The Global Epidemiology of Multiresistant Salmonella enterica Serovar Typhimurium DT104

Dale Hancock; John Gay; Daniel Rice; Margaret Davis; Clive Gay; Thomas Besser

doi:10.1128/9781555818050.ch11

Chapter 11 : The Global Epidemiology of Multiresistant Salmonella enterica Serovar Typhimurium DT104

Authors: Dale Hancock¹, John Gay¹, Daniel Rice¹, Margaret Davis¹, Clive Gay¹, Thomas Besser²

VIEW AFFILIATIONS HIDE AFFILIATIONS

Affiliations: 1: Field Disease Investigation Unit, College of Veterinary Medicine, Washington State University, Pullman, WA 99164-6610; 2: Department of Veterinary Microbiology and Pathology, College of Veterinary Medicine, Washington State University, Pullman, WA 99164-6610

Content Type: Monograph

Publication Year: 2000

Category: Clinical Microbiology

Book DOI: 10.1128/9781555818050

Chapter DOI: 10.1128/9781555818050.ch11

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

Preview this chapter:

The Global Epidemiology of Multiresistant Salmonella enterica Serovar Typhimurium DT104, Page 1 of 2

< Previous page | Next page > /docserver/preview/fulltext/10.1128/9781555818050/9781555812010_Chap11-1.gif /docserver/preview/fulltext/10.1128/9781555818050/9781555812010_Chap11-2.gif

Abstract:

This chapter reviews the epidemiological features of the global dissemination of multiresistant Salmonella enterica serovar typhimurium DT104, discusses the possible origins of this clone, hypothesizes about the possible mechanisms by which rapid global dissemination and displacement of other clones may have occurred, and discusses possible means of control. The clonal nature of mr-DT104 is well established by the genetics of antimicrobial resistance and by restriction fragment length polymorphism analyses. Nosocomial salmonellosis associated with nontyphoidal salmonellae occurs in some developing countries. Four hypothetical models are discussed with respect to their ability to explain the ecological characteristics typical of the agent. These models include: model 1: the enlarged niche hypothesis, model 2: the dissemination fitness hypothesis, model 3: the chance dissemination event hypothesis and model 4: the selection focus hypothesis. To date, the discussion of control efforts for mr-DT104 and similar clones has been limited primarily to debates on the use of antimicrobials in livestock, notably subtherapeutic antimicrobials. The epidemiology of multiresistant serovar Typhimurium is not confined by national borders but is global in nature, as well illustrated by mr-DT104. The available evidence indicates that these efforts should center on selection foci, such as calf-raising operations, which serve as reservoirs of serovar Typhimurium and as sites for clonal competition among epidemic multiresistant strains.

Citation: Hancock D, Gay J, Rice D, Davis M, Gay C, Besser T. 2000. The Global Epidemiology of Multiresistant Salmonella enterica Serovar Typhimurium DT104, p 217-243. In Brown C, Bolin C (ed), Emerging Diseases of Animals. ASM Press, Washington, DC. doi: 10.1128/9781555818050.ch11

Highlighted Text: Show | Hide

Full text loading...

References

/content/book/10.1128/9781555818050.chap11

1. Aarestrup, F. M.,, N. E. Jensen,, and D. L. Baggesen. 1997. Clonal spread of tetracycline-resistant Salmonlla typhimurium in Danish dairy herds. Vet. Rec. 140: 313– 314.

2. Anderson, E. S.,, L. R. Ward,, and M. S. de Saxe. 1977. Bacteriophage typing designations of Salmonella typhimurium. J. Hyg. 78: 297– 300.

3. Anderson, R. J.,, R. L. Walker,, D. W. Hird,, and P. C. Blanchard. 1997. Case-control study of an outbreak of clinical disease attributable to Salmonella menhaden infection in eight dairy herds. J. Am. Vet. Med. Assoc. 210: 528– 530.

4. Angulo, F. J.,, R. V. Tauxe,, and M. L. Cohen. 1998. Significance and sources of antimicrobial-resistant nontyphoidal Salmonella infections in humans in the United States: the need for prudent use of antimicrobial agents, including restricted use of fluoroquinolones, in food animals. Bov. Proc. 31: 1– 8.

5.Anonymous. 1969. Report of the Joint Committee on the Use of Antibiotics in Animal Husbandry and Veterinary Medicine ( Swann Committee). Her Majesty's Stationery Office, London, United Kingdom.

6. Arcangioli, M. A.,, S. Leroy-Setrin,, J. L. Martel,, and E. Chaslus-Dancla. 1999. A new chloramphenicol and florfenicol resistance gene flanked by two integron structures in Salmonella typhimurium DT104. FEMS Microbiol. Lett. 174: 327– 332.

7. Arcangioli, M. A.,, S. Leroy-Setrin,, J. L. Martel,, and E. Chaslus-Dancla. 2000. Evolution of chloramphenicol resistance, with emergence of cross-resistance to florfenicol, in bovine Salmonella Typhimurium strains implicates definitive phage type (DT) 104. J. Med. Microbiol. 49: 103– 110.

8. Asensi, M. D.,, A. R Costa,, E. Moura,, E. M. dos Reis,, and E. Hofer. 1995. Lysotypes and plasmidial profile of Salmonella serovar typhimurium isolated from children with enteric processes in the cities of Rio de Janeiro, RJ, and Salvador, BA—Brazil. Rev. Inst. Med. Trop. Sao Paulo 37: 297– 302.

