Progression of Salmonella Enteritidis phage type 4 strains in São Paulo State, Brazil

Irino, K.; Fernandes, S.A.; Tavechio, A.T.; Neves, B.C.; Dias, A.M.G.

doi:10.1590/S0036-46651996000300005

Abstracts

A total of 574 S. Enteritidis strains (383 from human sources and 191 from non-human sources) isolated between 1975-95, in São Paulo State, Brazil, were phagetyped. Among the strains isolated during the period of 1975-92, 80.9% of them belonged to phage type 8 (PT-8), but in 1993 strains of PT-4 accounted for 65.2% of all the S. Enteritidis isolates. In the following years, PT-4 strains accounted for 99.7% and 98.4% of phagetyped S. Enteritidis strains. The results obtained suggested that the current epidemic of S. Enteritidis in São Paulo State is clearly associated with the progression of PT-4 strains.

Salmonella; S. Enteritidis; Phage types

Um total de 574 cepas de Salmonella Enteritidis isoladas no período 1975-95, em São Paulo, Brasil, foram fagotipadas. Entre estas cepas, 383 eram de origem humana e 191 isoladas de materiais de origem não humana. Verificou-se que a grande maioria (80.9%) das cepas isoladas até 1992 pertencia ao fagotipo 8 (PT-8) e que cepas do fagotipo 4 (PT-4) começaram a predominar a partir de 1993. Cepas deste fagotipo corresponderam em 1993, 1994 e 1995, respectivamente, a 65.2%, 99.7% e 98.4% das amostras fagotipadas. O aumento da S. Enteritidis em São Paulo está claramente associado a disseminação de cepas PT-4.

MICROBIOLOGY

Progression of Salmonella Enteritidis phage type 4 strains in São Paulo State, Brazil

Disseminação de cepas de Salmonella Enteritidis do fagotipo 4 (PT-4) em São Paulo, Brasil

K. Irino; S.A. Fernandes; A.T. Tavechio; B.C. Neves; A.M.G. Dias

^{Correspondence to} Correspondence to: Kinue Irino Instituto Adolfo Lutz Seção de Bacteriologia Av. Dr. Arnaldo, 355 01246-902 São Paulo, Brazil Tel.: 011-3061-0111 ramal 213. Fax: 011-853-3505

SUMMARY

A total of 574 S. Enteritidis strains (383 from human sources and 191 from non-human sources) isolated between 1975-95, in São Paulo State, Brazil, were phagetyped. Among the strains isolated during the period of 1975-92, 80.9% of them belonged to phage type 8 (PT-8), but in 1993 strains of PT-4 accounted for 65.2% of all the S. Enteritidis isolates. In the following years, PT-4 strains accounted for 99.7% and 98.4% of phagetyped S. Enteritidis strains. The results obtained suggested that the current epidemic of S. Enteritidis in São Paulo State is clearly associated with the progression of PT-4 strains.

Keywords:Salmonella; S. Enteritidis; Phage types.

RESUMO

Um total de 574 cepas de Salmonella Enteritidis isoladas no período 1975-95, em São Paulo, Brasil, foram fagotipadas. Entre estas cepas, 383 eram de origem humana e 191 isoladas de materiais de origem não humana. Verificou-se que a grande maioria (80.9%) das cepas isoladas até 1992 pertencia ao fagotipo 8 (PT-8) e que cepas do fagotipo 4 (PT-4) começaram a predominar a partir de 1993. Cepas deste fagotipo corresponderam em 1993, 1994 e 1995, respectivamente, a 65.2%, 99.7% e 98.4% das amostras fagotipadas. O aumento da S. Enteritidis em São Paulo está claramente associado a disseminação de cepas PT-4.

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ACKNOWLEDGMENTS

We are very grateful to Dr. B. Rowe from the Division of Enteric Pathogens, Central Public Health Laboratories, Colindale, London, UK, for providing S. Enteritidis phages and type strains. We would like to thank our collegues from Regional Laboratories who provided S. Enteritidis strains.

