Chapter 4 : Molecular Subtyping, Source Tracking, and Food Safety

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Molecular Subtyping, Source Tracking, and Food Safety, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555815769/9781555813741_Chap04-1.gif /docserver/preview/fulltext/10.1128/9781555815769/9781555813741_Chap04-2.gif


This chapter focuses on the application of molecular subtyping methods for identifying and tracing sources of microbial pathogens in food and food-borne human diseases. It should be noted, however, that in addition to the food-borne pathogens, harmless or nonpathogenic microorganisms can also contaminate the food supply and contribute to spoilage. These microbes are generally part of the natural microbiota of raw foods and food products, which serves as an ideal growth medium for many organisms with nearly neutral pH, high water activity, and richness in nutrients. If left unchecked, growth of these harmless microorganisms on foods results in off odors and flavors and, ultimately, in an inedible food product. Many of the methods developed to inhibit the growth of nonpathogenic microbes in foods also restrict the growth of food-borne pathogens. The major advantage of pulsed-field gel electrophoresis (PFGE) profiling is that the technique can be widely applied to different bacterial species and is relatively simple and straightforward to perform in the laboratory. Outbreak investigation and epidemiological tracing have been the primary incentives encouraging the development of the PulseNet and FoodNet national systems for food-borne disease surveillance. In the future, the authors expect to see the application of new molecular genotyping systems with rapid throughput, such as those based on single-nucleotide polymorphisms, to generate high-quality genotypic data for microbial source tracking.

Citation: Whittam T, Bergholz T. 2007. Molecular Subtyping, Source Tracking, and Food Safety, p 93-136. In Santo Domingo J, Sadowsky M, Doyle M (ed), Microbial Source Tracking. ASM Press, Washington, DC. doi: 10.1128/9781555815769.ch4

Key Concept Ranking

Restriction Fragment Length Polymorphism
Mobile Genetic Elements
Pulsed-Field Gel Electrophoresis
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of Figure 1
Figure 1

Reported cases of food-borne illness in 2004 for 10 FoodNet sites (California, Colorado, Connecticut, Georgia, Maryland, Minnesota, New Mexico, New York, Oregon, and Tennessee).

Citation: Whittam T, Bergholz T. 2007. Molecular Subtyping, Source Tracking, and Food Safety, p 93-136. In Santo Domingo J, Sadowsky M, Doyle M (ed), Microbial Source Tracking. ASM Press, Washington, DC. doi: 10.1128/9781555815769.ch4
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

PFGE patterns of O157:H7. Lanes 1, 6, and 10 represent isolate G5244, which is a standard strain used to characterize molecular size. Lanes 3 and 9 represent isolates from cases involved in a single cluster. Lanes 2, 4, 7, and 8 represent isolates from other sporadic cases of disease. Lane 5 is an additional molecular size standard ( ). Copyright © 1997, Massachusetts Medical Society. All rights reserved.

Citation: Whittam T, Bergholz T. 2007. Molecular Subtyping, Source Tracking, and Food Safety, p 93-136. In Santo Domingo J, Sadowsky M, Doyle M (ed), Microbial Source Tracking. ASM Press, Washington, DC. doi: 10.1128/9781555815769.ch4
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3
Figure 3

(A) Sources of water pollution addressed by microbial source tracking. (B) Sources of food contamination in the food chain addressed by microbial subtyping.

Citation: Whittam T, Bergholz T. 2007. Molecular Subtyping, Source Tracking, and Food Safety, p 93-136. In Santo Domingo J, Sadowsky M, Doyle M (ed), Microbial Source Tracking. ASM Press, Washington, DC. doi: 10.1128/9781555815769.ch4
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 4
Figure 4

Routes of transmission for serotype Enteritidis ( ). (Reprinted from the Volume 89, no. 5, 2006. Copyright 2006 by AOAC International.)

Citation: Whittam T, Bergholz T. 2007. Molecular Subtyping, Source Tracking, and Food Safety, p 93-136. In Santo Domingo J, Sadowsky M, Doyle M (ed), Microbial Source Tracking. ASM Press, Washington, DC. doi: 10.1128/9781555815769.ch4
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 5
Figure 5

O157:H7 outbreaks in the United States from 1982 to 2002 ( ). axis is number of outbreaks.

Citation: Whittam T, Bergholz T. 2007. Molecular Subtyping, Source Tracking, and Food Safety, p 93-136. In Santo Domingo J, Sadowsky M, Doyle M (ed), Microbial Source Tracking. ASM Press, Washington, DC. doi: 10.1128/9781555815769.ch4
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 6
Figure 6

Estimated number of cases of salmonellosis attributed to domestic and imported food sources based on a Bayesian model ( ).

