Pasteurized Milk as a Vehicle of Infection in an Outbreak of Listeriosis
David W. Fleming, M.D., Stephen L. Cochi, M.D., Kristine L. MacDonald, M.D., Jack Brondum, D.V.M., M.S., Peggy S. Hayes, B.S., Brian D. Plikaytis, M.S., Marion B. Holmes, B.S., A. Audurier, Ph.D., Claire V. Broome, M.D., and Arthur L. Reingold, M.D.
Background and Methods Between June 30th and August 30th, 1983,49 patients in Massachusetts acquired listeriosis. Seven casesoccurred in fetuses or infants and 42 in immunosuppressed adults;14 patients (29 per cent) died. Of 40 Listeria monocytogenesisolates available for testing, 32 were serotype 4b. Two case–controlstudies, one matching for neighborhood of residence and theother for underlying disease, revealed that the illness wasstrongly associated with drinking a specific brand of pasteurizedwhole or 2 per cent milk (odds ratio = 9, P<0.01 for theneighborhood-matched study; odds ratio = 11.5, P<0.001 forthe illness-matched study).
Results The association with milk was further substantiatedby four additional analyses that suggested the presence of adose–response effect, demonstrated a protective effectof skim milk, associated cases with the same product in an independentstudy in another state, and linked a specific phage type withthe disease associated with milk. The milk associated with diseasecame from a group of farms on which listeriosis in dairy cowswas known to have occurred at the time of the outbreak. Multipleserotypes of L. monocytogenes were isolated from raw milk obtainedfrom these farms after the outbreak. At the plant where themilk was processed, inspections revealed no evidence of improperpasteurization.
Conclusions These results support the hypothesis that humanlisteriosis can be a foodborne disease and raise questions aboutthe ability of pasteurization to eradicate a large inoculumof L. monocytogenes from contaminated raw milk.
Source Information
From the Respiratory and Special Pathogens Epidemiology Branch, the Enteric Diseases Branch, the Respiratory and Special Pathogens Laboratory Branch, and the Statistical Services Branch, Division of Bacterial Diseases, Center for Infectious Diseases, Centers for Disease Control, Atlanta; the Division of Epidemiology, Vermont Department of Health, Burlington; the State Laboratory Institute, Massachusetts Department of Public Health, Boston; and the Laboratoire de Microbiology, Faculte de Medicine, 37032 Tours, France. Address reprint requests to Dr. Fleming at the Respiratory and Special Pathogens Epidemiology Branch, Bldg. 1, Rm. 5405, Centers for Disease Control, Atlanta, GA 30333.
Roberts, A. J., Williams, S. K., Wiedmann, M., Nightingale, K. K.
(2009). Some Listeria monocytogenes Outbreak Strains Demonstrate Significantly Reduced Invasion, inlA Transcript Levels, and Swarming Motility In Vitro. Appl. Environ. Microbiol.
75: 5647-5658
[Abstract][Full Text]
Wen, J., Anantheswaran, R. C., Knabel, S. J.
(2009). Changes in Barotolerance, Thermotolerance, and Cellular Morphology throughout the Life Cycle of Listeria monocytogenes. Appl. Environ. Microbiol.
75: 1581-1588
[Abstract][Full Text]
Latorre, A. A., Van Kessel, J. A. S., Karns, J. S., Zurakowski, M. J., Pradhan, A. K., Zadoks, R. N., Boor, K. J., Schukken, Y. H.
(2009). Molecular Ecology of Listeria monocytogenes: Evidence for a Reservoir in Milking Equipment on a Dairy Farm. Appl. Environ. Microbiol.
75: 1315-1323
[Abstract][Full Text]
(2009). Outbreak of Listeria monocytogenes Infections Associated With Pasteurized Milk From a Local Dairy--Massachusetts, 2007. JAMA
301: 820-822
[Full Text]
Guenther, S., Huwyler, D., Richard, S., Loessner, M. J.
(2009). Virulent Bacteriophage for Efficient Biocontrol of Listeria monocytogenes in Ready-To-Eat Foods. Appl. Environ. Microbiol.
75: 93-100
[Abstract][Full Text]
Jordan, S. J., Perni, S., Glenn, S., Fernandes, I., Barbosa, M., Sol, M., Tenreiro, R. P., Chambel, L., Barata, B., Zilhao, I., Aldsworth, T. G., Adriao, A., Faleiro, M. L., Shama, G., Andrew, P. W.
