals.

Because residue levels are seen only in food animals, the USDA-FSIS is responsiblefor monitoring them. In the past, antibiotics were used extensively to treat various animalillnesses. However, they are now used more selectively for therapeutic and disease-pre-vention purposes. Some antibiotics are fed to animals in subtherapeutic doses because theyincrease feed efficiency, i.e., enhance weight gain per amount of feed. All drugs are regu-lated so that only trace amounts are allowed in muscle foods, usually range below ppm (20).In many cases, the drugs must be withdrawn from the animals for a defined period beforethey are taken to market.

Major issues have developed over the use of antibiotics in animal feed and/or treat-ments and how this practice contributes to the generation of antibiotic-resistant strains ofbacteria. As noted in a recent review, the occurrence of antibiotic-resistant strains ofpathogenic bacteria has become a worldwide problem in the treatment of human infectiousdiseases (54). Though the use of antibiotics in animals is not entirely to blame for resistanceproblems, a growing body of evidence suggests that use of subtherapeutical level of an-tibiotic drugs in feed is a major contributor. Thus, within the past several years, world reg-ulatory agencies have moved to restrict antibiotic drugs used in treating human infectionsfrom use in both animal treatments and feed. In December of 1998, the European Unionproposed a ban on the use of certain antibiotics as animal feed additives, and the U.S. FDAproposed new guidelines that severely restrict the use in animals of any antibiotics that areessential for treating bacterial infections in humans (28).

D. Chemicals from Production or Processing

1. Heterocyclic Amines

The toxic and mutagenic properties of heterocyclic amines were discovered by accident inthe late 1970s by Takashi Sugionura and several of his coworkers at the National CancerCenter in Japan (70). They were evaluating the mutagenicity of cigarette smoke tars and de-cided to test foods that are commonly smoked, such as fish and meat. As expected, thefoods did contain mutagenic activity. However, the application of smoke alone did not ex-plain the large increase in mutagenicity observed with all the foods, indicating that someother type of compound was present.

Further investigation showed that several different amino acids present on the surfaceof a cooked (browned or grilled) food are pyrolyzed into potentially carcinogenic sub-stances. It is now known that tryptophan, phenylalanine, lysine, and glutamic acid each canyield several different types of mutagenic heterocyclic amines when exposed to the hightemperatures of broiling.

Physical variables such as temperature, time, and method of cooking significantly af-fect the mutagenic activity of cooked meat. Cooking temperature is the most important fac-tor; a marked decrease in mutagenic activity is observed when meat is fried at lower tem-peratures. Moreover, the surface of well-done charcoal-broiled steaks contains muchhigher levels of heterocyclic amines than that of boiled beef. Recent data also have shownan apparent correlation in women between consumption of well-done meats (presumablycontaining higher HCA levels) and incidence of breast cancer (80).

Several studies have suggested that these mutagens form in different types of meats.Hatch (42) has compiled an extensive list of heterocyclic amine levels in a variety of foods.Research on cooking temperatures suggests that the levels of heterocyclic amines vary con-

188 Fung et al.


siderably in a wide variety of processed meat products, according to Abdulkarim and Smith(1), and in restaurant-cooked meat products, according to Knize et al. (53).

2. Polycyclic Aromatic Hydrocarbons (PAHs)

These are highly mutagenic and carcinogenic compounds that are pyrolytic products ofburning fuel or organic compounds and are present in any type of smoke. They are foundprimarily in the environment, as a result of air pollution. However, PAHs have been foundin a variety of foods, especially grilled, roasted, and smoked fish and meats (6). Significantlevels are also present in grains, fruits, and vegetables. Charcoal-broiled and barbecuedmeats have some of the highest levels, about 30 to 40 times normal. Generation of PAHsoccurs primarily by cooking or combustion at high temperatures and involves carbohy-drates, peptides, and lipids. Lipid pyrolysis appears to cause the greatest production ofPAHs in grilled products.

The PAHs can enter the body by either ingestion or inhalation. Once absorbed, theyare activated by liver enzymes to produce compounds that can interact with either proteinsor DNA. The binding to DNA involves covalent bonding, which causes mutations andeventual carcinogenicity in some animal species. Though information is limited, PAHs arealso thought to cause immunosuppression reactions in some animals.

3. Nitrosamines

The N-nitrosamines are carcinogenic compounds formed from reactions between a sec-ondary amine (amino acid) and nitrogen oxides and nitrous acid originating from nitrate ornitrite added to processed meat products. The reaction generally does not occur to a greatextent unless high temperatures are applied; thus, levels of N-nitrosamines are low in mostmeat products.

