Prepared by the Listeria monocytogenes Risk Assessment Team
Table of Contents
The Food and Drug Administration, Center for Food Safety and Applied Nutrition (FDA), in consultation with the Department of Agriculture, Food Safety and Inspection Service (FSIS), is conducting a risk assessment to determine the prevalence and extent of consumer exposure to foodborne Listeria monocytogenes and to assess the resulting public health impact of such exposure. The risk assessment team is collecting data in four areas: the presence of L. monocytogenes in foods, the consumption levels of these foods, information from epidemiological investigations, and data from experimentation that defines the dose-response relationship between this pathogen and populations with different immune conditions. This report describes the status of the risk assessment after development of the structure and culmination of the initial data collection. In addition to being a progress report, this document is an invitation for comments on the planned approach, assumptions and objectives for completion of the risk assessment and to request communication of any additional data that are relevant to the risk assessment.
Introduction
A series of outbreaks in the early 1980's in cole slaw, pasteurized milk and Mexican-style cheese impelled the recognition of this bacteria as an important foodborne pathogen. An intensive period of research revealed much about the microorganisms ecology, characteristics, presence in foods and public health effects. This research was summarized in several reviews and books (Farber et al., 1996; Farber and Peterkin, 1991:Miller et al., 1990; Ryser and Marth, 1991). The National Advisory Committee on Microbiological Criteria for Foods presented its analysis and recommendations to FSIS, FDA and other U.S. Government agencies in 1991 (NACMCF, 1991). Control strategies the committee recommended were to develop an effective surveillance system, target efforts on specific foods, and use a HACCP-based control program to cover foods from processing to consumption to minimize the presence, survival and multiplication of L. monocytogenes in foods.
Based upon the known characteristics of this microorganism and the disease, FDA maintains a policy of "zero tolerance" for L. monocytogenes in ready to eat foods. In other words, the detection of any L. monocytogenes in a 25 gram sample renders the food adulterated within the meaning of the Federal Food, Drug, and Cosmetic Act, 21 U.S.C. 342(a)(1). As recently as 1995, FDA affirmed this policy, as reflected in the decision in United States v. Union Cheese Co., 902 F. Supp. 778, 784, 786 (N.D. Ohio 1995). USDA’s Food Safety and Inspection Service, which regulates meat and poultry, likewise has historically had a zero tolerance policy for L. monocytogenes in ready-to-eat products.
FDA, in collaboration with FSIS, is conducting this risk assessment to gather scientific information, particularly recent additions to the literature, needed to review current programs relating to the regulation of L. monocytogenes contamination in foods to ensure that such programs provide maximum public health protection.
Background
L. monocytogenes is a bacterium that occurs widely in both the agricultural (soil, plants, and water) and food processing environment. The bacterium is resistant to various environmental conditions such as high salt or acidity (Ryser and Marth, 1991). L. monocytogenes grows at low oxygen conditions and refrigeration temperatures, and survives for long periods in the environment, on foods, in the processing plant, and in the household refrigerator. Although frequently present in raw foods of both plant and animal origin, it also can be present in cooked foods due to post-processing contamination. L. monocytogenes has been isolated in such foods as raw and pasteurized fluid milk, cheeses (particularly soft-ripened varieties), ice cream, raw vegetables, fermented raw-meat sausages, raw and cooked poultry, raw meats (all types), and raw and smoked fish (Farber and Peterkin, 1991; FDA, 1999; Ryser and Marth, 1991). Even when L. monocytogenes is initially present at a low level in a contaminated food, the organism can multiply during storage, including storage at refrigeration temperatures. A survey of a wide variety of foods from the refrigerators of listeriosis patients in the United States found 11 percent of the samples contained L. monocytogenes (Pinner et al., 1992).
It is well established that ingestion of L. monocytogenes can cause serious human illness, listeriosis. (CAST, 1994; Rocourt and Cossart, 1997; Farber and Peterkin, 1991; Miller et al., 1990; Ryser and Marth, 1991). In 1997, the Centers for Disease Control and Prevention (CDC) Foodborne Diseases Active Surveillance Network (FoodNet) showed that of all food borne illnesses, the rate of hospitalization was highest for persons infected with L. monocytogenes (88 percent). Similarly, of all of the food borne pathogens tracked by CDC, L. monocytogenes had the highest case fatality rate in that 20 percent of persons hospitalized with listeriosis died. CDC also found that the incidence of listeriosis is 0.5 per 100,000 population, compared to a combined rate of 51.2 per 100,000 for all nine of the food borne illnesses surveyed (CDC, 1998). Thus, although serious, listeriosis is a relatively rare food borne illness. Most cases of listeriosis occur in pregnant women or individuals with a predisposing disease (such as alcoholism, diabetes, or cirrhosis of the liver) or an impaired immune system resulting from either a disease (such as AIDS) or immunosuppressive treatment for a malignancy or an organ transplant. (Rocourt and Cossart, 1997; Ryser and Marth, 1991).
Listeriosis has a long incubation time (up to 5 weeks) and a range of symptoms. Infection of a pregnant woman may result in flu-like symptoms with fever, muscular pain, or headache, or the listeriosis infection may be asymptomatic. Importantly, however, when a pregnant woman contracts listeriosis, the fetus or new borne infant is likely to suffer severe consequences from the maternal infection, including spontaneous abortion, fetal death, stillbirth, neonatal septicemia, or meningitis. In non-pregnant adults, septicemia and meningitis are the most common result of a listeriosis infection, although organ infections and mild gastroenteritis can also occur.
As noted, although the incidence of listeriosis is relatively low and the consequences of an infection may be severe, an estimated 2 to 6 percent of the healthy population harbors L. monocytogenes in their intestinal tract without signs of illness (Rocourt and Cossart, 1997; Ryser and Marth, 1991). Because the documented prevalence of L. monocytogenes in people and in commonly-eaten foods is much higher than the documented incidence of listeriosis, some experts believe that the ingestion of low levels of L. monocytogenes may not result in illness and thus, may not constitute a general public health hazard (Farber et al., 1996, ICMSF, 1994).
Other countries, including certain major trading partners of the United States, take a slightly different approach to L. monocytogenes contamination. Relying upon their interpretation of the existing scientific data, countries such as Canada and Denmark have a "non-zero tolerance" for L. monocytogenes for some classes of foods (ICMSF, 1994; IFST, 1995). For example, in Canada, ready-to-eat foods that have not been associated with an outbreak and do not allow any growth of L. monocytogenes during a 10 day period of refrigerated storage may contain up to 100 L. monocytogenes organisms per gram without being considered unlawful (Health Canada, 1994). Denmark has six classes of foods that have to meet various criteria for L. monocytogenes. In raw, ready to eat foods, for example, two of five samples can contain between 10 and 100 organisms per gram and no sample can exceed 100 organisms per gram. Although the course taken by other countries concerning L. monocytogenes contamination is not determinative of the U.S. approach, the policies of certain major trading partners provides further context to any reexamination of current U.S. policy.
Objectives of the Risk Assessment
As noted above, FDA and USDA/FSIS are jointly planning to conduct an assessment of the risk posed by L. monocytogenes to American consumers. A RA is a systematic and comprehensive collection of information and analysis of such information that promotes an understanding of the interactions of various factors in a complex situation and provides a basis for making decisions. The goal of this RA is to provide FDA and FSIS with the information needed to review current programs relating to the regulation of L. monocytogenes contamination in foods to assure that such programs provide maximum public health protection.
