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Trends in phage types of Salmonella enterica serovars Enteritidis and Typhimurium isolated in Slovakia from 1995 to 2009
Available online at www.sciencedirect.com
Diagnostic Microbiology and Infectious Disease 69 (2011) 454 – 456 www.elsevier.com/locate/diagmicrobio
Notes
Trends in phage types of Salmonella enterica serovars Enteritidis and Typhimurium isolated in Slovakia from 1995 to 2009 Lubica Majtanovaa,⁎, Juraj Majtana,b , Viktor Majtana a
National Reference Centre for Phage Typing of Salmonellae, Slovak Medical University, Limbova 14, 833 03, Bratislava, Slovakia b Institute of Zoology, Slovak Academy of Sciences, Dubravska cesta 9, 845 06 Bratislava, Slovakia Received 9 May 2010; accepted 19 October 2010
Abstract The phage typing of 3900 isolates of Salmonella Enteritidis and 1741 isolates of Salmonella Typhimurium has been carried out in the period 1995–2009. Among Salmonella Enteritidis in individual years, the most prevalent phage type (PT) was 8. The most predominant PTs of Salmonella Typhimurium were DT104 and U302. © 2011 Elsevier Inc. All rights reserved. Keywords: Phage type; Phage typing; Salmonella enterica; Serovars; Enteritidis; Typhimurium
Salmonella spp. continues to be important worldwide foodborne pathogens, causing infections in humans as well as in economically important animal groups. Despite of declining trend in reported cases of human salmonellosis in the European Union (EU) during the last 5 years (Lahuerta et al., 2010), infection with nontyphoidal Salmonella is still one of the most important causes of enteric illness in Slovakia (Hrivniaková and Sláčiková, 2009). Salmonella Enteritidis and Salmonella Typhimurium belong to the most common serovars isolated from human cases (Hrivniaková and Sláčiková, 2009). For epidemiologic purposes, differentiation of the strains of both serovars is essential; and phage typing has for decades been useful as a phenotypic, definitive method of choice in many countries. In Slovakia, phage typing as was described by the World Health Organization (WHO) Collaborative Centre for phage typing of Salmonella (Health Protection Agency, Colindale, London, UK) has been applied for surveillance of Salmonella Enteritidis and Salmonella Typhimurium in humans, food, and food production animals. Surveillance of human salmonella infections is coordinated in Slovakia by the National Reference Centre for Phage Typing of Salmonellae
⁎ Corresponding author. Tel.: +42-12-59370726; fax: +421-259370327. E-mail address: [email protected] (L. Majtanova). 0732-8893/$ – see front matter © 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.diagmicrobio.2010.10.017
(Slovak Medical University, Bratislava, Slovakia). In 1987, Ward et al. (1987) described a phage typing scheme for Salmonella Enteritidis. Nowadays, this typing system discriminates 96 phage types (PTs) using 17 typing phages. A typing scheme of Callow (1959) has been used for phage typing of Salmonella Typhimurium strains in Slovakia. Since 1997, the scheme of Anderson et al. (1977) has also been employed for phage typing. Anderson's phage typing system differentiates more than 200 PTs using 36 typing phages and additional 7 phages. Phage typing of both dominant Salmonella serovars has proven to be an important tool for strain characterization and the results obtained have been successfully used in surveillance, source attribute, and outbreak investigations (Baggesen and Wegener, 1994; Hald et al., 2007; Carrique-Mas et al., 2008; Farzan et al., 2008; Kasper et al., 2009). The purpose of this retrospective study was to provide insight into the trends of PT occurrence of Salmonella Enteritidis and Salmonella Typhimurium strains isolated from humans and food in Slovakia in the period from 1995 to 2009. The statistical analysis was performed by the χ2 test. A difference smaller than 0.05 was considered to be significant. A total of 3927 Salmonella Enteritidis and 1741 Salmonella Typhimurium strains that originated from different locations distributed throughout the country were isolated mainly from humans (stool) and partially also from food sources (eggs and meat). During the study period, there
L. Majtanova et al. / Diagnostic Microbiology and Infectious Disease 69 (2011) 454–456
Fig. 1. Distribution of Salmonella Enteritidis and Salmonella Typhimurium strains over the years 1995–2009 in the National Reference Centre for Phage Typing of Salmonellae. ⁎Statistically significant increasing trend of Salmonella Typhimurium occurrence (P b 0.001) was found.
