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2. HAZARD IDENTIFICATION

2.1 Summary

Over 2500 Salmonella enterica serotypes are recognized, and all are regarded as capable of producing disease in humans. Worldwide, salmonellosis is a leading cause of enteric infectious disease attributable to foods. Illnesses caused by the majority of Salmonella serotypes range from mild to severe gastroenteritis, and in some patients, bacteraemia, septicaemia and a variety of associated longer-term conditions. A wide range of foods has been implicated in foodborne illness due to Salmonella enterica. However, foods of animal origin, especially poultry and poultry products, including eggs, have been consistently implicated in sporadic cases and outbreaks of human salmonellosis.

2.2 Salmonella in foods and association with illness

Salmonellosis is one of the most frequently reported foodborne diseases worldwide.

Each year, approximately 40 000 Salmonella infections are culture-confirmed, serotyped, and reported to the United States Centers for Disease Control and Prevention (CDCs). Of total salmonellosis cases, an estimated 96% are caused by foods (Mead et al., 1999).

International data summarized by Thorns (2000) provides estimated incidences of salmonellosis per 100 000 people for the year 1997: 14 in the USA, 38 in Australia, and 73 cases per 100 000 in Japan. In the Europe Union, the estimates range from 16 cases per 100 000 (The Netherlands) to 120 cases per 100 000 in parts of Germany.

A review conducted in southern Latin America on foodborne outbreaks due to bacteria between the years 1995 and 1998 indicated that Salmonella were responsible for most (36.8%) of the reported cases in the region (Franco et al., in press). Salmonellosis infections were 55.1% of the reported foodborne disease cases reported from 1993 to 1996 in Korea (Bajk and Roh, 1998). "Salmonella species" was the causative agent reported most often in outbreaks in the European region, being responsible for 77.1% of the outbreaks recorded in which the etiologic agent was determined (WHO, 2001).

The genus Salmonella is considered to be a single species named Salmonella enterica. Serotyping differentiates the strains, and these are referred to by name as, for example, Salmonella enterica serotype Typhimurium, or as Salmonella Typhimurium (Hohmann, 2001). Salmonellae are gram-negative, motile (with a few exceptions), facultatively anaerobic bacteria (D’Aoust, 1997). Salmonellae grow between 8°C and 45°C, and at a pH of 4 to 8. With the exception of a limited number of human-host-adapted serotypes (also referred to as the typhoidal salmonellae), the members of the genus Salmonella are regarded as zoonotic or potentially zoonotic (Acha and Szyfres, 2001).

Non-typhoidal Salmonella enterica typically cause a self-limiting episode of gastroenteritis, characterized by diarrhoea, fever, abdominal cramps, and dehydration. The most cases are mild, and are generally not reported to public health agencies. However, more severe outcomes may result from the infection, depending on host factors and Salmonella serotype. Severe disease may occur in healthy individuals, but is most often seen in individuals who are immunocompromised, the very young, or the elderly. In addition, a small percent of cases in healthy individuals are complicated by chronic reactive arthritis.

In the United States of America alone, it has been estimated that 1.4 million cases, 16 430 hospitalizations and 582 deaths are caused by salmonellosis annually.

Costs of foodborne salmonellosis have been calculated for the United States of America population, and are estimated to be as high as US$ 2 329 million annually (in 1998 US dollars) for medical care and lost productivity (Frenzen et al., 1999).

A wide range of foods has been implicated in foodborne illness attributable to Salmonella enterica. Foods of animal origin, especially poultry, poultry products and raw eggs, are often implicated in sporadic cases and outbreaks of human salmonellosis (Bryan and Doyle, 1995; Humphrey, 2000). Recent years have seen increases in salmonellosis associated with contaminated fruits and vegetables. Other sources of exposure include water, handling of farm animals and pets, and human person-to-person when hand-mouth contact occurs without proper washing of hands.

Poultry is widely acknowledged to be a reservoir for Salmonella infections in humans due to the ability of Salmonella to proliferate in the gastrointestinal tract of chicken (Poppe, 2000) and subsequently survive on commercially processed broiler carcasses and edible giblets.

