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CHAPTER 4 APPLICATION OF THE MODEL TO MICROBIOLOGICAL HAZARDS In the report Meat and Poultry Inspection' published in 1985 9 a National Research Council committee stated that Salmonella spp. and Cam~vlobacter ieiuni were the currently recognized major poultry-borne causes ot illness in consumers, but that antemortem and postmortem ~ ~ ~ ~ inadequate to detect these organisms (NRC, 1985b) . That committee recommended that FSIS intensify its efforts to control and eliminate contamination with microorganisms that cause disease in consumers. _ , Inspection methods in effect at that time were _ Specific recommenda- tions to achieve this goal included education of producers, processors, food handlers, and consumers; determination of etiologic agents responsible for gross lesions resulting in condemnation; development of a trace-back capability to determine where pathogenic microorganisms contaminate the poultry between farm and table; and emphasis on the Hazard Analysis Critical Control Point (HACCP) concept in the inspection process (NRC, 1985b). This chapter summarizes a method for identifying and describing risks associated with microbiological contamination of chickens and applies these methods to an evaluation of specific pathogens. The committee made no effort to consider the occupational hazards presented by microorganisms in the workplace (i.e., in chicken slaughtering and processing plants), nor did it evaluate all Possible pathogens associated with chickens. Rather, a model for subsequent refinement, . . ~ ~ ~ ~ . ~ this chapter is designed to serve as including collection of additional data neecea For risk assessment or microorganisms, and to provide a basis for the development of initial risk-management strategies. METHODOLOGY USED TO DESCRIBE AND IDENTIFY RISKS Hazard Identification and Evaluation General Ancroach. Several basic questions arise in the identification and evaluation of the public health hazard associated with a specific microbial agent. For example, is the microorganism potentially hazardous to health, i.e., is it a pathogen in humans? How does susceptibility vary from person to person or group to group? Are 56

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57 all microorganisms in this species, class, or other classification equally hazardous? If the microorganism is a hazard, what disease can it cause? With what frequency does this microorganism cause disease? The question of whether a microorganism is harmful to health has traditionally been approached by linking known disease syndromes with specific microorganisms. The criteria necessary to identify a microorganism as the etiologic agent for a disease were codif fed in the late 19th century as Koch's postulates: the microorganism must always be found in the diseased animal, but not in healthy ones; the organism must be isolated from diseased animals and grown in pure culture away from the animal; the organism isolated in pure culture must initiate and reproduce the disease when reinoculated into susceptible animals; and the organism should be reisolated from the experimentally infected animals. Although documentation of all four criteria is not always possible for human pathogens because of ethical considerations, Koch's postulates provide a framework for determining whether a microorganism is hazardous to human health. In considering the potential health hazard of a microorganism, it is necessary to define the population under consideration. A large number of microorganisms are not pathogenic for normal people but can cause disease and death in susceptible hosts, e.g., persons with underlying diseases that compromise their immunocompetence or who have received chemotherapeutic agents that affect their immune response. For patients whose immune response is totally suppressed (such as patients receiving bone marrow transplants), virtually every microorganism is a potential pathogen, making it difficult to distinguish precisely between pathogens and nonpathogens without some notion of the immune status of the target population. In defining the health hazard caused by a particular microorganism, it is also necessary to understand the organism's virulence factors, or factors that serve as markers for virulence. For many microorganisms, only a small percentage of strains within a species possess a specific plasmid or chromosomally defined factors that permit the organism to cause disease. For example, Escherichia cold is the dominant aerobic bacterium in all normal human stool samples, and most strains of E. cold are harmless to a healthy adult; however, some carry specific virulence plasmids that have been associated with at least four distinct disease syndromes, including toxin-mediated secretory diarrhea and an invasive dysentery syndrome (Levine, 1985~. Similarly, only 1% of environmental Vibr' o parahaemolyticus strains produce a hemolysin, which is correlated with their ability to cause disease (Morris and Black, 19851. For many microorganisms, we still have only a rudimentary understanding of virulence factors. Further research may help to explain apparently contradictory data regarding the pathogenicity of certain species of microorganisms.