was the high frequency of Salmonella Enteritidis isolates occurrence compared to Salmonella Typhimurium, except on 2005–2009, when a statistically significant increasing trend of Salmonella Typhimurium occurrence was found (P b 0.001) (Fig. 1). During the period, 3900 isolates of Salmonella Enteritidis were analyzed by phage typing. A total of 3346 (85.8%) human isolates collected from outbreaks or sporadic cases were isolated from feces, and 554 (14.2 %) strains originated from food, mainly from eggs and egg products. Salmonella Typhimurium strains were collected from sporadic cases, and the total number of strains isolated from feces was 1722 (98.9%). In the case of this serovar only, 19 (1.1%) strains were isolated from food source (pork meat). Recent reported data support the generally accepted perception that the main sources of Salmonella infections in humans are eggs, egg
455
products, and different types of meat in the EU (European Food Safety Authority, 2010). The typing schemes for both serovars were obtained from the WHO Collaborative Centre for Phage Typing of Salmonella (Colindale, London, UK) and used to further differentiate of these strains. The number of Salmonella Enteritidis and Salmonella Typhimurium isolates from individual years and the most dominant PTs are shown in Table 1. A total of 3802 (97.5%) isolates of Salmonella Enteritidis were typeable and belonged to different PTs. The strains from outbreaks were mainly PT8, further PT4 and PT6. The most predominant PT of Salmonella Enteritidis was PT8 over the period of study. A number of authors found PT4 as a predominant PT in European countries (Scuderi, 1999; Tschäpe et al., 1999; Cruchaga et al., 2001; Rabsch et al., 2001; van Duijkeren et al., 2002; Collard et al. 2008). The distribution of PTs among sporadic cases of Enteritidis isolates was similar to that among outbreak-associated cases. PT8, the predominant PT over 15 years, may suggest that common reservoirs of infection were responsible for salmonella infections. In addition to these observations, it was found that 183 strains of Salmonella Enteritidis with PT8 (67% of the total PT8 food isolates), 58 strains with PT4 (59% of the total PT4 food isolates), and 44 strains with PT6 (45% of the total PT6 food isolates) were isolated from eggs and egg products. A total of 1343 Salmonella Typhimurium strains (77.1%) were typeable and belonged to different PTs. Using the Callow typing scheme, the most frequent PT of Salmonella Typhimurium was 2b (Table 1). According to Anderson's typing scheme, DT104 PT was identified for the first time in 1997. This PT became the first or second most prevalent type, except in 2004 and 2007. The strains of this PT began to emerge as a problem in the 1980s and soon spread to humans and domestic animals around the world (Threlfall, 2000). A major concern about the emergence of
Table 1 The most frequent PTs and number of Salmonella Enteritidis strains from 1995 to 2009 Year
1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009
Salmonella Enteritids
Salmonella Typhimurium
Total number of strains
The most common PTs (% of total isolates)
Total number of strains
The most common PTs (% of total isolates)
735 186 144 274 175 201 197 153 316 285 347 257 285 207 165
PT8 (72.6), PT2 (8.5), PT4 (7.9) PT8 (83.9), PT4 (5.4), PT1 (4.8) PT8 (35.4, PT6 (30.6), PT1 (22.9) PT8 (57.7), PT4 (14.6), PT1 (11.3) PT8 (60.6), PT4 (9.1), PT26 (3.4) PT8 (73.6), PT4 (3.9), PT6 (3.9) PT8 (53.8), PT4 (19.8), PT2 (5.1) PT8 (62.8), PT13a (18.2), PT6 (4.7) PT8 (46.9), PT15 (10.2), PT4 (6.3) PT8 (53.6), PT6 (5.4), PT1b (5.4) PT8 (34.1), PT13a (26.4), PT19 (2.9) PT8 (52.0), PT13a (11.4), PT21c (7.5) PT8 (34.1), PT4 (30.1), PT6 (17.0) PT8 (48.3), PT6 (15.6), PT13 (7.8) PT8 (50.9), PT4 (20.0), PT13 (6.7)
61 46 6 14 18 70 83 15 95 53 177 195 239 287 382