The evolution of the Salmonella enterica serotype Enteritidis (S. Enteritidis) pandemic beginning in the 1980s led to increased foodborne illnesses associated with poultry in many countries, specifically outbreaks and single cases associated with eggs and egg products (Levy et al., 1996; Rodrigue, Tauxe and Rowe, 1990; Thorns, 2000). Chicken, turkey and eggs were responsible for, respectively, 8.6%, 4.7% and 4.3% of 465 foodborne outbreaks caused by bacterial pathogens for which a vehicle was identified and that were reported to CDCs during the years 1988-1992 (Bean et al., 1997). Salmonella caused 12 of 18 outbreaks attributed to chicken, 6 of 12 turkey-associated occurrences, and 19 of 19 egg-related outbreaks. S. Enteritidis was responsible for the largest number of foodborne outbreaks, cases and deaths reported in the United States of America (Bean et al., 1997).

In southern Latin America, eggs and mayonnaise were the most common food products associated with outbreaks, but poultry meat was an equally important vehicle (Franco et al., in press). Of the reported foodborne outbreaks in Europe caused by an identified agent, more than one-third were confirmed to be caused by S. Enteritidis (WHO, 2001). Foods associated with S. Enteritidis outbreaks include egg and egg products (68.2%), cake and ice creams (8%), and poultry and poultry products (3%). Other vehicles include meat and meat products (4%), mixed foods (4%), fish and shellfish (2%), and milk and milk products (3%). In S. Typhimurium outbreaks, eggs and egg products (39%), meat and meat products (33%, frequently pork), and poultry and poultry products (10%) were reported as the vehicles of infection. A large number of other Salmonella serotypes were also involved in outbreaks in Europe, but specific serotypes were not reported.

2.3 Public health outcomes

Over 2500 Salmonella serotypes, also referred to as serovars, are known to cause illness in humans. As with all enteric pathogens, outcomes of exposure to Salmonella can range from no effects, to colonization of the gastrointestinal tract without any symptoms of illness, to colonization with the typical symptoms of acute gastroenteritis, and - less commonly - to invasive disease characterized by bacteraemia, sequelae, and, rarely, death.

In cases of acute gastroenteritis, the incubation period is generally 12-72 hours, commonly 12-36 hour. Illness lasts 2-7 days, and is characterized by the symptoms noted in the foregoing. Patients usually recover uneventfully within a week without antibiotic treatment. In some cases, severe diarrhoea requires medical interventions such as intravenous fluid rehydration. In cases where the pathogen enters the bloodstream, i.e. septicaemia or bacteraemia, symptoms include high fever, malaise, pain in the thorax and abdomen, chills and anorexia. In some patients, long-term effects or sequelae may occur, and a variety have been identified, including arthritis, osteoarthritis, appendicitis, endocarditis, pericarditis, meningitis, peritonitis and urinary tract infections (Bell, 2002). Typhoid, or enteric fever, caused by only a small number of specific serotypes, is discussed later in this section.

Severe illness resulting from salmonellosis is further exacerbated by the emergence of strains of Salmonella enterica that are multiple antibiotic resistant. The effects of underlying illnesses often complicate evaluation of the added clinical impact of resistant Salmonella However, in a study referring to the United States of America and the years 1989-90, after accounting for prior antimicrobial exposure and underlying illness, patients with resistant Salmonella were more likely to be hospitalized, and for a longer period of time (Lee et al., 1994).

Antibiotic therapy is not routinely recommended for the treatment of mild to moderate presumed or confirmed salmonella gastroenteritis in healthy individuals (Hohmann, 2001). Antimicrobial therapy should be initiated for those who are severely ill and for patients with risk factors for extra-intestinal spread of infection, after appropriate blood and faecal cultures are obtained. An intermittent period of faecal shedding may follow the acute illness, lasting from days to years. Buchwald and Blaser (1984) reviewed 32 reports and showed that the median duration of shedding following acute disease was 5 weeks, with less than 1% of patients becoming chronic carriers. Children may shed up to 106 to 107 salmonellae per gram faeces during convalescence (Cruickshank and Humphrey, 1987).

From United States of America data, it is estimated that, in general, 93% of individuals with symptoms of salmonellosis recover fully without a physician visit, 5% see a physician and recover fully, 1.1-1.5% of patients require hospitalization, and 0.04-0.1% of patients will die (Buzby et al., 1996; Mead et al., 1999).