In the 1970s and early 1980s, extensive concern existed about potential nitrosamineexposure from eating processed meat products. Because of this, the use of nitrate and ni-trite in curing meats was almost banned. Two major publications by the National Academyof Sciences provided insight on potential exposures to nitrosamines and nitrates and nitritesand the risk of cancer (58,59). Since then, nitrosamines have been found in a wide varietyof foods, such as cheeses, beer, dried milk, dried fish, and mushrooms.

Although the presence of nitrosamines in cured meat products still causes concern,the major regulatory thrust since the late 1970s has been on controlling the levels in bacon.Very specific regulations dictate maximum amounts of 120 ppm for sodium nitrite or 148ppm for potassium nitrite, and 500 ppm for sodium erythorbate or sodium ascorbate in theproduct (18). The final nitrosamine contained in the cooked (fried) bacon is not allowed tobe over 10 ppb, which is the level of detection.

The only other cured meat products that have been scrutinized closely for ni-trosamines are hams that had been smoked/cooked in rubber-containing elastic nets. Ap-parently, reactions at the surface and in the netting caused some nitrosamines to migrate tothe surface of the product (27). Although nets containing rubber are still in use, efforts areunder way to remove the precursors from the rubber.

Because of the tighter process control on nitrites and nitrates added to various curedmeat products, the debate over N-nitrosamines has subsided. As pointed out in the reviewby Cassens (14), the residual nitrite levels in cured meats have dropped dramatically fromthose reported in the 1970s. This indicates that cured meat products are not major sourcesof exposure to N-nitrosamines, as was once thought.

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V. PHYSICAL HAZARDS ASSOCIATED WITH MEATS:IDENTIFICATION AND CONTROL

Physical hazards, when compared to biological and chemical hazards, may not be dis-tributed as uniformly throughout the food product. Therefore, fewer individuals may be af-fected by a physical hazard event. Nonetheless, a HACCP plan must take into accountphysical hazards and their control (52).

Katsuyama also noted a distinction between physical contaminants that cause physi-cal injury and those that are aesthetically unpleasing. HACCP deals primarily with thosephysical contaminants that may cause injury. However, in some instances, control of filthadulteration, whether it results in a public health risk or not, comes under regulatory agencycontrol. This certainly is true for international regulatory guidelines (55). The filth consid-eration is also a part of the U.S. regulatory approach, recognizing the goal of harmoniza-tion of international food safety standards.

Physical hazards can result from incoming raw materials; poor personnel practices;and faulty processes, facilities, and equipment. The following list of examples of physicalhazards was compiled from Katsuyama (52) and Boyle and Getty (11):

Band-aidsBones/bone fragmentsBullets/shot/BBsCarcass ID tagsCigarette buttsDirt, rocksFeathersGasket materialsGlassGreaseGum, wrappersHairHypodermic needlesInsectsJewelry, buttonsMetalMold, mold matsPaint flakesPlasticsRodents/droppingsRubberWood splintersWriting pen caps

The control of these hazards begins with good manufacturing during preharvest man-agement through further processing and handling before receipt by the ultimate consumer.Additional controls include, for example, carcass and product trimming, carcass washing,bone separators, metal detectors, magnets, x-ray devices, visual evaluation of incoming rawmaterials for defects, employee training, equipment and facility maintenance, and propersanitation. However, complete control of the spectrum of potential physical hazards is im-possible with current technology. One problem is that detection technology does not exist

190 Fung et al.


for certain contaminants—for example, vinyl gloves or pieces. The ability to be able to de-tect particulate contaminants regardless of the composition is needed. In the absence of thattechnology, Katsuyama (52) provided the following list of strategies to help prevent andcontrol physical hazards in processing facilities:

Complying with good manufacturing practice regulationsUsing appropriate specifications for ingredients and suppliesObtaining letters of guarantee from all suppliersUtilizing vendor certificationIdentifying types and sources of physical hazardsDetermining critical control pointsInstalling equipment that can detect and/or remove physical hazardsMonitoring the critical control points and documenting control performanceTraining employees

Advances in the detection and control of physical hazards are needed and warrant in-creased research and development efforts.

