Skip to main content
Top
Published in: BMC Infectious Diseases 1/2012

Open Access 01-12-2012 | Research article

Improving resolution of public health surveillance for human Salmonella entericaserovar Typhimurium infection: 3 years of prospective multiple-locus variable-number tandem-repeat analysis (MLVA)

Authors: Vitali Sintchenko, Qinning Wang, Peter Howard, Connie WY Ha, Katina Kardamanidis, Jennie Musto, Gwendolyn L Gilbert

Published in: BMC Infectious Diseases | Issue 1/2012

Login to get access

Abstract

Background

Prospective typing of Salmonella enterica serovar Typhimurium (STM) by multiple-locus variable-number tandem-repeat analysis (MLVA) can assist in identifying clusters of STM cases that might otherwise have gone unrecognised, as well as sources of sporadic and outbreak cases. This paper describes the dynamics of human STM infection in a prospective study of STM MLVA typing for public health surveillance.

Methods

During a three-year period between August 2007 and September 2010 all confirmed STM isolates were fingerprinted using MLVA as part of the New South Wales (NSW) state public health surveillance program.

Results

A total of 4,920 STM isolates were typed and a subset of 4,377 human isolates was included in the analysis. The STM spectrum was dominated by a small number of phage types, including DT170 (44.6% of all isolates), DT135 (13.9%), DT9 (10.8%), DT44 (4.5%) and DT126 (4.5%). There was a difference in the discriminatory power of MLVA types within endemic phage types: Simpson's index of diversity ranged from 0.109 and 0.113 for DTs 9 and 135 to 0.172 and 0.269 for DTs 170 and 44, respectively. 66 distinct STM clusters were observed ranging in size from 5 to 180 cases and in duration from 4 weeks to 25 weeks. 43 clusters had novel MLVA types and 23 represented recurrences of previously recorded MLVA types. The diversity of the STM population remained relatively constant over time. The gradual increase in the number of STM cases during the study was not related to significant changes in the number of clusters or their size. 667 different MLVA types or patterns were observed.