However, both sporadic cases and outbreaks demonstrate that the health impacts in specific episodes of gastroenteritis can be particularly severe. Mattila et al. (1998) described a 1994 outbreak of S. Bovismorbificans in southern Finland from sprouted alfalfa seeds. Out of 191 respondents, 117 (61%) of the cases required a physician’s visit due to intestinal or extra-intestinal symptoms, and 21 (11%) individuals were hospitalized with a median hospital stay of 9 days. The authors state that most hospitalized patients were over 65 years of age. Of the subjects, 94 (49%) received antimicrobials (primarily fluoroquinolones) with a majority (78 out of 94 cases, or 83%) requiring antimicrobial treatment because of diarrhoea, fever, or a salmonella-positive urine sample. Duration of antimicrobial therapy (known for 70 patients) was 2 weeks or more in 44%, 10-12 days in 34% and 1 week or less in 21% of patients. The reason for the severity of the health outcomes in this outbreak was not determined, but it may have been associated with the numbers of salmonella that were consumed. Kanakoudi-Tsakalidou et al. (1998) conducted a prospective study of S. Enteritidis infection in nine children. Diarrhoea lasted 3-7 days, accompanied by fever in all cases. Four of the nine patients required hospitalization because of severe dehydration or bloody stools.

Inman et al. (1988) reported on a large outbreak in September 1984 of S. Typhimurium PT 22 in a group of police officers given a prepackaged box lunch. There were 473 individuals that fitted the case definition for salmonellosis, and they were mailed a questionnaire enquiring about symptoms associated with the gastroenteritis, with a 72% respondent rate. Out of 340 responders, 196 individuals experienced extra-enteric symptoms, including headaches (182 or 53.5%), joint pain (106 or 31.2%), redness or soreness in the eyes (37 or 10.9%), soreness in the mouth (15 or 4.4%) and skin rash (10 or 2.9%).

Mattila et al. (1998) identified a total of 210 cases with stool samples positive for S. Bovismorbificans for questionnaire follow-up regarding symptoms. Of the 191 (91%) respondents, 66 (35%) had articular symptoms, 52 (27%) experienced headaches, 8 (4%) had eye symptoms, and 7 (4%) had cutaneous symptoms, including one child who experienced erythema nodosum (a dermatological disorder characterized by the formation of tender, red nodules, usually located on the front of the legs). Cortazar et al. (1985) have likewise noted the association of erythema nodosum with Salmonella gastroenteritis.

Salmonella has been implicated as a triggering organism for reactive arthritis (ReA) and Reiter’s syndrome, in otherwise healthy individuals. Reactive arthritis is characterized by the development of synovitis (joint swelling and tenderness) within a few weeks after the occurrence of gastroenteritic symptoms. Maki-Ikola and Granfors (1992) summarized the clinical, epidemiological and laboratory data on Salmonella-triggered ReA. A review of extra-articular manifestations reported in 55 journal publications showed that these included urethritis, conjunctivitis, entesopathy, myalgia, weight loss exceeding 5 kg, dactylitis, erythema nodosum, oral ulcers, myocarditis, acute anterior uveitis, iritis, cholecystitis, keratitis, pharyngitis and pneumonia. Reiter’s syndrome is defined as the occurrence of arthritis with one or more extra-articular symptoms typical of the disease, such as conjunctivitis, iritis, urethritis and balanitis. The prognosis for ReA is usually favourable, with symptoms lasting for <1 year in most persons, although 5-18% may have symptoms that last more than 1 year and 15-48% may experience multiple episodes of arthritis.

Generally, 1-2% of a population infected by triggering organisms will develop ReA or Reiter’s syndrome (Keat, 1983; Smith, Palumbo and Walls, 1993). Maki-Ikola and Granfors (1992) reviewed several published outbreaks, totalling 5525 patients with salmonellosis, and estimated an incidence of reactive arthritis of 1.2-7.3% (mean: 3.5%).

Several researchers (Aho, Leirisalo-Repo and Repo, 1985; Archer, 1985; Calin, 1988) assert that HLA-B27-positive individuals are at higher risk for developing ReA, Reiter’s syndrome and ankylosing spondylitis after an enteric infection with triggering organisms. It is estimated that approximately 20% of HLA-B27-positive individuals who become ill with salmonellosis develop these chronic sequelae. However, a lack of correlation between ReA and HLA-B27 was been observed after S. Typhimurium and S. Heidelberg/S. Hadar outbreaks in Canada (Inman et al., 1988; Thomson et al., 1992; Thompson et al., 1995).

