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April 8, 1988, Vol 259, No. 14 >
ARTICLE | April 8, 1988

The Emergence of Grade A Eggs as a Major Source of Salmonella enteritidis Infections: Title and subTitle BreakNew Implications for the Control of Salmonellosis FREE

Michael E. St. Louis, MD; Dale L. Morse, MD; Morris E. Potter, DVM; Thomas M. DeMelfi; John J. Guzewich, MPH; Robert V. Tauxe, MD, MPH; Paul A. Blake, MD, MPH; Matthew L. Cartter, MD; Lyle Petersen, MD; Kathleen Gallagher, MPH; Joel R. Greenspan, MD; Kathleen F. Gensheimer, MD; David Dennis, MD; Eugene Schwartz, MD; William E. Parkin, DVM; Howard Rosenfeld, DVM; Stephen Schultz, MD; Stanley F. Kondracki, BS; Ernest J. Witte, VMD; Richard L. Vogt, MD; Nancy Puhr, MS; Larry Shipman, DVM; Nancy Hargrett-Bean, PhD
[+] Author Affiliations

Reprint requests to CID:DBD:EDB 1-5428, Centers for Disease Control, Atlanta, GA 30333 (Dr St. Louis).


JAMA. 1988;259(14):2103-2107. doi:10.1001/jama.1988.03720140023028
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References

From 1976 to 1986, reported Salmonella enteritidis infections increased more than sixfold in the northeastern United States. From January 1985 to May 1987, sixty-five foodborne outbreaks of S enteritidis were reported in the Northeast that were associated with 2119 cases and 11 deaths. Twenty-seven (77%) of the 35 outbreaks with identified food vehicles were caused by Grade A shell eggs or foods that contained such eggs. National data from 1973 to 1984 showed that S enteritidis outbreaks (44%) were more frequently associated with egg-containing foods than were outbreaks of other Salmonella serotypes (15%). Reflecting the geographic distribution of human illness, cultures of bulk raw eggs from pasteurization plants in the Northeast more frequently yielded S enteritidis (10%) than did eggs from other regions of the United States (0%). The epidemic rise in S enteritidis infections due to Grade A shell eggs is unlike past problems of salmonellosis associated with cracked or soiled eggs and raises the possibility of transovarian contamination of eggs with S enteritidis. New techniques may therefore be needed to control resurgent egg-associated salmonellosis in the United States.

(JAMA 1988;259:2103-2107)