Risk Assessment Plan:
The RA will seek and analyze four types of information: information concerning the level of L. monocytogenes contamination of foods and consumption levels of such foods (i.e., an exposure assessment), information concerning the epidemiology of food borne listeriosis and information regarding the human health consequences of such exposure (i.e., a dose-response analysis). Because of the significant role that epidemiology plays in the dose-response relationship, dose-response and epidemiology will be addressed together under the heading of Public Health.
1. The RA will determine the frequency of occurrence of L. monocytogenes in different classes of foods, particularly the ready-to-eat foods that are intended for consumption without additional heating. Ready-to-eat foods are represented by numerous types of dairy, seafood, meat, and plant products. The RA also will collect and analyze information on the number of viable organisms associated with these foods at the time of consumption. When data are collected at processing stages prior to consumption, the RA will utilize models for growth, survival, or thermal inactivation to estimate actual exposure of the consumer to L. monocytogenes.
2. The RA also will utilize food consumption databases to assess the amount of these foods that are consumed. The RA will use the information about the frequency of occurrence and numbers of L. monocytogenes and food consumption to estimate the number of L. monocytogenes cells consumed.
3. The RA will analyze epidemiological evidence concerning the foods implicated both in documented outbreaks and in sporadic cases of listeriosis, the numbers of L. monocytogenes consumed, the populations which became ill, and the severity of their illnesses.
4. The RA will include an evaluation of the dose-response relationship, which will describe the health effects from consuming specific numbers of L. monocytogenes organisms. The information that will form the basis of the dose-response relationship element of the RA may come from epidemiological, animal, or in vitro studies. FDA and FSIS recognize that the frequency and severity of illness may be affected by the food matrix, characteristics of specific strains of the organism, and variability in human susceptibility.
Exposure assessment, therefore, comprises prevalence/levels of L. monocytogenes in foods (#1) and the consumption of these foods (#2). The hazard assessment incorporates the epidemiology (#3) and experimental evidence (#4). The logical flow of the risk assessment is illustrated on Figure 1.
The RA will examine a number of issues, including which foods contribute most to the consumption of L. monocytogenes, what are the numbers of organisms when a food is contaminated, how frequently are foods heavily contaminated, are there common characteristics in the composition, processing or storage of contaminated foods, are some strains of L. monocytogenes more virulent that others, what is the extent of organism growth during storage (including storage at refrigeration temperatures), and what is the likelihood of illness to various subpopulations from consuming different numbers of L. monocytogenes. All assumptions and uncertainties in the RA will be identified and documented. The RA process will also include an evaluation of the adequacy of current scientific knowledge, data, and information. This will suggest where future research could be directed to reduce any uncertainty in the risk estimate that prevents a clear understanding of the causes and impact of listeriosis.
This risk assessment is concerned with the levels of L. monocytogenes present in the foods at the time of consumption. How those foods become contaminated at any particular level or the effects of a specified process, storage period or preparation practice is outside the immediate scope of this risk assessment. Upon completion of this assessment and the identification of specific foods which contribute the largest consumption of L. monocytogenes, it is anticipated that the risk managers in FDA would request a second phase of this risk assessment be developed to examine the causes of high levels in a food and anticipated effects of possible mitigations.
Table 1 lists the members of the risk assessment team. Risk management guidance is provided by senior FDA and FSIS officials, headed by Dr. R. L. Buchanan. The proposed time line for the project (Table 2) calls for this document to be presented in conjunction with a public meeting of the National Advisory Committee on Microbial Criteria for Foods (NACMCF). The risk assessment team will incorporate suggestions, recommendations and additional data from the May meeting and then begin the calculations and risk assessment phase. The target date to complete the risk assessment and present a draft report to the risk management team is September, 1999. Following internal review, presentations will be made and the risk assessment will be publicly available.
Table 1. Members of the risk assessment team. |
Leaders | ||
Richard C. Whiting* | FDA, CFSAN | |
Wesley Long | FDA, CFSAN | |
Epidemiology | ||
Patrick McCarthy, lead | FDA, CFSAN | |
John Bryce | FDA, CFSAN | |
L. monocytogenes in foods | ||
Anthony Hitchins, lead | FDA, CFSAN | |
Pauline Lerner | FDA, CFSAN | |
MaryLynne Datoc | FDA, ORA | |
Eric Ebel | USDA, FSIS | |
Wayne Schlosser | USDA, FSIS | |
Food consumption | ||
Mary Bender, lead | FDA, CFSAN | |
Eric Hanson | FDA, CFSAN | |
Nancie McCabe | FDA, CFSAN | |
Lori LeGault | FDA, CFSAN | |
Kathy Smith | FDA, CFSAN | |
Dose-Response | ||
Richard Raybourne, lead | FDA, CFSAN | |
Tina Rouse | FDA, CFSAN | |
Modeling-Statistics | ||
Clark Carrington | FDA, CFSAN | |
*
FDA, CFSAN, HFS-032, 200 C St. SW, Washington, DC 20204 phone 202-260-0511, fax 202-260-9653, e-mail rwhiting@bangate.fda.gov |
Table 2. Time-line for completion of risk assessment |
Develop plans and assemble risk assessment team | January 1999 |
Present initial plans to NACMCF | February 1999 |
Publish Federal Register Notice of Risk Assessment | |
Develop details of plan and begin data collection | |
Write Structure and Initial Data Survey Document | May 1999 |
Present progress to NACMCF and public | May 1999 |
Revise plans, complete data collection | |
Complete risk assessment calculations, draft report | |
Present report to NACMCF and public | Sep.-Oct. 1999 |
Finalize written report and distribute | |
Conduct additional risk assessment activities in response to subsequent questions from risk managers | November 1999 |
References
CAST. 1994. Foodborne Pathogens. Council for Agricultural Science and Technology, Task Force Report 122. Ames, IA.
CDC. 1998. Morbidity and Mortality Weekly Report., Incidence and Foodborne Illnesses-Foodnet, 1997. 47(37);782.
FDA. 1999. Bad Bug Book (Foodborne Pathogenic Microorganisms and Natural Toxins). Internet address: http://vm.cfsan.fda.gov/~mow/intro.html
Farber, J.M. and Peterkin, P.I. 1991. Listeria monocytogenes, a food-borne pathogen. Microbiol. Rev. 55:476-511.
Farber, J.M., Ross, W.H. and Harwig, J. 1996. Health risk assessment of Listeria monocytogenes in Canada. Int. J. Food Microbiol. 30:145-156.
FSIS. 1998. Salmonella Enteritidis risk assessment. Shell eggs and egg products. USDA, FSIS, Washington, DC.
Health Canada. 1994. Compliance Guide/Policy on Listeria Monocytogenes in Ready-to-Eat Foods.
ICMSF. 1994. Choice of sampling plan and criteria for Listeria monocytogenes. Int. J. Food Microbiol. 22:83-96.
IFST. 1995. Microbiological criteria for retail foods. Professional Food Microbiology Group, Inst. Food Science and Technology. Lett. Appl. Microbiol. 20:331-332.
Miller, A.L., Smith, J.L. and Somkuti, G.A. 1990. Foodborne Listeriosis. Soc. Indust. Microbiol., Elsevier, NY.
NACMCF. 1991. Listeria monocytogenes. Recommendations by the National Advisory Committee on Microbiological Criteria for Foods. International J. Food Microbiol. 14:185-246.
Pinner, R.W., Schuchat, A., Swaminathan, B., Hayes, P.S., Deaver, K.A., Weaver, R.E., Plikaytis, B.D., Reeves, M., Broome, C.V. and Wenger, J.D. 1992. Role of foods in sporadic listeriosis. 2. Microbiologic and epidemiologic investigation. JAMA 267:2046-2050.