Ike et al. (1986) reported an incidence of ReA on physical examination in 2.3% of patients with Salmonella-positive stools following the 1985 Chicago milk outbreak of S. Typhimurium gastroenteritis. Reiter’s syndrome occurred approximately 10-fold less often than ReA. In a follow-up study of the Chicago patients, Ike, Arnold and Eisenberg (1987) found that 20 out of 29 reported persistent symptoms of ReA after one year, and symptoms had actually worsened in six cases.

In September 1984, a Canadian outbreak of S. Typhimurium PT 22 occurred in 473 out of 1608 police officers given a prepackaged box lunch (Inman et al., 1988). A cohort of 137 out of 196 individuals experiencing extra-enteric manifestations agreed to participate in a follow-up. Questionnaires were mailed out to their physicians and were returned for 116 (85%) volunteers, further describing the acute phase of the illness, with 19 reported by the physician to have experienced joint pain. Inman et al. (1988) noted a positive correlation between duration of gastrointestinal symptoms and duration of joint symptoms. In 13 patients, symptoms were restricted to ReA, while Reiter's syndrome was present in 6 patients (Inman et al., 1988).

An outbreak in Sweden in 1990 involved 113 medical scientists attending a radiology symposium, who were exposed to food contaminated with S. Enteritidis (Locht, Kihlstrom and Lindstrom, 1993), with 108 (96%) developing symptoms of salmonellosis and 17 (15%) of the 108 also developing ReA. Of the individuals developing ReA, 9 (53%) were men and 8 (47%) were women, with a mean age of 48.5 years (range: 34-60 years old; Locht, Kihlstrom and Lindstrom, 1993; Smith, 1994).

In another Canadian outbreak (Thomson et al., 1992), 79 women and 4 men in attendance at a luncheon were exposed to S. Heidelberg and S. Hadar from eating contaminated potato salad, and 73 subsequently developed salmonellosis. In addition to S. Thompson, S. Hadar and S. Heidelberg were isolated from the stools of 21 patients. Six of the 73 ill individuals developed ReA (Thomson et al., 1992; Smith, 1994). Ages of individuals who developed ReA were not significantly different from those cases that did not develop ReA (Thomson et al., 1992).

A 1994 outbreak in Finland caused by sprouted alfalfa seeds contaminated with S. Bovismorbificans was recently reported by Mattila et al. (1998). Questionnaires were sent to all 210 subjects with positive stool cultures. Median age in the 191 (91%) respondents was 32 years (range: 1-90), with 80% being older than 16 years of age; 130 (68%) were female. A total of 66 (35%) subjects reported articular symptoms, and 51 of the cases reporting articular symptoms were examined and 13 were contacted by telephone. A total of 12% (22 out of 191) fulfilled the criteria for ReA: 19 adults and 3 children. The incidence of ReA was not significantly different between children (8%) and adults (12%) (Mattila et al., 1998).

Kanakoudi-Tsakalidou et al. (1998) followed 9 cases of juvenile ReA prospectively, concluding that the disease in children is generally mild, transient and self-limiting. Five out of 9 patients carried the HLA-B27 antigen and experienced a prolonged course for arthritis (mean duration 9.5 months).

The duration of ReA illness was evaluated in several studies:

2.4 Host-adapted Salmonella

Most, if not all Salmonella, are capable of causing systemic disease and can be isolated from extra-intestinal sites. For the majority of serovars, this manifestation of disease occurs infrequently and mainly in patients who are immunocompromised, in infants or the elderly. However, a small number of serovars are known to be primarily or exclusively limited in host range (host-adapted; Selander et al., 1990) and primarily cause more severe forms of disease, including in immunocompetent patients. The most important human-adapted serovar is S. Typhi, the agent of typhoid fever; others include S. Paratyphi A, S. Paratyphi C, and S. Sendai, which present a typhoid-like enteric fever (Selander et al., 1990). The incubation period for these diseases is 7-28 days after exposure, with an average of 14 days. Symptoms include: high fever, malaise, nausea, abdominal pain, anorexia, delirium, constipation in early stages, and, in later stages, approximately one-third of patients develop diarrhoea (Bell, 2002). Convalescence may take up to 8 weeks.