Conclusions

Prospective MLVA typing of STM allows the detection of community outbreaks and demonstrates the sustained level of STM diversity that accompanies the increasing incidence of human STM infections. The monitoring of novel and persistent MLVA types offers a new benchmark for STM surveillance.
A part of this study was presented at the MEEGID × (Molecular Epidemiology and Evolutionary Genetics of Infectious Diseases) Conference, 3-5 November 2010, Amsterdam, The Netherlands
Appendix
Available only for authorised users
Literature
1.
go back to reference Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'Brien SJ, et al: The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis. 2010, 50: 882-889. 10.1086/650733.CrossRefPubMed Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'Brien SJ, et al: The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis. 2010, 50: 882-889. 10.1086/650733.CrossRefPubMed
2.
go back to reference OzFoodNet Working G: Reported foodborne illness and gastroenteritis in Australia: annual report of the OzFoodNet network, 2004. Commun Dis Intell. 2005, 29 (2): 165-192. OzFoodNet Working G: Reported foodborne illness and gastroenteritis in Australia: annual report of the OzFoodNet network, 2004. Commun Dis Intell. 2005, 29 (2): 165-192.
3.
go back to reference Frenzen PDRT, Buzby JC, et al: Salmonella cost estimate updated using FoodNet data. Food Review. 1999, 22: 10-15. Frenzen PDRT, Buzby JC, et al: Salmonella cost estimate updated using FoodNet data. Food Review. 1999, 22: 10-15.
4.
go back to reference Jones TF, Schaffner W: Salmonella in imported mangos: shoeleather and contemporary epidemiologic techniques together meet the challenge. Clin Infect Dis. 2003, 37 (12): 1591-1592. 10.1086/379722.CrossRefPubMed Jones TF, Schaffner W: Salmonella in imported mangos: shoeleather and contemporary epidemiologic techniques together meet the challenge. Clin Infect Dis. 2003, 37 (12): 1591-1592. 10.1086/379722.CrossRefPubMed
5.
go back to reference Galanis EWD, Patrick ME, Binsztein N, Cieslik A, Chalermchaikit T, Aidera-Kane A, Ellis A, Angulo FJ, Wegener HC: Web-based surveillance and global Salmonella distribution, 2000-2002. Emerg Infect Dis. 2006, 12 (3): 381-388. 10.3201/eid1203.050854.CrossRefPubMedPubMedCentral Galanis EWD, Patrick ME, Binsztein N, Cieslik A, Chalermchaikit T, Aidera-Kane A, Ellis A, Angulo FJ, Wegener HC: Web-based surveillance and global Salmonella distribution, 2000-2002. Emerg Infect Dis. 2006, 12 (3): 381-388. 10.3201/eid1203.050854.CrossRefPubMedPubMedCentral
6.
go back to reference Hedberg CW, Greenblatt JF, Matyas BT, Lemmings J, Sharp DJ, Skibicki RT, Liang AP, for the Enteric Disease Investigation Timeline Study Work Group: Timeliness of enteric disease surveillance in 6 US states. Emerg Infect Dis. 2010, 14: 311-313.CrossRef Hedberg CW, Greenblatt JF, Matyas BT, Lemmings J, Sharp DJ, Skibicki RT, Liang AP, for the Enteric Disease Investigation Timeline Study Work Group: Timeliness of enteric disease surveillance in 6 US states. Emerg Infect Dis. 2010, 14: 311-313.CrossRef
7.
go back to reference Pearl D: The use of outbreak information in the interpretation of clustering of reported cases of Escherichia coli O157 in space and time in Alberta, Canada, 2000-2002. Epidemiol Infect 2006. 2006, 134 (4): 699-711.CrossRef Pearl D: The use of outbreak information in the interpretation of clustering of reported cases of Escherichia coli O157 in space and time in Alberta, Canada, 2000-2002. Epidemiol Infect 2006. 2006, 134 (4): 699-711.CrossRef
8.
go back to reference Graham SM: Nontyphoidal salmonellosis in Africa. Curr Opin Infect Dis. 2010, 23: 409-414. 10.1097/QCO.0b013e32833dd25d.CrossRefPubMed Graham SM: Nontyphoidal salmonellosis in Africa. Curr Opin Infect Dis. 2010, 23: 409-414. 10.1097/QCO.0b013e32833dd25d.CrossRefPubMed
9.
go back to reference Kingsley RA, Msefula CL, Thomson NR, Kariuki S, Holt KE, Gordon MA, Harris D, et al: Epidemic multiple drug resistant Salmonella Typhimurium causing invasive disease in sub-Saharan Africa have a distinct genotype. Genome Res. 2009, 19: 2279-2287. 10.1101/gr.091017.109.CrossRefPubMedPubMedCentral Kingsley RA, Msefula CL, Thomson NR, Kariuki S, Holt KE, Gordon MA, Harris D, et al: Epidemic multiple drug resistant Salmonella Typhimurium causing invasive disease in sub-Saharan Africa have a distinct genotype. Genome Res. 2009, 19: 2279-2287. 10.1101/gr.091017.109.CrossRefPubMedPubMedCentral