Rocourt, J. and Cossart, P. 1997. Listeria monocytogenes. In Doyle, M.P., Beuchat. L.R. and Montville, T.J. eds. Food Microbiology, Fundamentals and Frontiers. ASM Press, Washington, DC.
Ryser, E.T. and Marth, E.H. 1991. Listeria, listeriosis, and food safety. Dekker, NY.
Introduction
The goal of this work-group is to collect the available Listeria monocytogenes food contamination data which will be used in conjunction with U. S. dietary intake data collected by the Food Consumption Work Group to determine how much of the viable pathogen is consumed in the USA.
Conclusion
The contamination data collection phase is still in progress. A comprehensive universal database may be useful to allow extrapolation of the values from one food group to another closely related one.
Table 1. Food Categories and Types.
NO. | FOOD CATEGORIES | TYPE | NOTES | ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
SEAFOOD
1
| Fish
| Cooked (rte)
| Include fish sticks
| 2
|
| Raw
|
| 3
| Shellfish
| Cooked (rte)
| Mollusks and crustaceans; include crab and salmon cakes
| 4
|
| Raw
|
| 5
| Smoked Seafood
| Rte
|
| 6
| Miscellaneous Seafood Products
| Rte
| Dried, marinated
| DAIRY
| 1
| Cheese
| Soft
| Look for amount of unpasteurized consumed and Lm presence
| 2
|
| Other
|
| 3
| Ice Cream
|
| Ice milk, novelties, sherbet, desserts
| 4
| Fluid Milk
| Raw
| Include goat's milk
| 5
|
| Pasteurized
| Federal requirement; some states allow unpasteurized; include chocolate
| 6
| Misc. Dairy Products
|
| Yogurt, frozen yogurt, butter, shakes, drinks, cream, eggnog, dips, buttermilk, sour cream
| PASTRIES
| 1
| Cream Filled Pastries
|
|
| PRODUCE
| 1
| Vegetables—eaten raw
| Above ground
|
| 2
|
| Below ground
|
| 3
| Misc. Vegetable Products
|
| Pickled, dried, dehydrated, meatless hot dogs and other meat substitutes
| 4
| Fruits—eaten raw
| Near ground
|
| 5
|
| Not near ground
|
| 6
| Misc. Fruit Products
|
| Dried
| JUICES
| 1
| Fruit
| Pasteurized
|
| 2
|
| Unpasteurized
|
| 3
| Vegetable
| Pasteurized
|
| 4
|
| Unpasteurized
|
| SALADS
| 1
| Vegetable/Fruit-nut
|
| Include hummus
| 2
| Meat/Fish/Egg
|
|
| 3
| Misc. Mixed
|
| Include pasta salads
| MEATS
| 1
| Beef
| Intact (raw)
| Steak, roasts, corned beef
| 2
|
| Ground
|
| 3
|
| Cooked (rte)
| Steak, roasts, corned beef
| 4
| Pork
| Intact (raw)
| Ham, pork roast
| 5
|
| Cooked (rte)
| Ham, pork roast
| 6
| Lamb
| Intact raw)
|
| 7
|
| Cooked (rte)
|
| 8
| Poultry
| Cooked (rte)
| Chicken, turkey, duck
| 9
|
| Ground
|
| 10
| Deli—luncheon meats
| Bologna, hot dogs
|
| 11
|
| Fermented, Semi-dry
| Include sausages, pepperoni
| 12
|
| Beef, pork, poultry
| Include sliced and chopped meats, such as ham, roast beef, chicken, turkey, duck
| >13
| Misc. bulk and link sausages
|
|
| 14
| Jerky and Dried meats
|
|
| 15
| Exotic
| Spreads, pate, loaves
| Include venison
| SANDWICHES/SUBS
| 1
| Burgers
| Cheeseburger, hamburger
| Served hot
| 2
| Deli
| Various meats, eggs, seafood, veggie
| Served cold; Corned/roast beef, steak, lamb, bacon, ham, pork, chicken, turkey, salami, sausage, egg, tuna, shrimp, crab
| MISC. MIXED DISHES
| 1
| Mexican
| With cheese
|
| 2
|
| Without cheese
|
| MISCELLANEOUS
| 1
| Salad dressing
| Blue cheese
|
| 2
| Egg Products
|
|
| |
REFERENCE | PLACE | FOOD GROUP | COMPONENTS | STATE | LISTERIA | NUMBER POSITIVE | TOTAL SAMPLED | CFU / G or mL
McLauchlin90
UK
Sandwiches
TOTAL
rte
Monocytogenes
58
796
.
McLauchlin90
UK
sandwiches
TOTAL
rte
Monocytogenes
3
796
1000
Ng & Seah95
Sing.
sandwiches
TOTAL
rte
Monocytogenes
0
11
.
Wilson 1996
UK
sandwiches
chicken & salad
rte
Monocytogenes
1
725
63000
Wilson 1996
UK
sandwiches
chicken & salad
rte
Monocytogenes
1
725
100
Wilson 1996
UK
sandwiches
ham & tomato
rte
Monocytogenes
1
725
200
Wilson 1996
UK
sandwiches
egg & bacon
rte
Monocytogenes
1
725
1400
Wilson 1996
UK
sandwiches
chicken
rte
Monocytogenes
1
1
100
Wilson 1996
UK
sandwiches
TOTAL
rte
all species
113
725
100
WNYJWG91a
UK
sandwiches
TOTAL
rte
Monocytogenes
10
103
.
WNYJWG91a
UK
sandwiches
TOTAL
rte
Monocytogenes
1
103
nd
WNYJWG91a
UK
sandwiches
TOTAL
rte
Monocytogenes
1
103
<20
WNYJWG91a
UK
sandwiches
TOTAL
rte
Monocytogenes
3
103
20-100
WNYJWG91a
UK
sandwiches
TOTAL
rte
Monocytogenes
2
103
100-1000
WNYJWG91a
UK
sandwiches
TOTAL
rte
Monocytogenes
3
103
1000+
WNYJWG91a
UK
sandwiches
meat
rte
Monocytogenes
7
46
.
WNYJWG91a
UK
sandwiches
meat
rte
Monocytogenes
1
46
nd
WNYJWG91a
UK
sandwiches
meat
rte
Monocytogenes
1
46
<20
WNYJWG91a
UK
sandwiches
meat
rte
Monocytogenes
2
46
20-100
WNYJWG91a
UK
sandwiches
meat
rte
Monocytogenes
1
46
1000-1000
WNYJWG91a
UK
sandwiches
meat
rte
Monocytogenes
2
46
1000+
WNYJWG91a
UK
sandwiches
fish
rte
Monocytogenes
0
21
.
WNYJWG91a
UK
sandwiches
egg/egg mayonnaise
rte
Monocytogenes
0
0
.
WNYJWG91a
UK
sandwiches
other
rte
Monocytogenes
3
36
.
WNYJWG91a
UK
sandwiches
other
rte
Monocytogenes
1
36
20-100
WNYJWG91a
UK
sandwiches
other
rte
Monocytogenes
1
36
100-1000
WNYJWG91a
UK
sandwiches
other
rte
Monocytogenes
1
36
1000+
|
References
A. Foods in general
Anderson, J. K., and Nørrung, B. 1995. Occurrence of Listeria monocytogenes in Danish retail foods. Annex II, Danish Government Comments, Codex Alimentarius CL 1995/32-FH. Control of Listeria monocytogenes in foods.