Recebido para publicação em 06/05/1996

Aceito para publicação em 02/07/1996

1. ALTEKRUSE, S.; KOEHLER, J.; HICKMAN-BRENNER, F.; TAUXE, R. V. & FERRIS, K. - A comparison of Salmonella enteritidis phage types from egg-associated outbreaks and implicated laying flocks. Epidem. Infect., 110: 17-22, 1993.
2. BINKIN, N.; SCUDERI, G.; NOVACO, F. et al. - Egg-related Salmonella enteritidis, Italy, 1991. Epidem. Infect., 110: 227-237, 1993.
3. CALZADA, C.T.; NEME, S.N.; IRINO, K. et al. Sorotipos de Salmonella identificados no período 1977-82, no Instituto Adolfo Lutz, Săo Paulo, Brasil. Rev. Inst. Adolfo Lutz, 44: 1-18, 1984.
4. CENTERS FOR DISEASE CONTROL - Outbreak of Salmonella enteritidis associated with nationally distributed ice cream products Minnesota, South Dakota, and Wisconsin, 1994. MMWR, 43: 740-741, 1994.
5. CENTERS FOR DISEASE CONTROL - Outbreak of Salmonella enteritidis associated with consumption of raw shell eggs, 1991. MMWR, 41: 369-372, 1992.
6. CLARK, G.M.; KAUFMANN, A.F. & GANGAROSA, E.J. Epidemiology of an international outbreak of Salmonella agona. Lancet, 11: 490-493, 1973.
7. FERNANDES, S.A.; TAVECHIO, A.T.; NEVES, B.C. et al. - Sahnonela Enteritidis: atual sorotipo no Estado de S. Paulo e susceptibilidade aos agentes antimicrobianos. In: CONGRESSO BRASILEIRO DE MICROBIOLOGIA, 18, Santos, 1995. p. 103, MMH 170.
8. HICKMAN-BRENNER, F.W.; STUBBS, A.D. & FARMER III, J.J. - Phage typing of Salmonella enteritidis in the United States. J. clin. Microbiol., 29: 2817-2823, 1991.
9. HINTON, M.; THRELFALL, E.J. & ROWE, B. - The invasiveness of different strains of Salmonella enteritidis phage type 4 for young chickens. FEMS Microbiol. Lett., 70: 193-196, 1990.
10. KATOULI, M.; SEUFFER, R.H.; WOLLIN, R.; KUHN, I. & MOLLBY, R. - Variations in biochemical phenotypes and phage types of Salmonella enteritidis in Germany 1980-92. Epidem. Infect., 111: 199-207, 1993.
11. KHAKHRIA, R.; DUCK, D. & LIOR, H. - Distribution of Salmonella enteritidis phage types in Canada. Epidem. Infect., 106: 25-32, 1991.
12. MORRIS Jr., J.G.; DWYER, D.M.; HOGE, C.W. et al. - Changing clonal patterns of Salmonella enteritidis in Maryland: evaluation of strains isolated between 1985 and 1990. J. clin. Microbiol., 30: 1301-1303, 1992.
13. PESSÔA, G.V.A.; IRINO, K.; CALZADA, C.T. et al. - Ocorręncia de bactérias enteropatogęnicas em Săo Paulo, no septenio 1970-76. I. Sorotipos de Salmonella isolados e identificados. Rev. Inst. Adolfo Lutz, 38: 87-105, 1978.
14. POHL, P.; LINTERMANS, P.; MARIN, M. & COUTURIER, M. - Epidemiological study of Salmonella enteritidis strains of animal origin in Belgium. Epidem. Infect., 106: 11-16, 1991.
15. POPPE, C.; IRWIN, R.J.; FORSBERG, C.M.; CLARKE, R.C. & OGGEL, J. - The prevalence of Salmonella enteritidis and other Salmonella spp. among Canadian registered commercial layer flocks. Epidem. Infect., 106: 259-270, 1991.
16. POPOFF, M.Y. & LE MINOR, L. - Formules antigéniques des sérovars de Salmonella. Paris, Centre Collaborateur OMS de Réference et de Recherches pour les Salmonella, 1992. p. 145.
17. RODRIGUE, D.C.; TAUXE, R.V. & ROWE, B. - International increase in Salmonella enteritidis: A new pandemic? Epidem. Infect., 105: 21-27, 1990.
18. ST. LOUIS, M.E.; MORSE, D.L.; POTTER, M.E. et al. - The emergence of grade A eggs as a major source of Salmonella enteritidis infections. J. Amer. med. Ass., 259: 2103-2107, 1988.
19. STALEY, J.; BURNENS, A.P.; THRELFALL, E.J.; CHOW-DRY, N. & GOLDSWORTHY, M. - Genetic relationship among strains of Salmonella enteritidis in a national epidemic in Switzerland. Epidem. Infect., 108: 213-220, 1992.
20. STEVENS, A.; JOSEPH, C.; BRUCE, J. et al. - A large outbreak of Salmonella enteritidis phage type 4 associated with eggs from overseas. Epidem. Infect., 103: 425-433, 1989.
21. TAUNAY, A.E. - Diagnóstico bacteriológico das salmonelas de origem animal: sua importância e freqüęncia no município de S. Paulo. Rev. Inst. Adolfo Lutz, 28: 43-69, 1968.
22. TAUNAY, A.E.; FERNANDES, S.A.; TAVECHIO, A.T. et al. - The role of Public Health Laboratory in the problem of salmonellosis in Săo Paulo State, Brazil. Rev. Inst. Med. trop. S. Paulo, 38: 119-129, 1996.
23. THRELFALL, E.J. & CHART, H. - Interrelationships between strains of Salmonella enteritidis. Epidem. Infect., 111: 1-8, 1993.
24. VAN DE GIESSEN, A.W.; DUFRENNE, J.B.; RITMEESTER, W.S. et al. - The identification of Salmonella enteritidis infected poultry flocks associated with an outbreak of human salmonellosis. Epidem. Infect., 109: 405-411, 1992.
25. WARD, L.R.; DE SA, J.D.H. & ROWE, B. A phage-typing scheme for Salmonella enteritidis. Epidem. Infect., 99: 291-294, 1987.
²⁶
WORLD HEALTH ORGANIZATION. Salmonellosis control: the role of animal and product hygiene. Wld. Hlth. Org. techn. Rep. Ser. (774), 1988.

