Skip to main content
Top
Published in: BMC Public Health 1/2015

Open Access 01-12-2015 | Research article

Spatial-temporal epidemiology of human Salmonella Enteritidis infections with major phage types (PTs 1, 4, 5b, 8, 13, and 13a) in Ontario, Canada, 2008–2009

Authors: Csaba Varga, David L. Pearl, Scott A. McEwen, Jan M. Sargeant, Frank Pollari, Michele T. Guerin

Published in: BMC Public Health | Issue 1/2015

Login to get access

Abstract

Background

In Ontario and Canada, the incidence of human Salmonella enterica serotype Enteritidis (S. Enteritidis) infections have increased steadily during the last decade. Our study evaluated the spatial and temporal epidemiology of the major phage types (PTs) of S. Enteritidis infections to aid public health practitioners design effective prevention and control programs.

Methods

Data on S. Enteritidis infections between January 1, 2008 and December 31, 2009 were obtained from Ontario’s disease surveillance system. Salmonella Enteritidis infections with major phage types were classified by their annual health region-level incidence rates (IRs), monthly IRs, clinical symptoms, and exposure settings. A scan statistic was employed to detect retrospective phage type-specific spatial, temporal, and space-time clusters of S. Enteritidis infections. Space-time cluster cases’ exposure settings were evaluated to identify common exposures.

Results

1,336 cases were available for analysis. The six most frequently reported S. Enteritidis PTs were 8 (n = 398), 13a (n = 218), 13 (n = 198), 1 (n = 132), 5b (n = 83), and 4 (n = 76). Reported rates of S. Enteritidis infections with major phage types varied by health region and month. International travel and unknown exposure settings were the most frequently reported settings for PT 5b, 4, and 1 cases, whereas unknown exposure setting, private home, food premise, and international travel were the most frequently reported settings for PT 8, 13, and 13a cases.
Diarrhea, abdominal pain, and fever were the most commonly reported clinical symptoms. A number of phage type-specific spatial, temporal, and space-time clusters were identified. Space-time clusters of PTs 1, 4, and 5b occurred mainly during the winter and spring months in the North West, North East, Eastern, Central East, and Central West regions. Space-time clusters of PTs 13 and 13a occurred at different times of the year in the Toronto region. Space-time clusters of PT 8 occurred at different times of the year in the North West and South West regions.