2b (55.7), 2c (16.4) 2b (56.5), 2c (19.6) DT104 (66.7), 2 (33.3) 2b (42.9) 2b (50.0), DT104 (11.1) 2b (14.7), DT104 (7.4) 2b (34.9), DT104 (10.8), 1 var. 2 (1.2) DT104 (26.7), DT68 (13.3), DT193 (13.3) DT104 (43.2), DT41 (7.4), ST193 (4.2) DT104 (25.0), DT1 (9.6), DT2 (5.8) DT20a (40.4), DT120 (10.5), DT104 (8.2) DT104 (21.1), U302 (14.7), DT120 (10.0) U302 (25.1), DT120 (20.2), DT104 (15.7) DT104 (18.6), U302 (18.3), DT193 (12.9) U302 (19.1), DT104 (17.3), DT193 (14.1)
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L. Majtanova et al. / Diagnostic Microbiology and Infectious Disease 69 (2011) 454–456
Salmonella Typhimurium DT104 is the chromosomally encoded pentadrug resistance, which is a common characteristic of isolates from many different countries (van Duijkeren et al., 2002). Besides DT104, the most frequently identified PTs during the study were DT193, U302, DT20a, DT68, DT1, and DT2. The most commonly identified PTs of Salmonella Typhimurium from European countries were DT193, DT120, U302, U292, and DT104 (European Food Safety Authority, 2010). In addition to these results, U302 PT was identified as the most dominant PT in 8 isolates (42% of the total food isolates) that originated from food source (pork meat). Phage typing compared to genotyping methods such as pulse field gel electrophoresis and multilocus variablenumber tandem-repeat analysis is a cheap and less laborintensive method based on simple technology. Thus, a large number of Salmonella strains can be subjected for screening not only in the developed parts of the world but also in developing countries. On the other hand, phage typing depends very much on the experience of the individual laboratory and on support from the reference center that coordinates the maintenance of phages. Therefore, interpretation of results may vary between laboratories. Although phage typing as a phenotypic method currently has limitations, it plays an important role in surveillance and control of the common Salmonella serovars. The findings of both dominant Salmonella serovars (Enteritidis and Typhimurium) over 15 years showed that Enteritidis PT8 and Typhimurium PTs DT104 and U302 were the most prevalent in human and food.
Acknowledgments This work was supported by the Ministry of Health of the Slovak Republic under the project “Molecular analysis of antibiotic resistance of nontyphoid salmonella serovars”. The authors thank Dr Elizabeth de Pinna (Health Protection Agency, Colindale, London, UK) for providing of Salmonella specific phages and typing schemes.
References Anderson ES, Ward LR, de Saxe MJ, de Sa JHD (1977) Bacteriophagetyping designations of Salmonella typhimurium. J Hyg 78:297–300.
Baggesen DL, Wegener HC (1994) Phage types of Salmonella enterica ssp. enterica serovar typhimurium isolated from production animals and humans in Denmark. Acta Vet Scand 35:349–354. Callow BR (1959) A new phage-typing scheme for Salmonella typhimurium. J Hyg 57:349–359. Carrique-Mas JJ, Papadopoulou C, Evans SJ, Wales A, Teale CJ, Davies RH (2008) Trends in phage types and antimicrobial resistance of Salmonella enterica serovars Enteritidis isolated from animals in Great Britain from 1990 to 2005. Vet Rec 162:541–546. Collard JM, Bertrand S, Dierick K, Godard C, Wildemauwe C, Vermeersch K, Duenlot J, Immerseel F, Pasmans F, Imberechts H, Quinet C (2008) Drastic decrease of Salmonella Enteritidis isolated from humans in Belgium in 2005, shift in phage types and influence on foodborne outbreaks. Epidemiol Infect 136:771–781. Cruchaga S, Echeita A, Aladuena A, Garcia-Pena J, Frias N, Usera MA (2001) Antimicrobial resistance in salmonellae from humans, food and animals in Spain in 1998. J Antimicrob Chemother 47:315–321. European Food Safety Authority (2010) The community summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in the European Union in 2008. EFSA J 8:1496. Farzan A, Friendship RM, Dewey CE, Muckle AC, Gray JT, Funk J (2008) Distribution of Salmonella serovars and phage types on 80 Ontario swine farms in 2004. Can J Vet Res 72:1–6. Hald T, Lo Fo Wong DM, Aarestrup FM (2007) The attribution of human infections with antimicrobial resistant Salmonella bacteria in Denmark to sources of animal origin. Foodborne Pathog Dis 