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58 It is also necessary to understand the disease syndrome and related manifestations . Some microorganisms may only cause mild disease, such as the relatively mild diarrhea seen with many nontoxigenic species of Vibrio; other organisms, such as Salmonella, may also be associated with bacteremia, meningitis, other serious morbidity, and death. Host susceptibility may influence the extent of disease caused by a microorganism. For example, Salmonella bacteremia is more likely to be seen in a patient with sickle-cell disease or an underlying malignancy, whereas meningitis occurs most frequently in neonates. Virulence factors may also influence the severity of disease. For example, strains of Vibrio cholerae that lack the gene for cholera toxin production generally cause only mild disease, whereas fully toxigenic strains can cause rapidly progressive dehydration and circulatory collapse in a previously healthy adult. Finally, one needs to have data on the extent of disease caused by the microorganism (are there 10 cases in the United States per year, or 10,000?) and some index of disease severity, such as the number of hospitalizations or deaths attributable to the microorganism. The overall public health impact of a microorganism that causes a large number of mild cases resulting in few hospitalizations and no deaths may be significantly less than one responsible for only a few cases but with high rates of hospitalization and mortality. Sources of Data. The extent of the human health hazard presented by certain microorganisms must usually be determined by synthesizing data from a variety of sources, including studies in volunteers, animal models, and epidemiological studies. Approximations of disease incidence can be based on epidemiological data and on numbers of cases and deaths reported through state and national reporting systems. For ethical reasons, studies in volunteers are generally limited to healthy adults and to agents that cause only mild disease or for which there is good, effective therapy, but they can provide the best data on pathogenicity, permitting direct testing of Koch's postulates. These studies may also be useful in determining the relationship between dose and infection rates, in characterizing the disease syndrome, and, with an appropriate experimental design, in identifying specific virulence factors. However, they generally cannot be used to develop data on the disease in immunocompromised persons or other high-risk hosts. Many microorganisms are adapted to specific species, so that they cause disease in only one or a few host species. Therefore9 animal models cannot always be used to determine whether a specific microorganism will be pathogenic in humans. Once it has been shown that specific disease manifestations in an animal correlate with disease manifestations in humans, e.g., the correlation between the ability of an E. cold strain to cause keratoconjunctivitis in the guinea pig and its ability to invade enterocytes and cause dysentery in humans (Sereny, 1955), animal models can be useful in characterizing virulence factors or in identifying markers for virulence.

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59 Epidemiological studies can provide evidence that an organism is pathogenic by fulfilling one or more of Koch's postulates. For example, studies may demonstrate that a certain microorganism is often found among patients with diarrhea but not among controls, suggesting that the microorganism is respons ible for the diarrhea. Similarly, a study of disease outbreaks may demonstrate that one microorganism is significantly associated with illness among patients and is present in the food or other product incriminated as the cause of the outbreak. Epidemiological studies also permit characterization of microbial disease syndromes and can provide information on susceptibility and disease manifestations in persons other than normal healthy adults. Long-term follow-up may also be possible in such studies, permitting identification of chronic syndromes that may not be apparent in short-term experiments in volunteers. Approximations of incidence can be based on information From epidemiological studies and data reported through national reporting systems. For example, the Centers for Disease Control (CDC) collects national surveillance data on diseases caused by many specific microorganisms, including some of the food-borne bacterial pathogens. However, the number of cases reported through these systems is only a fraction of the actual number. Cases are not reported if a patient does not seek medical attention (e.g., when microorganisms cause relatively mild disease), if the doctor does not order appropriate diagnostic tests (such as a stool culture) for patients that are seen, or if the positive test result is not reported to the appropriate health authorities. By using information from outbreak investigations and other epidemiological studies, it may be possible to obtain a very rough estimate of the actual number of cases that occur for each reported case. For example, it has been estimated that only 1 out of every 20 Shigella infections in the United States is reported (Rosenberg et al., 1977), and possibly as few as 1 out of every 100 Salmonella cases (Aserkoff et al., 1970~. Rates of hospitalization and mortality (which may be more complete) derived from epidemiological studies can also be used to estimate incidence rates in the community. Dose-Resnonse Studies General Approach. For any one person, a certain number of microorganisms is usually necessary to establish an infection; no infection results when fewer microorganisms are present. This threshold value may differ widely from person to person or time to time, depending on such factors as host susceptibility, the method and vehicle with which the inoculum is presented, and the virulence of the microorganism. Nonetheless, it is sometimes possible to estimate the percentage of normal, healthy adults that will become infected after exposure to a viral or bacterial inoculum of known size.