Avoyne, C., Butin, M., Delaval, J., and Bind, J.-L. 1997. Detection of Listeria spp. in food samples by immunomagnetic capture: ListerScreen method. J. Food Protect. 60:377-384.
De Simón, M., Tarragó, C., and Ferrer, M. D. 1992. Incidence of Listeria monocytogenes in fresh foods in Barcelona (Spain). Intl. J. Food Microbiol. 16:153-156.
Farber, J. M., Sanders, G. W., and Johnston, M. A. 1989. A survey of various foods for the presence of Listeria species. J. Food Protect. 52:456-458.
FDA. 1998. Incidence of Listeria monocytogenes in food samples collected by FDA. FDA Microbiological Information System.
Greenwood, M. H., Roberts, D., and Burden, P. 1991. The occurrence of Listeria species in milk and dairy products: A national survey in England and Wales. J. Food Protect. Intl. J. Food Microbiol. 12:197-206.
Hayes, P. S., Graves, L. M., Swaminathan, B., Ajello, G. W., Malcolm, G. B., Weaver, R. E., Ransom, R., Deaver, K., Plikaytis, B. D., Schuchat, A., Wenger, J. D., Pinner, R. W., Broome, C. and the Listeria Study Group. 1992. Comparison of three selective enrichment methods for the isolation of Listeria monocytogenes from naturally contaminated foods. J. Food Protect. 55:952-959.
Iida, T., Kanzaki, M., Nakama, A., Kokubo, Y., Maruyama, T. and Kaneuchi, C. 1998. Detection of Listeria monocytogenes in humans, animals and foods. J. Vet. Med. Sci. 60:1341-1343.
Lahellec, C., Salvat, G., and Brisabois, A. 1996. Incidence des Listeria dans les denrees alimentaires. Path. Biol. 44:808-815.
McLaughlin, J. and Gilbert, R. J. 1990. Listeria in food. Report from the PHLS Committee on Listeria and Listeriosis. PHLS Microbiology Digest 7:54-55.
Ng, D. L. K., and Seah, H. L. 1995. Isolation and identification of Listeria monocytogenes from a range of foods in Singapore. Food Control 6:171-173.
Ryu, C-H., Igimi, S., Inoue, S., and Kumagai, S. 1992. The incidence of Listeria spp. in retail foods in Japan. Intl. J. Food Microbiol. 16:157-160.
Teufel, P. and Bendzulla, C. 1993. Bundesweite erhebung zum vorkommen von Listeria monocytogenes in lebensmitteln. Abshulßbericht. Pp 1-58. Bundesinstitut für gesundheitlichen Verbraucherschultz und Veterinärmedzin, Berlin, Germany.
USDA/FSIS. 1998. Listeria monocytogenes testing of ready-to-eat products, 1994-1998.
WNYJWG. 1991. Listeria in food. Report of the West and North Yorkshire Joint Working Group on a two year survey of the presence of Listeria in food.
Wilson, I. G. 1995. Occurrence of Listeria species in ready to eat foods. Epidemiol. Infect. 115:519-526.
Wilson, I. G. 1996. Occurrence of Listeria species in prepacked retail sandwiches. Epidemiol. Infect. 117:89-93.
B. Listeria in Seafood
Dillon, R., Patel, T., and Ratnam, S. 1994. Occurrence of Listeria in hot and cold smoked seafood products. Intl. J. Food Micro. 73-33.
Dillon, R.M., and Patel, T.R. 1992. Listeria in Seafoods. J. Food Protection 55:1009-1015.
Farber, J. M. and Peterkin, P. I. 1991. Listeria monocytogenes, a foodborne pathogen. Microbiological Reviews 55(3):476-511.
Fuchs, R. S. and Reilly,. 1992. The incidence and significance of Listeria monocytogenes in seafoods. Quality Assurance in the Fish Industry, eds. H.H.Huss et al. 217-229.
Heinitz, M. L. and Johnson, J. M. 1998. The incidence of Listeria spp., and Clostridium botulinism in smoked fish and shellfish. J. Food Protection 61(3):318-323.
Ryser, E.T. and Marth, E.H. (eds.). 1999. Listeria, Listeriosis, and Food Safety, 2nd ed., Marcel Dekker, Inc., N.Y. 630 pp.
Weagent, S.D., Sado, P.N., Colburn, K.G., Torkelson, J.D., Stanley, F.A., Krane, S.H., Shields, S.C., and Thayer, T.F. 1988. The incidence of Listeria species and in frozen seafood products. J. Food Protection 51:655-7.
C. Listeria in Dairy Foods
Beckers, H.J., Soentoro, P.S.S., and Delfgoti-van A. 1987. The occurrence of Listeria monocytogenes in soft cheeses and raw milk and its resistance to heat. International Journal of Food Microbiology 4:249-256.
Cantoni, C., Valenti, M., and Comi, G. 1988. Listeria in formaggi e in salumi, Industrie Alimentari XXVII.(Ottobre):859-861.
Casarotti, V. T., Gallo, C. R., Camargo, R., 1994. Occorrencia de Listeria monoytogenes em leite cru, leite posteurizado tipo C e queijo minas frescal comercializados en Piracicaba - S. P. Archivos LatinoAmericanos De Nurticion.
Comi, G. and Cantoni, C. 1988. Alcuni aspetti della presenza di L. monocytogenes dei Formaggi. Industrie Alimentari XXVII(Febbraio)104-108.
Comi, G., Cantoni, C., and d'Aubert, S. 1987. Indagine sulla presenza di Listeria monocytogenes nei formaggi. Industrie Alimentari(Marzo):216-218.
Coveney, H.M., Fitzgerald, G.F., and Daly C. 1994. A study of the microbiological status of Irish farmhouse cheeses with emphasis on selected pathogenic and spoilage micro-organisms, Journal of Applied Bacteriology 77:621-630.
DeBoer, E. and Kuik, D. 1987. A Survey of the Microbiological Quality of Blue-Veined Cheeses. Neth. Milk Dairy J. 41:227-237.
Farber, J.M., Johnston, M.A., Purvis, U., and Loit A. 1987. Surveillance of soft and semi-soft cheeses for the presence of Listeria spp. International Journal of Food Microbiology 5:157-163.
Gohil, V. S., Ahmed, M. A., Davies, R., and Robinson, R., 1995. Incidence of Listeria spp. in Retail Foods in the United Arab Emirates. Journal of Food Protection (January).
Greenwood, M.H., Roberts, D., and Burden P. 1991. The occurrence of Listeria species in milk and dairy products; a national survey in England and Wales. Interntl. J. Food Microbiology 12:197-206
Klinger, I. And Rosenthal, I. 1997. Public health and the safety of milk and milk products from sheep and goats. Rev. Sci. Tech 16(2):482-484.
Loncarevic, S., Danielsson-Tham, M.L., and Tham, W. 1995. Occurrence of Listeria monocytogenes in soft and semi-soft cheeses in retail outlets in Sweden. International Journal of Food Microbiology 26:245-250.
Pini, P. N., and Gilbert, R. J. 1988. A comparison of two procedures for the isolation of Listeria monocytogenes from raw chickens and soft cheeses. International Journal of Food Microbiology.
Pini, P. N. and Gilbert, R. J. 1987. The occurrence in the U.K. of Listeria species in raw chickens and soft cheeses. International Journal of Food Microbiology 6:317-326.