Citation: Whittam T, Bergholz T. 2007. Molecular Subtyping, Source Tracking, and Food Safety, p 93-136. In Santo Domingo J, Sadowsky M, Doyle M (ed), Microbial Source Tracking. ASM Press, Washington, DC. doi: 10.1128/9781555815769.ch4
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Angulo, F. J., and, D. L. Swerdlow. 1998. Salmonella enteritidis infections in the United States. J.Am. Vet. Med. Assoc. 213: 17291731.
2. Arias, C. R.,, M. J. Pujalte,, E. Garay, and, R. Aznar. 1998. Genetic relatedness among environmental, clinical, and diseased-eel Vibrio vulnificus isolates from different geographic regions by ribotyping and randomly amplified polymorphic DNA PCR. Appl. Environ. Microbiol. 64: 34033410.
3. Aslam, M.,, G. G. Greer,, F. M. Nattress,, C. O. Gill, and, L. M. McMullen. 2004. Genotypic analysis of Escherichia coli recovered from product and equipment at a beef-packing plant. J.Appl. Microbiol. 97: 7886.
4. Aslam, M.,, F. Nattress,, G. Greer,, C. Yost,, C. Gill, and, L. McMullen. 2003. Origin of contamination and genetic diversity of Escherichia coli in beef cattle. Appl. Environ. Microbiol. 69: 27942799.
5. Autio, T.,, S. Hielm,, M. Miettinen,, A. M. Sjoberg,, K. Aarnisalo,, J. Bjorkroth,, T. Mattila-Sandholm, and, H. Korkeala. 1999. Sources of Listeria monocytogenes contamination in a cold-smoked rainbow trout processing plant detected by pulsed-field gel electrophoresis typing. Appl. Environ. Microbiol. 65: 150155.
6. Ayling, R. D.,, M. J. Woodward,, S. Evans, and, D. G. Newell. 1996. Restriction fragment length polymorphism of polymerase chain reaction products applied to the differentiation of poultry campylobacters for epidemiological investigations. Res. Vet. Sci. 60: 168172.
7. Baloga, A. O., and, S. K. Harlander. 1991. Comparison of methods for discrimination between strains of Listeria monocytogenes from epidemiological surveys. Appl. Environ. Microbiol. 57: 23242331.
8. Barkocy-Gallagher, G. A.,, T. M. Arthur,, G. R. Siragusa,, J. E. Keen,, R. O. Elder,, W. W. Laegreid, and, M. Koohmaraie. 2001. Genotypic analyses of Escherichia coli O157:H7 and O157 nonmotile isolates recovered from beef cattle and carcasses at processing plants in the Midwestern states of the United States. Appl. Environ. Microbiol. 67: 38103818.
9. Batz, M. B.,, M. P. Doyle,, G. Morris,, Jr., J. Painter,, R. Singh,, R. V. Tauxe,, M. R. Taylor, and, D. M. Wong. 2005. Attributing illness to food. Emerg. Infect. Dis. 11: 993999.
10. Baumler, A.J.,, R. M. Tsolis,, T.A. Ficht, and, L. G. Adams. 1998. Evolution of host adaptation in Salmonella enterica. Infect. Immun. 66: 45794587.
11. Beltran, P.,, J. M. Musser,, R. Helmuth,, J.J. Farmer III,, W. M. Frerichs,, I. K. Wachsmuth,, K. Ferris,, A. C. McWhorter,, J. G. Wells,, A. Cravioto, and, R. K. Selander. 1988. Toward a population genetic analysis of Salmonella: genetic diversity and relationships among strains of serotypes S. choleraesuis,, S. derby,, S. dublin, S. enteritidis,, S. heidelberg,, S. infantis,, S. newport, and, S. typhimurium. Proc. Natl. Acad. Sci. USA 85: 77537757.
12. Bender, J. B.,, C. W. Hedberg,, J. M. Besser,, D.J. Boxrud,, K. L. MacDonald, and, M. T. Osterholm. 1997. Surveillance by molecular subtype for Escherichia coli O157:H7 infections in Minnesota by molecular subtyping. N. Engl. J. Med. 337: 388394.
13. Best, E. L.,, A. J. Fox,, J. A. Frost, and, F. J. Bolton. 2005. Real-time single-nucleotide polymorphism profiling using Taqman technology for rapid recognition of Campylobacter jejuni clonal complexes. J. Med. Microbiol. 54: 919925.
14. Bopp, D. J.,, B. D. Sauders,, A. L. Waring,, J. Ackelsberg,, N. Dumas,, E. Braun-Howland,, D. Dziewulski,, B. J. Wallace,, M. Kelly,, T. Halse,, K. A. Musser,, P. F. Smith,, D. L. Morse, and, R.J. Limberger. 2003. Detection, isolation, and molecular subtyping of Escherichia coli O157:H7 and Campylobacter jejuni associated with a large waterborne outbreak. J. Clin. Microbiol. 41: 174180.
15. Botteldoorn, N.,, L. Herman,, N. Rijpens, and, M. Heyndrickx. 2004. Phenotypic and molecular typing of Salmonella strains reveals different contamination sources in two commercial pig slaughterhouses. Appl. Environ. Microbiol. 70: 53055314.
16. Botteldoorn, N.,, M. Heyndrickx,, N. Rijpens,, K. Grijspeerdt, and, L. Herman. 2003. Salmonella on pig carcasses: positive pigs and cross contamination in the slaughterhouse. J. Appl. Microbiol. 95: 891903.
17. Breuer, T.,, D. H. Benkel,, R. L. Shapiro,, W. N. Hall,, M. M. Winnett,, M. J. Linn,, J. Neimann,, T. J. Barrett,, S. Dietrich,, F. P. Downes,, D. M. Toney,, J. L. Pearson,, H. Rolka,, L. Slutsker, and, P. M. Griffin. 2001. A multistate outbreak of Escherichia coli O157:H7 infections linked to alfalfa sprouts grown from contaminated seeds. Emerg. Infect. Dis. 7: 977982.