VI. CURRENT REGULATORY POLICIES AND INSPECTION

A. Concepts of Hazard Analysis Critical Control Points (HACCP)

HACCP is an acronym referring to Hazard Analysis and Critical Control Point system. Theobjectives of HACCP are to provide safe food for consumption and prevent chemical,physical, or biological hazards from occurring in food products. Originally, HACCP wasdeveloped jointly around 1959 by the Pillsbury Company, the National Aeronautics andSpace Administration (NASA), and the United States Army Natick Research and Devel-opment Laboratories to assure safe foods for the U.S. space program (7,68). Later, HACCPwas adopted voluntarily by several food companies in the United States as a preventive sys-tem to assure safe products and to reduce costs associated with unsafe food (e.g., recalls,lawsuits, or shutdowns). Following the Jack-in-the-Box E. coli outbreak in 1993, theUSDA recommended that HACCP be mandatory in all meat and poultry plants. That rec-ommendation was adopted, and on July 25, 1996, the Pathogen Reduction Final Rule man-dating HACCP implementation was published. Also, several deadlines for implementationof HACCP were set:

1. Jan. 26, 1998, in large meat and poultry plants, i.e., with �500 employees.2. Jan. 25, 1999, in smaller plants, i.e., with 10 or more employees but 500.3. Jan. 25, 2000, in very small plants, i.e., with 10 employees or having annual

sales of $2.5 million.

HACCP has seven principles that need to be met:

1. Conduct Hazard Analysis (HA): The HACCP team brainstorms to list and iden-tify potential chemical, physical, or biological hazards during food production orpreparation. Also, the team determines the significance of a hazard (e.g., low riskor high risk) and identifies preventive measures.

2. Identify Critical Control Points (CCPs): A CCP is a point in the process where acontrol can be applied and a potential food safety hazard prevented, eliminated,or reduced. A CCP decision tree can be used to help determine if a point in theprocess is a CCP or a Control Point (CP; any point at which a hazard can be con-

Meat Safety 191


trolled). Once a CCP has been identified, a method for its control needs to be de-termined.

3. Establish Critical Limits (CLs): Critical limits are needed for preventive mea-sures associated with each CCP. They serve as boundaries for CCPs and help in-dicate when a deviation from the acceptable level has occurred.

4. Establish CCP Monitoring Procedures: Monitoring procedures are necessary toadjust the process and maintain control during production or food preparation.

5. Establish Corrective Actions (CAs): When monitoring indicates deviations,CAs are implemented to adjust for the deviation. In case of noncompliance, it isimportant to address the cause of the deviation, how the problem was corrected,and disposition of the product. Also, records of CA should be maintained (i.e., incase of deviations).

6. Establish Verification Procedures: These can be conducted by the HACCP teamor by outside consultants. The goal is to show that the CCPs, CLs, and theHACCP system as a whole are working.

7. Establish Recordkeeping Procedures: Records on HACCP team, product de-scription and intended use of product, flow diagram of process(es), CCPs, typeof hazards, preventive measures, CLs, monitoring procedures, CAs, and verifi-cation procedures should be kept in an accessible location. This is important iscases where deviation(s) occurred.

For a HACCP system to be incorporated successfully into a food process, all of theprinciples must be implemented carefully for the specific process. Because the HACCPteam has the responsibility of developing a successful HACCP, one of the first steps in-volves careful identification of that team or individual(s) who will serve as the leadHACCP person/people for your establishment. According to the USDA’s HACCP regula-tion, individual(s) developing HACCP plans must have successfully completed a course ofinstruction in the application of the seven HACCP principles to meat or poultry processing.Therefore, it is important to make sure that the individual(s) completes the required train-ing. A list of introductory HACCP courses can be obtained from North American Meat Pro-cessors (NAMP) or by calling the International HACCP Alliance (409) 862-2036. Aftercompletion of the HACCP training, the individual(s) should have a working knowledge ofthe process required to develop and implement a HACCP program. The individual(s) alsoshould have a HACCP reference book and handouts from the training course that shouldhelp them move forward. HACCP-trained individual(s) then should identify the peopleneeded on the HACCP team.

After the HACCP team members are identified, the next step involves gathering doc-uments and materials that are needed to adequately develop the HACCP plan. This includesa copy of the actual HACCP regulation (Final Rule) and the technical amendments and is-sue papers related to the regulation. These documents can be obtained from the NAMP of-fice, by downloading from the Internet, or by contacting USDA. The following Web sitesalso provide information that may be useful:

http://ifse.tamu.edu/haccpall.html (International HACCP Alliance)http://www.usda.gov/agency/fsis/homepage.htm (USDA-FSIS)

B. Operational Steps in HACCP

It is understood that each establishment operates slightly differently from the next, even ifthey are producing the same products. Therefore, each HACCP team may not need to use

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http://ifse.tamu.edu/

http://www.usda.gov/

the same type of information. The items listed below are fairly basic, and each team can addor delete material from the list as needed. The main thing is that the identified material shouldbe available to the HACCP team members as they begin to develop the HACCP plan.