Conclusions

Phage type-specific differences in exposure settings, and spatial-temporal clustering of S. Enteritidis infections were demonstrated that might guide public health surveillance of disease outbreaks. Our study methodology could be applied to other foodborne disease surveillance data to detect retrospective high disease rate clusters, which could aid public health authorities in developing effective prevention and control programs.
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(6):882–9.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(6):882–9.CrossRefPubMed
2.
go back to reference Ruzante JM, Majowicz SE, Fazil A, Davidson VJ. Hospitalization and deaths for select enteric illnesses and associated sequelae in Canada, 2001–2004. Epidemiol Infect. 2011;139(6):937–45.CrossRefPubMed Ruzante JM, Majowicz SE, Fazil A, Davidson VJ. Hospitalization and deaths for select enteric illnesses and associated sequelae in Canada, 2001–2004. Epidemiol Infect. 2011;139(6):937–45.CrossRefPubMed
3.
go back to reference Thomas MK, Murray R, Flockhart L, Pintar K, Pollari F, Fazil A, et al. Estimates of the burden of foodborne illness in Canada for 30 specified pathogens and unspecified agents, circa 2006. Foodborne Pathog Dis. 2013;10(7):639–48.CrossRefPubMedPubMedCentral Thomas MK, Murray R, Flockhart L, Pintar K, Pollari F, Fazil A, et al. Estimates of the burden of foodborne illness in Canada for 30 specified pathogens and unspecified agents, circa 2006. Foodborne Pathog Dis. 2013;10(7):639–48.CrossRefPubMedPubMedCentral
7.
go back to reference European Food Safety Authority (EFSA). The Community Summary Report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in the European Union in 2008. EFSA J. 2010;8(1):1496.CrossRef European Food Safety Authority (EFSA). The Community Summary Report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in the European Union in 2008. EFSA J. 2010;8(1):1496.CrossRef
8.
go back to reference Varga C, Middleton D, Walton R, Savage R, Tighe MK, Allen V, et al. Evaluating risk factors for endemic human Salmonella Enteritidis infections with different phage types in Ontario. Canada using multinomial logistic regression and a case-case study approach. BMC Public Health. 2012;12:866.CrossRefPubMedPubMedCentral Varga C, Middleton D, Walton R, Savage R, Tighe MK, Allen V, et al. Evaluating risk factors for endemic human Salmonella Enteritidis infections with different phage types in Ontario. Canada using multinomial logistic regression and a case-case study approach. BMC Public Health. 2012;12:866.CrossRefPubMedPubMedCentral
9.
go back to reference Taylor M, Leslie M, Ritson M, Stone J, Cox W, Hoang L, et al. Investigation of the concurrent emergence of Salmonella enteritidis in humans and poultry in British Columbia, Canada, 2008-2010. Zoonoses Public Health. 2012;59(8):584–92.CrossRefPubMed Taylor M, Leslie M, Ritson M, Stone J, Cox W, Hoang L, et al. Investigation of the concurrent emergence of Salmonella enteritidis in humans and poultry in British Columbia, Canada, 2008-2010. Zoonoses Public Health. 2012;59(8):584–92.CrossRefPubMed
10.
go back to reference Centers for Disease Control and Prevention (CDC). Salmonella enteritidis infections associated with foods purchased from mobile lunch trucks - Alberta, Canada, October 2010-February. MMWR Morb Mortal Wkly Rep 2013. 2011;62(28):567–9. Centers for Disease Control and Prevention (CDC). Salmonella enteritidis infections associated with foods purchased from mobile lunch trucks - Alberta, Canada, October 2010-February. MMWR Morb Mortal Wkly Rep 2013. 2011;62(28):567–9.
11.
go back to reference Marcus R, Varma JK, Medus C, Boothe EJ, Anderson BJ, Crume T, et al. Re-assessment of risk factors for sporadic Salmonella serotype Enteritidis infections: a case–control study in five FoodNet Sites, 2002–2003. Epidemiol Infect. 2007;135(1):84–92.CrossRefPubMed Marcus R, Varma JK, Medus C, Boothe EJ, Anderson BJ, Crume T, et al. Re-assessment of risk factors for sporadic Salmonella serotype Enteritidis infections: a case–control study in five FoodNet Sites, 2002–2003. Epidemiol Infect. 2007;135(1):84–92.CrossRefPubMed
12.
go back to reference Lee SS, Wong NS. The clustering and transmission dynamics of pandemic influenza A (H1N1) 2009 cases in Hong Kong. J Infect. 2011;63(4):274–80.CrossRefPubMed Lee SS, Wong NS. The clustering and transmission dynamics of pandemic influenza A (H1N1) 2009 cases in Hong Kong. J Infect. 2011;63(4):274–80.CrossRefPubMed