18. Buchrieser, C.,, V. V. Gangar,, R. L. Murphree,, M. L. Tamplin, and, C. W. Kaspar. 1995. Multiple Vibrio vulnificus strains in oysters as demonstrated by clamped homogeneous electric field gel electrophoresis. Appl. Environ. Microbiol. 61: 11631168.
19. Cai, S.,, D. Y. Kabuki,, A. Y. Kuaye,, T. G. Cargioli,, M. S. Chung,, R. Nielsen, and, M. Wiedmann. 2002. Rational design of DNA sequence-based strategies for subtyping Listeria monocytogenes. J. Clin. Microbiol. 40: 33193325.
20. Call, D. R.,, M. K. Borucki, and, T. E. Besser. 2003. Mixed-genome microarrays reveal multiple serotype and lineage-specific differences among strains of Listeria monocytogenes. J. Clin. Microbiol. 41: 632639.
21. Call, D. R.,, M. K. Borucki, and, F. J. Loge. 2003. Detection of bacterial pathogens in environmental samples using DNA microarrays. J. Microbiol. Methods 53: 235243.
22. Castillo, A.,, I. Mercado,, L. M. Lucia,, Y. Martinez-Ruiz,, J. Ponce de Leon,, E. A. Murano, and, G. R. Acuff. 2004. Salmonella contamination during production of cantaloupe: a binational study. J. Food Prot. 67: 713720.
23. Centers for Disease Control and Prevention. 2005. Preliminary FoodNet data on the incidence of infection with pathogens transmitted commonly through food—10 sites, United States, 2004. Morb. Mortal. Wkly. Rep. 54: 352356.
24. Centers for Disease Control and Prevention. 2005. Summary of notifiable diseases—United States, 2003. Morb. Mortal. Wkly. Rep. 52: 185.
25. Chan, E. S.,, J. Aramini,, B. Ciebin,, D. Middleton,, R. Ahmed,, M. Howes,, I. Brophy,, I. Mentis,, F. Jamieson,, F. Rodgers,, M. Nazarowec-White,, S. C. Pichette,, J. Farrar,, M. Gutierrez,, W. J. Weis,, L. Lior,, A. Ellis, and, S. Isaacs. 2002. Natural or raw almonds and an outbreak of a rare phage type of Salmonella enteritidis infection. Can. Commun. Dis. Rep. 28: 9799.
26. Chiou, C. S.,, S. Y. Hsu,, S. I. Chiu,, T. K. Wang, and, C. S. Chao. 2000. Vibrio para-haemolyticus serovar O3:K6 as cause of unusually high incidence of food-borne disease outbreaks in Taiwan from 1996 to 1999. J. Clin. Microbiol. 38: 46214625.
27. Chizhikov, V.,, A. Rasooly,, K. Chumakov, and, D. D. Levy. 2001. Microarray analysis of microbial virulence factors. Appl. Environ. Microbiol. 67: 32583263.
28. Clark, C. G.,, T. M. A. C. Kruk,, L. Bryden,, Y. Hirvi,, R. Ahmed, and, F. G. Rodgers. 2003. Subtyping of Salmonella enterica serotype Enteritidis strains by manual and automated PstI -SphI ribotyping. J. Clin. Microbiol. 41: 2733.
29. Craun, G. F.,, R. L. Calderon, and, M. F. Craun. 2005. Outbreaks associated with recreational water in the United States. Int. J. Environ. Health Res. 15: 243262.
30. Davies, R. H., and, C. Wray. 1995. Mice as carriers of Salmonella enteritidis on persistently infected poultry units. Vet. Rec. 137: 337341.
31. Davis, M. A.,, D. D. Hancock,, D. H. Rice,, D. R. Call,, R. DiGiacomo,, M. Samadpour,and, T. E. Besser. 2003. Feedstuffs as a vehicle of cattle exposure to Escherichia coli O157:H7 and Salmonella enterica. Vet. Microbiol. 95: 199210.
32. Desai, M.,, E. J. Threlfall, and, J. Stanley. 2001. Fluorescent amplified-fragment length polymorphism subtyping of the Salmonella enterica serovar Enteritidis phage type 4 clone complex. J. Clin. Microbiol. 39: 201206.
33. Destro, M. T.,, M. F. Leitao, and, J. M. Farber. 1996. Use of molecular typing methods to trace the dissemination of Listeria monocytogenes in a shrimp processing plant. Appl. Environ. Microbiol. 62: 705711.
34. Dingle, K. E.,, F. M. Colles,, D. R. Wareing,, R. Ure,, A.J. Fox,, F. E. Bolton,, H.J. Bootsma,, R. J. Willems,, R. Urwin, and, M. C. Maiden. 2001. Multilocus sequence typing system for Campylobacter jejuni. J. Clin. Microbiol. 39: 1423.
35. Duim, B.,, T. M. Wassenaar,, A. Rigter, and, J. Wagenaar. 1999. High-resolution genotyping of Campylobacter strains isolated from poultry and humans with amplified fragment length polymorphism fingerprinting. Appl. Environ. Microbiol. 65: 23692375.
36. Elder, R. O.,, J. E. Keen,, G. R. Siragusa,, G. A. Barkocy-Gallagher,, M. Koohmaraie, and, W. W. Laegreid. 2000. Correlation of enterohemorrhagic Escherichia coli O157 prevalence in feces, hides, and carcasses of beef cattle during processing. Proc. Natl. Acad. Sci. USA 97: 29993003.
37. Feil, E. J.,, B. C. Li,, D. M. Aanensen,, W. P. Hanage, and, B. G. Spratt. 2004. eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J. Bacteriol. 186: 15181530.
38. Ferguson, D. D.,, J. Scheftel,, A. Cronquist,, K. Smith,, A. Woo-Ming,, E. Anderson,, J. Knutsen,, A. K. De, and, K. Gershman. 2005. Temporally distinct Escherichia coli O157 outbreaks associated with alfalfa sprouts linked to a common seed source—Colorado and Minnesota, 2003. Epidemiol. Infect. 133: 439447.
39. Finlay, B. B. 2001. Microbiology. Cracking Listeria’s password. Science 292: 16651667.