Correspondence to:

Kinue Irino

Instituto Adolfo Lutz Seção de Bacteriologia

Av. Dr. Arnaldo, 355

01246-902 São Paulo, Brazil

Tel.: 011-3061-0111 ramal 213. Fax: 011-853-3505

Publication Dates

Publication in this collection
22 Sept 2006
Date of issue
June 1996

History

Accepted
02 July 1996
Received
06 May 1996

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

[1] 1. ALTEKRUSE, S.; KOEHLER, J.; HICKMAN-BRENNER, F.; TAUXE, R. V. & FERRIS, K. - A comparison of Salmonella enteritidis phage types from egg-associated outbreaks and implicated laying flocks. Epidem. Infect., 110: 17-22, 1993.

[2] 2. BINKIN, N.; SCUDERI, G.; NOVACO, F. et al. - Egg-related Salmonella enteritidis, Italy, 1991. Epidem. Infect., 110: 227-237, 1993.

[3] 3. CALZADA, C.T.; NEME, S.N.; IRINO, K. et al. Sorotipos de Salmonella identificados no período 1977-82, no Instituto Adolfo Lutz, Săo Paulo, Brasil. Rev. Inst. Adolfo Lutz, 44: 1-18, 1984.

[4] 4. CENTERS FOR DISEASE CONTROL - Outbreak of Salmonella enteritidis associated with nationally distributed ice cream products Minnesota, South Dakota, and Wisconsin, 1994. MMWR, 43: 740-741, 1994.

[5] 5. CENTERS FOR DISEASE CONTROL - Outbreak of Salmonella enteritidis associated with consumption of raw shell eggs, 1991. MMWR, 41: 369-372, 1992.

[6] 6. CLARK, G.M.; KAUFMANN, A.F. & GANGAROSA, E.J. Epidemiology of an international outbreak of Salmonella agona. Lancet, 11: 490-493, 1973.

[7] 7. FERNANDES, S.A.; TAVECHIO, A.T.; NEVES, B.C. et al. - Sahnonela Enteritidis: atual sorotipo no Estado de S. Paulo e susceptibilidade aos agentes antimicrobianos. In: CONGRESSO BRASILEIRO DE MICROBIOLOGIA, 18, Santos, 1995. p. 103, MMH 170.

[8] 8. HICKMAN-BRENNER, F.W.; STUBBS, A.D. & FARMER III, J.J. - Phage typing of Salmonella enteritidis in the United States. J. clin. Microbiol., 29: 2817-2823, 1991.

[9] 9. HINTON, M.; THRELFALL, E.J. & ROWE, B. - The invasiveness of different strains of Salmonella enteritidis phage type 4 for young chickens. FEMS Microbiol. Lett., 70: 193-196, 1990.