(2008). Listeria monocytogenes Biofilm-Associated Protein (BapL) May Contribute to Surface Attachment of L. monocytogenes but Is Absent from Many Field Isolates. Appl. Environ. Microbiol.
74: 5451-5456
[Abstract][Full Text]
Sperry, K. E. V., Kathariou, S., Edwards, J. S., Wolf, L. A.
(2008). Multiple-Locus Variable-Number Tandem-Repeat Analysis as a Tool for Subtyping Listeria monocytogenes Strains. J. Clin. Microbiol.
46: 1435-1450
[Abstract][Full Text]
Lee, H.-Y., Park, J.-H., Seok, S.-H., Baek, M.-W., Kim, D.-J., Lee, B.-H., Kang, P.-D., Kim, Y.-S., Park, J.-H.
(2005). Potential antimicrobial effects of human lactoferrin against oral infection with Listeria monocytogenes in mice. J Med Microbiol
54: 1049-1054
[Abstract][Full Text]
Kabuki, D. Y., Kuaye, A. Y., Wiedmann, M., Boor, K. J.
(2004). Molecular Subtyping and Tracking of Listeria monocytogenes in Latin-Style Fresh-Cheese Processing Plants. J DAIRY SCI
87: 2803-2812
[Abstract][Full Text]
Drevets, D. A., Leenen, P. J. M., Greenfield, R. A.
(2004). Invasion of the Central Nervous System by Intracellular Bacteria. Clin. Microbiol. Rev.
17: 323-347
[Abstract][Full Text]
Chastanet, A., Derre, I., Nair, S., Msadek, T.
(2004). clpB, a Novel Member of the Listeria monocytogenes CtsR Regulon, Is Involved in Virulence but Not in General Stress Tolerance. J. Bacteriol.
186: 1165-1174
[Abstract][Full Text]
Stabel, J. R.
(2003). Effective Methods for Postharvest Intervention in Dairy Processing. J DAIRY SCI
86: E10-15
[Abstract][Full Text]
Lukinmaa, S., Miettinen, M., Nakari, U.-M., Korkeala, H., Siitonen, A.
(2003). Listeria monocytogenes Isolates from Invasive Infections: Variation of Sero- and Genotypes during an 11-Year Period in Finland. J. Clin. Microbiol.
41: 1694-1700
[Abstract][Full Text]
Salcedo, C., Arreaza, L., Alcala, B., de la Fuente, L., Vazquez, J. A.
(2003). Development of a Multilocus Sequence Typing Method for Analysis of Listeria monocytogenes Clones. J. Clin. Microbiol.
41: 757-762
[Abstract][Full Text]
Mizuki, M., Nakane, A., Sekikawa, K., Tagawa, Y.-i., Iwakura, Y.
(2002). Comparison of Host Resistance to Primary and Secondary Listeria monocytogenes Infections in Mice by Intranasal and Intravenous Routes. Infect. Immun.
70: 4805-4811
[Abstract][Full Text]
Lauer, P., Chow, M. Y. N., Loessner, M. J., Portnoy, D. A., Calendar, R.
(2002). Construction, Characterization, and Use of Two Listeria monocytogenes Site-Specific Phage Integration Vectors. J. Bacteriol.
184: 4177-4186
[Abstract][Full Text]
De Cesare, A., Bruce, J. L., Dambaugh, T. R., Guerzoni, M. E., Wiedmann, M.
(2001). Automated Ribotyping Using Different Enzymes To Improve Discrimination of Listeria monocytogenes Isolates, with a Particular Focus on Serotype 4b Strains. J. Clin. Microbiol.
39: 3002-3005
[Abstract][Full Text]
Vazquez-Boland, J. A., Kuhn, M., Berche, P., Chakraborty, T., Dominguez-Bernal, G., Goebel, W., Gonzalez-Zorn, B., Wehland, J., Kreft, J.
(2001). Listeria Pathogenesis and Molecular Virulence Determinants. Clin. Microbiol. Rev.
14: 584-640
[Abstract][Full Text]
Manohar, M., Baumann, D. O., Bos, N. A., Cebra, J. J.