10.
go back to reference Rabsch W: Salmonella typhimurium phage typing for pathogens. Methods Mol Biol. 2007, 394: 177-211. 10.1007/978-1-59745-512-1_10.CrossRefPubMed Rabsch W: Salmonella typhimurium phage typing for pathogens. Methods Mol Biol. 2007, 394: 177-211. 10.1007/978-1-59745-512-1_10.CrossRefPubMed
11.
go back to reference Winokur PL: Molecular epidemiological techniques for Salmonella strain discrimination. Front Biosci. 2003, 8 (24): 1- Winokur PL: Molecular epidemiological techniques for Salmonella strain discrimination. Front Biosci. 2003, 8 (24): 1-
12.
go back to reference Jeoffreys NJ, James GS, Chiew R, Gilbert GL: Practical evaluation of molecular subtyping and phage typing in outbreaks of infection due to Salmonella enterica serotype typhimurium. Pathology. 2001, 33 (1): 66-72.CrossRefPubMed Jeoffreys NJ, James GS, Chiew R, Gilbert GL: Practical evaluation of molecular subtyping and phage typing in outbreaks of infection due to Salmonella enterica serotype typhimurium. Pathology. 2001, 33 (1): 66-72.CrossRefPubMed
13.
go back to reference Fakhr MK, Nolan LK, Logue CM: Multilocus sequence typing lacks the discriminatory ability of pulsed-field gel electrophoresis for typing Salmonella enterica serovar Typhimurium. J Clin Microbiol. 2005, 43 (5): 2215-2219. 10.1128/JCM.43.5.2215-2219.2005.CrossRefPubMedPubMedCentral Fakhr MK, Nolan LK, Logue CM: Multilocus sequence typing lacks the discriminatory ability of pulsed-field gel electrophoresis for typing Salmonella enterica serovar Typhimurium. J Clin Microbiol. 2005, 43 (5): 2215-2219. 10.1128/JCM.43.5.2215-2219.2005.CrossRefPubMedPubMedCentral
14.
go back to reference Lindstedt B-A, Vardund T, Aas L, Kapperud G: Multiple-locus variable-number tandem-repeats analysis of Salmonella enterica subsp. enterica serovar Typhimurium using PCR multiplexing and multicolor capillary electrophoresis. J Microbiol Methods. 2004, 59 (2): 163-172. 10.1016/j.mimet.2004.06.014.CrossRefPubMed Lindstedt B-A, Vardund T, Aas L, Kapperud G: Multiple-locus variable-number tandem-repeats analysis of Salmonella enterica subsp. enterica serovar Typhimurium using PCR multiplexing and multicolor capillary electrophoresis. J Microbiol Methods. 2004, 59 (2): 163-172. 10.1016/j.mimet.2004.06.014.CrossRefPubMed
15.
go back to reference Torpdahl M, Sørensen G, Lindstedt B-A, Nielsen EM: Tandem repeat analysis for surveillance of human Salmonella Typhimurium Infections. Emerg Infect Dis. 2007, 13 (3): 388-395. 10.3201/eid1303.060460.CrossRefPubMedPubMedCentral Torpdahl M, Sørensen G, Lindstedt B-A, Nielsen EM: Tandem repeat analysis for surveillance of human Salmonella Typhimurium Infections. Emerg Infect Dis. 2007, 13 (3): 388-395. 10.3201/eid1303.060460.CrossRefPubMedPubMedCentral
16.
go back to reference van Belkum A: Tracing isolates of bacterial species by multilocus variable number of tandem repeat analysis (MLVA). FEMS Immunol Med Microbiol. 2007, 49: 22-27. 10.1111/j.1574-695X.2006.00173.x.CrossRefPubMed van Belkum A: Tracing isolates of bacterial species by multilocus variable number of tandem repeat analysis (MLVA). FEMS Immunol Med Microbiol. 2007, 49: 22-27. 10.1111/j.1574-695X.2006.00173.x.CrossRefPubMed
17.
go back to reference Lindstedt B-A, Torpdahl M, Nielsen EM, Vardund T, Aas L, Kapperud G: Harmonization of the multiple-locus variable-number tandem repeat analysis method between Denmark and Norway for typing Salmonella Typhimurium isolates and closer examination of the VNTR loci. J Appl Microbiol. 2007, 102: 728-735. 10.1111/j.1365-2672.2006.03134.x.CrossRefPubMed Lindstedt B-A, Torpdahl M, Nielsen EM, Vardund T, Aas L, Kapperud G: Harmonization of the multiple-locus variable-number tandem repeat analysis method between Denmark and Norway for typing Salmonella Typhimurium isolates and closer examination of the VNTR loci. J Appl Microbiol. 2007, 102: 728-735. 10.1111/j.1365-2672.2006.03134.x.CrossRefPubMed
18.
go back to reference Malorny B, Junker E, Helmuth R: Multi-locus variable-number tandem repeat analysis for outbreak studies of Salmonella enterica serotype Enteritidis. BMC Microbiol. 2008, 8: 84-10.1186/1471-2180-8-84.CrossRefPubMedPubMedCentral Malorny B, Junker E, Helmuth R: Multi-locus variable-number tandem repeat analysis for outbreak studies of Salmonella enterica serotype Enteritidis. BMC Microbiol. 2008, 8: 84-10.1186/1471-2180-8-84.CrossRefPubMedPubMedCentral