REFERENCES

1 +
 Increasing rate of Salmonella enteritidis infections in the Northeastern United States. MMWR 1987;;36:10-11.
2 +
Feldman RA, Riley LW:  Epidemiology of Salmonella and Shigella infections in the United States , in Takeda Y, Miwatani T (eds): Bacterial Diarrheal Diseases . Tokyo, KTK Scientific Publishers, 1985;, pp 103-116.
3 +
Rowe B, Hall MLM, Ward LR, et al:  Epidemic spread of Salmonella hadar in England and Wales. Br Med J 1980;;280:1065-1066.
4 +
Taylor DN, Bled JM, Munro JS, et al:  Salmonella dublin infections in the United States, 1979-1980. J Infect Dis 1982;;146:323-327.
5 +
Edwards PR, Ewing WH: Identification of Enterobacteriaceae , ed 4. New York, Elsevier Science Publishing Co Inc, 1986;.
6 +
 Storage and preparation of samples: Salmonella detection , in Laboratory Methods for Egg Products . US Dept of Agriculture, 1984;, pp 1-2,1-10.
7 +
O'Brien TF, Hopkins JD, Gilleece ES, et al:  Molecular epidemiology of antibiotic resistance in Salmonella from animals and human beings in the United States. N Engl J Med 1982;;307:1-6.
8 +
Cohen ML, Blake PA:  Trends in foodborne salmonellosis outbreaks, 1963-1975. J Food Protect 1977;;40:798-800.
9 +
Centers for Disease Control: Proceedings of the National Conference on Salmonellosis , publication 1262. US Dept of Health, Education, and Welfare, 1965;.
10 +
Peel B:  Occurrence of salmonellas in raw and pasteurized liquid whole egg. Queensland J Agriculture Animal Sci 1977;;33:13-21.
11 +
Taylor J, McCoy JH:  Salmonella and Arizona infections , in Riemann H (ed): Foodborne Infections and Intoxications . Orlando, Fla, Academic Press Inc, 1969;, p 3.
12 +
Philbrook FR, MacCready RA, Van Roekel H, et al:  Salmonellosis spread by a dietary supplement of avian source. N Engl J Med 1960;;263:713-718.
13 +
Chapman PA, Rhodes P, Rylands W:  Salmonella typhimurium phage type 141 infections in Sheffield during 1984 and 1985. Communicable Dis Rep 1987;;15:3-4.
14 +
Sanders E, Sweeney FJ Jr, Friedman EA, et al:  An outbreak of hospital-associated infections due to Salmonella derby. JAMA 1963;;186:984-986.
15 +
Ager EA, Nelson KE, Galton MM, et al:  Two outbreaks of egg-borne salmonellosis and implications for their prevention. JAMA 1967;;199:372-378.
16 +
Thatcher FS, Montford J:  Egg-products as a source of salmonellae in processed foods. Can J Public Health 1962;;53:61-69.
17 +
Gunn RA, Markakis G:  Salmonellosis associated with homemade ice cream: An outbreak report and summary of outbreaks in the United States in 1966 to 1978. JAMA 1978;;240:1885-1886.
18 +
Taylor DN, Bopp C, Birkness K, et al:  An outbreak of salmonellosis associated with a fatality in a healthy child: A large dose and severe illness. Am J Epidemiol 1984;;119:907-912.
19 +
Blaser MJ, Rafuse EM, Wells JG, et al:  An outbreak of salmonellosis involving multiple vehicles. Am J Epidemiol 1981;;114:663-670.
20 +
Board RG:  The course of microbial infection of the hen's egg. J Appl Bacteriol 1966;;29:319-341.
21 +
Williams JE, Dillard LH, Hall GO:  The penetration patterns of Salmonella typhimurium through the outer structures of chicken eggs. Avian Dis 1968;;12:445-466.
22 +
Ayres JC, Kraft AA, Board RG, et al:  Sanitation practices in egg handling and breaking plants and the application of several disinfectants for sanitizing eggs. J Appl Bacteriol 1967;;30:106-116.
23 +
Vadehra DV, Baker RC, Naylor HB:  Salmonella infection of cracked eggs. Poultry Sci 1969;;48:954-957.
24 +
Morehouse LG, Wedman EE:  Salmonella and other disease-producing organisms in animal byproducts: A survey. J Am Vet Med Assoc 1961;;139:989-995.
25 +
Snoeyenbos CH:  Pullorum disease , in Hofsted MS, Calnek BW, Helmboldt CF, et al (eds): Diseases of Poultry , ed 7. Ames, Iowa State University Press, 1978;, pp 80-100.
26 +
 Eggs and Salmonella infections. Br Med J 1944;;2:760-761.
27 +
Snoeyenbos GH, Smyzer CF, Van Roekel H:  Salmonella infections of the ovary and peritoneum of chickens. Avian Dis 1969;;13:668-670.
28 +
Faddoul GP, Fellows GW:  A five-year survey of the incidence of Salmonellae in avian species. Avian Dis 1966;;10:296-304.
29 +
Baker RC, Hogarty S, Poon W, et al:  Survival of Salmonella typhimurium and Staphylococcus aureus in eggs cooked by different methods. Poultry Sci 1983;;62:1211-1216.
30 +
Dabbah R, Moats WA, Edwards VM:  Survivor curves of selected Salmonella enteritidis serotypes in liquid whole egg homogenates at 60°C. Poultry Sci 1971;;50:1772-1776.
31 +
National Poultry Improvement Plan and Auxiliary Provisions , publication APHIS 91-40. US Dept of Agriculture, 1985;.