(2001). Gut Colonization of Mice with actA-Negative Mutant of Listeria monocytogenes Can Stimulate a Humoral Mucosal Immune Response. Infect. Immun.
69: 3542-3549
[Abstract][Full Text]
Jeffers, G. T., Bruce, J. L., McDonough, P. L., Scarlett, J., Boor, K. J., Wiedmann, M.
(2001). Comparative genetic characterization of Listeria monocytogenes isolates from human and animal listeriosis cases. Microbiology
147: 1095-1104
[Abstract][Full Text]
Barker, C., Park, S. F.
(2001). Sensitization of Listeria monocytogenes to Low pH, Organic Acids, and Osmotic Stress by Ethanol. Appl. Environ. Microbiol.
67: 1594-1600
[Abstract][Full Text]
Franciosa, G., Tartaro, S., Wedell-Neergaard, C., Aureli, P.
(2001). Characterization of Listeria monocytogenes Strains Involved in Invasive and Noninvasive Listeriosis Outbreaks by PCR-Based Fingerprinting Techniques. Appl. Environ. Microbiol.
67: 1793-1799
[Abstract][Full Text]
Norton, D. M., Scarlett, J. M., Horton, K., Sue, D., Thimothe, J., Boor, K. J., Wiedmann, M.
(2001). Characterization and Pathogenic Potential of Listeria monocytogenes Isolates from the Smoked Fish Industry. Appl. Environ. Microbiol.
67: 646-653
[Abstract][Full Text]
Clark, E. E., Wesley, I., Fiedler, F., Promadej, N., Kathariou, S.
(2000). Absence of Serotype-Specific Surface Antigen and Altered Teichoic Acid Glycosylation among Epidemic-Associated Strains of Listeria monocytogenes. J. Clin. Microbiol.
38: 3856-3859
[Abstract][Full Text]
Briandet, R., Meylheuc, T., Maher, C., Bellon-Fontaine, M. N.
(1999). Listeria monocytogenes Scott A: Cell Surface Charge, Hydrophobicity, and Electron Donor and Acceptor Characteristics under Different Environmental Growth Conditions. Appl. Environ. Microbiol.
65: 5328-5333
[Abstract][Full Text]
Miettinen, M. K., Siitonen, A., Heiskanen, P., Haajanen, H., Björkroth, K. J., Korkeala, H. J.
(1999). Molecular Epidemiology of an Outbreak of Febrile Gastroenteritis Caused by Listeria monocytogenes in Cold-Smoked Rainbow Trout. J. Clin. Microbiol.
37: 2358-2360
[Abstract][Full Text]
Schwarzer, N., Nost, R., Seybold, J., Parida, S. K., Fuhrmann, O., Krull, M., Schmidt, R., Newton, R., Hippenstiel, S., Domann, E., Chakraborty, T., Suttorp, N.
(1998). Two Distinct Phospholipases C of Listeria monocytogenes Induce Ceramide Generation, Nuclear Factor-{kappa}B Activation, and E-Selectin Expression in Human Endothelial Cells. J. Immunol.
161: 3010-3018
[Abstract][Full Text]
Rowan, N. J., Anderson, J. G.
(1998). Effects of Above-Optimum Growth Temperature and Cell Morphology on Thermotolerance of Listeria monocytogenes Cells Suspended in Bovine Milk. Appl. Environ. Microbiol.
64: 2065-2071
[Abstract][Full Text]
Rosman, N. P., Roberts, D. J.
(1997). Case 15-1997- Respiratory Distress and Seizure in a Neonate. NEJM
336: 1439-1446
[Full Text]
Dalton, C. B., Austin, C. C., Sobel, J., Hayes, P. S., Bibb, W. F., Graves, L. M., Swaminathan, B., Proctor, M. E., Griffin, P. M.
(1997). An Outbreak of Gastroenteritis and Fever Due to LIsteria monocytogenes in Milk. NEJM
336: 100-106
[Abstract][Full Text]
Schlech, W. F.