40. Fitzgerald, C.,, L. O. Helsel,, M. A. Nicholson,, S. J. Olsen,, D. L. Swerdlow,, R. Flahart,, J. Sexton, and, P. I. Fields. 2001. Evaluation of methods for subtyping Campylobacter jejuni during an outbreak involving a food handler. J. Clin. Microbiol. 39: 23862390.
41. Foley, S. L.,, S. Simjee,, J. Meng,, D. G. White,, P. F. McDermott, and, S. Zhao. 2004. Evaluation of molecular typing methods for Escherichia coli O157:H7 isolates from cattle, food, and humans. J. Food Prot. 67: 651657.
42. Frye, D. M.,, R. Zweig,, J. Sturgeon,, M. Tormey,, M. LeCavalier,, I. Lee,, L. Lawani, and, L. Mascola. 2002. An outbreak of febrile gastroenteritis associated with delicatessen meat contaminated with Listeria monocytogenes. Clin. Infect. Dis. 35: 943949.
43. Gast, R. K., and, P. S. Holt. 2001. Multiplication in egg yolk and survival in egg albumen of Salmonella enterica serotype Enteritidis strains of phage types 4, 8, 13a, and 14b. J. Food Prot. 64: 865868.
44. Giovannacci, I.,, S. Queguiner,, C. Ragimbeau,, G. Salvat,, J. L. Vendeuvre,, V. Carlier, and, G. Ermel. 2001. Tracing of Salmonella spp. in two pork slaughter and cutting plants using serotyping and macrorestriction genotyping. J. Appl. Microbiol. 90: 131147.
45. Graves, L. M.,, B. Swaminathan,, M. W. Reeves,, S. B. Hunter,, R. E. Weaver,, B. D. Plikaytis, and, A. Schuchat. 1994. Comparison of ribotyping and multilocus enzyme electrophoresis for subtyping of Listeria monocytogenes isolates. J. Clin. Microbiol. 32: 29362943.
46. Guard-Bouldin, J.,, R. K. Gast,, T. J. Humphrey,, D. J. Henzler,, C. Morales, and, K. Coles. 2004. Subpopulation characteristics of egg-contaminating Salmonella enterica serovar Enteritidis as defined by the lipopolysaccharide O chain. Appl. Environ. Microbiol. 70: 27562763.
47. Guard-Petter, J.,, D.J. Henzler,, M. M. Rahman, and, R. W. Carlson. 1997. On-farm monitoring of mouse-invasive Salmonella enterica serovar Enteritidis and a model for its association with the production of contaminated eggs. Appl. Environ. Microbiol. 63: 15881593.
48. Gudmundsdottir, S.,, B. Gudbjornsdottir,, H. L. Lauzon,, H. Einarsson,, K. G. Kristinsson, and, M. Kristjansson. 2005. Tracing Listeria monocytogenes isolates from cold-smoked salmon and its processing environment in Iceland using pulsed-field gel electrophoresis. Int. J. Food Microbiol. 101: 4151.
49. Hahm, B. K.,, Y. Maldonado,, E. Schreiber,, A. K. Bhunia, and, C. H. Nakatsu. 2003. Subtyping of foodborne and environmental isolates of Escherichia coli by multiplex-PCR, rep-PCR, PFGE, ribotyping and AFLP. J. Microbiol. Methods 53: 387399.
50. Hald, T.,, D. Vose,, H. C. Wegener, and, T. Koupeev. 2004. A Bayesian approach to quantify the contribution of animal-food sources to human salmonellosis. Risk Anal. 24: 255269.
51. Hardnett, F. P.,, R. M. Hoekstra,, M. Kennedy,, L. Charles, and, F. J. Angulo. 2004. Epidemiologic issues in study design and data analysis related to FoodNet activities. Clin. Infect. Dis. 38: S121S126.
52. Hedberg, C. W.,, M. J. David,, K. E. White,, K. L. MacDonald, and, M. T. Osterholm. 1993. Role of egg consumption in sporadic Salmonella enteritidis and Salmonella typhimurium infections in Minnesota. J. Infect. Dis. 167: 107111.
53. Henzler, D. J., and, H. M. Opitz. 1992. The role of mice in the epizootiology of Salmonella enteritidis infection on chicken layer farms. Avian Dis. 36: 625631.
54. Herikstad, H.,, S. Yang,, T. J. Van Gilder,, D. Vugia,, J. Hadler,, P. Blake,, V. Deneen,, B. Shiferaw, and, F. J. Angulo. 2002. A population-based estimate of the burden of diarrhoeal illness in the United States: FoodNet, 1996–7. Epidemiol. Infect. 129: 917.
55. Hilborn, E. D.,, J. H. Mermin,, P. A. Mshar,, J. L. Hadler,, A. Voetsch,, C. Wojtkunski,, M. Swartz,, R. Mshar,, M. A. Lambert-Fair,, J. A. Farrar,, M. K. Glynn, and, L. Slutsker. 1999. A multistate outbreak of Escherichia coli O157:H7 infections associated with consumption of mesclun lettuce. Arch. Intern. Med. 159: 17581764.
56. Hoffman, A. D.,, K. L. Gall,, D. M. Norton, and, M. Wiedmann. 2003. Listeria monocytogenes contamination patterns for the smoked fish processing environment and for raw fish. J. Food Prot. 66: 5260.
57. Hu, H.,, R. Lan, and, P. R. Reeves. 2002. Fluorescent amplified fragment length polymorphism analysis of Salmonella enterica serovar Typhimurium reveals phage-type-specific markers and potential for microarray typing. J. Clin. Microbiol. 40: 34063415.
58. Humphrey, T.J. 1994. Contamination of egg shell and contents with Salmonella enteritidis: a review. Int. J. Food Microbiol. 21: 3140.
59. Inglis, T. J.,, A. Clair,, J. Sampson,, L. O’Reilly,, S. Vandenberg,, K. Leighton, and, A. Watson. 2003. Real-time application of automated ribotyping and DNA macrorestriction analysis in the setting of a listeriosis outbreak. Epidemiol. Infect. 131: 637645.