Pinto, B. and Reali, D. 1996. Prevalence of Listeria monocytogenes and other Listerias in Italian-make soft cheeses. Department of Public Health and Biostatistics, University of Pisa-Italy.
Rodler, M. and Korbler, W. 1989. Examination of Listeria monocytogenes in milk products, Acta Microbiologica Hungarica 36(2-3):259-261.
Sanchez-Rey, R., Poullet, B., Caceres, P., and Larriba, G. 1993. Microbiological Quality and Incidence of Some Pathogenic Microorganisms in La Serena Cheese Throughout Ripening. Journal of Food Protection, 56(10):879-881.
Tonge, R., Utzinger, D., and Arias, L.M. 1994. Incidence of Listeria monocytogenes in pasteurized ice cream and soft cheese in Costa Rica, 1992 Rev. Biol. Trop. 42(1/2):327-328.
Weber, V. A., Baumann, C., Potel, J., and Friess, H. 1988. Nachweis van Listeria monocytogenes und Listeria innocua in Kase. Berl, Munch, Tierarztl. Wschr.
D. Listeria in Vegetables
Albrecht, J., Hamouz, F., Sumner, S., and Melch, V. 1994. Microbial Evaluation of Vegetable Ingredients in Salad Bars. Journal of Food Protection 58:683-685.
Allerberger, F., and Guggenbichler, J. P., Listeriosis in Austria: Report of an Outbreak in 1986. Acta Microbiologica Hungarica (1989).
Bendig, J.W.A. and Strangeways, J.E.M. 1989. Listeria in Hospital Lettuce, The Lancet (March 18):616-617.
Beuchat, L.R., Berrang, M.E., and Brackett, R.E. 1990. Presence and public health implicaitons of Listeria monocytogenes on vegetables. Foodborne Listeriosis, Chapter 25, 175-181.
Bibi, A. and Bari A. 1992. Incidence of Listeria monocytogenes in Frozen and Refrigerated Vegetables Under Pakistan Conditions, Pakistan J. Zool. 24(3):231-233.
Breer, C. and Schopfer, K. 1989. Listerien in Nahrungsmitteln. Schweiz med. Wschr.
Caserio, G., 1989. Listeria in carni, pesce, pollame, poste farcite e vegetali. Industrie Alimentari.
Farber, J.M., Sanders, G.W., and Johnston, M.A. 1989. A Survey of Various Foods for the Presence of Listeria species. Journal of Food Protection 52(7):456-458.
Hagenmaier, R.D., and Baker, R. 1997. A Survey of the Microbial Population and Ethanol Content of Bagged Salad. Journal of Food Protection 61(3):357-359.
Hao, D. Y. Y., Reuchat, L. R., and Brackett, R. E. 1987. Comparison of Media and Methods of Detecting and Enumerating Listeria monocytogenes in Refrigerated Cabbage. Applied and Environmental Microbiology (May).
Heisick, J.E., Wagner, D.E., Nierman, M.L., and Peeler, J.T. 1989. Listeria spp. Found on Fresh Market Produce. Applied and Environmental Microbiology (Aug.):1925-1927.
Ho, J.L., Shands, K.N., Friedland, G., Eckind, P., and Fraser, D.W. 1986. An Outbreak of Type 4b Listeria monocytogenes Infection Involving Patients from Eight Boston Hospitals, Arch Intern Med. 146(March):520-524.
Kerr, K.G, Dealer, S.F., and Lacey, R.W. 1988, Materno-Fetal Listeriosis from Cook-Chill and Refrigerated Food, The Lancet, November 12, 1988, 1133.
Lopez Osornio, M.M. and Chaves, A.R. 1997. Enhancement of Shelf Life of Grated Beetroots. Journal of Food Protection 60(10):1230-1234.
Magnuson, J.A., King, Jr., A.D., and Torok, T. 1990. Microflora of Partially Processed Lettuce. Applied and Environmental Microbiology (Dec.):3851-3854.
Marranzano, M., Pitrolo, S., Vicari, O., and Fallico, R. 1996. Presenza di Listeria spp. in ortaggi. 1st Di Igiene e Medicina preventiva, Universita di Catania.
Monge, R. and Arias M.L. 1996. Presencia de microorganismos patengenos en hortalizas de consumo crudo en Costa Rica. Archivos LatinoAmericanos de Nutrition 46(4):292-294.
Petran, R. L., Zottola, E. A., and Garvani, R. B. 1988. Incidence of Listeria monocytogenes in Market Samples of Fresh and Frozen Vegetables. Journal of Food Science. 1988.
Ryser, E.T. and Marth, E.H. 1991. Listeria, Listeriosis, and Food Safety, Second Edition, Revised and Expanded
Sizmur, K. and Walker, C.W. 1988. Listeria in Prepacked Salads. The Lancet (May 21):1167.
Steinbruegge, E. G., Maxcy, R. B., and Liewen, M. B. 1988. Fate of Listeria monocytogenes on Ready to Serve Lettuce. Journal of Food Protection (August).
Tang, M.Y., Cheong, Y.M., and Zainuldin, T. 1994. Incidence of Listeria spp. In Vegetables in Kuala Lumpur. Med. J. Malaysia 49(3):217-222.
Tiwari, N.P. and Aldenrath, S.G. 1989. Isolation of Listeria monocytogenes from Food Products on Four Selective Plating Media. Journal of Food Protection 53(5):382-385.
Velani, S. and Roberts D. Listeria monocytogenes and other Listeria spp. in prepacked mixed salads and individual salad ingredients. PHLS Microbiology Digest 8(1):21-22.
Background
Epidemiological investigations of outbreaks and sporadic cases of listeriosis have clearly demonstrated that the consumption of contaminated food is responsible for a high proportion of human listeriosis cases (Rocourt, 1997; Tappero, 1995). Since the mid 80s, progress in microbiological detection and epidemiological investigations with increased use of case-control studies have demonstrated that all kinds of foods, at each step of the food chain, can transmit the disease (Rocourt, 1995). However, the importance of ingestion of specific contaminated foods in sporadic disease, which account for the majority of listeriosis cases, is unclear (Pinner, 1992; Schuchat, 1992). Because of the widespread nature of the organism, it has been nearly impossible to eliminate it from the food supply (Farber, 1991b; Shelef, 1989). The ability of L. monocytogenes to grow at refrigeration temperatures, coupled with appearance of the pathogen in raw and processed meats, as well as poultry, vegetables, fruit, dairy, and seafood products, makes this bacterium a serious threat to susceptible consumers and to the entire food industry (Ryser, 1989; Farber, 1991b; Schlech, 1991). In addition, a number of the foods associated with transmission of listeriosis have been highly processed, have extended shelf lives at refrigerated temperatures, are capable of supporting the growth of L. monocytogenes, and are consumed without further cooking (i.e., ready-to-eat) (McLauchlin, 1996). L. monocytogenes is also more heat resistant than most vegetative microbes (Farber, 1988), can be isolated in foods that have been adequately frozen (Tappero, 1995), and occurs in the home through cross-contamination with other foods (Schuchat, 1991).
The purpose of the food consumption module is to model the consumption of foods that have a high potential for L. monocytogenes contamination. These foods represent a subset of all foods that comprise an individual’s total diet. We will not include foods that have not been linked to L. monocytogenes contamination, such as grain products (e.g., bread, cookies, cakes), soft drinks, selected fruits (e.g., apples, bananas, avocados, lemons), cooked mixed dishes (e.g., lasagna, soups), and cooked vegetables. Once the levels of contamination of L.monocytogenes are identified for various foods in the Contamination Module, we will finalize food categories and provide the distributions of food consumption for those categories. With the food contamination data, we will then develop exposure estimates for not only the aggregate US population but also for different subpopulations that are particularly susceptible to listeriosis.