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60 When determining the dose response of i nfectious agents, one must also consider the rate of asymptomatic or subclinical infection. Not all persons who become infected with a microorganism develop signs and symptoms of disease . Asymptomatic infections may be quite common, and may be dependent on many factors. For example, only one out of every two or three young adults infected with Epstein-Barr virus will develop s igns and symptoms of infectious mononuclear is; few children infected with the virus will have any symptoms at all. Some infectious agents cause disease by producing toxins that may cause an incremental increase in the severity of illness with increasing toxin levels, rather than a threshold response. The botulinal toxin is one example: food-borne botulism is caused by a preformed neurotoxin present in contaminated food, and disease manifestations and severity correlate directly with the amount of toxin consumed. Sources of Data. Dose-response data on humans are derived primarily from experiments in volunteers. In these studies, the bacterial or viral inoculum can be carefully controlled; however, they are restricted to healthy adults and usually use a defined laboratory strain that may have atypical virulence. Data on the dose response of food-borne pathogens have also been collected in investigations of outbreaks. These are based on estimates of the amount of food consumed and measurements of the concentration of the pathogen present in the implicated food, usually hours or days after the disease outbreak, during which time there may be significant changes in the size of the inoculum. Potential for Human Exposure General Approach. Microorganisms may be transmitted to humans in a variety of ways, including person-to-person transmission, (e.g., through sexual and fecal-oral contact), exposure to air-borne, food-borne, water-borne, and vector-borne pathogens, and contact with contaminated objects. Spread of disease by broiler chickens almost exclusively involves food-borne transmission, although direct contact or air-borne routes may be important in occupational exposures in poultry slaughter and processing plants. Microorganisms may be introduced into food at a number of points. Many of them, including CampYlobacter and Salmonella, are present in the gut flora of animals and may contaminate the surface of the carcass during slaughter or subsequent processing. The actual number of microorganisms present at any one time (and the percentage of carcasses contaminated) may vary widely, depending on temperature, product conditions, and how the product is handled. Most microorganisms are killed during cooking. Infection can occur if the poultry is eaten raw or if parts of it are undercooked. In the kitchen, cooked foods can be contaminated by raw poultry and other foods, by soil, or by food handlers. Once present in a kitchen, these microorganisms may contaminate a variety of foods, including chicken.