60. Isaacs, S.,, J. Aramini,, B. Ciebin,, J. A. Farrar,, R. Ahmed,, D. Middleton,, A. U. Chandran,, L.J. Harris,, M. Howes,, E. Chan,, A. S. Pichette,, K. Campbell,, A. Gupta,, L. Y. Lior,, M. Pearce,, C. Clark,, F. Rodgers,, F. Jamieson,, I. Brophy, and, A. Ellis. 2005. An international outbreak of salmonellosis associated with raw almonds contaminated with a rare phage type of Salmonella enteritidis. J. Food Prot. 68: 191198.
61. Jarvis, G. N.,, M. G. Kizoulis,, F. Diez-Gonzalez, and, J. B. Russell. 2000. The genetic diversity of predominant Escherichia coli strains isolated from cattle fed various amounts of hay and grain. FEMS Microbiol. Ecol. 32: 225233.
62. Jay, M. T.,, V. Garrett,, J. C. Mohle-Boetani,, M. Barros,, J. A. Farrar,, R. Rios,, S. Abbott,, R. Sowadsky,, K. Komatsu,, R. Mandrell,, J. Sobel, and, S. B. Werner. 2004. A multistate outbreak of Escherichia coli O157:H7 infection linked to consumption of beef tacos at a fast-food restaurant chain. Clin. Infect. Dis. 39: 17.
63. Jolley, K. A.,, M. S. Chan, and, M. C. Maiden. 2004. mlstdbNet—distributed multi-locus sequence typing (MLST) databases. BMC Bioinformatics 5: 86.
64. Kabuki, D. Y.,, A. Y. Kuaye,, M. Wiedmann, and, K. J. Boor. 2004. Molecular subtyping and tracking of Listeria monocytogenes in Latin-style fresh-cheese processing plants. J. Dairy Sci. 87: 28032812.
65. Keys, C.,, S. Kemper, and, P. Keim. 2005. Highly diverse variable number tandem repeat loci in the E. coli O157:H7 and O55:H7 genomes for high-resolution molecular typing. J. Appl. Microbiol. 98: 928940.
66. Kramer, J. M.,, J. A. Frost,, F. J. Bolton, and, D. R. Wareing. 2000. Campylobacter contamination of raw meat and poultry at retail sale: identification of multiple types and comparison with isolates from human infection. J. Food Prot. 63: 16541659.
67. Kudva, I. T.,, P. S. Evans,, N. T. Perna,, T. J. Barrett,, F. M. Ausubel,, F. R. Blattner, and, S. B. Calderwood. 2002. Strains of Escherichia coli O157:H7 differ primarily by insertions or deletions, not single-nucleotide polymorphisms. J. Bacteriol. 184: 18731879.
68. Lappi, V. R.,, J. Thimothe,, K. K. Nightingale,, K. Gall,, V. N. Scott, and, M. Wiedmann. 2004. Longitudinal studies on Listeria in smoked fish plants: impact of intervention strategies on contamination patterns. J. Food Prot. 67: 25002514.
69. Lecuit, M.,, S. Vandormael-Pournin,, J. Lefort,, M. Huerre,, P. Gounon,, C. Dupuy,, C. Babinet, and, P. Cossart. 2001. A transgenic model for listeriosis: role of internalin in crossing the intestinal barrier. Science 292: 17221725.
70. Lee, T.M.,, L.L. Chang,, C. Y. Chang,, J. C. Wang,, T. M. Pan,, T. K. Wang, and, S.F. Chang. 2000. Molecular analysis of Shigella sonnei isolated from three well-documented outbreaks in school children. J. Med. Microbiol. 49: 355360.
71. Liebana, E.,, L. Garcia-Migura,, C. Clouting,, F. A. Clifton-Hadley,, M. Breslin, and, R. H. Davies. 2003. Molecular fingerprinting evidence of the contribution of wildlife vectors in the maintenance of Salmonella Enteritidis infection in layer farms. J. Appl. Microbiol. 94: 10241029.
72. Liebana, E.,, L. Garcia-Migura,, J. Guard-Petter,, S. W. McDowell,, S. Rankin,, H. M. Opitz,, F. A. Clifton-Hadley, and, R. H. Davies. 2002. Salmonella enterica serotype Enteritidis phage types 4, 7, 6, 8, 13a, 29 and 34: a comparative analysis of genomic fingerprints from geographically distant isolates. J. Appl. Microbiol. 92: 196209.
73. Lindsay, J. A. 1997. Chronic sequelae of foodborne disease. Emerg. Infect. Dis. 3: 443352.
74. Lindstedt, B. A. 2005. Multiple-locus variable number tandem repeats analysis for genetic fingerprinting of pathogenic bacteria. Electrophoresis 26: 25672582.
75. Lindstedt, B. A.,, T. Vardund,, L. Aas, and, G. Kapperud. 2004. Multiple-locus variable-number tandem-repeats analysis of Salmonella enterica subsp. enterica serovar Typhimurium using PCR multiplexing and multicolor capillary electrophoresis. J. Microbiol. Methods 59: 163172.
76. MacDonald, P. D.,, R. E. Whitwam,, J. D. Boggs,, J. N. MacCormack,, K. L. Anderson,, J. W. Reardon,, J. R. Saah,, L. M. Graves,, S. B. Hunter, and, J. Sobel. 2005. Outbreak of listeriosis among Mexican immigrants as a result of consumption of illicitly produced Mexican-style cheese. Clin. Infect. Dis. 40: 677682.
77. Madden, R. H.,, L. Moran, and, P. Scates. 1998. Frequency of occurrence of Campylobacter spp. in red meats and poultry in Northern Ireland and their subsequent subtyping using polymerase chain reaction-restriction fragment length polymorphism and the random amplified polymorphic DNA method. J. Appl. Microbiol. 84: 703708.