9. Ayliffe, G. A. 1997. The progressive intercontinental spread of methicillin-resistant Staphylococcus aureus. Clin. Infect. Dis. 24( Suppl. 1): S74– S79.

10. Baggesen, D. L.,, and H. C. Wegener. 1994. Phage types of Salmonella enterica ssp. Enterica serovar typhimurium isolated from production animals and humans in Denmark. Acta Vet. Scand. 35: 349– 354.

11. Baggesen, D. L.,, and F. M. Aarestrup. 1998. Characterisation of recently emerged multiple antibiotic-resistant Salmonella enterica serovar typhimurium DT104 and other multiresistant phage types from Danish pig herds. Vet. Rec. 143: 95– 97.

12. Bailey, J. S.,, R. J. Buhr,, and N. A. Cox. 1996. Effect of hatching cabinet sanitation treatments on Salmonella cross-contamination and hatchability of broiler eggs. Poult. Sci. 75: 191– 196.

13. Bartoloni, A.,, F. Cutts,, S. Leoni,, C. C. Austin,, A. Mantella,, P. Guglielmetti,, M. Roselli,, E. Salazar,, and F. Paradisi. 1998. Patterns of antimicrobial use and antimicrobial resistance among healthy children in Bolivia. Trop. Med. Int. Health 3: 116– 123.

14. Baulmer, A.,, B. M. Hargis,, and R. M. Tsolis. 1999. Tracing the origins of Salmonella outbreaks. Science 287: 50– 52.

15. Berends, B. R.,, H. A. Urlings,, J. M. Snijders,, and F. Van Knapen. 1996. Identification and quantification of risk factors in animal management and transport regarding Salmonella spp. in pigs. Int. J. Food Microbiol. 30: 37– 53.

16. Besser, T. E.,, C. C. Gay,, J. M. Gay,, D. D. Hancock,, D. Rice,, L. C. Pritchett,, and E. D. Erickson. 1997. Salmonellosis associated with typhimurium DT104 in the USA. Vet. Rec. 140: 75.

17. Besser, T. E.,, M. Goldoft,, L. C. Pritchett,, R. Khakhria,, D. D. Hancock,, D. H. Rice,, J. M. Gay,, W. Johnson,, and C. C. Gay. 2000. Multiresistant Salmonella Typhimurium DT104 infections of humans and domestic animals in the Pacific Northwest of the United States. Epidemiol. Infect. 124: 193– 200.

18. Bjorkman, J.,, D. Hughes,, and D. I. Andersson. 1998. Virulence of antibiotic-resistant Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 95: 3949– 3953.

19. Blackburn, B. O.,, K. Sutch,, and R. Harrington Jr.. 1980. The changing distribution of Salmonella dublin in the United States. Proc. Annu. Meet. U.S. Anim. Health Assoc. 84: 445– 451.

20. Briggs, C. E.,, and P. M. Fratamico. 1999. Molecular characterization of an antibiotic resistance gene cluster of Salmonella typhimurium DT104. Antimicrob. Agents Chemother. 43: 846– 849.

21. Buchrieser, C.,, R. Brosch,, O. Buchrieser,, A. Kristl,, J. B. Luchansky,, and C. W. Kaspar. 1997. Genomic analyses of Salmonella enteritidis phage type 4 strains from Austria and phage type 8 strains from the United States. Zentbl. Bakteriol. Mikrobiol. Hyg. Ser. A 285: 379– 388.

22. Butterfield, J.,, J. C. Coulson,, S. V. Kearsey,, P. Monaghan,, J. H. McCoy,, and G. E. Spain. 1983. The herring gull Larus argentatus as a carrier of salmonella. J. Hyg. (Lond). 91: 429– 436.

23. Casin, I.,, J. Breuil,, A. Brisabois,, F. Moury,, F. Grimont,, and E. Collate. 1999. Multidrug-resistant human and animal Salmonella typhimurium isolates in France belong predominantly to a DT104 clone with the chromosome- and integron-encoded beta-lactamase PSE-1. J. Infect. Dis. 179: 1173– 1182.

24. Centers for Disease Control. 1982. Multiresistant salmonella and other infections in adopted infants from India. Morb. Mortal. Wkly. Rep. 31: 285– 287.

25. Centers for Disease Control and Prevention. 1999. Incidence of foodborne illnesses: preliminary data from the foodborne diseases active surveillance network (FoodNet), United States, 1998. Morb. Mortal. Wkly. Rep. 48: 189– 194.

26. Centers for Disease Control and Prevention. 1999. Outbreak of Salmonella serotype Muenchen infections associated with unpasteurized orange juice—United States and Canada, June 1999. Morb. Mortal. Wkly. Rep. 48: 582– 585.

27.Centers for Disease Control and Prevention. 1999. Salmonella fact sheets, Office of Communications, Atlanta, Ga.

28. Centers for Epidemiology and Animal Health. 1996. Biosecurity Practices of U.S. Dairy Herds. U.S. Department of Agriculture, Animal and Plant Health Inspection Services, Centers for Epidemiology and Animal Health, Fort Collins, Co.

29. Chriel, M.,, H. Stryhn,, and G. Dauphin. 1999. Generalised linear mixed models analysis of risk factors for contamination of Danish broiler flocks with Salmonella typhimurium. Prev. Vet. Med. 40: 1– 17.