(1997). Listeria Gastroenteritis -- Old Syndrome, New Pathogen. NEJM
336: 130-132
[Full Text]
Tappero, J. W., Schuchat, A., Deaver, K. A., Mascola, L., Wenger, J. D., the Listeriosis Study Group, , Swaminathan, B., Hayes, P. S., Graves, L. M., Reeves, M. W., Weaver, R. E., Rothrock, G., Pattni, B., Krauss, K. M., Reingold, A. L., Ewert, D., Castillon, M., Stephens, D., Farley, M., Harvey, R. C., Baughman, W., Harrison, L. H., Billmann, L. H., Skala, M., Huber, M., Zenker, P., Quinlisk, P., Smithee, L. M. K., Lefkowitz, L. Jr, Rados, M. S.
(1995). Reduction in the Incidence of Human Listeriosis in the United States: Effectiveness of Prevention Efforts?. JAMA
273: 1118-1122
[Abstract]
Hirschl, R. B., Butler, M., Coburn, C. E., Bartlett, R. H., Baumgart, S.
(1994). Listeria monocytogenes and Severe Newborn Respiratory Failure Supported With Extracorporeal Membrane Oxygenation. Arch Pediatr Adolesc Med
148: 513-517
[Abstract]
Schuchat, A., Deaver, K. A., Wenger, J. D., Plikaytis, B. D., Mascola, L., Pinner, R. W., Reingold, A. L., Broome, C. V., Listeria Study Group, , Swaminathan, B., Hayes, P. S., Graves, L., Pierce, R., Przybyszewski, V., Ransom, R., Reeves, M., Weaver, R., Anderson, G., Stone, E., Krauss, K., Castillon, M., Harvey, C., Stull, T., Stephens, D., Farley, M., Archer, P., Strack, J., Istre, G., Rados, M., Taylor, J., Lefkowitz, L.
(1992). Role of Foods in Sporadic Listeriosis: I. Case-Control Study of Dietary Risk Factors. JAMA
267: 2041-2045
[Abstract]
Pinner, R. W., Schuchat, A., Swaminathan, B., Hayes, P. S., Deaver, K. A., Weaver, R. E., Plikaytis, B. D., Reeves, M., Broome, C. V., Wenger, J. D., Listeria Study Group, , Ajello, G., Przybyszewski, V., Malcolm, G., Ransom, R., Graves, L. M., Egal, M., Pierce, R., Anderson, G., Stone, E., Krauss, K., Reingold, A., Castillon, M., Mascola, L., Harvey, C., Stull, T., Stephens, D., Farley, M., Archer, P., Strack, J., Istre, G., Rados, M., Taylor, J., Lefkowitz, L.
(1992). Role of Foods in Sporadic Listeriosis: II. Microbilogic and Epidemiologic Investigation. JAMA
267: 2046-2050
[Abstract]
Schlech, W. F. III
(1992). Expanding the Horizons of Foodborne Listeriosis. JAMA
267: 2081-2082
[Abstract]
Moe, G.
(1991). Invited Review: Enteral Feeding and Infection in the Immunocompromised Patient. Nutr Clin Pract
6: 55-64
[Abstract]
Mascola, L., Sorvillo, F., Neal, J., Iwakoshi, K., Weaver, R.
(1989). Surveillance of Listeriosis in Los Angeles County, 1985-1986: A First Year's Report. Arch Intern Med
149: 1569-1572
[Abstract]
Chirgwin, K., Gleich, S.
(1989). Listeria monocytogenes Osteomyelitis. Arch Intern Med
149: 931-932
[Abstract]
Gellin, B. G., Broome, C. V.
(1989). Listeriosis. JAMA
261: 1313-1320
[Abstract]
(1989). Update -- Listeriosis and Pasteurized Milk. JAMA
261: 1119-1119
Ciesielski, C. A., Hightower, A. W., Parsons, S. K., Broome, C. V.
(1988). Listeriosis in the United States: 1980-1982. Arch Intern Med
148: 1416-1419
[Abstract]
Schlech, W. F. III
(1986). Listeriosis: New Pieces to an Old Puzzle. Arch Intern Med
146: 459-460
[Abstract]
Ho, J. L., Shands, K. N., Friedland, G., Eckind, P., Fraser, D. W.
(1986). An Outbreak of Type 4b Listeria monocytogenes Infection Involving Patients From Eight Boston Hospitals. Arch Intern Med
146: 520-524
[Abstract]
(1985). Leads from the MMWR. JAMA
254: 474-480
Barza, M.
(1985). Listeriosis and Milk. NEJM
312: 438-440
[Full Text]