78. Maiden, M. C.,, J. A. Bygraves,, E. Feil,, G. Morelli,, J. E. Russell,, R. Urwin,, Q. Zhang,, J. Zhou,, K. Zurth,, D. A. Caugant,, I. M. Feavers,, M. Achtman, and, B. G. Spratt. 1998. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Natl. Acad. Sci. USA 95: 31403145.
79. Markkula, A.,, T. Autio,, J. Lunden, and, H. Korkeala. 2005. Raw and processed fish show identical Listeria monocytogenes genotypes with pulsed-field gel electrophoresis. J. Food Prot. 68: 12281231.
80. Martin, I. E.,, S. D. Tyler,, K. D. Tyler,, R. Khakhria, and, W. M. Johnson. 1996. Evaluation of ribotyping as epidemiologic tool for typing Escherichia coli serogroup O157 isolates. J. Clin. Microbiol. 34: 720723.
81. Martinez, I.,, L. M. Rorvik,, V. Brox,, J. Lassen,, M. Seppola,, L. Gram, and, B. Fonnesbech-Vogel. 2003. Genetic variability among isolates of Listeria monocytogenes from food products, clinical samples and processing environments, estimated by RAPD typing. Int. J. Food Microbiol. 84: 285297.
82. Martinez-Urtaza, J.,, A. Lozano-Leon,, A. DePaola,, M. Ishibashi,, K. Shimada,, M. Nishibuchi, and, E. Liebana. 2004. Characterization of pathogenic Vibrio para-haemolyticus isolates from clinical sources in Spain and comparison with Asian and North American pandemic isolates. J. Clin. Microbiol. 42: 46724678.
83. McLauchlin, J.,, G. Ripabelli,, M. M. Brett, and, E.J. Threlfall. 2000. Amplified fragment length polymorphism (AFLP) analysis of Clostridium perfringens for epidemiological typing. Int. J. Food Microbiol. 56: 2128.
84. Mead, P. S.,, L. Slutsker,, V. Dietz,, L. F. McCaig,, J. S. Bresee,, C. Shapiro,, P. M. Griffin, and, R. V. Tauxe. 1999. Food-related illness and death in the United States. Emerg. Infect. Dis. 5: 607625.
85. Micheli, M. R.,, R. Bova,, E. Pascale, and, E. D’Ambrosio. 1994. Reproducible DNA fingerprinting with the random amplified polymorphic DNA (RAPD) method. Nucleic Acids Res. 22: 19211922.
86. Nakamura, M.,, N. Nagamine,, M. Norimatsu,, S. Suzuki,, K. Ohishi,, M. Kijima,, Y. Tamura, and, S. Sato. 1993. The ability of Salmonella enteritidis isolated from chicks imported from England to cause transovarian infection. J. Vet. Med. Sci. 55: 135136.
87. Noller, A. C.,, M. C. McEllistrem,, A. G. Pacheco,, D. J. Boxrud, and, L. H. Harrison. 2003. Multilocus variable-number tandem repeat analysis distinguishes outbreak and sporadic Escherichia coli O157:H7 isolates. J. Clin. Microbiol. 41: 53895397.
88. Noller, A. C.,, M. C. McEllistrem,, O. C. Stine,, J. G. Morris, Jr.,, D. J. Boxrud,, B. Dixon, and, L. H. Harrison. 2003. Multilocus sequence typing reveals a lack of diversity among Escherichia coli O157:H7 isolates that are distinct by pulsed-field gel electrophoresis. J. Clin. Microbiol. 41: 675679.
89. Olsen, S. J.,, M. Patrick,, S. B. Hunter,, V. Reddy,, L. Kornstein,, W. R. MacKenzie,, K. Lane,, S. Bidol,, G. A. Stoltman,, D. M. Frye,, I. Lee,, S. Hurd,, T. F. Jones,, T. N. LaPorte,, W. Dewitt,, L. Graves,, M. Wiedmann,, D. J. Schoonmaker-Bopp,, A. J. Huang,, C. Vincent,, A. Bugenhagen,, J. Corby,, E. R. Carloni,, M. E. Holcomb,, R. F. Woron,, S. M. Zansky,, G. Dowdle,, F. Smith,, S. Ahrabi-Fard,, A. R. Ong,, N. Tucker,, N. A. Hynes, and, P. Mead. 2005. Multistate outbreak of Listeria monocytogenes infection linked to delicatessen turkey meat. Clin. Infect. Dis. 40: 962967.
90. Owen, R. J., and, S. Leeton. 1999. Restriction fragment length polymorphism analysis of the flaA gene of Campylobacter jejuni for subtyping human, animal and poultry isolates. FEMS Microbiol. Lett. 176: 345350.
91. Patrick, M. E.,, P. M. Adcock,, T. M. Gomez,, S. F. Altekruse,, B. H. Holland,, R. V. Tauxe, and, D. L. Swerdlow. 2004. Salmonella enteritidis infections, United States, 1985—1999. Emerg. Infect. Dis. 10: 17.
92. Petersen, L., and, D. G. Newell. 2001. The ability of Fla-typing schemes to discriminate between strains of Campylobacter jejuni. J. Appl. Microbiol. 91: 217224.
93. Piffaretti, J. C.,, H. Kressebuch,, M. Aeschbacher,, J. Bille,, E. Bannerman,, J. M. Musser,, R. K. Selander, and, J. Rocourt. 1989. Genetic characterization of clones of the bacterium Listeria monocytogenes causing epidemic disease. Proc. Natl. Acad. Sci. USA 86: 38183822.
94. Pupo, G. M.,, R. Lan, and, P. R. Reeves. 2000. Multiple independent origins of Shigella clones of Escherichia coli and convergent evolution of many of their characteristics. Proc. Natl. Acad. Sci. USA 97: 1056710572.
95. Qi, W.,, D. W. Lacher,, A. C. Bumbaugh,, K. E. Hyma,, L. M. Ouellette,, T. M. Large,, C. L. Tarr, and, T. S. Whittam. 2004. EcMLST: an online database for multilocus sequence typing of pathogenic Escherichia coli. Proceedings of the 2004 IEEE Computational Systems Bioinformatics Conference.
96. Rangel, J. M.,, P. H. Sparling,, C. Crowe,, P. M. Griffin, and, D. L. Swerdlow. 2005. Epidemiology of Escherichia coli O157:H7 outbreaks, United States, 1982–2002. Emerg. Infect. Dis. 11: 603609.