4:313–326. Hrivniaková L, Sláčiková M (2009) The occurrence of Salmonella infections in Slovak Republic during 2008. The scientific conference of Slovak national reference center for surveillance of infectious diseases. Abstract :21 (in Slovak). Kasper SS, Fretz R, Kornschober C, Allerberger F, Schmid D (2009) Imported Salmonella enteritidis cases: a multiphage outbreak among Austrian vacationers in Turkey, 2008. Wien Klin Wochenschr 121:144–148. Lahuerta A, Helwigh B, Mäkelä P (2010) Zoonoses in Europe distribution and trends—the EFSA-ECDC community summary report 2008. Euro Surrveill 15:19476. Rabsch W, Tschäpe H, Bäumler AJ (2001) Non-typhoidal salmonellosis: emerging problems. Microbes Infect 3:237–247. Scuderi G (1999) Epidemiology of Salmonella enterica serovar Enteritidis infections in Italy. In: Salmonella enterica serovar Enteritidis in humans and animals. Epidemiology, pathogenesis, and control. Saeed AM, Ed. Ames: Iowa State University Press, pp. 111–115. Threlfall EJ (2000) Epidemic Salmonella typhimurium DT104—a truly international multiresistant clone. J Antimicrob Chemother 46:7–10. Tschäpe H, Liesegang A, Gericke B, Prager R, Rabsch W, Helmuth R (1999) Ups and downs of Salmonella enterica serovar Enteritidis in Germany. In: Salmonella enterica serovar Enteritidis in humans and animals. Epidemiology, pathogenesis and control. Saeed AM, Ed. Ames: Iowa State University, Press, pp. 51–61. van Duijkeren E, Wannet WJB, Houwers DJ, van Pelt W (2002) Serotype and phage type distribution of Salmonella strains isolated from humans, cattle, pigs and chickens in the Netherlands from 1984 to 2001. J Clin Microbiol 40:3980–3985. Ward LR, de Sa JD, Rowe B (1987) A phage typing scheme for Salmonella enteritidis. Epidemiol Infect 99:291–294.
Diagnostic Microbiology and Infectious Disease 69 (2011) 454 – 456 www.elsevier.com/locate/diagmicrobio
Notes
Trends in phage types of Salmonella enterica serovars Enteritidis and Typhimurium isolated in Slovakia from 1995 to 2009 Lubica Majtanovaa,⁎, Juraj Majtana,b , Viktor Majtana a
National Reference Centre for Phage Typing of Salmonellae, Slovak Medical University, Limbova 14, 833 03, Bratislava, Slovakia b Institute of Zoology, Slovak Academy of Sciences, Dubravska cesta 9, 845 06 Bratislava, Slovakia Received 9 May 2010; accepted 19 October 2010
Abstract The phage typing of 3900 isolates of Salmonella Enteritidis and 1741 isolates of Salmonella Typhimurium has been carried out in the period 1995–2009. Among Salmonella Enteritidis in individual years, the most prevalent phage type (PT) was 8. The most predominant PTs of Salmonella Typhimurium were DT104 and U302. © 2011 Elsevier Inc. All rights reserved. Keywords: Phage type; Phage typing; Salmonella enterica; Serovars; Enteritidis; Typhimurium
Salmonella spp. continues to be important worldwide foodborne pathogens, causing infections in humans as well as in economically important animal groups. Despite of declining trend in reported cases of human salmonellosis in the European Union (EU) during the last 5 years (Lahuerta et al., 2010), infection with nontyphoidal Salmonella is still one of the most important causes of enteric illness in Slovakia (Hrivniaková and Sláčiková, 2009). Salmonella Enteritidis and Salmonella Typhimurium belong to the most common serovars isolated from human cases (Hrivniaková and Sláčiková, 2009). For epidemiologic purposes, differentiation of the strains of both serovars is essential; and phage typing has for decades been useful as a phenotypic, definitive method of choice in many countries. In Slovakia, phage typing as was described by the World Health Organization (WHO) Collaborative Centre for phage typing of Salmonella (Health Protection Agency, Colindale, London, UK) has been applied for surveillance of Salmonella Enteritidis and Salmonella Typhimurium in humans, food, and food production animals. Surveillance of human salmonella infections is coordinated in Slovakia by the National Reference Centre for Phage Typing of Salmonellae