30. Christensen, J.,, D. L. Baggesen,, V. Soerensen,, and B. Svensmark. 1999. Salmonella level of Danish swine herds based on serological examination of meat-juice samples and Salmonella occurrence measured by bacteriological follow-up. Prev. Vet. Med. 40: 277– 292.

31. Cohen, M. L.,, and R. V. Tauxe. 1986. Drug-resistant Salmonella in the United States: an epidemiologic perspective. Science 234: 964– 969.

32. Connerton, R.,, J. Wain,, T. T. Hien,, T. Ali,, C. Parry,, N. T. Chinh,, H. Vinh,, V. A. Ho,, T. S. Diep,, N. P. Day,, N. J. White,, G. Dougan,, and J. J. Farrar. 2000. Epidemic typhoid in Vietnam: molecular typing of multiple-antibiotic-resistant Salmonella enterica serotype Typhi from four outbreaks. J. Clin. Microbiol. 38: 895– 897.

33. Coulson, J. C.,, J. Butterfield,, and C. Thomas. 1983. The herring gull Larus argentatus as a likely transmitting agent of Salmonella montevideo to sheep and cattle. J. Hyg. (Lond.) 91: 437– 443.

34. Crowcroft, N. S.,, O. Ronveaux,, D. L. Monnet,, and R. Mertens. 1999. Methicillin-resist-ant Staphylococcus aureus and antimicrobial use in Belgian hospitals. Infect. Control Hosp. Epidemiol. 20: 31– 36.

35. Dahl, J.,, A. Wingstrand,, B. Nielsen,, and D. L. Baggesen. 1997. Elimination of Salmonella typhimurium infection by the strategic movement of pigs. Vet. Rec. 140: 679– 681.

36. Das, A. S.,, D. N. Mazumder,, D. Pal,, and U. K. Chattopadhyay. 1996. A study of nosocomial diarrhea in Calcutta. Indian J. Gastroenterol. 15: 12– 13.

37. Davies, R. H.,, and C. Wray. 1997. Distribution of salmonella contamination in ten animal feedmills. Vet. Microbiol. 57: 159– 169.

38. Davis, M. A.,, D. D. Hancock,, T. E. Besser,, D. H. Rice,, J. M. Gay,, C. Gay,, L. Gearhart,, and R. DiGiacomo. 1999. Changes in antimicrobial resistance among Salmonella enterica serovar Typhimurium isolates from humans and cattle in the northwestern United States. Emerg. Infect. Dis. 5: 802– 806.

39. Eld, K.,, A. Gunnarsson,, T. Holmberg,, B. Hurvell,, and M. Wierup. 1991. Salmonella isolated from animals and feedstuffs in Sweden during 1983-1987. Acta Vet. Scand. 32: 2261– 2277.

40. Evans, S.,, and R. Davies. 1996. Case control study of multiple resistant Salmonella Typhimurium DT104 infection in Great Britain. Vet. Rec. 139: 557– 558.

41. Fantasia, M.,, E. Filetici,, S. Arena,, and S. Mariotti. 1998. Serotype and phage type distribution of salmonellas from human and non-human sources in Italy in the period 1973-1995. Eur. J. Epidemiol. 14: 701– 710.

42. Fedorka-Cray, P. J.,, D. A. Dargatz,, L. A. Thomas,, and J. T. Gray. 1998. Survey of Salmonella serotypes in feedlot cattle. J. Food Prot. 61: 525– 530.

43. Fenlon, D. R. 1983. A comparison of salmonella serotypes found in the feces of gulls feeding at a sewage works with serotypes present in the sewage. J. Hyg. (Lond). 91: 47– 52.

44. Giraud, E.,, A. Brisabois,, J. L. Martel,, and E. Chaslus-Dancla. 1999. Comparative studies of mutations in animal isolates and experimental in vitro- and in vivo-selected mutants of Salmonella spp. suggest a counterselection of highly fluoroquinolone-resist-ant strains in the field. Antimicrob. Agents Chemother. 43: 2131– 2137.

45. Givney, R.,, A. Vickery,, A. Holliday,, M. Pegler,, and R. Benn. 1998. Evolution of an endemic methicillin-resistant Staphylococcus aureus population in an Australian hospital from 1967 to 1996. J. Clin. Microbiol. 36: 552– 556.

46. Glynn, M. K.,, C. Bopp,, M. S. Dewitt,, P. Dabney,, M. Mokhtar,, and F. J. Angulo. 1998. Emergence of multidrug-resistant Salmonella enterica serotype Typhimurium DTI04 infections in the United States. N. Engl. J. Med. 338: 1333– 1338.

47. Goldstein, F. W.,, and J. F. Acar. 1995. Epidemiology of quinolone resistance: Europe and North and South America. Drugs 49( Suppl.2): 36– 42.

48. Gracey, M.,, P. Ostergaard,, S. W. Adnan,, and J. B. Iveson. 1979. Fecal pollution of surface waters in Jakarta. Trans. R. Soc. Trop. Med. Hyg. 73: 306– 308.

49. Gracey, M.,, J. B. Iveson,, and S. Suharyono. 1980. Human salmonella carriers in a tropical urban environment. Trans. R. Soc. Trop. Med. Hyg. 74: 479– 482.