97. Rice, D. H.,, K. M. McMenamin,, L. C. Pritchett,, D. D. Hancock, and, T. E. Besser. 1999. Genetic subtyping of Escherichia coli O157 isolates from 41 Pacific Northwest USA cattle farms. Epidemiol. Infect. 122: 479484.
98. Ross, I. L., and, M. W. Heuzenroeder. 2005. Use of AFLP and PFGE to discriminate between Salmonella enterica serovar Typhimurium DT126 isolates from separate food-related outbreaks in Australia. Epidemiol. Infect. 133: 635644.
99. Saeed, A.M.,, S.T. Walk,, M.M. Arshad, and, T. S. Whittam. 2006. Clonal structure and variation in virulence of Salmonella Enteritidis isolated from mice, chickens, and humans. J. Assoc. Off. Anal. Chem. 89: 504511.
100. Sails, A. D.,, B. Swaminathan, and, P. I. Fields. 2003. Utility of multilocus sequence typing as an epidemiological tool for investigation of outbreaks of gastroenteritis caused by Campylobacter jejuni. J. Clin. Microbiol. 41: 47334739.
101. Salama, N.,, K. Guillemin,, T. K. McDaniel,, G. Sherlock,, L. Tompkins, and, S. Falkow. 2000. A whole-genome microarray reveals genetic diversity among Helicobacter pylori strains. Proc. Natl. Acad. Sci. USA 97: 1466814673.
102. Sauders, B. D.,, K. Mangione,, C. Vincent,, J. Schermerhorn,, C. M. Farchione,, N. B. Dumas,, D. Bopp,, L. Kornstein,, E. D. Fortes,, K. Windham, and, M. Wiedmann. 2004. Distribution of Listeria monocytogenes molecular subtypes among human and food isolates from New York State shows persistence of human disease-associated Listeria monocytogenes strains in retail environments. J. Food Prot. 67: 14171428.
103. Schroeder, C. M.,, A. L. Naugle,, W. D. Schlosser,, A.T. Hogue,, F.J. Angulo,, J. S. Rose,, E. D. Ebel,, W. T. Disney,, K. G. Holt, and, D. P. Goldman. 2005. Estimate of illnesses from Salmonella enteritidis in eggs, United States, 2000. Emerg. Infect. Dis. 11: 113115.
104. Scott, T. M.,, T. M. Jenkins,, J. Lukasik,and, J. B. Rose. 2005. Potential use of a host associated molecular marker in Enterococcus faecium as an index of human fecal pollution. Environ. Sci. Technol. 39: 283287.
105. Selander, R. K.,, P. Beltran,, N. H. Smith,, R. Helmuth,, F. A. Rubin,, D. J. Kopecko,, K. Ferris,, B. D. Tall,, A. Cravioto, and, J. M. Musser. 1990. Evolutionary genetic relationships of clones of Salmonella serovars that cause human typhoid and other enteric fevers. Infect. Immun. 58: 22622275.
106. Selander, R. K.,, J. M. Musser,, D.A. Caugant,, M. N. Gilmour, and, T. S. Whittam. 1987. Population genetics of pathogenic bacteria. Microb. Pathog. 3: 17.
107. Shere, J. A.,, K.J. Bartlett, and, C. W. Kaspar. 1998. Longitudinal study of Escherichia coli O157:H7 dissemination on four dairy farms in Wisconsin. Appl. Environ. Microbiol. 64: 13901399.
108. Simpson, J. M.,, J. W. Santo Domingo, and, D.J. Reasoner. 2002. Microbial source tracking: state of the science. Environ. Sci. Technol. 36: 52795288.
109. Spratt, B. G., and, M. C. Maiden. 1999. Bacterial population genetics, evolution and epidemiology. Philos. Trans. R. Soc. Lond. B Biol. Sci. 354: 701710.
110. St. Louis, M. E.,, D. L. Morse,, M. E. Potter,, T. M. DeMelfi,, J.J. Guzewich,, R. V. Tauxe, and, P. A. Blake. 1988. The emergence of grade A eggs as a major source of Salmonella enteritidis infections. New implications for the control of salmonellosis. JAMA 259: 21032107.
111. Swaminathan, B.,, T. J. Barrett,, S. B. Hunter, and, R. V. Tauxe. 2001. PulseNet: the molecular subtyping network for foodborne bacterial disease surveillance, United States. Emerg. Infect. Dis. 7: 382389.
112. Swaminathan, B.,, S. B. Hunter,, P. M. Desmarchelier,, P. Gerner-Smidt,, L. M. Graves,, S. Harlander,, R. Hubner,, C. Jacquet,, B. Pedersen,, K. Reineccius,, A. Ridley,, N. A. Saunders, and, J.A. Webster. 1996. WHO-sponsored international collaborative study to evaluate methods for subtyping Listeria monocytogenes: restriction fragment length polymorphism (RFLP) analysis using ribotyping and Southern hybridization with two probes derived from L. monocytogenes chromosome. Int. J. Food Microbiol. 32: 263278.
113. Tamplin, M. L.,, J. K. Jackson,, C. Buchrieser,, R. L. Murphree,, K. M. Portier,, V. Gangar,, L. G. Miller, and, C. W. Kaspar. 1996. Pulsed-field gel electrophoresis and ribotype profiles of clinical and environmental Vibrio vulnificus isolates. Appl. Environ. Microbiol. 62: 35723580.
114. Thiagarajan, D.,, A. M. Saeed, and, E. K. Asem. 1994. Mechanism of transovarian transmission of Salmonella enteritidis in laying hens. Poult. Sci. 73: 8998.
115. Thimothe, J.,, K. K. Nightingale,, K. Gall,, V. N. Scott, and, M. Wiedmann. 2004. Tracking of Listeria monocytogenes in smoked fish processing plants. J. Food Prot. 67: 328341.
116. Todd, E. C. 1989. Costs of acute bacterial foodborne disease in Canada and the United States. Int. J. Food Microbiol. 9: 313326.