1. Written sanitation standard operating procedures (SSOPs) manual or documentand the Deviation/Corrective Action records generated from the SSOP program. ThePathogen Reduction/HACCP regulation requires each establishment to have a writtenSSOP. The records generated from the SSOPs may help identify problem areas and shouldbe useful as you evaluate your overall process.

2. Plant production practices (Standard Operating Procedures). If your establish-ment has an operational standard operating procedures guide, then it could be used by theteam. If not, then it is important to make sure that the team members know and understandthe actions required to produce your product(s).

3. Product descriptions and/or recipes. The regulation requires that each plan con-tains a product description providing information about the product and its end users.Therefore, if you already have written information about the products, it can be incorpo-rated into the HACCP plan as needed.

4. Information on the establishment’s prior recalls and customer complaints thatare related to food safety. The HACCP team should be aware of the plant’s history. Oneway to help is to provide information on recalls and customer complaints that are related tofood safety.

5. Establishment data. If you have been collecting micro data, then it will be im-portant for the HACCP team to have this information to help identify trends. Informationon such factors as room/cooler/freezer temperatures, oven temperatures, and line speedsalso may help the team members.

After as much information as possible has been identified and gathered, the HACCPteam should review and use the information as it develops the HACCP plan. The team alsoshould keep a copy of all the supporting documents that they used to make their decisions.This will help with future revisions of the HACCP plan.

Identifying the lead individual(s) participating in a training program, appointing theHACCP team, and gathering the necessary information are the basic steps to getting started.Then the HACCP team can begin using its knowledge and information to develop a flowchart, provide the product description, and design a HACCP plan that can be implementedsuccessfully to help your establishment continue to produce the safest food supply possi-ble. Developing a HACCP plan is not something that occurs overnight, but it is somethingthat you can accomplish. All you have to do is get started. However, when you are work-ing on a HACCP plan, SAFETY should be the most important concern.

C. Potential for Recall of Meat and Poultry Products

Theoretically, under a HACCP system, the likelihood of product recalls should be reducedgreatly. If the manufacturing process is controlled properly, then the output of that processalso should be under control, and the finished product should meet all company and regu-latory safety requirements. When a process failure occurs, the HACCP monitoring proce-dures should alert the operator and the proscribed corrective action procedures should pre-vent nonconformities in the finished product.

However, even under the best of circumstances, unforeseen events may sometimesresult in the need to remove adulterated or misbranded products from the marketplace.

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Therefore, all companies involved in food production, processing, distribution, and retail-ing must establish procedures for conducting a product withdrawal or recall. In addition,the designation of a “crisis management team” and the establishment of policy to addressthe public relations concerns that may arise in conjunction with a product withdrawal or re-call are necessary components of a HACCP system.

A recall is a voluntary procedure initiated by a company in an effort to remove anadulterated product from the marketplace. The USDA does not have the authority to ordera recall, but in a situation when a company is deemed to be insufficiently cooperative, it caninitiate its own seizure actions against the products in question (43).

As far as we know, in all instances where product withdrawal or recalls have beennecessary, companies regulated by the USDA have been cooperative, and the USDA hasnot had to resort to product seizures. Indeed, in most instances, the proper and necessarystrategy for a company to pursue is to cooperate with the government regulatory agency,and show its customers and consumers that it is able to promptly, decisively, and effec-tively deal with the problem and move on. Because of the general industry adherence to thispattern and a generally high level of government professionalism in this area, recalls andrecall procedures historically have not been sources of controversy.

Recently, questions have arisen as to whether the USDA and FDA have sufficient au-thority with respect to recalls and on record-keeping and trace-back requirements for meatand poultry products. Controversy also has surrounded several recent recalls where recallaction has been triggered entirely upon epidemiological supposition unsupported by anyhard data, and inaccurate information was provided to consumers in USDA press releases.

Each of these areas of controversy is addressed, at least in part, by industry initiativeon trace back; by authorizing legislation that has been proposed by USDA; and by the pro-posed regulation on pathogen reduction and HACCP, which ultimately will result in themandatory implementation of HACCP in all federally inspected meat and poultry plants.

For example, the record-keeping requirements associated with a HACCP plan shouldenhance a company’s ability to conduct a product withdrawal or recall, and the trace-backcomponent of voluntary producer quality assurance programs may facilitate the identifica-tion of the source of contamination in a foodborne illness outbreak.

D. USDA Policy on Recalls

In 1988, USDA’s FSIS published a revised directive to address the recall of meat and prod-ucts (34). The directive established a system for classification of recalls based on the pub-lic health hazard presented by the product being recalled.