50. Hancock, D. D.,, S. E. Wikse,, A. B. Lichtenwalner,, R. B. Wescott,, and C. C Gay. 1989. Distribution of cysticercosis in Washington. Am. J. Vet. Res. 50: 564– 570.

51. Hancock, D. D.,, T. V. Lynn,, T. E. Besser,, and S. E. Wikse. 1997. Feasibility of preharvest food safety control. Compend. Contin. Ed. Pract. Vet. 19: S200.

52. Hardman, R. M.,, C. M. Wathes,, and C. Wray. 1991. Transmission of salmonellae among calves penned individually. Vet. Rec. 129: 327– 329.

53. Herikstad, H.,, P. Hayes,, M. Mokhtar,, M. L. Fracaro,, E. J. Threlfall,, and F. J. Angulo. 1997. Emerging quinolone-resistant Salmonella in the United States. Emerg. Infect. Dis. 3: 371– 372.

54. Hird, D. W.,, M. Pappaioanou,, and B. P. Smith. 1984. Case-control study of risk factors associated with isolation of Salmonella saintpaul in hospitalized horses. Am. J. Epidemiol. 120: 852– 864.

55. Hogue, A.,, J. Akkina,, F. Angulo,, R. Johnson,, K. Petersen,, S. Saini,, and W. Schlosser. 1997. Situation assessment: Salmonella typhimurium DT104. U.S. Department of Agriculture, Food Safety and Inspection Service, Washington, D.C.

56. Hollinger, K.,, C. Wray,, S. Evans,, S. Pascoe,, S. Chappell,, and Y. Jones. 1998. Salmonella typhimurium DT104 in cattle in Great Britain. J. Am. Vet. Med. Assoc. 213: 1732– 1733.

57. House, J. K.,, R. C. Mainar-Jaime,, B. P. Smith,, A. M. House,, and D. Y. Kamiya. 1999. Risk factors for nosocomial Salmonella infection among hospitalized horses. J. Am. Vet. Med. Assoc. 214: 1511– 1516.

58. Imberechts, H.,, M. De Filette,, C. Wray,, Y. Jones,, C. Godard,, and P. Pohl. 1998. Salmonella typhimurium phage type DT104 in Belgian livestock. Vet. Rec. 143: 424– 425.

59. Izumiya, H.,, K. Tamura,, J. Terajima,, and H. Watanabe. 1999. Salmonella enterica serovar Typhimurium phage type DT104 and other multi-drug resistant strains in Japan. Jpn. J. Infect. Dis. 52: 133.

60. Johnston, W. S.,, G. K. MacLachlan,, and G. F. Hopkins. 1979. The possible involvement of seagulls (Larus sp) in the transmission of salmonella in dairy cattle. Vet. Rec. 105: 526– 527.

61. Johnston, W. S.,, D. Munro,, W. J. Reilly,, and J. C. Sharp. 1981. An unusual sequel to imported Salmonella zanzibar. J. Hyg. (Lond.) 87: 525– 528.

62. Johnston, W. S.,, G. F. Hopkins,, G. K. Maclachlan,, and J. C. Sharp. 1986. Salmonella in sewage effluent and the relationship to animal and human disease in the north of Scotland. Vet. Rec. 119: 201– 203.

63. Jones, P. W.,, P. Collins,, G. T. H. Brown,, and M. Aitken. 1982. Transmission of Salmonella mbandaka to cattle from contaminated feed. J. Hyg. (Lond.) 88: 2255– 2263.

64. Kariuki, S.,, O. Olsvik,, E. Mitema,, J. Gathuma,, and N. Mirza. 1993. Acquired tetracycline resistance genes in nosocomial Salmonella typhimurium infection in a Kenyan hospital. East Afr. Med. J. 70: 255– 258.

65. Kariuki, S.,, C. Gilks,, J. Kimari,, A. Obanda,, J. Muyodi,, P. Waiyaki,, and C. A. Hart. 1999. Genotype analysis of Escherichia coli strains isolated from children and chickens living in close contact. Appl. Environ. Microbiol. 65: 472– 476.

66. Karpiskova, R.,, and M. Mikulaskova. 1995. Salmonella phage types distribution in the Czech Republic in 1991-1994. Cent. Eur. J. Public Health 3: 161– 162.

67. Khakhria, R.,, G. Bezanson,, D. Duck,, and H. Lior. 1983. The epidemic spread of Salmonella typhimurium phage type 10 in Canada (1970-1979). Can. J. Microbiol. 29: 1583– 1588.

68. Killalea, D.,, L. R. Ward,, D. Roberts,, J. de Louvois,, F. Sufi,, J. M. Stuart,, G. P. Wall,, M. Susman,, M. Schwieger,, P. J. Sanderson,, I. S. Fisher,, P. S. Mead,, O. N. Gill,, C. L. Bartlett,, and B. Rowe. 1996. International epidemiological and microbiological study of outbreak of Salmonella agona infection from a ready to eat savory snack. I. England and Wales and the United States. Br. Med. J. 313: 1105– 1107.

69. Kinde, H.,, D. H. Read,, A. Ardans,, R. E. Breitmeyer,, D. Willoughby,, H. E. Little,, D. Kerr,, R. Gireesh,, and K. V. Nagaraja. 1996. Sewage effluent: likely source of Salmonella enteritidis, phage type 4 infection in a commercial chicken layer flock in southern California. Avian Dis. 40: 672– 676.