13.
go back to reference So HC, Pearl DL, von Königslöw T, Louie M, Chui L, Svenson LW. Spatio-temporal scan statistics for the detection of outbreaks involving common molecular subtypes: using human cases of Escherichia coli O157:H7 provincial PFGE pattern 8 (National Designation ECXAI.0001) in Alberta as an example. Zoonoses Public Health. 2013;60(5):341–8.CrossRefPubMed So HC, Pearl DL, von Königslöw T, Louie M, Chui L, Svenson LW. Spatio-temporal scan statistics for the detection of outbreaks involving common molecular subtypes: using human cases of Escherichia coli O157:H7 provincial PFGE pattern 8 (National Designation ECXAI.0001) in Alberta as an example. Zoonoses Public Health. 2013;60(5):341–8.CrossRefPubMed
14.
15.
go back to reference Wang T, Xue F, Chen Y, Ma Y, Liu Y. The spatial epidemiology of tuberculosis in Linyi City, China, 2005-2010. BMC Public Health.2012; 12:885. Wang T, Xue F, Chen Y, Ma Y, Liu Y. The spatial epidemiology of tuberculosis in Linyi City, China, 2005-2010. BMC Public Health.2012; 12:885.
16.
go back to reference Torabi M, Rosychuk RJ. An examination of five spatial disease clustering methodologies for the identification of childhood cancer clusters in Alberta, Canada. Spat Spatiotemporal Epidemiol. 2011;2(4):321–30.CrossRefPubMed Torabi M, Rosychuk RJ. An examination of five spatial disease clustering methodologies for the identification of childhood cancer clusters in Alberta, Canada. Spat Spatiotemporal Epidemiol. 2011;2(4):321–30.CrossRefPubMed
17.
go back to reference Varga C, Pearl DL, McEwen SA, Sargeant JM, Pollari F, Guerin MT. Incidence, distribution, seasonality, and demographic risk factors of Salmonella Enteritidis human infections in Ontario, Canada, 2007-2009. BMC Infect Dis. 2013;13:212.CrossRefPubMedPubMedCentral Varga C, Pearl DL, McEwen SA, Sargeant JM, Pollari F, Guerin MT. Incidence, distribution, seasonality, and demographic risk factors of Salmonella Enteritidis human infections in Ontario, Canada, 2007-2009. BMC Infect Dis. 2013;13:212.CrossRefPubMedPubMedCentral
18.
go back to reference Middleton D, Savage R, Tighe MK, Vrbova L, Walton R, Whitfield Y, et al. Risk factors for sporadic domestically acquired Salmonella serovar Enteritidis infections: a case-control study in Ontario, Canada. Epidemiol Infect 2013. 2011;142(7):1411–21.CrossRef Middleton D, Savage R, Tighe MK, Vrbova L, Walton R, Whitfield Y, et al. Risk factors for sporadic domestically acquired Salmonella serovar Enteritidis infections: a case-control study in Ontario, Canada. Epidemiol Infect 2013. 2011;142(7):1411–21.CrossRef
19.
go back to reference Nesbitt A, Ravel A, Murray R, McCormick R, Savelli C, Finley R, et al. Integrated surveillance and potential sources of Salmonella Enteritidis in human cases in Canada from 2003 to 2009. Epidemiol Infect. 2012;140(10):1757–72.CrossRefPubMed Nesbitt A, Ravel A, Murray R, McCormick R, Savelli C, Finley R, et al. Integrated surveillance and potential sources of Salmonella Enteritidis in human cases in Canada from 2003 to 2009. Epidemiol Infect. 2012;140(10):1757–72.CrossRefPubMed
20.
go back to reference Tighe MK, Savage R, Vrbova L, Toolan M, Whitfield Y, Varga C, et al. The epidemiology of travel-related Salmonella Enteritidis in Ontario, Canada, 2010-2011. BMC Public Health. 2012;12(1):310.CrossRefPubMedPubMedCentral Tighe MK, Savage R, Vrbova L, Toolan M, Whitfield Y, Varga C, et al. The epidemiology of travel-related Salmonella Enteritidis in Ontario, Canada, 2010-2011. BMC Public Health. 2012;12(1):310.CrossRefPubMedPubMedCentral
21.
go back to reference Arcury TA, Gesler WM, Preisser JS, Sherman J, Spencer J, Perin J. The effects of geography and spatial behavior on health care utilization among the residents of a rural region. Heal Serv Res. 2005;40(1):135–56.CrossRef Arcury TA, Gesler WM, Preisser JS, Sherman J, Spencer J, Perin J. The effects of geography and spatial behavior on health care utilization among the residents of a rural region. Heal Serv Res. 2005;40(1):135–56.CrossRef
23.
go back to reference Government of Ontario. Health Protection and Promotion Act R.S.O.1990 H.7. 1990 Part VI. 77.6 (1) - 77.6 (7). Government of Ontario. Health Protection and Promotion Act R.S.O.1990 H.7. 1990 Part VI. 77.6 (1) - 77.6 (7). 
25.
go back to reference Bale JA, de Pinna EM, Threlfall EJ, Ward LR. Kauffmann-White Scheme - 2007: Salmonella Identification - Serotypes and Antigenic Formulae. London: Health Protection Agency; 2007. Bale JA, de Pinna EM, Threlfall EJ, Ward LR. Kauffmann-White Scheme - 2007: Salmonella Identification - Serotypes and Antigenic Formulae. London: Health Protection Agency; 2007.