1. Class I

Involves a health hazard situation where there is a reasonable probability that the use of theproduct will cause serious, adverse, health consequences or death.

2. Class II

Involves a potential health hazard situation where there is a remote probability of serious,adverse, health consequences from the use of the product.

3. Class III

Involves a situation where the use of the product is not likely to cause adverse health con-sequences.

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4. Nomenclature Used in Recall

The FSIS also provided recall oversight; monitoring the effectiveness of the recall; and co-ordinating activities between federal, state, and local agencies and foreign governments.The directive also provides definitions that are useful in establishing a corporate crisis man-agement strategy.

a. Recall. The voluntary removal by a firm from commerce of distributed meat orpoultry products when there is reason to believe that such products are adulterated or mis-branded under the provisions of the Federal Meat Inspection Act or the Poultry ProductsInspection Act. “Recall” does not include a market withdrawal or a stock recovery.

b. Correction. The firm’s modification, relabeling, or destruction of a productwith the concurrence of FSIS.

c. Recalling Firm. The firm that initiates a recall or, in the case of an FSIS-re-quested recall, the firm that has primary responsibility for the manufacturing and/or mar-keting of the product to be recalled.

d. Firm-Initiated Recall. A recall that is initiated by a firm without a formal re-quest from FSIS.

e. FSIS-Requested Recall. A recall initiated by a firm in response to a formal re-quest from FSIS.

f. Case Number. The number or code assigned to recall incident for use by FSISto identify the investigation or product recall.

g. Health Hazard Evaluation. An evaluation of the health hazard presented by aproduct being recalled or considered for recall. The evaluation will be conducted by a teamof FSIS experts with access to other individuals or agencies as deemed necessary.

h. Emergency Program Team. A team of representatives from various FSIS divi-sions and staffs assembled to respond to potential or real health hazard incidents reportedto EPA. Representatives from the following Agency units may be members of the team:Chemistry Division, Compliance, Emergency Programs Staff, Epidemiology Branch, Ex-port Coordination Staff, Foreign Programs Division, Field Service Laboratories Division,Mathematics and Statistics Division, Import Inspection Division, Information and Legisla-tive Affairs, Microbiology Division, Residue Operations Staff, Processed Products Inspec-tion Division, Residue Evaluation and Planning Division, and Regional Operations, MPIO.The team may be activated by the Director, EPA, whenever deemed necessary, and itsmembers will report to the Director, EPA, for the purpose of conducting assignments re-lated to the health hazard incident.

i. Recall Strategy. The action plan recommended by or to the recalling firm andfollowed by FSIS in monitoring a recall.

j. Depth of Recall. The level of product distribution to which the recall is to ex-tend:

Consumer or user level, including any intermediate wholesale or retail level.Retail level—the level immediately preceding the consumer or user level.Wholesale level—the distribution level between the manufacturer and the retailer.

This level may not be encountered in every recall situation; i.e., the manufacturermay sell directly to the retail outlet.

k. Public Notification. A public notification to alert the public and trade that ei-ther a product is being recalled because it presents a serious health hazard or that a situa-tion exists for which such notification is deemed to be in the public interest. The necessity

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for public notification will be considered on a case-by-case basis for each recall. However,all Class I recalls will result in the issuance of a press release or another form of public no-tification, unless so exempted by the Administrator, FSIS. The situations where this ex-emption will be permitted are (a) when data are sufficient to support the conclusion that thesuspect product in commerce is under control by FSIS or another federal or state agencyand that the likelihood that any product is in the hands of consumers is extremely remoteor (b) when public notification already has been made by another government agency (stateor federal) and for which the text, format, and method of notification are acceptable toFSIS. However, information on any recall action of any classification will be made avail-able to the public or press when inquiry is made, provided that such information is not ex-empt under the Freedom of Information Act.

l. Effectiveness Reviews. Reviews for the purpose of verifying that adequate no-tice about the recall has been provided to all consignees. Adequacy of notice is determinedby the degree to which the implicated product in fact is retrieved by, or on behalf of, the of-ficial establishment and is disposed of properly. The number of effectiveness reviews to beconducted will be determined on a case-by-case basis by the Assistant Deputy Administra-tor, Compliance Program. The reviews will be conducted in accordance with Complianceprocedures and will focus upon the following elements:

Recall levelHealth hazardInitial effectiveness review findingsRecall firm’s actions

A sufficient number of effectiveness reviews will be made to provide assurance thatrecall action is conducted in an effective manner and that appropriate efforts are made tolocate and return the product being recalled. In the event that effectiveness reviews discloserecalled product remaining in commerce, the recalling firm must be notified. If the firmdoes not take prompt action to properly dispose of the product, the Assistant Deputy Ad-ministrator, Compliance program, may detain and seize product or initiate other action asappropriate.