70. Kinde, H.,, M. Adelson,, A. Ardans,, E. H. Little,, D. Willoughby,, D. Berchtold,, H. Read,, R. Breitmeyer,, D. Kerr,, R. V. Tarbell,, and E. D. Hughes. 1997. Prevalence of Salmonella in municipal sewage treatment plant effluents in southern California. Avian Dis. 41: 392– 398.

71. Krytenburg, D.,, D. D. Hancock,, D. H. Rice,, T. E. Besser,, C. C. Gay,, and J. M. Gay. 1998. Salmonella enterica in cattle feeds from the Pacific Northwest. Anim. Feed Sci. Technol. 75: 75– 79.

72. Lamb, V. A.,, C. G. Mayhall,, A. C. Spadora,, S. M. Markowitz,, J. J. Fanner 3d,, and H. P. Dalton. 1984. Outbreak of Salmonella typhimurium gastroenteritis due to an imported strain resistant to ampicillin, chloramphenicol, and trimethoprim-sulfamethoxazole in a nursery. J. Clin. Microbiol. 20: 1076– 1079.

73. Lance, S. E.,, G. Y. Miller,, D. D. Hancock,, P. C. Bartlett,, and L. E. Heider. 1992. Salmonella infections in neonatal dairy calves. J. Am. Vet. Med. Assoc. 201: 864– 868.

74. Ling, J.,, P. Y. Chau,, and B. Rowe. 1987. Salmonella serotypes and incidence of multiply-resistant salmonellae isolated from diarrheal patients in Hong Kong from 1973-82. Epidemiol. Infect. 99: 295– 306.

75. Low, J. C.,, M. Angus,, G. Hopkins,, D. Munro,, and S. C. Rankin. 1997. Antimicrobial resistance of Salmonella enterica typhimurium DTI 04 isolates and investigation of strains with transferable apramycin resistance. Epidemiol. Infect. 118: 97– 103.

76. Mahajan, R.,, M. Mathur,, A. Kumar,, P. Gupta,, M. M. Faridi,, and V. Talwar. 1995. Nosocomial outbreak of Salmonella typhimurium infection in a nursery intensive care unit (NICU) and pediatric ward. J. Commun. Dis. 27: 10– 14.

77. Mahipal, S.,, M. A. Chaudhry,, J. N. S. Yadava,, and S. C. Sanyal. 1992. The spectrum of antibiotic resistance in human and veterinary isolates of Escherichia coli collected from 1984-86 in Northern India. J. Antimicrob. Chem. 29: 159– 168.

78. Malmqvist, M.,, K. G. Jacobsson,, P. Haggblom,, F. Cerenius,, L. Sjoland,, and A. Gun-narsson. 1995. Salmonella isolated from animals and feedstuffs in Sweden during 1988-1992. Acta Vet. Scand. 36: 21– 39.

79. Malorny, B.,, A. Schroeter,, and R. Helmuth. 1999. Incidence of quinolone resistance over the period 1986 to 1998 in veterinary Salmonella isolates from Germany. Antimicrob. Agents Chemother. 43: 2278– 2282.

80. Matsushita, S.,, N. Konishi,, M. Arimatsu,, A. Kai,, S. Yamada,, S. Morozumi,, H. Izu-miya,, J. Terajima,, and H. Watanabe. 1999. Drug-resistance and definitive type 104 of Salmonella serovar typhimurium isolated from sporadic cases in Tokyo, 1980-1998. Kansenshogaku Zasshi 73: 1087– 1094.

81. McConnell, M. M.,, H. R. Smith,, J. Leonardopoulous,, and E. S. Anderson. 1979. The value of plasmid studies in the epidemiology of infections due to drug-resistant Salmonella wien. J. Infect. Dis. 139: 178– 190.

82. 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: 607– 625.

83. Melloul, A. A.,, and L. Hassani. 1999. Salmonella infection in children from the waste-water-spreading zone of Marrakesh city. J. Appl. Microbiol. 87: 536– 539.

84. Mermin, J. H.,, J. M. Townes,, M. Gerber,, N. Dolan,, E. D. Mintz,, and R. V. Tauxe. 1998. Typhoid fever in the United States, 1985-1994: changing risks of international travel and increasing antimicrobial resistance. Arch. Intern. Med. 158: 633– 638.

85. Metzer, E.,, V. Agmon,, N. Andoren,, and D. Cohen. 1998. Emergence of multidrug-resistant Salmonella enterica serotype Typhimurium phage-type DT104 among salmonellae causing enteritis in Israel. Epidemiol Infect. 121: 555– 559.

86. Mohan, V. P.,, K. B. Sharma,, D. S. Agarwal,, G. Purinima,, and P. K. Pillai. 1995. Plasmid profile and phage type of Salmonella typhimurium trains encountered in different regions of India. Comp. Immunol. Microbiol. Infect. Dis. 18: 283– 290.

87. Molbak, K.,, D. L. Baggesen,, F. M. Aarestrup,, J. M. Ebbesen,, J. Engberg,, K. Fryden-dahl,, P. Gerner-Smidt,, A. M. Petersen,, and H. C. Wegener. 1999. An outbreak of multidrug-resistant, quinolone-resistant Salmonella enterica serotype typhimurium DT104. N. Engl. J. Med. 341: 1420– 1425.