Genetically, these differ from the majority of Salmonella serovars that typically cause gastroenteritis, and have distinctly different virulence attributes (Bäumler, Tsolis and Heffron, 2000). In the United States of America, 70% of the estimated 824 cases of typhoid fever per year have been associated with foreign travel (Mead et al., 1999). The principal source of the human-adapted serovars is human faecal contamination of water or prepared foods. Other host adapted strains of human importance include S. Dublin (cattle-adapted), and S. Cholerasuis (pig-adapted) both of which are markedly more frequently isolated from blood or other extragastrointestinal sites in humans than other typically foodborne serovars (McDonough et al., 1999; Olsen et al., 2001; Sockett, 1993). In some parts of the world, humans are a secondary host for S. Cholerasuis, producing severe enteric fever and high mortality (Selander et al., 1990).

2.5 Defining the scope of the risk assessments

The disease outcome of concern in the risk management request for risk assessment was acute gastroenteritis associated with Salmonella enterica in poultry. Human-host-adapted, predominantly invasive Salmonella serotypes (e.g. S. Typhi, S. Paratyphi) were not considered in developing the dose-response model. Disease outcomes that may occur beyond the diagnosis of gastroenteritis were not included in the risk estimations. Similarly, severity of disease outcomes attributable to antibiotic resistant strains of Salmonella were not estimated, nor for the more highly invasive Salmonella serotypes that are not commonly associated with poultry, i.e. S. Dublin and S. Cholerasuis.

2.6 References cited in Chapter 2

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Archer, D.L. 1985. Enteric microorganisms in rheumatoid diseases: causative agents and possible mechanisms. Journal of Food Protection, 48: 538-545.

Archer, D.L., & Young, F.E. 1988. Contemporary Issues: Diseases with a food vector. Clinical Microbiology Reviews, 1: 377-398.

Bajk, G.J., & Roh, W.S. 1998. Estimates of cases and social economic costs of foodborne salmonellosis in Korea. Journal of Food Hygiene and Safety, 13: 299-304.

Bäumler, A.J., Tsolis, R.W, & Heffron, F. 2000. Virulence mechanisms of Salmonella and their genetic basis.

Bean, N.H., Goulding, J.S., Daniels, M.T., & Angulo, F.J. 1997. Surveillance for foodborne disease outbreaks - United States, 1988-1992. Journal of Food Protection, 60: 1265-1286.

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Calin, A. 1988. Ankylosing spondylitis. Clinics in Rheumatic Diseases, 11: 41-60.

Cortazar, A.C., Rodriguez, A.P., Baranda, M.M., & Errasti, C.A. 1985. Salmonella gastroenteritis and erythema nodosum. Canadian Medical Association Journal, 133: 120.

Cruickshank, J.G., & Humphrey, T.J. 1987. The carrier foodhandler and non-typhoid salmonellosis. Epidemiology and Infection, 98: 223-230.

D’Aoust, J.Y. 1997. Salmonella Species. In: M.P. Doyle, L.R. Beuchat and T.J. Montville (eds). Food microbiology: Fundamentals and frontiers. Washington, DC: American Society for Microbiology Press.

Franco, B.D.G., Landgraf, M., Destro, M.T., & Gelli, D. (in press). Foodborne diseases in Southern South America. In: M.D. Miliotis and J. Bier (eds). International handbook on foodborne pathogens. New York, NY: Marcel Dekker.

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Humphrey, T. 2000. Public health aspects of Salmonella infection. pp. 245-262, in: C. Wray and A. Wray (eds). Salmonella in Domestic Animals. Wallingford, UK: CABI Publishing.

Ike, R., Arnold, W., Simon, C., Eisenberg, G., Batt, M., & White, G. 1986. Reactive arthritis syndrome (RAS) following an epidemic of Salmonella gastroenteritis (SG). Clinical Research, 34: A618-A618.

Ike, R.W., Arnold, W.J., & Eisenberg, G.M. 1987. p. S245, in 1st Annual Meeting of the American Rheumatolgy Association, 1987. Cited in Archer and Young, 1988.

Inman, R.D., Johnston, M.E., Hodge, M., Falk, J., & Helewa, A. 1988. Postdysenteric reactive arthritis. A clinical and immunogenetic study following an outbreak of salmonellosis. Arthritis and Rheumatism, 31: 1377-1383.

Kanakoudi-Tsakalidou, F., Pardalos, G., Pratsidou-Gertsi, P., Kansouzidou-Kanakoudi, A., & Tsangaropoulou-Stinga, H. 1998. Persistent or severe course of reactive arthritis following Salmonella enteritidis infection: A Prospective study of 9 cases. Scandinavian Journal of Rheumatology, 27: 431-434.