m. Monitor. To observe and record data concerning a firm’s recall and to conducteffectiveness reviews.

n. Recall Evaluation. The evaluation of final reports after recall action is com-pleted to determine the recall’s effectiveness. It will include the percent of product re-turned, its disposition, and the number and level of consignees reviewed. The recall evalu-ation will for the basis for terminating the recall.

o. Termination of a Recall. Officially, when the Agency determines that all rea-sonable efforts have been made to remove or correct the violative product and proper dis-position has been made according to the degree of hazard. For monitoring purposes, FSISwill classify a recall action “completed” at the time when the firm has actually retrieved andimpounded all outstanding product that could reasonably be expected to be recovered, orhas completed all product corrections.

p. Market Withdrawal. A firm’s removal or correction at its own volition of a dis-tributed product involving a minor infraction that would not warrant legal action by FSISor that involves no violation of the FMIA or PPIA or health hazard.

q. Stock Recovery. A firm’s removal or correction of product that has not beenmarketed or that has not left the direct control of the firm, i.e., the product is located onpremises owned by, or under the control of, the firm, and no portion of the lot has been re-leased for sale or use.

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E. Processes of Conducting a Recall

The process of conducting a recall includes the following six steps:

1. Health Hazard Evaluation

An evaluation of the health hazard presented by a product being considered for recall, orbeing recalled, will be conducted by a team of FSIS experts in cooperation with other indi-viduals or agencies as deemed necessary. The evaluation will include at least the followingfactors:

Nature of the violation or defectWhether any illness or injuries already have occurred from the use of the productAssessment of the likelihood of occurrence of the hazardAssessment of the consequences (immediate or long range) of occurrence of the haz-

ard

2. Recall Classification

A recall classification will be assigned to product recalls based on the health hazard evalu-ation or the assessment of the nature of the deception or other defect. The FSIS will assignthe classification, i.e., Class I, Class II, Class III, to indicate the relative degree of healthhazard of the product being considered for recall or being recalled.

3. Recall Strategy

A recall strategy will be developed to assist in the conduct of a recall and take into accountthe following factors:

Recall classification assigned by FSISDepth of recallExtent of notification being made to the trade or publicAction plan to coordinate the removal and return or correction of the product from

the marketplaceEffectiveness reviews

Elements of a recall strategy will include:Results of the health hazard

Ease in identifying the productDegree to which the product’s deficiency is obvious to the consumerDegree to which production remains unused in the marketplaceAmount of product involvedArea of distributionAction taken or planned by the recalling firm

4. Recall Recommendation

The EPA Staff will prepare the recall recommendation for submission to the Deputy Ad-ministrator, MPIO. The recall recommendation will include:

Health hazard evaluationRecall classificationRecall strategy

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5. Recall Request

The recall recommendation will be reviewed by the Deputy Administrator, MPIO. The fi-nal decision to request a product recall will be made with the concurrence of the Adminis-trator, FSIS. After the decision to recall, the Deputy Administrator, MPIO, or designee willcontact the firm to make the formal request for a recall. The appropriate federal, state, orlocal agencies will be notified of the product recall.

6. Termination of Recall

A recall will be considered officially terminated when FSIS determines that the recall ac-tion is completed, that proper disposition has been made of the violative product, and thatno further emergency action is pending. The Director, EPA, will assemble the informationand reports necessary to make this determination and will make the recommendation forterminating the recall to the Deputy Administrator, MPIO. The recommendation will be re-viewed by the Deputy Administrator, MPIO. It is important to note that a memorandum ofunderstanding between FSIS and FDA has been established to set forth the working ar-rangements between the two regulatory agencies in conducting Class I and Class II recallsof food.

HACCP by design is a preventive system. If implemented and operated properly,food produced under a HACCP system should be safe, and the potential for product recallsshould be reduced greatly. In the event that a recall becomes necessary, however, a crisismanagement policy that is in place and periodically tested also will serve as a means of lim-iting the potential financial loss and loss of consumer confidence that may be associatedwith a product recall. The combination of a HACCP system and a well-designed crisis man-agement policy will provide the most effective assurance that food products will be safe andinsurance against the potential devastating effects of a food safety crisis and public recall.

F. Imported Products: State vs. Federal Programs and AgenciesInvolved

Imported food products must meet the same regulatory requirements as products manufac-tured in the United States. The USDA office of field operations has an import/export divi-sion that oversees plants outside the United States that import meat and poultry products.