88. Nastasi, A.,, M. R. Villafrate,, and C. Mammina. 1990. Characterization of strains of Salmonella enterica subsp. enterica serovar Wien isolated in Italy: an epidemiological evaluation. Microbiologica 13: 317– 321.

89. Ottolenghi, A. C.,, and V. V. Hamparian. 1987. Multiyear study of sludge application to farmland: prevalence of bacterial enteric pathogens and antibody status of farm families. Appl. Environ. Microbiol. 53: 1118– 1124.

90. Pacer, R. E.,, J. S. Spika,, M. C. Thurmond,, N. Hargrett-Bean,, and M. E. Potter. 1989. Prevalence of Salmonella and multiple antimicrobial-resistant Salmonella in California dairies. J. Am. Vet. Med. Assoc. 195: 59– 63.

91. Patton, W. N.,, G. M. Smith,, M. J. Leyland,, and A. M. Geddes. 1985. Multiply resistant Salmonella typhimurium septicaemia in an immunocompromised patient successfully treated with ciprofloxacin. J. Antimicrob. Chemother. 16: 667– 669.

92. Pignato, S.,, A. Nastasi,, C. Mammina,, M. Fantasia,, and G. Giammanco. 1996. Phage types and ribotypes of Salmonella enteritidis in southern Italy. Zentralbl. Bakteriol. Milcrobiol. Hyg. Ser. A 283: 399– 405.

93. Poirel, L.,, M. Guibert,, S. Bellais,, T. Naas,, and P. Nordmann. 1999. Integron- and carbenicillinase-mediated reduced susceptibility to amoxicillin-clavulanic acid in isolates of multidrug-resistant Salmonella enterica serotype Typhimurium DT104 from French patients. Antimicrob. Agents Chemother. 43: 1098– 1104.

94. Poppe, C.,, N. Smart,, R. Khakhria,, W. Johnson,, J. Spika,, and J. Prescott. 1998. Salmonella typhimurium DT104: a virulent and drug-resistant pathogen. Can. Vet. J. 39: 559– 565.

95. Prager, R.,, A. Liesegang,, W. Rabsch,, B. Gericke,, W. Thiel,, W. Voigt,, R. Helmuth,, L. Ward,, and H. Tschape. 1999. Clonal relationship of Salmonella enterica serovar typhimurium phage type DT104 in Germany and Austria. Zentbl. Bakteriol. Mikrobiol. Hyg. Ser. A 289: 399– 414.

96. Puohiniemi, R.,, T. Heiskanen,, and A. Siitonen. 1997. Molecular epidemiology of two international sprout-borne Salmonella outbreaks. J. Clin. Microbiol. 35: 2487– 2491.

97. Radostits, O. M.,, D. C. Blood,, and C. C. Gay. 1994. Veterinary Medicine: A Textbook of the Diseases of Cattle, Sheep, Pigs, Goats, and Horses, 8th ed., p. 730– 745. Bailliére Tindall, London, United Kingdom.

98. Rao, P. S.,, V. Rajashekar,, G. K. Varghese,, and P. G. Shivananda. 1993. Emergence of multidrug-resistant Salmonella typhi in rural southern India. Am. J. Trop. Med. Hyg. 48: 108– 111.

99. Reilly, W. J.,, G. I. Forbes,, G. M. Paterson,, and J. C. Sharp. 1981. Human and animal salmonellosis in Scotland associated with environmental contamination, 1973-1979. Vet. Rec. 108: 553– 555.

100. Ridley, A.,, and E. J. Threlfall. 1998. Molecular epidemiology of antibiotic resistanc e genes in multiresistant epidemic Salmonella typhimurium DT 104. Microb. Drug Resist. 4: 113– 118.

101. Riley, L. W.,, B. S. Ceballos,, L. R. Trabulsi,, M. R. Fernandes de Toledo,, and P. A. Blake. 1984. The significance of hospitals as reservoirs for endemic multiresistant Salmonella typhimurium causing infection in urban Brazilian children. J. Infect. Dis. 150: 236– 241.

102. Rowe, B.,, E. J. Threlfall,, L. R. Ward,, and A. S. Ashley. 1979. International spread of multiresistant strains of Salmonella typhimurium phage types 204 and 193 from Britain to Europe. Vet. Rec. 105: 468– 469.

103. Rowe, B.,, L. R. Ward,, and E. J. Threlfall. 1997. Multidrug-resistant Salmonella typhi: a worldwide epidemic. Clin. Infect. Dis. 24( Suppl. 1): S106– S109.

104. Rubino, S.,, E. Muresu,, M. Solinas,, M. Santona,, B. Paglietti,, A. Azara,, A. Schiaffino,, A. Santona,, A. Maida,, and P. Cappuccinelli. 1999. IS200 fingerprint of Salmonella enterica serotype Typhimurium human strains isolated in Sardinia. Epidemiol. Infect. 120: 215– 222.

105. Saidi, S. M.,, Y. Iijima,, W. K. Sang,, A. K. Mwangudza,, J. O. Oundo,, K. Taga,, M. Aihara,, K. Nagayama,, H. Yamamoto,, P. G. Waiyaki,, and T. Honda. 1997. Epidemiological study on infectious diarrheal diseases in children in a coastal rural area of Kenya. Microbiol. Immunol. 41: 773– 778.