Keat, A. 1983. Reiter's syndrome and reactive arthritis in perspective. New England Journal of Medicine, 309: 1606-1615.

Lee, L.A., Puhr, N.D., Maloney, E.K., Bean, N.H., & Tauxe, R.V. 1994. Increase in antimicrobial-resistant Salmonella infections in the United States, 1989-1990. Journal of Infectious Diseases, 170: 128-134.

Levy, M., Fletcher, M., Moody, M., and 27 others. (1996) Outbreaks of Salmonella serotype enteritidis infection associated with consumption of raw shell eggs - United States, 1994-1995. Morbidity and Mortality Weekly Report, 45: 737-742.

Locht, H., Kihlstrom, E., & Lindstrom, F.D. 1993. Reactive arthritis after Salmonella among medical doctors: Study of an outbreak. Journal of Rheumatology, 20: 845-848.

Maki-Ikola, O., & Granfors, K. 1992. Salmonella-triggered reactive arthritis. Scandinavian Journal of Rheumatology, 21: 265-270.

Mattila, L., Leirisalo-Repo, M., Pelkonen, P., Koskimies, S., Granfors, K., & Siitonen, A. 1998. Reactive arthritis following an outbreak of Salmonella bovismorbificans infection. Journal of Infection, 36: 289-295.

McDonough, P.L., Fogelman, D., Shin, S.J., Brunner, M.A., & Lein, D.H. 1999. Salmonella enterica serotype Dublin infection: an emerging infectious disease for the Northeastern United States. Journal of Clinical Microbiology, 37: 2418-2427.

Mead, P.S., Slutsker, L., Dietz, V., McCraig, L.F., Bresee, J.S., Shapiro, C., Griffin, P.M., & Tauxe, R.V. 1999. Food-related illness and death in the United States. Emerging Infectious Diseases, 5: 607-625.

Olsen, S.J., Bishop, R., Brenner, F.W., Roels, T.H., Bean, N., Tauxe, R.V., & Slutsker, L. 2001. The changing epidemiology of Salmonella: Trends in serotypes isolated from humans in the United States, 1987-1997. The Journal of Infectious Diseases, 183: 753-761.

Poppe, C. 2000. Salmonella infections in the domestic fowl. pp. 107-132, in: C. Wray and A. Wray (eds). Salmonella in Domestic Animals. New York, NY: CAB International.

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Selander, R.K., Beltran, P., Smith, N.H., Helmuth, R., Rubin, F.A., Kopecko, D.J., Ferris, K., Tall, B.D., Cravioto, A., & Musser, J.M. 1990. Evolutionary genetic relationships of clones of Salmonella serovars that cause typhoid and other enteric fevers. Infection and Immunity, 58: 2262-2275.

Smith, J.L. 1994. Arthritis and foodborne bacteria. Journal of Food Protection, 57: 935-941.

Smith, J.L., Palumbo, S.A., & Walls, I. 1993. Relationship between foodborne bacterial pathogens and the reactive arthritides. Journal of Food Safety, 13: 209-236.

Sockett, P.N. 1993. The economic and social impact of human salmonellosis in England and Wales: A study of the costs and epidemiology of illness and the benefits of prevention. University of London. [Thesis]

Thomson, G.T.D., Chiu, B., Derubeis, D., Falk, J., & Inman, R.D. 1992. Immunoepidemiology of post-Salmonella reactive arthritis in a cohort of women. Clinical Immunology and Immunopathology, 64: 227-232.

Thompson, G.T.D., DeRubeis, D.A., Hodge, M.A., Rajanaygam, C., & Inman, R.D. 1995. Post-salmonella reactive arthritis: late clinical sequelae in a point source cohort. American Journal of Medicine, 98: 13-21.

Thorns, C.J. 2000. Bacterial food-borne zoonoses. Revenue scientifique et technique Office international des epizooties, 19(1): 226-239.

WHO. 2001. World Health Organization Surveillance Programme for Control of Foodborne Infections and Intoxications in Europe. Seventh Report, 1993-1998. Edited by K. Schmidt and C. Tirado. Published by the Federal Institute for Health Protection of Consumers and Veterinary Medicine (BgVV), Berlin, Germany. (FAO/WHO Collaborating Centre for Research and Training in Food Hygiene and Zoonoses) (see pages 415, 422-423.


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