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61 Epidemiological studies can often link or attribute outbreaks of food-borne disease to specific products, such as chicken. However 9 the key point in the chain of transmission generally is the kitchen itself: for most food-borne pathogens, highly contaminated meat will not cause disease if properly cooked and handled. Conversely, minimal contamination can lead to maj or disease outbreaks if pathogenic microorganisms are allowed to contaminate an entire kitchen and if food prepared in the kitchen is subsequently mishandled. For many microorganisms, it is possible to measure the level of contamination of a product at each stage of processing. Unfortunately, it is unclear how the level of contamination observed during the processing of such products as raw chicken correlates with the potential for disease transmission. In formal attempts to assess risk, one must recognize the difference between measurable levels of product contamination and disease occurrence. Although the correlation can never be fully resolved, additional data from carefully focused and coordinated epidemiological-microbiological studies could greatly reduce the level of uncertainty. Sources of Data. The U.S. Department of Agriculture and Food and Drug Administration collect some data on levels of product contamination with certain microorganisms at various stages of processing and distribution. More detailed data, and data on additional microorganisms, have been reported in the literature. Data showing a direct link between product contamination and disease in the community (and subsequent disappearance of disease in association with elimination of contamination) have been published for some microorganisms and some products, but there are few data available on raw chicken or its major pathogens (Bryan, 1980a; CDC, 1983a,b; Horwitz and Gangarosa, 1976~. The CDC collects data on food-borne disease outbreaks through its national food-borne disease surveillance system. As in other national reporting systems and for individual cases of disease, however, there is undoubtedly significant underreporting and an emphasis on more serious illnesses. For example, almost all outbreaks of botulism are reported, whereas outbreaks of other illnesses involving only a few persons with relatively mild symptoms frequently are not investigated or reported. Data on routes of transmission can be obtained from outbreak reports and from case-control studies of specific pathogens. In properly designed case-control studies, it may be possible to determine the percentage of reported cases due to one microorganism that can be attributed to broiler chickens, i.e., attributable risk. To completely characterize the risk associated with microbial contamination of chicken, there must be sufficient data from which to predict changes in disease occurrence that would result from changes in levels of product contamination at each of several steps from production to the consumer's table. Such data are likely to show an

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62 increasing correlation between the potential for diseases to occur and microbial contamination as one moves from production to the ingestion of poultry products. The microbial load on the cooked, ready-to-eat product is the only reliable indicator of disease potential, and the further removed from this point data are obtained, the less reliable they are. Characterization Of Risk There are sufficient data to clearly establish many microorganisms as a hazard to human health and to estimate (very roughly) the risk of illness associated with eating contaminated chicken. It is also possible to identify where microorganisms may be introduced during processing (see Figures 3-1 and 3-2 in Chapter 3) and to quantitate microbial contamination at those points. These control points, and their identification as part of an HACCP system, have been discussed in detail in a previous report of the National Research Council (NRC, 1985a) . Microorganisms contaminating chicken during processing may die off or reproduce rapidly before reaching the consumer, depending on environmental and product conditions Thus, levels of contamination on the dinner plate may have little relation to data obtained at the time of slaughter or in the kitchen prior to cooking. Therefore, measurement of the risk posed by microbial contamination of a specific food item e, such as chicken, must involve identification and enumeration of cases of illness within an exposure group in addition to sampling during production. APPLICATION OF METHODS TO INDIVIDUAL AND GROUPS OF POULTRY-BORNE PATHOGENS Many pathogenic microorganisms have been associated with the production of chickens or with eating chicken. Following are some examples, which are broken down into three general categories: 1. Bacteria known to be pathogenic in humans that are carried on or transmitted by broiler chickens at retail: CampYlobacter jejuni, Salmonella spp. (excluding S. typhi) Yersinia enterocolitica 2. Bacteria known to be pathogenic in humans that have been associated with eating chicken: Bacillus cereus Clostridium botulinum Clostridium perfringens Shigella sppe Staphylococcus aureus