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1 +
 Increasing rate of Salmonella enteritidis infections in the Northeastern United States. MMWR 1987;;36:10-11.
2 +
Feldman RA, Riley LW:  Epidemiology of Salmonella and Shigella infections in the United States , in Takeda Y, Miwatani T (eds): Bacterial Diarrheal Diseases . Tokyo, KTK Scientific Publishers, 1985;, pp 103-116.
3 +
Rowe B, Hall MLM, Ward LR, et al:  Epidemic spread of Salmonella hadar in England and Wales. Br Med J 1980;;280:1065-1066.
4 +
Taylor DN, Bled JM, Munro JS, et al:  Salmonella dublin infections in the United States, 1979-1980. J Infect Dis 1982;;146:323-327.
5 +
Edwards PR, Ewing WH: Identification of Enterobacteriaceae , ed 4. New York, Elsevier Science Publishing Co Inc, 1986;.
6 +
 Storage and preparation of samples: Salmonella detection , in Laboratory Methods for Egg Products . US Dept of Agriculture, 1984;, pp 1-2,1-10.
7 +
O'Brien TF, Hopkins JD, Gilleece ES, et al:  Molecular epidemiology of antibiotic resistance in Salmonella from animals and human beings in the United States. N Engl J Med 1982;;307:1-6.
8 +
Cohen ML, Blake PA:  Trends in foodborne salmonellosis outbreaks, 1963-1975. J Food Protect 1977;;40:798-800.
9 +
Centers for Disease Control: Proceedings of the National Conference on Salmonellosis , publication 1262. US Dept of Health, Education, and Welfare, 1965;.
10 +
Peel B:  Occurrence of salmonellas in raw and pasteurized liquid whole egg. Queensland J Agriculture Animal Sci 1977;;33:13-21.
11 +
Taylor J, McCoy JH:  Salmonella and Arizona infections , in Riemann H (ed): Foodborne Infections and Intoxications . Orlando, Fla, Academic Press Inc, 1969;, p 3.
12 +
Philbrook FR, MacCready RA, Van Roekel H, et al:  Salmonellosis spread by a dietary supplement of avian source. N Engl J Med 1960;;263:713-718.
13 +
Chapman PA, Rhodes P, Rylands W:  Salmonella typhimurium phage type 141 infections in Sheffield during 1984 and 1985. Communicable Dis Rep 1987;;15:3-4.
14 +
Sanders E, Sweeney FJ Jr, Friedman EA, et al:  An outbreak of hospital-associated infections due to Salmonella derby. JAMA 1963;;186:984-986.
15 +
Ager EA, Nelson KE, Galton MM, et al:  Two outbreaks of egg-borne salmonellosis and implications for their prevention. JAMA 1967;;199:372-378.
16 +
Thatcher FS, Montford J:  Egg-products as a source of salmonellae in processed foods. Can J Public Health 1962;;53:61-69.
17 +
Gunn RA, Markakis G:  Salmonellosis associated with homemade ice cream: An outbreak report and summary of outbreaks in the United States in 1966 to 1978. JAMA 1978;;240:1885-1886.
18 +
Taylor DN, Bopp C, Birkness K, et al:  An outbreak of salmonellosis associated with a fatality in a healthy child: A large dose and severe illness. Am J Epidemiol 1984;;119:907-912.
19 +
Blaser MJ, Rafuse EM, Wells JG, et al:  An outbreak of salmonellosis involving multiple vehicles. Am J Epidemiol 1981;;114:663-670.
20 +
Board RG:  The course of microbial infection of the hen's egg. J Appl Bacteriol 1966;;29:319-341.
21 +
Williams JE, Dillard LH, Hall GO:  The penetration patterns of Salmonella typhimurium through the outer structures of chicken eggs. Avian Dis 1968;;12:445-466.
22 +
Ayres JC, Kraft AA, Board RG, et al:  Sanitation practices in egg handling and breaking plants and the application of several disinfectants for sanitizing eggs. J Appl Bacteriol 1967;;30:106-116.
23 +
Vadehra DV, Baker RC, Naylor HB:  Salmonella infection of cracked eggs. Poultry Sci 1969;;48:954-957.
24 +
Morehouse LG, Wedman EE:  Salmonella and other disease-producing organisms in animal byproducts: A survey. J Am Vet Med Assoc 1961;;139:989-995.
25 +
Snoeyenbos CH:  Pullorum disease , in Hofsted MS, Calnek BW, Helmboldt CF, et al (eds): Diseases of Poultry , ed 7. Ames, Iowa State University Press, 1978;, pp 80-100.
26 +
 Eggs and Salmonella infections. Br Med J 1944;;2:760-761.
27 +
Snoeyenbos GH, Smyzer CF, Van Roekel H:  Salmonella infections of the ovary and peritoneum of chickens. Avian Dis 1969;;13:668-670.
28 +
Faddoul GP, Fellows GW:  A five-year survey of the incidence of Salmonellae in avian species. Avian Dis 1966;;10:296-304.
29 +
Baker RC, Hogarty S, Poon W, et al:  Survival of Salmonella typhimurium and Staphylococcus aureus in eggs cooked by different methods. Poultry Sci 1983;;62:1211-1216.
30 +
Dabbah R, Moats WA, Edwards VM:  Survivor curves of selected Salmonella enteritidis serotypes in liquid whole egg homogenates at 60°C. Poultry Sci 1971;;50:1772-1776.
31 +
National Poultry Improvement Plan and Auxiliary Provisions , publication APHIS 91-40. US Dept of Agriculture, 1985;.

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