Selection Of Food Products For Risk Assessment
The first step in determining estimates of food consumption was to select appropriate food products to include in the risk assessment. In order to delineate foods that have a high potential for L. monocytogenes, we completed a comprehensive review of the literature. We concentrated on five subject areas that address the epidemiological and microbiological aspects of L. monocytogenes. Those subject areas with associated citations include:
1.OUTBREAKS (Ryser, 1999; Farber, 1991a; Schuchat, 1991; CDC, 1998, 1999; Ho, 1986; Heisick, 1989; Riedo, 1994; Schlech, 1996; Simpson, 1996; Dalton, 1997; Fleming, 1985; Linnan, 1988; Schwartz, 1989);
2.SPORADIC CASES (Ryser, 1999; Farber, 1991a; Tappero, 1995; Pinner 1992; Schuchat, 1991, 1992; Mascola, 1988, 1989; Schwartz, 1988; CDC, 1992);
3.RECALLS by the United States (US) Food and Drug Administration (FDA), US Department of Agriculture/Food Safety and Inspection Service (USDA/FSIS) and the Canadian government (Ryser, 1999; Farber, 1991a);
4.SELECTED LITERATURE related to prevalence and incidence of L. monocytogenes through analytical testing in North America (the United States and Canada) (Ryser, 1999; Farber, 1989, 1991a, 1998a, 1998b; Shelef, 1989; Johnson, 1988; Heinitz, 1998; Weagant, 1988; Miles, 1991; Dillon, 1992; Dillon, 1994; Boerlin, 1997; Petran, 1988; Berrang, 1989; Heisick, 1989; Steinbruegge, 1988; Lin, 1996; Beuchat, 1990, 1991, 1997, 1998; Odumeru, 1997; Pearson, 1990; Sado, 1998; Datta, 1988; Piyasena, 1998; Genigeorgis, 1991; Glass, 1998); and
5.SELECTED LITERATURE (outbreak, sporadic cases, and prevalence and incidence studies of L. monocytogenes) in other countries around the world:
All references used in the food consumption module and cited in the text will be included in the reference list, sorted by subject matter. Those general subjects are divided into background, listeriosis, and food groups (produce, dairy, seafood, and meat and poultry).
Data Sources: U. S. Food Consumption Data Bases
The US government conducts two large-scale, nationwide food consumption surveys of the US population. The Continuing Survey of Food Intakes by Individuals (CSFII 1994-96) is the latest survey conducted by the Agricultural Research Service of the USDA. The survey consists of:
The second nationwide survey of food consumption is the National Health and Nutrition Examination Survey (NHANES III) (1988-94), conducted by the National Center for Health Statistics in the Center for Disease Control (CDC) of the Department of Health and Human Services. The survey consists of:
In order to provide estimates of exposure to L. monocytogenes via distributions of food consumption, we initially plan to use data from both the CSFII 94-96 and NHANES III data bases. We will first determine the amount of each food that is eaten (in grams) at an eating occasion, though we will most likely base the final distributions on the amount of the food eaten per person per day.
Limitations of the Food Consumption Data Bases
Selected Foods
Each of the food consumption data bases contains a food code to identify each food. We have reviewed over 7,200 food codes and have grouped the foods implicated with contamination of L. monocytogenes (outbreaks, sporadic cases, recalls, analytical testing) into food categories. The initial food groupings are listed in Table 1 of the Food Contamination Module, but may be modified based upon levels of L. monocytogenes identified in that module.
Reduction Of Uncertainty
A major source of uncertainty in the Food Consumption Module lies with the precision in determining a reasonable proportion of the food group that will more closely model the consumption of the specific foods within the group that is at higher risk (e.g., raw milk within all fluid milk). For several foods or food categories, we plan to consider a correction factor that will provide a more appropriate distribution of higher risk foods consumed. We hope, in turn, that such factors will help to reduce the uncertainty inherent in data estimation. Initial issues include:Results indicate that, 1.4% of the respondents reported that they had drunk raw milk during the past 12 months. Although federal law requires milk in interstate commerce to be pasteurized, some states allow milk consumed within the state to be sold and drunk as raw. Several studies have shown that L. monocytogenes is frequently present in raw milk, but it is inactivated by standard pasteurization (Bradshaw, 1985).
In order to estimate the distribution of fluid milk that is consumed, we plan to assume that 1.4% of the amount consumed is unpasteurized milk and use those data to estimate the consumption of fluid milk that is most at risk for L. monocytogenes.
In addition, we will consider at a later date that L. monocytogenes can be cultured from approximately 5% of raw (unpasteurized) milk samples (CDC, 1988) and possibly include that correction factor.
Example:
1410101
Type=2 (semisoft)
Category=3 (pasteurization optional but frequently used)
Pasteurization required?=2 (no)
Surveillance and epidemiology of L. monocytogenes =1 and 2 (recall and outbreak)
Risk designation=3 (highest)
4. Juice: The FDA economic analysis used for the juice HACCP regulation estimated the proportion of unpasteurized apple and orange juices consumed to be 1.7%. Because there were no data available to estimate the amount of unpasteurized vegetable juice consumed, they again used 1.7%. In order to estimate the distribution of unpasteurized juices that are consumed, we plan to assume that 1.7% of the fruit and vegetable juices consumed are unpasteurized and use those data to estimate the consumption of juice that is most at risk for L. monocytogenes. Also, it is not apparent that L monocytogenes will survive in citrus juices, although one study shows that acid-adapted cells showed greatly improved survival in low-pH foods (orange juice and salad dressing) (Gahan, 1996).
ReferencesA. Background, Review Articles, Foods Linked To Listeriosis, Recalls
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Code of Federal Regulations, Section 21 CFR, Part 133
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Goulet, V., C. Jacquet, V. Vaillant, I. Rebiere, E. Mouret, C. Lorente, E. Maillot, F. Stainer, and J. Rocourt. 1995. Listeriosis from consumption of raw-milk cheeses. Lancet. 345(8964):1581-1582.
Greenwood, M.H., D. Roberts, and P. Burden. 1991. The occurrence of Listeria species in milk and dairy products: a national survey in England and Wales. 12(2-3):197-206.
Herbst, S.T. The New Food Lovers Companion: comprehensive definitions of over 4000 food, wine, and culinary terms. 1995. New York: Barron’s Educational Series, Inc
Jensen, A., W. Frederiksen, and P. Gerner-Smidt. 1994. Risk factors for listeriosis in Denmark, 1989-1990. Scand J Infect Dis. 26 (2):171-178.
Johnson, E.A., J.H. Nelson, and M. Johnson. 1990a. Microbiological safety of cheese made from heat-treated milk, Part 1. Executive summary, introduction and history. J Food Prot. 53(5):441-452.
Johnson, E.A., J.H. Nelson, and M. Johnson. 1990b. Microbiological safety of cheese made from heat-treated milk, Part ll. Microbiology. J Food Prot. 53(6):519-540.
Johnson, E.A., J.H. Nelson, and M. Johnson. 1990c. Microbiological safety of cheese made from heat-treated milk, Part lll. Technology, discussion, recommendations, bibliography. J Food Prot. 53(7):610-623.
Linnan, M.J., L. Mascola, X.D. Lou, V. Goulet, S. May, C. Salminen, D. W. Hird, M.L. Yonekura, P. Hayes, R. Weaver, et.al. 1988. Epidemic listeriosis associated with Mexican-style cheese. N Engl J Med. 319(13):823-828.