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63 Contamination by these human pathogens probably occurs during processing and preparation. 3. Microorganisms known to be pathogenic in chickens that are of questionable pathogenic significance for healthy humans when carried on or transmitted by broiler chickens at retail: Bacteria: Haemophilus gallinarum Pasteurella multocida Escherichia cold MYcobacterium avium Mycop ~ asma spp. Clostridium colinum ChlamYd~a psittaci Viruses and associated diseases: Picornavirus (encephalomyelitis) Alphavirus (equine encephalitis) Herpesvirus (Marek's disease, infective laryngotracheitis) Par~yxovirus (Newcastle disease) Adenovirus (adenoviral tracheitis) Poxvirus (fowl pox) Coronavirus (infectious bronchitis) Orthomyxovirus (avian influenza) Reovirus (viral arthritis Fungi: Aspergillus spp. DactYlar~a spp. Parasites: CrYptoscoridium _ For some of these microorganisms, their significance as human pathogens and information on their transmission by broiler chickens are discussed in the following paragraphs. Known Human Pathogens Carried on or Transmitted by Broiler Chickens at Retail CampYlobacter jejuni Hazard Identification and Evaluation. The gram-negative bacterium CampYlobacter ieiuni has recently been implicated as one of the most common bacterial causes of- gastroenter~t~s among both children and adults (Pai et al., 1979; Skirrow, 1977) . Studies ~n the United States, Canada, and Europe have demonstrated that C. jejuni is significantly more common in stool samples from patients with diarrhea than in samcles from healthY controls (Blaser et al., 1983a). in a clinical al., 1983b). _ , , _ _ ~ _ _ _ Ingestion of C. iejuni by volunteers has resulted diarrhea! syndrome (Black et al., 1983; Blaser et

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64 C. jejuni is pathogenic for normal, healthy adults (Black et al., - 1983; Blaser and Reller, 1981~. Illness may be more severe in elderly or debilitated patients, and the rare deaths from C. jejuni infection have occurred mostly in that group (Blaser and Reller, 1981~. Virulence factors and pathogenic properties of C. jeJuni include invasiveness, enterotoxin production, and cytotoxin production (Kl~pstein et al., 1985~. Some investigators have suggested that diarrhea-assoc~ated strains are more likely to have one or more of these properties than strains isolated from asymptomatic individuals (Klipstein et al., 1985; Ruiz-Palacios et al., 1983), but these results have not been confirmed by some other investigators (Mathan et al., 1984). Predominant symptoms among patients identified by positive stool culture include diarrhea, abdominal pain, malaise, fever, nausea, and vomiting (Blaser and Reller, 1981; SKCDPH, 1984) . Up to 80% of patients have fever, and approximately 50t give a history of bloody diarrhea (Blaser et al ., 1983a; SKCDPH, 1984) . Abdominal pain is severe enough to mimic acute appendicitis in about 19 of cases (Skirrow, 1977~. Complications rarely include toxic megacolon, gastrointestinal hemorrhage, convulsions (in children with high fevers), a typhoid-like syndrome, meningitis, reactive arthritis (in men with the HLA-B27 histocompatibility antigen), urinary tract infect) ons , and cholecystitis (Blaser and Reller, 1981~. Illness is reported most frequently among children less than a year old, and among young adults 20 to 29 years of age (Blaser et al., 1983b ; CDSC, 1981; Finch and Riley' 1984; Riley and Finch, 1985)0 Illnesses vary widely in severity, ranging from mild diarrhea lasting less than 24 hours to severe bloody diarrhea with abdominal pain and fever lasting several weeks. Some investigators have reported that most patients recover in less than a week (Blaser and Reller, 1981; Butzler and Skirrow, 1979), but a recent study of 225 culture-confirmed cases indicates that the average duration of illness is 13.5 days (SKCDPH, 1984~. In that study, 15 (6.7~) of the 225 patients were hospitalized up to 11 days as a result of their infection, most