106. Sanches, I. S.,, Z. C. Saraiva,, T. C. Tendeiro,, J. M. Serra,, D. C. Dias,, and H. de Lencastre. 1998. Extensive intra-hospital spread of a methicillin-resistant staphylococcal clone. Int. J. Infect. Dis. 3: 26– 31.

107. Sandrou, D. K.,, and I. S. Arvanitoyannis. 1999. Implementation of hazard analysis critical control point in the meat and poultry industry. Food Rev. Int. 15: 265– 308.

108. Schrag, S. J.,, V. Perrot,, and B. R. Levin. 1997. Adaptation to the fitness costs of antibiotic resistance in Escherichia coli. Proc. R. Soc. Lond. B 264: 1287– 1291.

109. Seyfarth, A. M.,, H. C. Wegener,, and N. Frimodt-Moller. 1997. Antimicrobial resistance in Salmonella enterica subsp. enterica serovar typhimurium from humans and production animals. J. Antimicrob. Chemother. 40: 67– 75.

110. Sharma, K. B.,, M. B. Bhat,, A. Pasricha,, and S. Vaze. 1979. Multiple antibiotic resistance among salmonellae in India. J. Antimicrob. Chemother. 5: 15– 21.

111. Skov, M. N.,, O. Angen,, M. Chriel,, J. E. Olsen,, and M. Bisgaard. 1999. Risk factors associated with Salmonella enterica serovar typhimurium infection in Danish broiler flocks. Poult. Sci. 78: 848– 854.

112. Smith, B. P.,, L. Da Roden,, M. C. Thurmond,, G. W. Dilling,, H. Konrad,, J. A. Pelton,, and J. P. Picanso. 1994. Prevalence of salmonellae in cattle and in the environment on California dairies. J. Am. Vet. Med. Assoc. 205: 467– 471.

113. Tarr, P. E.,, L. Kuppens,, T. C. Jones,, B. Ivanoff,, P. G. Aparin,, and D. L. Heymann. 1999. Considerations regarding mass vaccination against typhoid fever as an adjunct to sanitation and public health measures: potential use in an epidemic in Tajikistan. Am. J. Trop. Med. Hyg. 61: 163– 170.

114. Terajima, J.,, A. Nakamura,, and H. Watanabe. 1998. Epidemiological analysis of Salmonella enterica Enteritidis isolates in Japan by phage-typing and pulsed-field gel electrophoresis. Epidemiol Infect. 120: 223– 229.

115. Threlfall, E. J.,, L. R. Ward,, and B. Rowe. 1978. Epidemic spread of a chloramphenicol-resistant strain of Salmonella typhimurium phage type 204 in bovine animals in Britain. Vet. Rec. 103: 438– 440.

116. Threlfall, E. J.,, B. Rowe,, J. L. Ferguson,, and L. R. Ward. 1985. Increasing incidence of resistance to gentamicin and related aminoglycosides in Salmonella typhimurium phage type 204c in England, Wales and Scotland. Vet. Rec. 117: 355– 357.

117. Threlfall, E. J.,, B. Rowe,, and L. R. Ward. 1993. A comparison of multiple drug resistance in salmonellas from humans and food animals in England and Wales, 1981 and 1990. Epidemiol. Infect. 111: 189– 197.

118. Threlfall, E. J.,, J. A. Frost,, L. R. Ward,, and B. Rowe. 1994. Epidemic in cattle and humans of Salmonella typhimurium DT 104 with chromosomally integrated multiple drug resistance. Vet. Rec. 134: 577.

119. Threlfall, E. J.,, F. J. Angulo,, and P. G. Wall. 1998. Ciprofloxacin-resistant Salmonella typhimurium DT104. Vet. Rec. 142: 255.

120. Threlfall, E. J.,, L. R. Ward,, M. D. Hampton,, A. M. Ridley,, B. Rowe,, D. Roberts,, R. J. Gilbert,, P. Van Someren,, P. G. Wall,, and P. Grimont. 1998. Molecular fingerprinting defines a strain of Salmonella enterica serotype Anatum responsible for an international outbreak associated with formula-dried milk. Epidemiol. Infect. 121: 289– 293.

121. Tillotson, K.,, C. J. Savage,, M. D. Salman,, C. R. Gentry-Weeks,, D. Rice,, P. J. Fedorka-Cray,, D. A. Hendrickson,, R. L. Jones,, W. Nelson,, and J. L. Traub-Dargatz. 1997. Outbreak of Salmonella infantis infection in a large animal veterinary teaching hospital. J. Am. Vet. Med. Assoc. 211: 1554– 1557.

122. Timoney, J. F.,, H. C. Neibert,, and F. W. Scott. 1978. Feline salmonellosis: a nosocomial outbreak and experimental studies. Cornell Vet. 68: 211– 219.

123. Trueman, K. F.,, R. J. Thomas,, A. R. MacKenzie,, L. E. Eaves,, and P. F. Duff. 1996. Salmonella dublin infection in Queensland dairy cattle. Aust. Vet. 74: 367– 369.

124. Turnidge, J. 1995. Epidemiology of quinolone resistance, Eastern hemisphere. Drugs 49 Suppl. 2: 43– 47.

125. Uhaa, I. J.,, D. W. Hird,, D. C. Hirsh,, and S. S. Jang. 1988. Case-control study of risk factors associated with nosocomial Salmonella krefeld infection in dogs. Am. J. Vet. Res. 49: 1501– 1505.