117. Trevejo, R. T.,, S. L. Abbott,, M. I. Wolfe,, J. Meshulam,, D. Yong, and, G. R. Flores. 1999. An untypeable Shigella flexneri strain associated with an outbreak in California. J. Clin. Microbiol. 37: 23522353.
118. Urisman, A.,, K. F. Fischer,, C. Y. Chiu,, A. L. Kistler,, S. Beck,, D. Wang, and, J. L. DeRisi. 2005. E-Predict: a computational strategy for species identification based on observed DNA microarray hybridization patterns. Genome Biol. 6: R78.
119. Velge, P.,, A. Cloeckaert, and, P. Barrow. 2005. Emergence of Salmonella epidemics: the problems related to Salmonella enterica serotype Enteritidis and multiple antibiotic resistance in other major serotypes. Vet. Res. 36: 267288.
120. Versalovic, J.,, T. Koeuth, and, J. R. Lupski. 1991. Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res. 19: 68236831.
121. Welsh, J., and, M. McClelland. 1990. Fingerprinting genomes using PCR with arbitrary primers. Nucleic Acids Res. 18: 72137218.
122. Whittam, T. S. 1996. Genetic variation and evolutionary processes in natural populations of Escherichia coli, p. 27082720. In F. C. Neidhardt,, R. Curtiss III,, J. L. Ingraham,, E. C. C. Lin,, K. B. Low,, B. Magasanik,, W. S. Reznikoff,, M. Riley,, M. Schaechter, and, H. E. Umbarger ( ed.), Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd ed. American Society for Microbiology, Washington, D.C.
123. Whittam, T. S.,, I. K. Wachsmuth, and, R. A. Wilson. 1988. Genetic evidence of clonal descent of Escherichia coli O157:H7 associated with hemorrhagic colitis and hemolytic uremic syndrome. J. Infect. Dis. 157: 11241133.
124. Whittam, T. S., and, R. A. Wilson. 1988. Genetic relationships among pathogenic Escherichia coli of serogroup O157. Infect. Immun. 56: 24672473.
125. Wick, L. M.,, W. Qi,, D. W. Lacher, and, T. S. Whittam. 2005. Evolution of genomic content in the stepwise emergence of Escherichia coli O157:H7. J. Bacteriol. 187: 17831791.
126. Wiedmann, M. 2002. Subtyping of bacterial foodborne pathogens. Nutr. Rev. 60: 201208.
127. Wiedmann, M.,, J. L. Bruce,, C. Keating,, A. E. Johnson,, P. L. McDonough, and, C. A. Batt. 1997. Ribotypes and virulence gene polymorphisms suggest three distinct Listeria monocytogenes lineages with differences in pathogenic potential. Infect. Immun. 65: 27072716.
128. Williams, J. G.,, A. R. Kubelik,, K.J. Livak,, J.A. Rafalski, and, S. V. Tingey. 1990. DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Res. 18: 65316535.
129. Wilson, W. J.,, C. L. Strout,, T. Z. DeSantis,, J. L. Stilwell,, A. V. Carrano, and, G. L. Andersen. 2002. Sequence-specific identification of 18 pathogenic microorganisms using microarray technology. Mol. Cell. Probes 16: 119127.
130. Wonderling, L.,, R. Pearce,, F. M. Wallace,, J. E. Call,, I. Feder,, M. Tamplin, and, J. B. Luchansky. 2003. Use of pulsed-field gel electrophoresis to characterize the heterogeneity and clonality of Salmonella isolates obtained from the carcasses and feces of swine at slaughter. Appl. Environ. Microbiol. 69: 41774182.
131. Wong, S.,, D. Street,, S. I. Delgado, and, K. C. Klontz. 2000. Recalls of foods and cosmetics due to microbial contamination reported to the U.S. Food and Drug Administration. J. Food Prot. 63: 11131116.
132. Yeung, P. S.,, M. C. Hayes,, A. DePaola,, C. A. Kaysner,, L. Kornstein, and, K. J. Boor. 2002. Comparative phenotypic, molecular, and virulence characterization of Vibrio para-haemolyticus O3:K6 isolates. Appl. Environ. Microbiol. 68: 29012909.
133. Yuki, N.,, K. Susuki,, M. Koga,, Y. Nishimoto,, M. Odaka,, K. Hirata,, K. Taguchi,, T. Miyatake,, K. Furukawa,, T. Kobata, and, M. Yamada. 2004. Carbohydrate mimicry between human ganglioside GM1 and Campylobacter jejuni lipooligosaccharide causes Guillain-Barre syndrome. Proc. Natl. Acad. Sci. USA 101: 1140411409.
134. Zhang, W.,, B. M. Jayarao, and, S. J. Knabel. 2004. Multi-virulence-locus sequence typing of Listeria monocytogenes. Appl. Environ. Microbiol. 70: 913920.


Generic image for table
Table 1

Bacterial, viral, and parasitic agents that contribute to the burden of food-borne illness in the United States

Citation: Whittam T, Bergholz T. 2007. Molecular Subtyping, Source Tracking, and Food Safety, p 93-136. In Santo Domingo J, Sadowsky M, Doyle M (ed), Microbial Source Tracking. ASM Press, Washington, DC. doi: 10.1128/9781555815769.ch4
Generic image for table
Table 2

Summary of potential advantages and disadvantages of some of the alternative subtyping methods for food-borne pathogens

Citation: Whittam T, Bergholz T. 2007. Molecular Subtyping, Source Tracking, and Food Safety, p 93-136. In Santo Domingo J, Sadowsky M, Doyle M (ed), Microbial Source Tracking. ASM Press, Washington, DC. doi: 10.1128/9781555815769.ch4

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error