19.
go back to reference Cho S, Whittam TS, Boxrud DJ, Bartkus JM, Rankin SC, Wilkins MJ, et al: Use of multiple-locus variable number tandem repeat analysis and phage typing for subtyping of Salmonella Enteritidis from sporadic human cases in the United States. J Appl Microbiol. 2009, 108: 859-867.CrossRefPubMed Cho S, Whittam TS, Boxrud DJ, Bartkus JM, Rankin SC, Wilkins MJ, et al: Use of multiple-locus variable number tandem repeat analysis and phage typing for subtyping of Salmonella Enteritidis from sporadic human cases in the United States. J Appl Microbiol. 2009, 108: 859-867.CrossRefPubMed
20.
go back to reference Dyet KH, Turbitt E, Carter PE: Multiple-locus variable-number tandem-repeat analysis for discriminating within Salmonella entericaserovar Typhimurium definitve types and investigation of outbreaks. Epidemiol Infect. 2010, Dyet KH, Turbitt E, Carter PE: Multiple-locus variable-number tandem-repeat analysis for discriminating within Salmonella entericaserovar Typhimurium definitve types and investigation of outbreaks. Epidemiol Infect. 2010,
21.
go back to reference Chiou C-S, Hung C-S, Torpdahl M, Watanabe H, Tung SK, Terajima J, Liang S-Y, Wang Y-W: Development and evaluation of multilocus variable number tandem repeat analysis for fine typing and phylogenetic analysis of Salmonella enterica serovar Typhimurium. Intern J Food Microbiol. 2010, 142: 67-73. 10.1016/j.ijfoodmicro.2010.06.001.CrossRef Chiou C-S, Hung C-S, Torpdahl M, Watanabe H, Tung SK, Terajima J, Liang S-Y, Wang Y-W: Development and evaluation of multilocus variable number tandem repeat analysis for fine typing and phylogenetic analysis of Salmonella enterica serovar Typhimurium. Intern J Food Microbiol. 2010, 142: 67-73. 10.1016/j.ijfoodmicro.2010.06.001.CrossRef
22.
go back to reference Gallego B, Sintchenko V, Wang Q, Hiley L, Gilbert GL, Coiera E: Biosurveillance of emerging biothreats using scalable genotype clustering. J Biomed Inform. 2009, 42 (1): 66-73. 10.1016/j.jbi.2008.07.002.CrossRefPubMed Gallego B, Sintchenko V, Wang Q, Hiley L, Gilbert GL, Coiera E: Biosurveillance of emerging biothreats using scalable genotype clustering. J Biomed Inform. 2009, 42 (1): 66-73. 10.1016/j.jbi.2008.07.002.CrossRefPubMed
23.
go back to reference Anderson ES, Ward LR, Saxe MJ, de Sa JD: Bacteriophage-typing designations of Salmonella typhimurium. J Hygiene. 1977, 78 (2): 297-300. 10.1017/S0022172400056187.CrossRef Anderson ES, Ward LR, Saxe MJ, de Sa JD: Bacteriophage-typing designations of Salmonella typhimurium. J Hygiene. 1977, 78 (2): 297-300. 10.1017/S0022172400056187.CrossRef
24.
go back to reference Gilbert GL: Using MLVA to type strains of Salmonella Typhimurium in New South Wales. New South Wales Public Health Bulletin. 2008, 19: 29-31. 10.1071/NB07116.CrossRefPubMed Gilbert GL: Using MLVA to type strains of Salmonella Typhimurium in New South Wales. New South Wales Public Health Bulletin. 2008, 19: 29-31. 10.1071/NB07116.CrossRefPubMed
26.
go back to reference Rounds JM, Hedberg CW, Meyer S, Boxrud DJ, Smith KE: Salmonella enterica pulsed-field gel electrophoresis clusters, Minnesota, USA, 2001-2007. Emerg Inf Dis. 2010, 16 (11): 1678-1685.CrossRef Rounds JM, Hedberg CW, Meyer S, Boxrud DJ, Smith KE: Salmonella enterica pulsed-field gel electrophoresis clusters, Minnesota, USA, 2001-2007. Emerg Inf Dis. 2010, 16 (11): 1678-1685.CrossRef
27.
go back to reference Hunter PR, Gaston MA: Numerical index of the discriminatory ability of typing systems: an application of Simpson's index of diversity. J Clin Microbiol. 1988, 26: 2465-2466.PubMedPubMedCentral Hunter PR, Gaston MA: Numerical index of the discriminatory ability of typing systems: an application of Simpson's index of diversity. J Clin Microbiol. 1988, 26: 2465-2466.PubMedPubMedCentral
28.
go back to reference Magurran AE: Ecological diversity and its measurement. 1988, Chapman & Hall, 169-CrossRef Magurran AE: Ecological diversity and its measurement. 1988, Chapman & Hall, 169-CrossRef
29.
go back to reference Sintchenko V, Gallego B: Laboratory-guided detection of disease outbreaks: three generations of surveillance systems. Arch Pathol Lab Med. 2009, 133 (6): 916-925.PubMed Sintchenko V, Gallego B: Laboratory-guided detection of disease outbreaks: three generations of surveillance systems. Arch Pathol Lab Med. 2009, 133 (6): 916-925.PubMed
30.