[10] 10. KATOULI, M.; SEUFFER, R.H.; WOLLIN, R.; KUHN, I. & MOLLBY, R. - Variations in biochemical phenotypes and phage types of Salmonella enteritidis in Germany 1980-92. Epidem. Infect., 111: 199-207, 1993.

[11] 11. KHAKHRIA, R.; DUCK, D. & LIOR, H. - Distribution of Salmonella enteritidis phage types in Canada. Epidem. Infect., 106: 25-32, 1991.

[12] 12. MORRIS Jr., J.G.; DWYER, D.M.; HOGE, C.W. et al. - Changing clonal patterns of Salmonella enteritidis in Maryland: evaluation of strains isolated between 1985 and 1990. J. clin. Microbiol., 30: 1301-1303, 1992.

[13] 13. PESSÔA, G.V.A.; IRINO, K.; CALZADA, C.T. et al. - Ocorręncia de bactérias enteropatogęnicas em Săo Paulo, no septenio 1970-76. I. Sorotipos de Salmonella isolados e identificados. Rev. Inst. Adolfo Lutz, 38: 87-105, 1978.

[14] 14. POHL, P.; LINTERMANS, P.; MARIN, M. & COUTURIER, M. - Epidemiological study of Salmonella enteritidis strains of animal origin in Belgium. Epidem. Infect., 106: 11-16, 1991.

[15] 15. POPPE, C.; IRWIN, R.J.; FORSBERG, C.M.; CLARKE, R.C. & OGGEL, J. - The prevalence of Salmonella enteritidis and other Salmonella spp. among Canadian registered commercial layer flocks. Epidem. Infect., 106: 259-270, 1991.

[16] 16. POPOFF, M.Y. & LE MINOR, L. - Formules antigéniques des sérovars de Salmonella. Paris, Centre Collaborateur OMS de Réference et de Recherches pour les Salmonella, 1992. p. 145.

[17] 17. RODRIGUE, D.C.; TAUXE, R.V. & ROWE, B. - International increase in Salmonella enteritidis: A new pandemic? Epidem. Infect., 105: 21-27, 1990.

[18] 18. ST. LOUIS, M.E.; MORSE, D.L.; POTTER, M.E. et al. - The emergence of grade A eggs as a major source of Salmonella enteritidis infections. J. Amer. med. Ass., 259: 2103-2107, 1988.

[19] 19. STALEY, J.; BURNENS, A.P.; THRELFALL, E.J.; CHOW-DRY, N. & GOLDSWORTHY, M. - Genetic relationship among strains of Salmonella enteritidis in a national epidemic in Switzerland. Epidem. Infect., 108: 213-220, 1992.

[20] 20. STEVENS, A.; JOSEPH, C.; BRUCE, J. et al. - A large outbreak of Salmonella enteritidis phage type 4 associated with eggs from overseas. Epidem. Infect., 103: 425-433, 1989.

[21] 21. TAUNAY, A.E. - Diagnóstico bacteriológico das salmonelas de origem animal: sua importância e freqüęncia no município de S. Paulo. Rev. Inst. Adolfo Lutz, 28: 43-69, 1968.

[22] 22. TAUNAY, A.E.; FERNANDES, S.A.; TAVECHIO, A.T. et al. - The role of Public Health Laboratory in the problem of salmonellosis in Săo Paulo State, Brazil. Rev. Inst. Med. trop. S. Paulo, 38: 119-129, 1996.

[23] 23. THRELFALL, E.J. & CHART, H. - Interrelationships between strains of Salmonella enteritidis. Epidem. Infect., 111: 1-8, 1993.

[24] 24. VAN DE GIESSEN, A.W.; DUFRENNE, J.B.; RITMEESTER, W.S. et al. - The identification of Salmonella enteritidis infected poultry flocks associated with an outbreak of human salmonellosis. Epidem. Infect., 109: 405-411, 1992.

[25] 25. WARD, L.R.; DE SA, J.D.H. & ROWE, B. A phage-typing scheme for Salmonella enteritidis. Epidem. Infect., 99: 291-294, 1987.

[26] ²⁶
WORLD HEALTH ORGANIZATION. Salmonellosis control: the role of animal and product hygiene. Wld. Hlth. Org. techn. Rep. Ser. (774), 1988.

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