Listeriosis. The situation 2 years after the outbreak caused by "Vacherin Mont-d’Or" soft cheese. 1991. Wkly Epidemiol Rec. 66 (5)28-29.
Loncarevic, S., M.L. Danielsson-Tham, and W. Tham. 1995. Occurrence of Listeria monocytogenes in soft and semi-soft cheeses in retail outlets in Sweden. Int J Food Microbiol. 26(2)245-250.
Loncarevic, S., M.L. Danielsson-Tham, P. Gerner-Smidt, L. Sahlstrom, and W. Tham. 1998. Potential sources of human listeriosis in Sweden. Food Micro. 15(1):65-69.
Mascola, L., F. Sorvillo, J. Neal, K. Iwakoshi, and R. Weaver. 1989. Surveillance of listeriosis in Los Angeles County, 1985-1986. A first year’s report. Arch Intern Med. 149(7):1569-1572.
McLauchlin, J., M.H. Greenwood, and P.N. Pini,. 1990. The occurrence of Listeria monocytogenes in cheese from a manufacturer associated with a case of listeriosis. Int J Food Microbiol. 10(3-4):255-262.
Pearson, L.J., and E.H. Marth. 1990. Listeria monocytogenes--threat to a safe food supply: a review. J Dairy Sci. 73(4):912-928.
Pinto, B., and D. Reali. 1996. Prevalence of Listeria monocytogenes and other listerias in Italian-made soft cheeses. Zentralbl Hyg Umweltmed. 199(1):60-68.
Piyasena, P., S. Liou, and R. C. McKellar. 1998. Predictive modelling of inactivation of Listeria spp. in bovine milk during high-temperature short-time pasteurization. Int J Food Microbiol. 39(3):167-173.
Swardson, A. April 22, 1999. In a ferment over cheese bacteria scare making French review production methods. pp. A18-19. The Washington Post, Washington, DC.
D. SeafoodBen Embarek, P.K. 1994. Presence, detection and growth of Listeria monocytogenes in seafoods: a review. Int J of Food Microbiology 23:17-34.
Boerlin, P., F. Boerlin-Petzold, E. Bannerman, J. Bille, and T. Jemmi. 1997. Typing Listeria monocytogenes isolates from fish products and human listeriosis cases. Appl Environ Microbiol 63(4):1338-1343.
Brett, M.S., P. Short, and J. McLauchlin. 1998. A small outbreak of listeriosis associated with smoked mussels. Int J Food Microbiol 43(3):223-229.
Cortesi, M.L., T. Sarli, A. Santoro, N. Murru, and T. Pepe. 1997. Distribution and behavior of Listeria monocytogenes in three lots of naturally-contaminated vacuum-packed smoked salmon stored at 2 and 10 degrees C. Int J Food Microbiol. 37(2-3):209-214.
Dillon, R., M. Ronda, R. Thankor, and R. Patel. 1992. Listeria in seafoods: A Review. J Food Protection 55(12):1009-1015.
Dillon, R., T. Patel, and S. Ratnam. 1994. Occurrence of Listeria in hot and cold smoked seafood products. Int J Food Microbiol 22(1):73-77.
Ericsson, H., A. Eklow, M.L. Danielsson-Tham, S. Loncarevic, L.O. Mentzing, I. Persson, H. Unnerstad, and W. Tham. 1997. An outbreak of listeriosis suspected to have been caused by rainbow trout. J Clin Microbiol 35(11):2904-2907.
Hartemink, R., and F. Georgsson. 1991. Incidence of Listeria species in seafood and seafood salads. Int J Food Microbiol 12(2-3):189-195.
Heinitz, M.L., and J.M. Johnson. 1998. The incidence of Listeria spp., Salmonella spp., and Clostridium botulinum in smoked fish and shellfish. J Food Prot 61(3):318-323.
Jeyasekaran, G., I. Karunasagar, and I. Karunasagar. 1996. Incidence of Listeria spp. in tropical fish. Int J Food Microbiol 31(1-3):333-340.
Jemmi, T., and A. Keusch. 1992. Behavior of Listeria monocytogenes during processing and storage of experimentally contaminated hot-smoked trout. Int J Food Microbiol 15(3-4):339-346.
Jorgensen, L.V., and H.H.Huss. 1998. Prevalence and growth of Listeria monocytogenes in naturally contaminated seafood. Int J Food Microbiol 42(1-2):127-131.
Lennon, D., B. Lewis, C. Mantell, D. Becroft, B. Dove, K. Farmer, S. Tonkin, N. Yates, R. Stamp, and K. Mickleson. 1984. Epidemic perinatal listeriosis. Pediatr Infect Dis 3(1):30-34.
Loncarevic, S., W. Tham, and M.L. Danielsson-Tham. 1996. Prevalence of Listeria monocytogenes and other Listeria spp. in smoked and ‘gravad’ fish. Acta Vet Scand 37(1):13-18.
Miles, L., and J.R. Motes. 1991. Incidence of Listeria spp. in shrimp, oysters, and estuarine waters. J Food Protection 54(3):170-173.
Rorvik, L.M., D.A. Caugant, and M. Yndestad. 1995. Contamination pattern of Listeria monocytogenes and other Listeria spp. in a salmon slaughterhouse and smoked salmon processing plant. Int J Food Microbiol 25(1):19-27.
Rorvik, L.M., E. Skjerve, B.R. Knudsen, and M. Yndestad. 1997. Risk factors for contamination of smoked salmon with Listeria monocytogenes during processing. Int J Food Microbiol 37(2-3):215-219.
Weagant, S. D., P.N. Sado, K.G. Colburn, J.D. Torkelson, F.A. Stanley, M.H. Krane, S.C. Shields, and C.F. Thayer. 1988. The Incidence of Listeria species in frozen seafood products. J Food Protection 51(8):655-657.
E. Meat And PoultryCenters for Disease Control and Prevention. 1998. Multistate outbreak of listeriosis – United States, 1998. MMWR. 47(50):1085-1086.
Centers for Disease Control and Prevention. 1999. Update: Multistate outbreak of listeriosis – United States, 1998-1999. MMWR. 47(51):1117-1118
Farber, J.M., J.Y. D’Aoust, M. Diotte, A. Sewell, and E. Daley. 1998b. Survival of Listeria spp. on raw whole chickens cooked in microwave ovens. J Food Prot 61(11):1465-1469.
Fenlon, D.R., J. Wilson, and W. Donachie. 1996. The incidence and level of Listeria monocytogenes contamination of food sources at primary production and initial processing. J Appl Bacteriol 81(6):641-650.
Gilbert, R.J., J. McLauchlin, and S.K. Velani. 1993. The contamination of pate by Listeria monocytogenes in England and Wales in 1989 and 1990. Epidemiol Infect 110(3):543-551.
Goulet, V., J. Rocourt, I. Rebiere, C. Jacquet, C. Moyse, P. Dehaumont, G. Salvat, and P. Veit. 1998. Listeriosis outbreak associated with the consumption of rillettes in France in 1993. J Infect Dis 177(1):155-160.
Houang, E., and R. Hurley. 1991. Isolation of Listeria species from precooked chilled foods. J Hosp Infect 19(4):231-238.
Jacquet, C., B. Catimel, R. Brosch, C. Buchrieser, P. Dehaumont, V. Goulet, A. Lepoutre, P. Veit, and J. Rocourt. 1995. Investigations related to the epidemic strain involved in the French listeriosis outbreak in 1992. Appl Environ Microbiol 61(6):2242-2246.