126. Vahaboglu, H.,, L. M. Hall,, L. Mulazimoglu,, S. Dodanli,, I. Yildirim,, and D. M. Liver-more. 1995. Resistance to extended-spectrum cephalosporins, caused by PER-1 beta-lac-tamase, in Salmonella typhimurium from Istanbul, Turkey. J. Med. Microbiol. 43: 294r– 299.

127. Vahaboglu, H.,, S. Dodanli,, C. Eroglu,, R. Ozturk,, G. Soyletir,, L. Yildirim,, and V. Avkan. 1996. Characterization of multiple-antibiotic-resistant Salmonella typhimurium strains: molecular epidemiology of PER-l-producing isolates and evidence for nosocomial plasmid exchange by a clone. J. Clin. Microbiol 34: 2942– 2946.

128. Van Beneden, C. A.,, W. E. Keene,, R. A. Strang,, D. H. Werker,, A. S. King,, B. Mahon,, K. Hedberg,, A. Bell,, M. T. Kelly,, V. K. Balan,, W. R. MacKenzie,, and D. Fleming. 1999. Multinational outbreak of Salmonella enterica serotype Newport infections due to contaminated alfalfa sprouts. JAMA 281: 158– 162.

129. van der Zee A.,, H. Verbakel,, J. C. van Zon,, I. Frenay,, A. van Belkum,, M. Peeters,, A. Suiting,, and A. Bergmans. 1999. Molecular genotyping of Staphylococcus aureus strains: comparison of repetitive element sequence-based PCR with various typing methods and isolation of a novel epidemicity marker. J. Clin. Microbiol 37: 342– 349.

130. Wall, P. G.,, D. Morgan,, K. Lamden,, M. Ryan,, M. Griffin, E. J. Threlfal,, L. R. Ward,, and B. Rowe. 1994. A case control study of infection with an epidemic strain of multiresistant Salmonella typhimurium DT104 in England and Wales. Commun. Dis. Rep. 14; 4: R130– 5.

131. Wall, P. G.,, E. J. Threlfall,, L. R. Ward,, and B. Rowe. 1996. Multiresistant Salmonella typhimurium DT104 in cats: a public health risk. Lancet 348: 471.

132. Wegener, H. C.,, D. L. Baggesen,, and K. Gaarslev. 1994. Salmonella typhimurium phage types from human salmonellosis in Denmark 1988-1993. APMIS 102: 521– 525.

133.World Health Organization. 1997. Multi-drug resistant Salmonella typhimurium. World Health Organization Fact Sheet 139. World Health Organization, Geneva, Switzerland.

134. Wray, C.,, J. N. Todd,, and M. Hinton. 1987. Epidemiology of Salmonella typhimurium infection in calves: excretion of S. typhimurium in the faeces of calves in different management systems. Vet. Rec. 121: 293– 296.

135. Wray, C.,, N. Todd,, I. McLaren,, Y. Beedell,, and B. Rowe. 1990. The epidemiology of Salmonella infection of calves: the role of dealers. Epidemiol Infect. 105: 295– 305.

136. Wray, C.,, N. Todd,, I. M. McLaren,, and Y. E. Beedell. 1991. The epidemiology of Salmonella in calves: the role of markets and vehicles. Epidemiol Infect. 107: 521– 525.

137. Yoder, D. R.,, E. D. Ebel,, D. D. Hancock,, and B. A. Combs. 1994. Investigation of an outbreak of bovine cysticercosis in an Idaho feedlot. J. Am. Vet. Med. Assoc. 205: 45– 50

Tables

The Global Epidemiology of Multiresistant Salmonella enterica Serovar Typhimurium DT104

[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555818050.chap11-1,webId=/content/author/10.1128/9781555818050.chap11-1,properties={foaf_givenname=Dale, foaf_name=Dale Hancock, foaf_surname=Hancock, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555818050.chap11-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555818050.chap11-2,webId=/content/author/10.1128/9781555818050.chap11-2,properties={foaf_givenname=John, foaf_name=John Gay, foaf_surname=Gay, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555818050.chap11-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555818050.chap11-3,webId=/content/author/10.1128/9781555818050.chap11-3,properties={foaf_givenname=Daniel, foaf_name=Daniel Rice, foaf_surname=Rice, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555818050.chap11-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555818050.chap11-4,webId=/content/author/10.1128/9781555818050.chap11-4,properties={foaf_givenname=Margaret, foaf_name=Margaret Davis, foaf_surname=Davis, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555818050.chap11-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555818050.chap11-5,webId=/content/author/10.1128/9781555818050.chap11-5,properties={foaf_givenname=Clive, foaf_name=Clive Gay, foaf_surname=Gay, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555818050.chap11-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555818050.chap11-6,webId=/content/author/10.1128/9781555818050.chap11-6,properties={foaf_givenname=Thomas, foaf_name=Thomas Besser, foaf_surname=Besser, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555818050.chap11-aff2]]}]]

/content/10.1128/9781555818050.chap11.tab11-1

Table 1

Year of first known isolations, by species and country, of serovar Typhimurium with resistance pattern ACSSuT and phage type 104 a

10.1128/9781555818050/tab11-1_thmb.gif

10.1128/9781555818050/tab11-1.gif

Table 1

Year of first known isolations, by species and country, of serovar Typhimurium with resistance pattern ACSSuT and phage type 104 a