⁎ Corresponding author. Tel.: +42-12-59370726; fax: +421-259370327. E-mail address: [email protected] (L. Majtanova). 0732-8893/$ – see front matter © 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.diagmicrobio.2010.10.017
(Slovak Medical University, Bratislava, Slovakia). In 1987, Ward et al. (1987) described a phage typing scheme for Salmonella Enteritidis. Nowadays, this typing system discriminates 96 phage types (PTs) using 17 typing phages. A typing scheme of Callow (1959) has been used for phage typing of Salmonella Typhimurium strains in Slovakia. Since 1997, the scheme of Anderson et al. (1977) has also been employed for phage typing. Anderson's phage typing system differentiates more than 200 PTs using 36 typing phages and additional 7 phages. Phage typing of both dominant Salmonella serovars has proven to be an important tool for strain characterization and the results obtained have been successfully used in surveillance, source attribute, and outbreak investigations (Baggesen and Wegener, 1994; Hald et al., 2007; Carrique-Mas et al., 2008; Farzan et al., 2008; Kasper et al., 2009). The purpose of this retrospective study was to provide insight into the trends of PT occurrence of Salmonella Enteritidis and Salmonella Typhimurium strains isolated from humans and food in Slovakia in the period from 1995 to 2009. The statistical analysis was performed by the χ2 test. A difference smaller than 0.05 was considered to be significant. A total of 3927 Salmonella Enteritidis and 1741 Salmonella Typhimurium strains that originated from different locations distributed throughout the country were isolated mainly from humans (stool) and partially also from food sources (eggs and meat). During the study period, there
L. Majtanova et al. / Diagnostic Microbiology and Infectious Disease 69 (2011) 454–456
Fig. 1. Distribution of Salmonella Enteritidis and Salmonella Typhimurium strains over the years 1995–2009 in the National Reference Centre for Phage Typing of Salmonellae. ⁎Statistically significant increasing trend of Salmonella Typhimurium occurrence (P b 0.001) was found.
was the high frequency of Salmonella Enteritidis isolates occurrence compared to Salmonella Typhimurium, except on 2005–2009, when a statistically significant increasing trend of Salmonella Typhimurium occurrence was found (P b 0.001) (Fig. 1). During the period, 3900 isolates of Salmonella Enteritidis were analyzed by phage typing. A total of 3346 (85.8%) human isolates collected from outbreaks or sporadic cases were isolated from feces, and 554 (14.2 %) strains originated from food, mainly from eggs and egg products. Salmonella Typhimurium strains were collected from sporadic cases, and the total number of strains isolated from feces was 1722 (98.9%). In the case of this serovar only, 19 (1.1%) strains were isolated from food source (pork meat). Recent reported data support the generally accepted perception that the main sources of Salmonella infections in humans are eggs, egg
455
products, and different types of meat in the EU (European Food Safety Authority, 2010). The typing schemes for both serovars were obtained from the WHO Collaborative Centre for Phage Typing of Salmonella (Colindale, London, UK) and used to further differentiate of these strains. The number of Salmonella Enteritidis and Salmonella Typhimurium isolates from individual years and the most dominant PTs are shown in Table 1. A total of 3802 (97.5%) isolates of Salmonella Enteritidis were typeable and belonged to different PTs. The strains from outbreaks were mainly PT8, further PT4 and PT6. The most predominant PT of Salmonella Enteritidis was PT8 over the period of study. A number of authors found PT4 as a predominant PT in European countries (Scuderi, 1999; Tschäpe et al., 1999; Cruchaga et al., 2001; Rabsch et al., 2001; van Duijkeren et al., 2002; Collard et al. 2008). The distribution of PTs among sporadic cases of Enteritidis isolates was similar to that among outbreak-associated cases. PT8, the predominant PT over 15 years, may suggest that common