commonly (13 of the 15) for 5 days or less (SKCDPH, 1984). Since the late 1970s 9 most clinical microbiology laboratories in the United Kingdom have included cultures for Campylobacter as part of their routine evaluation of stool specimens (CDSC, 1981~. In 1981 there were about 12,500 reported isolations of Campylobacter, giving an annual isolation rate of approximately 28 per 100,000 population (Blaser et al., 1983b; CDSC, 1981~. Some clinical laboratories in the United States still do not routinely culture stool samples for Campylobacter, and nationwide surveillance for Campylobacter, which began In January 1983, is still not uniformly applied. During the first year , 42 states reported 8, 282 isolates of C . j e juni (Riley and Finch, 1985 ~ O In all 33 states that participated for at least 1l months in 1983, the number of Campylobacter isolates exceeded the

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65 number of Shigella isolates reported. In four states, there were more Campylobacter isolates than Salmonella isolates. Until national surveillance data are more complete, the best estimates of CampYlobacter incidence in the United States will continue to come from laboratories serving defined population groups. In the metropolitan area of Denver, Colorado, investigators found that the annual incidence of reported Campylobacter infections was 17.2 per 100,000 people (Blaser et al. , 1983b). In the Seattle-King County Department of Public Health (SKCDPH) study (which did not include active recruitment of patients with diarrhea), the annual incidence was estimated to be 100 per 100,000 (SKCDPH, 1984~. For children less than 1 year or age, rates were 332.9 per 100,000 for males and 194.9 per 100,000 for females. The figures in both of the above studies are based on reported isolation of Campylobacter from stool samples. One study in England projected a 1.1% (1,100 per 100,000) mean annual rate of Campylobacter infection in a defined population (Kendall and Tanner, 1982) or approximately 40 times the reported annual rate of isolations ~ 28 per 100, 000) . Blaser et al. (1983b) have estimated that in developed countries such as the United States, the incidence of Camped obacter infections, whether symptomatic or not, is about 1% to 2% per year (1,000-2,000 per 100,0009. The SKCDPH data (with a relatively high incidence rate) suggest that the annual incidence of hospitalized cases would be approximately 7 per 100,000 if all hospitalized cases in the study population were correctly identified. Data are inadequate to calculate mortality rates (Blaser et al., 1983b). Dose-Response Studies. For campylobanteriosis, information on dose response is based on a few studies involving small numbers of volunteers and is difficult to interpret. In volunteer studies with C. jejuni strain A3004, for example, 5 of 10 healthy adult volunteers ingesting 8 x 102 colony-formin~ units (cfu) became infected, and one of the 5 became ill. At 8 x 10 cfu, 6 of 10 were infected, but none were ill. The rate of infection increased with increase" in the size of the inoculum until 100% were infected at a dose of 10 cfu. At 9 x 104 cfu, the rate of illness was 46%; however, as the size of inoculum was increased, the rate of illness at each dose level ranged from only 9% to 22% (Black et al., 1983~. These data, in which the dose varied 100,000-fold, show that risk is far from linear with dose, perhaps because of marked variability in susceptibility. Epidemiological studies of both person-to-person and water-borne transmission of C. jejuni suggest that relatively small inocula are capable of causing disease (Blaser et al., 1983b). No outbreaks have been reported where it has been possible to clearly associate infection rate with a known inoculum.

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66 Potential for Human Exposure. The prevalence of C . j ejuni infection in live broiler chickens is highly variable. Microbiological surveys of live broilers have demonstrated that grow- out premises are inconsistently infected and that infection in one poultry housing unit does not mean that other housing units on the scone premises contain infected birds (Smitherman et al., 1984~0 Within infected flocks, however, infection rates tend to be high, and fecal samples6from infected chickens tend to be heavily contaminated (e.g., 10 cfu/g of feces) (Grant et al., 1980; Smitherman et al., 1984)e Ce iejuni has been found at many points during slaughter and processing, and a significant proportion of the broiler chicken carcasses available for retail sale carry the microorganism (Table 