go back to reference Santos AC, Roberts JA, Cook AJC, Simons R, Sheehan R, Lane C, Adak GK, Clifton-Hadley FA, Rodrigues LC: Salmonella Typhimurium and Salmonella Enteritidis in England: cost to patients, their families, and primary and community health services of the NHS. Epidemiol Infect. 2010, 139 (5): 742-753.CrossRefPubMed Santos AC, Roberts JA, Cook AJC, Simons R, Sheehan R, Lane C, Adak GK, Clifton-Hadley FA, Rodrigues LC: Salmonella Typhimurium and Salmonella Enteritidis in England: cost to patients, their families, and primary and community health services of the NHS. Epidemiol Infect. 2010, 139 (5): 742-753.CrossRefPubMed
31.
go back to reference Prendergast DM, O'Grady D, Fanning S, Cormican M, Delappe N, Egan J, Mannion C, Fanning J, Gutierrez M: Application of multiple locus variable number of tandem repeat analysis (MLVA), phage typing and antimicrobial susceptibility testing to subtype Salmonella enterica serovar Typhimurium isolated from pig farms, pork slaughterhouses and meat producing plants in Ireland. Food Microbiol. 2011, 28: 1087-1094. 10.1016/j.fm.2011.02.013.CrossRefPubMed Prendergast DM, O'Grady D, Fanning S, Cormican M, Delappe N, Egan J, Mannion C, Fanning J, Gutierrez M: Application of multiple locus variable number of tandem repeat analysis (MLVA), phage typing and antimicrobial susceptibility testing to subtype Salmonella enterica serovar Typhimurium isolated from pig farms, pork slaughterhouses and meat producing plants in Ireland. Food Microbiol. 2011, 28: 1087-1094. 10.1016/j.fm.2011.02.013.CrossRefPubMed
32.
go back to reference Ethelberg S, Lisby M, Torpdahl M, Sørensen G, Neimann J, Rasmissen P, Bang S, Stamer U, Bertil Hansson H, Nygard K, Lau Baggesen D, Nielsen EM, Mølbak K, Helms M: Prolonged restaurant-associated outbreak of mutlidrug-resistant Salmonella Typhimurium among patients from several European countries. Clin Microbiol Infect. 2004, 10: 904-910. 10.1111/j.1469-0691.2004.00990.x.CrossRefPubMed Ethelberg S, Lisby M, Torpdahl M, Sørensen G, Neimann J, Rasmissen P, Bang S, Stamer U, Bertil Hansson H, Nygard K, Lau Baggesen D, Nielsen EM, Mølbak K, Helms M: Prolonged restaurant-associated outbreak of mutlidrug-resistant Salmonella Typhimurium among patients from several European countries. Clin Microbiol Infect. 2004, 10: 904-910. 10.1111/j.1469-0691.2004.00990.x.CrossRefPubMed
33.
go back to reference Hall R: Outbreak of gastroenteritis due to Salmonella typhimurium phage type 135a following consumption of raw egg. Commun Dis Intell. 2002, 26 (2): 285-287. Hall R: Outbreak of gastroenteritis due to Salmonella typhimurium phage type 135a following consumption of raw egg. Commun Dis Intell. 2002, 26 (2): 285-287.
34.
go back to reference Reynolds A, Moffatt CRM, Dyda A, Hundy RL, Kaye AL, Krsteski R, Rockliff S, Kampen R, Kelly PM, O'Brien ED: An outbreak of gastroenteritis due to Salmonella Typhimurium phage type 170 associated with consumption of a dessert containing raw egg. Commun Dis Intell. 2010, 34: 329-333. Reynolds A, Moffatt CRM, Dyda A, Hundy RL, Kaye AL, Krsteski R, Rockliff S, Kampen R, Kelly PM, O'Brien ED: An outbreak of gastroenteritis due to Salmonella Typhimurium phage type 170 associated with consumption of a dessert containing raw egg. Commun Dis Intell. 2010, 34: 329-333.
35.
go back to reference Hopkins KL, Maguire C, Best E, Liebana E, Threlfall EJ: Stability of multiple-locus variable-number tandem repeats in Salmonella enterica Serovar Typhimurium. J Clin Microbiol. 2007, 45: 3058-3061. 10.1128/JCM.00715-07.CrossRefPubMedPubMedCentral Hopkins KL, Maguire C, Best E, Liebana E, Threlfall EJ: Stability of multiple-locus variable-number tandem repeats in Salmonella enterica Serovar Typhimurium. J Clin Microbiol. 2007, 45: 3058-3061. 10.1128/JCM.00715-07.CrossRefPubMedPubMedCentral
Metadata
Title
Improving resolution of public health surveillance for human Salmonella entericaserovar Typhimurium infection: 3 years of prospective multiple-locus variable-number tandem-repeat analysis (MLVA)
Authors
Vitali Sintchenko
Qinning Wang
Peter Howard
Connie WY Ha
Katina Kardamanidis
Jennie Musto
Gwendolyn L Gilbert
Publication date
01-12-2012
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2012
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/1471-2334-12-78

Other articles of this Issue 1/2012

BMC Infectious Diseases 1/2012 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.