Johnson, J.L., M.P. Doyle, and R.G. Cassens. 1988. Survival of Listeria monocytogenes in ground beef. Int J Food Microbiol 6(3):243-247.
McLauchlin J., S.M. Hall, S.K. Velani, and R.J. Gilbert. 1991. Human listeriosis and pate: a possible association. BMJ 303(6805):773-775.
Morris, I.J., and C.D. Ribeiro. 1991. The occurrence of Listeria species in pate: the Cardiff experience 1989. Epidemiol Infect 107(1):111-117.
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Salvat, G., M.T. Toquin, Y. Michel, and P. Colin. 1995. Control of Listeria monocytogenes in the delicatessen industries: the lessons of a listeriosis outbreak in France. Int J Food Microbiol 25(1):75-81.
Schwartz, B., C.A. Ciesielski, C.V. Broome, S. Gaventa, G.R. Brown, B.G. Gellin, A.W. Hightower, and L. Mascola. 1988. Association of sporadic listeriosis with consumption of uncooked hot dogs and undercooked chicken. Lancet 2(8614):779-782.
Trussel, M. 1989. The occurrence of Listeria in the production of processed meat, salami, and mettwurst. Schweiz Arch Tierheilkd 131(7):409-412, 417-421.
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Introduction
Dose-response is the term used to relate the number of ingested organisms to the outcome of the ingestion event (illness, death, etc.) for a given population. Although microbiological dose-response models are in the nascent stages of development, data collected from epidemiological investigations, clinical trials, and animal studies still provide useful insights.
There are no known human clinical trials with Listeria monocytogenes. therefore, epidemiologic investigations provide the only opportunity to directly collect information on the susceptible human populations. The more complete investigations provide information on the pathogen levels in implicated foods and the number and immune status of ill and exposed-asymptomatic persons. Because L. monocytogenes is an intercellular pathogen that is mechanistically similar to other human disease, a large number of animal studies have been conducted for many years. This risk assessment will attempt to utilize the data from these animal studies, as described below, to provide information useful for dose-response modeling.
This Public Health Module will focus primarily on three parameters (or data inputs) to model L. monocytogenes dose-response. The parameters are consistent with the disease triangle that considers the environment (in this case the food matrix), the pathogen (virulence characteristics or factors), and the host (susceptibility or immune status factors). Data to feed into the parameters come from humans (outbreaks, case reports, case-controlled studies), animals (mice, rats, primates, and other species), and in vitro studies.
Listeriosis
L. monocytogenes is a microbial pathogen which has been found in low concentrations world-wide, in soil, water, vegetation, slaughterhouse waste, animal feed, and the gastrointestinal tract of over 50 different animals, including man. However, the ability of the organism to survive and grow in adverse environments and the severity of the illness it causes makes L. monocytogenes a dangerous foodborne pathogen. Thirteen serotypes of L. monocytogenes have been identified, and most human cases of listeriosis are caused by serotypes 1/2a, 1/2b, and 4b. (Ryser and Marth, 1998; Gray and Killinger, 1966; Schuchat et al., 1991)
Pathology
Recent studies have shown that L. monocytogenes is carried in the gut of about 5% of the general population and that the large intestine is the principle reservoir for the organism in humans. L. monocytogenes causes illness by penetrating the lining of the gastrointestinal tract. Once it has invaded the tissue, the organism can protect itself against phagocytosis, grow, and migrate throughout the host. A spectrum of illness severity is observed resulting from exposure to Listeria, ranging from asymptomatic carriers through non-invasive gastrointestinal disease to systemic or invasive conditions. A partial list of systemic illness and disease caused by L. monocytogenes includes bacteremia, bacterial meningitis, conjunctivitis, CNS infection, cutaneous infection, encephalitis, endocarditis, meningoencephalitis, miscarriage, neonatal disease, osteomyelitis, peritonitis, pleural infection, pneumonia, premature birth, prodromal illness in pregnant women, septicemia, and stillbirth. Milder symptoms associated with listeriosis, i.e., diarrhea, fever, headache, and myalgia, are often the result of high doses of L. monocytogenes in otherwise healthy individuals. The mortality rate of the severe form of listeriosis is about 20% of those hospitalized. (Slutsker and Schuchat, 1999; Schuchat et al., 1991; Farber and Peterkin, 1991; Ryser and Marth, 1998)
Epidemiology
Most cases of listeriosis occur sporadically. Mild cases may go unnoticed or unreported and in these cases the cause of the illness is usually not determined. However, there have been some sporadic cases and several large outbreaks where the vehicle of infection was determined or suspected to be food. (Schuchat et al., 1991; Ryser and Marth, 1998; Linnan et al., 1988)
Not everyone exposed to foodborne L. monocytogenes develops listeriosis. Persons who become ill must be susceptible and receive a sufficient dose of the virulent organism. Most human cases of listeriosis occur in persons that have suppressed T-cell-mediated immunity. Those most at risk of infection are pregnant women, neonates, the elderly, and the immunocompromised. The immunocompromised include persons taking immunosuppressive medications, and persons with chronic illness like cancer, diabetes and alcoholism. Healthy adults have a relative low risk of illness from L. monocytogenes. Listeriosis in children, adolescents, and young adults is rare but does occur superimposed upon other disorders. In older patients, listeriosis is usually superimposed on neoplastic disease, diabetes, or other severe illness. It's been suggested that susceptibility is enhanced if the host is simultaneously being infected by another bacteria or virus. (Schwatrz et al., 1989; Gray and Killinger, 1966; Schuchat et al., 1991; Linnan et al., 1988; Salamina et al., 1996; Gellin and Broome, 1989; Farber and Peterkin, 1991)
Parameters for Dose-Response Characterization
Illness
Frequency of listeriosis cases and outbreaks provides an estimate of the magnitude of response to Listeria exposure.
Severity data provides information on the relative number of individuals with different disease states like fever, gastrointestinal distress, meningitis, and death (including fetal).
Virulence
Human studies provide data on characteristics of disease-associated strains such as virulence factors, serotypes, phagetypes, 16S ribosomal DNA patterns, etc.
Animal studies provide data on the role virulence determinants play in in vivo pathogenesis. Most of the mechanistic data is derived from the L. monocytogenes mouse model
In vitro studies provide mechanistic data on host cell invasion, survival in host cells, and cell-to-cell spread.
Food Vehicle
This parameter assumes variability in the relationship between the physical/ chemical nature of a Listeria-contaminated food and the fate of the organism following ingestion. This variance would influence the number of organisms required to produce illness. This parameter includes data on the number of Listeria in particular food types associated with disease outbreaks and data on protective or enhancing effects, relative to infection, associated with particular food chemical and physical characteristics.
Human studies provide data on numbers of Listeria isolated from outbreak-associated foods.
In vitro studies
Susceptibility
This parameter assumes that human subpopulations exhibit varying degrees of susceptibility to listeriosis based on certain intrinsic biological characteristics. The variability in susceptibility would influence the number of organisms required to produce illness and the type of illness produced. Information on this parameter includes epidemiologic and case reports of conditions which predispose to infection, and studies with animal surrogates on the role of host defense components in susceptibility to Listeria infection.
Human studies include information on prevalence and severity of listeriosis in cancer patients, AIDS patients, the elderly and other immunosuppressed populations.
Animal studies include information on morbidity and mortality (including surrogate endpoints), mouse strains with specific immune dysfunctions (knockouts) and pathogenic mechanisms.
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