4-1~. Persons eating raw or rare chickens contaminated with C. iejuni may ingest sufficient numbers of microorganisms to become infected. CampYlobacter can also enter the kitchen via contaminated broiler carcasses and subsequently cross-contaminate other foods. In one study of commercial and institutional kitchens, Hutchinson et al. (1983) found that the hands of workers and kitchen work surfaces often became contaminated with CampYlobacter during the preparation of raw chicken. This is similar to the environmental contamination that occurs during the preparation of chicken contaminated by Escherichia cold (De Wit et al., 1979~. Several studies have shown an epidemiological link between chicken and gastroenteritis caused by C. Unit. Raw chicken eaten by military recruits during a training exercise was implicated in an outbreak in the Netherlands (Brouwer et al., 1979), and ingestion of poorly cooked chicken was associated with illness at a barbecue in Colorado (Blaser et al., 1983b) . In another study in Colorado, sporadic it lness was associated with the handling of raw chickens in home kitchens (Hopkins and Scott, 1983~. Consumption of chicken was associated with sporadic illness in Sweden (Norkrans and Svedham, 1982) and in urban areas of the Federal Republic of Germany (Kiss, 1983~. In the SKCDPH (1984) study, significantly more (p = 0.00003) patients with C. iejuni-caused enteritis had eaten chicken than had controls. The relative risk for chicken consumption was 2.4 (95% confidence interval [CI], 1.6-3.6~ ; for rare or raw chicken, it was 7~6 (95% CI, 2.1-27.6~; and for cooked chicken, it was 2.3 (95% CI, 1.5-3.51. The method of Walter (1975) was used to estimate that 48.2% of C. jejuni cases were attributable to eating chicken. The link - between chicken and human illness was reinforced by finding similarities in antibiograms, plasmid content, and serotypes of C. jejuni isolates taken from poultry at retail and from human cases (SKCDPH, 1984). Characterization of Risk. The studies cited above indicate that C. iejuni is clearly pathogenic for humans, resulting in as many as 1, 000 to 2, 000 cases per 100, 000 people annually in the United States (Blaser et al., 1983b). Epidemiological studies suggest that at least 48% of Camp~lobacter cases are attributable to chicken (SKCDPH, 1984~.

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89 Craven, P. C., W. B. Baine, D. C. Mackel, W. H. Barker, E. J. Gangarosa, M. Goldfield, H..Rosenfeld, R. Altman, G. Lachapelle, J. W. Davies, and R. C. Swanson. 1975. International outbreak of Salmonella eastbourne infection traced to contaminated chocolate. Lancet 1:788-793. Crittenden, L. B. 1976. The epidemiology of avian lymphoid leukosis. Cancer Res. 36:570-573. Current, W. L. 1985. Cryptosporidiosis . J . Am. Vet. Med. Assoc. 187:1334-1338. Damsker, B., and E. J . Bottone. 1985 . Mycobacterium avium-Mycobacterium intracellulare from the intestinal tracts of patients with the acquired immunodeficiency syndrome: Concepts regarding acquisition and pathogenes~s. J. Infect. Dis. 151:179-181. Dardiri , A. H., A. ~ . Yates , and T . D . Fl anagan. 1962 . The reaction to infection with the B1 strain of Newcastle disease virus in man. Am. J . Vet. Res . 23: 918- 921. de Groote, G., J e Vandepitte, and G. Wauters. 1982. Surveillance of human Yersinia enterocolit~ca infections in Belgium: 1963-1978. J. Infect. 4:189-197. De Wit , J . C ., G . Broekhuizen, and E . H . Kampelmacher . 1979. Cross - contamination during the preparation of frozen chickens in the kitchen. J . Hyg. 83: 27 - 32 . Durfee, P. T., M. M. Pullen, R. W. Currier II, and R. L. Parker. 1975. Human psittacosis associated with commercial processing ot turkeys . J . Am. Vet . Med. Assoc . 167: 804- 808 . Faddoul, G. P., and G. W. Fellows . 1966 . A five-year survey of the incidence of salmonellae in avian spec~es . Avian Dis . 10: 296 - 304 . Fagerberg, D. J ., and C . L. Quarles . 1982 . Final Report, Phases I, II, III, 1978-1981. Data Base for Drug Resistant Bacteria for Animals. Prepared for the U.S. Food and Drug Administration. FDA Contract No. 223-77-7032. Animal Sciences Department, Colorado State University, Fort Collins, Colo. t1590 pp.] Fenner, F., B. R. McAuslan, C. A. Mims, 3. Sambrook, and D. O. White. 1974. Viral oncogenesis: RNA viruses. Pp. 508-542 in The Biology of Anima1 Viruses, 2nd ed. Academic Press, New York. Filstein, M. R., A. B. Ley, M. S. Vernon, K. A. Gaffney, and L. T. Glickman. 1981. Epidemic of psittacosis in a college of veterinary med~cine. J. Am. Vet. Med. Assoc. 179: 569-574.

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