Following are names and Web site addresses for some government agencies that canbe contacted for further information and updates on HACCP and guidelines and regulationsrelated to food safety:

FSIS www.fsis.usda.govCDC www.cdc.govCVM www.fda.gov/cvmCFSAN www.cfsan.fda.gov

G. Definitions

1. Control: (a) to manage the conditions of an operation to maintain compliancewith established criteria; (b) the state wherein correct procedures are being fol-lowed and criteria are being met.

2. Control point: any point, step, or procedure at which biological, physical, orchemical factors can be controlled.

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www.fsis.usda.gov

www.cdc.gov

www.fda.gov/

www.cfsan.fda.gov

3. Corrective action: procedures to be followed when a deviation occurs.4. Critical control point (CCP): a point, step, or procedure at which control can be

applied and a food safety hazard can be prevented, eliminated, or reduced to ac-ceptable levels.

5. CCP decision tree: a sequence of questions to determine whether a control isCCP.

6. Critical limit: a criterion that must be met for each preventive measure associ-ated with a critical control point.

7. Deviation: failure to meet a critical limit.8. HACCP plan: the written document that is based upon the principles of

HACCP and delineates the procedures to be followed to assure the control of aspecific process or procedure.

9. HACCP plan revalidation: one aspect of verification in which a documentedperiodic review of the HACCP plan is done by the HACCP team with the pur-pose of modifying the plan as necessary.

10. HACCP plan validation: the initial review by the HACCP team to ensure thatall elements of the HACCP plan are accurate.

11. HACCP system: the result of the implementation of the HACCP plan.12. HACCP team: the group of people that is responsible for developing a HACCP

plan.13. Hazard: a biological, chemical, or physical property that may cause a food to be

unsafe for consumption.14. Monitor: to conduct a planned sequence of observations or measurements to

assess whether a CCP is under control and to produce an accurate record for fu-ture use in verification.

15. Preventive measure: a physical, chemical, or other factor that can be used tocontrol an identified health hazard.

16. Risk: an estimate of the likely occurrence of a hazard.17. Severity: the seriousness of a hazard.18. Verification: the use of methods, procedures, or tests in addition to those used

in monitoring to determine if the HACCP system is in compliance with theHACCP plan and/or whether the plan needs modification and revalidation.

VII. MEAT SAFETY IN THE FUTURE

A. Food/Meat Safety and Research Needs

During the past several decades, meat scientists and food microbiologists have been per-forming a variety of valuable and fruitful research activities to promote meat science andmeat safety.

A number of factors are important to the livestock and meat industry. For example,product quality (i.e., tenderness consistency) and processing efficiencies (i.e., centralizedprocessing and precooking) are important targets for the industry. However, those consid-erations must be consistent with safety of the product and vice versa. With that focus inmind, it is imperative that all segments from producers to processor to retailer to consumerbe involved to help assure meat safety.

Practices are needed at the live animal level that can be implemented realistically andmay reduce hazards that can be carried to the final product. Identification of those practices

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has been difficult, and demonstrating quantitatively that a preharvest practice reduces theincidence of foodborne disease is unlikely. Therefore, producers may implement practiceson the theoretical contingency that they will help reduce the incidence of a hazard. Perhaps,future research will lead to such improvements as vaccines or competitive exclusion agentsthat will function as classical control technologies at a critical control point in preharvestHACCP. That research demands significant attention by the scientific community.

The most progress in meat safety research has been made at the processing level, be-cause this is a logical point to achieve broad-spectrum hazard control or elimination. Ascompared to the number of live animal producers, there are fewer processing facilitiesthrough which the product passes and can be subjected to hazard control. Nonetheless, theideal system realizes hazard control preharvest and this is coupled with the postharvestgains (49).

Postharvest intervention systems that integrate chemical, physical, and thermalstrategies require further investigation to determine their synergy. However, those systemsmust be coupled with appropriate subsequent handling of the product, whether it be by pur-veyors, food service, retail stores, or the ultimate consumers. There is a need to discern themost correct information transfer system(s) to ensure that postprocessing education com-pletes the concept of safety from live animal to consumer (50).

In summary, progress toward safer meat is realized ideally by integration of prehar-vest and postharvest intervention strategies. No one step in the system is “the place” wheresafety can be achieved totally. Even though good progress has been made, progress throughadditional research still holds significant potential. However, this must be integrated withaggressive technology and information transfer.

B. Domestic and International Meat Safety in the Future and MeatSafety Standards

Just as they do in other areas of life, political and economic interdependencies exist be-tween nations engaged in the trade of meat and meat products. Consequently, a discussionof domestic meat safety issues cannot be separated from international political issues.