28.
29.
30.
go back to reference Kulldorff M, Athas W, Feuer E, Miller B, Key C. Evaluating cluster alarms: A space-time scan statistic and brain cancer in Los Alamos. Am J Public Health. 1998;88:1377–80.CrossRefPubMedPubMedCentral Kulldorff M, Athas W, Feuer E, Miller B, Key C. Evaluating cluster alarms: A space-time scan statistic and brain cancer in Los Alamos. Am J Public Health. 1998;88:1377–80.CrossRefPubMedPubMedCentral
31.
go back to reference Besag J, Clifford J. Sequential Monte Carlo p-values. Biometrika. 1991;78:301–30.CrossRef Besag J, Clifford J. Sequential Monte Carlo p-values. Biometrika. 1991;78:301–30.CrossRef
34.
go back to reference Kafatos G, Andrews N, Gillespie IA, Charlett A, Adak GK, De Pinna E, et al. Impact of reduced numbers of isolates phage-typed on the detection of Salmonella outbreaks. Epidemiol Infect. 2009;137(6):821–7.CrossRefPubMed Kafatos G, Andrews N, Gillespie IA, Charlett A, Adak GK, De Pinna E, et al. Impact of reduced numbers of isolates phage-typed on the detection of Salmonella outbreaks. Epidemiol Infect. 2009;137(6):821–7.CrossRefPubMed
35.
go back to reference Guerin MT, Martin SW, Darlington GA. Temporal clusters of Salmonella serovars in humans in Alberta, 1990-2001. Can J Public Health. 2005;96(5):390–5.PubMed Guerin MT, Martin SW, Darlington GA. Temporal clusters of Salmonella serovars in humans in Alberta, 1990-2001. Can J Public Health. 2005;96(5):390–5.PubMed
36.
go back to reference Vrbova L, Johnson K, Whitfield Y, Middleton D. A descriptive study of reportable gastrointestinal illnesses in Ontario, Canada, from 2007 to 2009. BMC Public Health. 2012;12:970.CrossRefPubMedPubMedCentral Vrbova L, Johnson K, Whitfield Y, Middleton D. A descriptive study of reportable gastrointestinal illnesses in Ontario, Canada, from 2007 to 2009. BMC Public Health. 2012;12:970.CrossRefPubMedPubMedCentral
37.
go back to reference Pires SM, Evers EG, van Pelt W, Ayers T, Scallan E, Angulo FJ, et al. Attributing the human disease burden of foodborne infections to specific sources. Foodborne Pathog Dis. 2009;6:417–24.CrossRefPubMed Pires SM, Evers EG, van Pelt W, Ayers T, Scallan E, Angulo FJ, et al. Attributing the human disease burden of foodborne infections to specific sources. Foodborne Pathog Dis. 2009;6:417–24.CrossRefPubMed
38.
go back to reference Kimura AC, Reddy V, Marcus R, Cieslak PR, Mohle-Boetani JC, Kassenborg HD. Chicken consumption is a newly identified risk factor for sporadic Salmonella enterica serotype Enteritidis infections in the United States: a case–control study in FoodNet sites. Clin Infect Dis. 2004;38 Suppl 3:S244–52.CrossRefPubMed Kimura AC, Reddy V, Marcus R, Cieslak PR, Mohle-Boetani JC, Kassenborg HD. Chicken consumption is a newly identified risk factor for sporadic Salmonella enterica serotype Enteritidis infections in the United States: a case–control study in FoodNet sites. Clin Infect Dis. 2004;38 Suppl 3:S244–52.CrossRefPubMed
39.
go back to reference Beatty ME, Shevick G, Shupe-Ricksecker K, Bannister E, Tulu A, Lancaster K, et al. Large Salmonella Enteritidis outbreak with prolonged transmission attributed to an infected food handler, Texas, 2002. Epidemiol Infect. 2009;137(3):417–27.CrossRefPubMed Beatty ME, Shevick G, Shupe-Ricksecker K, Bannister E, Tulu A, Lancaster K, et al. Large Salmonella Enteritidis outbreak with prolonged transmission attributed to an infected food handler, Texas, 2002. Epidemiol Infect. 2009;137(3):417–27.CrossRefPubMed
40.
go back to reference Hedican E, Hooker C, Jenkins T, Medus C, Jawahir S, Leano F, et al. Restaurant Salmonella Enteritidis outbreak associated with an asymptomatic infected food worker. J Food Prot. 2009;72(11):2332–6.PubMed Hedican E, Hooker C, Jenkins T, Medus C, Jawahir S, Leano F, et al. Restaurant Salmonella Enteritidis outbreak associated with an asymptomatic infected food worker. J Food Prot. 2009;72(11):2332–6.PubMed
41.
go back to reference Medus C, Smith KE, Bender JB, Leano F, Hedberg CW. Salmonella infections in food workers identified through routine public health surveillance in Minnesota: impact on outbreak recognition. J Food Prot. 2010;73(11):2053–8.PubMed Medus C, Smith KE, Bender JB, Leano F, Hedberg CW. Salmonella infections in food workers identified through routine public health surveillance in Minnesota: impact on outbreak recognition. J Food Prot. 2010;73(11):2053–8.PubMed