reservoirs of infection were responsible for salmonella infections. In addition to these observations, it was found that 183 strains of Salmonella Enteritidis with PT8 (67% of the total PT8 food isolates), 58 strains with PT4 (59% of the total PT4 food isolates), and 44 strains with PT6 (45% of the total PT6 food isolates) were isolated from eggs and egg products. A total of 1343 Salmonella Typhimurium strains (77.1%) were typeable and belonged to different PTs. Using the Callow typing scheme, the most frequent PT of Salmonella Typhimurium was 2b (Table 1). According to Anderson's typing scheme, DT104 PT was identified for the first time in 1997. This PT became the first or second most prevalent type, except in 2004 and 2007. The strains of this PT began to emerge as a problem in the 1980s and soon spread to humans and domestic animals around the world (Threlfall, 2000). A major concern about the emergence of
Table 1 The most frequent PTs and number of Salmonella Enteritidis strains from 1995 to 2009 Year
1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009
Salmonella Enteritids
Salmonella Typhimurium
Total number of strains
The most common PTs (% of total isolates)
Total number of strains
The most common PTs (% of total isolates)
735 186 144 274 175 201 197 153 316 285 347 257 285 207 165
PT8 (72.6), PT2 (8.5), PT4 (7.9) PT8 (83.9), PT4 (5.4), PT1 (4.8) PT8 (35.4, PT6 (30.6), PT1 (22.9) PT8 (57.7), PT4 (14.6), PT1 (11.3) PT8 (60.6), PT4 (9.1), PT26 (3.4) PT8 (73.6), PT4 (3.9), PT6 (3.9) PT8 (53.8), PT4 (19.8), PT2 (5.1) PT8 (62.8), PT13a (18.2), PT6 (4.7) PT8 (46.9), PT15 (10.2), PT4 (6.3) PT8 (53.6), PT6 (5.4), PT1b (5.4) PT8 (34.1), PT13a (26.4), PT19 (2.9) PT8 (52.0), PT13a (11.4), PT21c (7.5) PT8 (34.1), PT4 (30.1), PT6 (17.0) PT8 (48.3), PT6 (15.6), PT13 (7.8) PT8 (50.9), PT4 (20.0), PT13 (6.7)
61 46 6 14 18 70 83 15 95 53 177 195 239 287 382
2b (55.7), 2c (16.4) 2b (56.5), 2c (19.6) DT104 (66.7), 2 (33.3) 2b (42.9) 2b (50.0), DT104 (11.1) 2b (14.7), DT104 (7.4) 2b (34.9), DT104 (10.8), 1 var. 2 (1.2) DT104 (26.7), DT68 (13.3), DT193 (13.3) DT104 (43.2), DT41 (7.4), ST193 (4.2) DT104 (25.0), DT1 (9.6), DT2 (5.8) DT20a (40.4), DT120 (10.5), DT104 (8.2) DT104 (21.1), U302 (14.7), DT120 (10.0) U302 (25.1), DT120 (20.2), DT104 (15.7) DT104 (18.6), U302 (18.3), DT193 (12.9) U302 (19.1), DT104 (17.3), DT193 (14.1)
456
L. Majtanova et al. / Diagnostic Microbiology and Infectious Disease 69 (2011) 454–456
Salmonella Typhimurium DT104 is the chromosomally encoded pentadrug resistance, which is a common characteristic of isolates from many different countries (van Duijkeren et al., 2002). Besides DT104, the most frequently identified PTs during the study were DT193, U302, DT20a, DT68, DT1, and DT2. The most commonly identified PTs of Salmonella Typhimurium from European countries were DT193, DT120, U302, U292, and DT104 (European Food Safety Authority, 2010). In addition to these results, U302 PT was identified as the most dominant PT in 8 isolates (42% of the total food isolates) that originated from food source (pork meat). Phage typing compared to genotyping methods such as pulse field gel electrophoresis and multilocus variablenumber tandem-repeat analysis is a cheap and less laborintensive method based on simple technology. Thus, a large number of Salmonella strains can be subjected for screening not only in the developed parts of the world but also in developing countries. On the other hand, phage typing depends very much on the experience of the individual laboratory and on support from the reference center that coordinates the maintenance of phages. Therefore, interpretation of results may vary between laboratories. Although phage typing as a phenotypic method currently has limitations, it plays an important role in surveillance and control of the common Salmonella serovars. The findings of both dominant Salmonella serovars (Enteritidis and Typhimurium) over 15 years showed that Enteritidis PT8 and Typhimurium PTs DT104 and U302 were the most prevalent in human and food.