In keeping with the move from a principally organoleptic (sight-, smell-, touch-,taste-based) inspection system to the more science-based HACCP system, the U.S. regula-tory agencies and meat industry have worked together toward implementation. The U.S.implementation of HACCP has not been easy or ideologically complete. Nonetheless,HACCP has been implemented, and the meat inspection system likely will continue to re-flect a hybrid of the organoleptic-based inspection and the new science-based HACCP. TheU.S. meat industry and regulatory agencies are committed to going beyond an inspectionsystem limited largely to processing operations to include a farm (preharvest) to table(postharvest) approach. It is reasoned that by addressing safety issues at the live animal,processing, marketing, food service, and retail levels using the HACCP approach, safetygains at each level will be at least additive and likely synergistic. No one point in the chain(e.g., live animal) is the ultimate intervention point but rather the combination of interven-tions at CCPs throughout the chain from producer to consumers will reduce risk to both thedomestic and international communities (12).

The international community has worked through several avenues to harmonizefood/meat safety issues in recognition of ever-expanding international trade. The jointFAO/WHO Food Standards Programme and the Codex Alimentarius Commission (CAC)effort in 1962 is a pivotal example.

200 Fung et al.


To further advance that effort, food safety guidelines were reinforced at the Twenty-Second Session of the CAC held in Geneva, Switzerland in 1997. From that meeting, theCommission adopted the following guidelines:

Recommended International Code of Practice—General Principles of Food HygieneGuidelines for the Application of the Hazard Analysis and Critical Control Point

(HACCP) SystemPrinciples for the Establishment and Application of Microbiological Criteria for

FoodsGuidelines for the Exchange of Information between Countries on Rejections of Im-

ported FoodGuidelines for the Design, Operation, Assessment, and Accreditation of Food Import

and Export Inspection and Certification SystemsGuidelines for the Assessment of the Competence of Testing Laboratories Involved

in the Import and Export Control of Foods (55).

Additionally, Lupien (55) reported that Codex decided on the following statementsto balance the role of science and “other factors” in food/meat safety.

1. The food standards, guidelines, and other recommendations of Codex Alimenta-rius shall be based on the principle of sound scientific analysis and evidence, in-volving a thorough review of all relevant information, in order that the standardsassure the quality and safety of the food supply.

2. When elaborating and deciding upon food standards, Codex Alimentarius willhave regard, where appropriate, for other legitimate factors relevant for thehealth protection of consumers and for the promotion of fair practices in foodtrade.

3. In this regard, it is noted that food labeling plays an important role in furtheringboth of these objectives.

4. When the situation arises that members of Codex agree on the necessary level ofprotection of public health but hold differing views about other considerations,members may abstain from acceptance of the relevant standard without neces-sarily preventing the decision by Codex.

Considering that the HACCP system was recognized in the aforementioned guide-lines, the U.S. approach to meat safety is consistent with international efforts to harmonizemeat safety issues. Although progress in harmonization is being made, much work remains.That work entails standardized international training in, for example, HACCP, sanitation,food microbiology, hygiene, toxicology, and related issues. This harmonization also willbe impacted by how well the World Trade Organization (WTO) members base their na-tional food safety measures on international standard guidelines and other recommenda-tions adopted by Codex Alimentarius (55). These considerations must be balanced withother factors that impact compliance with WTO “science-based” recommendations. Thepolitics of nontariff trade barriers have resulted in science-based decisions by the WTO be-ing circumvented. Legitimate concerns that go beyond the “science” of safety and impacttrade decisions include other actions and consideration by the WTO. Specifically, theUraguay Round Agreement of the WTO also took into consideration (a) public and moralvalues and (b) the health and life of not only humans but animals and plants when arbitrat-ing trade issues (78). Though legitimate, those considerations must not be misused to avoidresponding to otherwise science-based food safety concerns.

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VIII. SUMMARY

Meat safety is a concern of meat producers, processors, retailer, distributors, food handlers,and eventually the consumers. This chapter started with the current status of meat safetyand new developments in issues such as meat irradiation, dietary supplements, geneticallymodified foods, and consumers’ knowledge and practices in meat safety. It continued witha discussion of the history of meat industry safety, microbiological hazards, and rapidmethods and automation in microbiology testing related to monitoring microbial meatsafety. Chemical and physical hazards related to meat were then presented and discussed.The chapter concluded with a detailed discussion of HACCP and current regulatory poli-cies and inspection. A look into the future of meat safety completed the chapter, which con-tains a wealth of information along with some speculations into the needs, predictions, andfuture directions relative to the safety of this important food commodity.

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