43.
go back to reference Wagner VR, Silveira JB, Tondo EC. Salmonelloses in the State of Rio Grande do Sul, southern Brazil, 2002 to 2004. Braz J Microbiol. 2014;44(3):723–9.CrossRefPubMedPubMedCentral Wagner VR, Silveira JB, Tondo EC. Salmonelloses in the State of Rio Grande do Sul, southern Brazil, 2002 to 2004. Braz J Microbiol. 2014;44(3):723–9.CrossRefPubMedPubMedCentral
44.
go back to reference Ethelberg S, Olsen KE, Gerner-Smidt P, Mølbak K. Household outbreaks among culture-confirmed cases of bacterial gastrointestinal disease. Am J Epidemiol. 2004;159(4):406–12.CrossRefPubMed Ethelberg S, Olsen KE, Gerner-Smidt P, Mølbak K. Household outbreaks among culture-confirmed cases of bacterial gastrointestinal disease. Am J Epidemiol. 2004;159(4):406–12.CrossRefPubMed
45.
go back to reference Aiken AM, Lane C, Adak GK. Risk of Salmonella infection with exposure to reptiles in England, 2004–2007. Euro Surveill. 2010;15(22):19581.PubMed Aiken AM, Lane C, Adak GK. Risk of Salmonella infection with exposure to reptiles in England, 2004–2007. Euro Surveill. 2010;15(22):19581.PubMed
46.
go back to reference Sauteur PM, Relly C, Hug M, Wittenbrink MM, Berger C. Risk factors for invasive reptile-associated salmonellosis in children. Vector Borne Zoonotic Dis. 2013;13(6):419–21.CrossRef Sauteur PM, Relly C, Hug M, Wittenbrink MM, Berger C. Risk factors for invasive reptile-associated salmonellosis in children. Vector Borne Zoonotic Dis. 2013;13(6):419–21.CrossRef
47.
go back to reference Johnson LR, Gould LH, Dunn JR, Berkelman R, Mahon BE, Foodnet Travel Working Group. Salmonella infections associated with international travel: a Foodborne Diseases Active Surveillance Network (FoodNet) study. Foodborne Pathog Dis. 2011;8(9):1031–7.CrossRefPubMed Johnson LR, Gould LH, Dunn JR, Berkelman R, Mahon BE, Foodnet Travel Working Group. Salmonella infections associated with international travel: a Foodborne Diseases Active Surveillance Network (FoodNet) study. Foodborne Pathog Dis. 2011;8(9):1031–7.CrossRefPubMed
48.
go back to reference Ravel A, Nesbitt A, Marshall B, Sittler N, Pollari F. Description and burden of travel-related cases caused by enteropathogens reported in a Canadian community. J Travel Med. 2011;18:8–19.CrossRefPubMed Ravel A, Nesbitt A, Marshall B, Sittler N, Pollari F. Description and burden of travel-related cases caused by enteropathogens reported in a Canadian community. J Travel Med. 2011;18:8–19.CrossRefPubMed
49.
go back to reference Scallan E, Jones TF, Cronquist A, Thomas S, Frenzen P, Hoefer D, et al. Factors associated with seeking medical care and submitting a stool sample in estimating the burden of foodborne illness. Foodborne Pathog Dis. 2006;3(4):432–8.CrossRefPubMed Scallan E, Jones TF, Cronquist A, Thomas S, Frenzen P, Hoefer D, et al. Factors associated with seeking medical care and submitting a stool sample in estimating the burden of foodborne illness. Foodborne Pathog Dis. 2006;3(4):432–8.CrossRefPubMed
50.
go back to reference MacDougall L, Majowicz S, Doré K, Flint J, Thomas K, Kovacs S, et al. Under-reporting of infectious gastrointestinal illness in British Columbia, Canada: who is counted in provincial communicable disease statistics? Epidemiol Infect. 2008;136(2):248–56.CrossRefPubMed MacDougall L, Majowicz S, Doré K, Flint J, Thomas K, Kovacs S, et al. Under-reporting of infectious gastrointestinal illness in British Columbia, Canada: who is counted in provincial communicable disease statistics? Epidemiol Infect. 2008;136(2):248–56.CrossRefPubMed
52.
go back to reference Jacob CJ, Powell DA. Where does foodborne illness happen-in the home, at foodservice, or elsewhere-and does it matter? Foodborne Pathog Dis. 2009;6(9):1121–3.CrossRefPubMed Jacob CJ, Powell DA. Where does foodborne illness happen-in the home, at foodservice, or elsewhere-and does it matter? Foodborne Pathog Dis. 2009;6(9):1121–3.CrossRefPubMed
Metadata
Title
Spatial-temporal epidemiology of human Salmonella Enteritidis infections with major phage types (PTs 1, 4, 5b, 8, 13, and 13a) in Ontario, Canada, 2008–2009
Authors
Csaba Varga
David L. Pearl
Scott A. McEwen
Jan M. Sargeant
Frank Pollari
Michele T. Guerin
Publication date
01-12-2015
Publisher
BioMed Central
Published in
BMC Public Health / Issue 1/2015
Electronic ISSN: 1471-2458
DOI
https://doi.org/10.1186/s12889-015-2592-6

Other articles of this Issue 1/2015

BMC Public Health 1/2015 Go to the issue