Acknowledgments This work was supported by the Ministry of Health of the Slovak Republic under the project “Molecular analysis of antibiotic resistance of nontyphoid salmonella serovars”. The authors thank Dr Elizabeth de Pinna (Health Protection Agency, Colindale, London, UK) for providing of Salmonella specific phages and typing schemes.
References Anderson ES, Ward LR, de Saxe MJ, de Sa JHD (1977) Bacteriophagetyping designations of Salmonella typhimurium. J Hyg 78:297–300.
Baggesen DL, Wegener HC (1994) Phage types of Salmonella enterica ssp. enterica serovar typhimurium isolated from production animals and humans in Denmark. Acta Vet Scand 35:349–354. Callow BR (1959) A new phage-typing scheme for Salmonella typhimurium. J Hyg 57:349–359. Carrique-Mas JJ, Papadopoulou C, Evans SJ, Wales A, Teale CJ, Davies RH (2008) Trends in phage types and antimicrobial resistance of Salmonella enterica serovars Enteritidis isolated from animals in Great Britain from 1990 to 2005. Vet Rec 162:541–546. Collard JM, Bertrand S, Dierick K, Godard C, Wildemauwe C, Vermeersch K, Duenlot J, Immerseel F, Pasmans F, Imberechts H, Quinet C (2008) Drastic decrease of Salmonella Enteritidis isolated from humans in Belgium in 2005, shift in phage types and influence on foodborne outbreaks. Epidemiol Infect 136:771–781. Cruchaga S, Echeita A, Aladuena A, Garcia-Pena J, Frias N, Usera MA (2001) Antimicrobial resistance in salmonellae from humans, food and animals in Spain in 1998. J Antimicrob Chemother 47:315–321. European Food Safety Authority (2010) The community summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in the European Union in 2008. EFSA J 8:1496. Farzan A, Friendship RM, Dewey CE, Muckle AC, Gray JT, Funk J (2008) Distribution of Salmonella serovars and phage types on 80 Ontario swine farms in 2004. Can J Vet Res 72:1–6. Hald T, Lo Fo Wong DM, Aarestrup FM (2007) The attribution of human infections with antimicrobial resistant Salmonella bacteria in Denmark to sources of animal origin. Foodborne Pathog Dis 4:313–326. Hrivniaková L, Sláčiková M (2009) The occurrence of Salmonella infections in Slovak Republic during 2008. The scientific conference of Slovak national reference center for surveillance of infectious diseases. Abstract :21 (in Slovak). Kasper SS, Fretz R, Kornschober C, Allerberger F, Schmid D (2009) Imported Salmonella enteritidis cases: a multiphage outbreak among Austrian vacationers in Turkey, 2008. Wien Klin Wochenschr 121:144–148. Lahuerta A, Helwigh B, Mäkelä P (2010) Zoonoses in Europe distribution and trends—the EFSA-ECDC community summary report 2008. Euro Surrveill 15:19476. Rabsch W, Tschäpe H, Bäumler AJ (2001) Non-typhoidal salmonellosis: emerging problems. Microbes Infect 3:237–247. Scuderi G (1999) Epidemiology of Salmonella enterica serovar Enteritidis infections in Italy. In: Salmonella enterica serovar Enteritidis in humans and animals. Epidemiology, pathogenesis, and control. Saeed AM, Ed. Ames: Iowa State University Press, pp. 111–115. Threlfall EJ (2000) Epidemic Salmonella typhimurium DT104—a truly international multiresistant clone. J Antimicrob Chemother 46:7–10. Tschäpe H, Liesegang A, Gericke B, Prager R, Rabsch W, Helmuth R (1999) Ups and downs of Salmonella enterica serovar Enteritidis in Germany. In: Salmonella enterica serovar Enteritidis in humans and animals. Epidemiology, pathogenesis and control. Saeed AM, Ed. Ames: Iowa State University, Press, pp. 51–61. van Duijkeren E, Wannet WJB, Houwers DJ, van Pelt W (2002) Serotype and phage type distribution of Salmonella strains isolated from humans, cattle, pigs and chickens in the Netherlands from 1984 to 2001. J Clin Microbiol 40:3980–3985. Ward LR, de Sa JD, Rowe B (1987) A phage typing scheme for Salmonella enteritidis. Epidemiol Infect 99:291–294.