Restricted accessResearch articleFirst published online 2021-07
Area-Level Clustering of Shiga Toxin–Producing Escherichia coli Infections and Their Socioeconomic and Demographic Factors in Ontario,Canada: An Ecological Study
Shiga toxin–producing Escherichia coli (STEC) infections are an important health burden for human populations in Ontario and worldwide. We assessed 452 STEC cases that were reported to Ontario's reportable disease surveillance system between 2015 and 2017. A retrospective scan statistic using a Poisson model was used to detect high-rate STEC clusters at the forward sortation area (FSA; the first three digits of a postal code) level. A significant spatial cluster in the southwest region of Ontario was identified. A case–case logistic regression analysis was applied to compare FSA-level socioeconomic and demographic characteristics among STEC cases included inside the spatial cluster with cases outside of the cluster. Cases included in the spatial cluster had higher odds of living in FSAs with a low median family income, low proportion of lone-parent families, and low proportion of the visible minority population. In addition, STEC cases inside the cluster had higher odds of coming from rural FSAs. Our study demonstrated that STEC cases were spatially clustered in Ontario and their clustering was associated with FSA-level socioeconomic and demographic determinants of cases.
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References
1.
AdamsNL, ByrneL, RoseTC, AdakGK, JenkinsC, CharlettA, et al.Influence of socio-economic status on Shiga toxin–producing Escherichia coli (STEC) infection incidence, risk factors and clinical features. Epidemiol Infect, 2019; 147:e215.
2.
AdamsNL, ByrneL, SmithGA, ElsonR, HarrisJP, SalmonR, et al.Shiga toxin–producing Escherichia coli O157, England and Wales, 1983–2012. Emerg Infect Dis, 2016; 22:590–597.
3.
BentancorA, RumiM V., CarbonariC, GerhardtE, LarzábalM, VilteDA, et al.Profile of Shiga toxin–producing Escherichia coli strains isolated from dogs and cats and genetic relationships with isolates from cattle, meat and humans. Vet Microbiol, 2012; 156:336–342.
4.
BrubacherJ, AllenDM, DérySJ, ParkesMW, ChhetriB, MakS, et al.Associations of five food- and water-borne diseases with ecological zone, land use and aquifer type in a changing climate. Sci Total Environ, 2020; 728:138808.
5.
Bruce-Grey-Owen Sound Health Unit. The Investigative Report on the Walkerton Outbreak of Waterborne Gastroenteritis: May–June 2000. Bruce-Grey-Owen Sound Health Unit. 2000. Available at: https://www.publichealthgreybruce.on.ca/Portals/0/Topics/WaterSafety/Public_Drinking/Walkerton/WalkertonReport/REPORT_Oct00.PDF Accessed December1, 2020.
6.
BruyandM, Mariani-KurkdjianP, GoualiM, de ValkH, KingLA, Le HelloS, et al.Hemolytic uremic syndrome due to Shiga toxin–producing Escherichia coli infection. Med Mal Infect, 2018; 48:167–174.
7.
BruyandM, Mariani-KurkdjianP, Hello SLe, KingLA, Cauteren DVan, LefevreS, et al.Paediatric haemolytic uraemic syndrome related to Shiga toxin–producing Escherichia coli, an overview of 10 years of surveillance in France, 2007 to 2016. Eurosurveillance, 2019; 24:1–9.
8.
ByrneL, JenkinsC, LaundersN, ElsonR, AdakGK. The epidemiology, microbiology and clinical impact of Shiga toxin–producing Escherichia coli in England, 2009–2012. Epidemiol Infect, 2015; 143:3475–3487.
9.
ChangM, GrosecloseSL, ZaidiAA, BradenCR. An ecological analysis of sociodemographic factors associated with the incidence of salmonellosis, shigellosis, and E. coli O157:H7 infections in US counties. Epidemiol Infect, 2009; 137:810–820.
10.
ColemanBL, LouieM, SalvadoriMI, McEwenSA, NeumannN, SibleyK, et al.Contamination of Canadian private drinking water sources with antimicrobial resistant Escherichia coli. Water Res, 2013; 47:3026–3036.
11.
ConradCC, StanfordK, Narvaez-BravoC, CallawayT, McAllisterT. Farm fairs and petting zoos: A review of animal contact as a source of zoonotic enteric disease. Foodborne Pathog Dis, 2017; 14:59–73.
12.
CroweSJ, BottichioL, ShadeLN, WhitneyBM, CorralN, MeliusB, et al.Shiga toxin–producing E. coli infections associated with flour. N Engl J Med, 2017; 377:2036–2043.
13.
DesjardinsMR, WhitemanA, CasasI, DelmelleE. Space-time clusters and co-occurrence of chikungunya and dengue fever in Colombia from 2015 to 2016. Acta Trop, 2018; 185:77–85.
14.
ElsonR, GraceK, VivancosR, JenkinsC, AdakGK, O'BrienSJ, et al.A spatial and temporal analysis of risk factors associated with sporadic Shiga toxin–producing Escherichia coli O157 infection in England between 2009 and 2015. Epidemiol Infect, 2018; 146:1928–1939.
15.
FriesemaIHM, Van De KassteeleJ, De JagerCM, HeuvelinkAE, Van PeltW. Geographical association between livestock density and human Shiga toxin–producing Escherichia coli O157 infections. Epidemiol Infect, 2011; 139:1081–1087.
16.
GouldLH, ModyRK, OngKL, ClogherP, CronquistAB, GarmanKN, et al.Increased recognition of non-O157 Shiga toxin–producing Escherichia coli infections in the United States during 2000–2010: Epidemiologic features and comparison with E. coli O157 infections. Foodborne Pathog Dis, 2013; 10:453–460.
17.
GreenCG, KrauseDO, WylieJL. Spatial analysis of Campylobacter infection in the Canadian province of Manitoba. Int J Health Geogr, 2006; 5:1–14.
18.
HadlerJL, ClogherP, HuangJ, LibbyT, CronquistA, WilsonS, et al.The relationship between census tract poverty and Shiga toxin–producing E. coli risk, analysis of foodnet data, 2010–2014. Open Forum Infect Dis, 2018; 5:2010–2014.
19.
HanJ, ZhuL, KulldorffM, HostovichS, StinchcombDG, TatalovichZ, et al.Using Gini coefficient to determining optimal cluster reporting sizes for spatial scan statistics. Int J Health Geogr, 2016; 15:27.
20.
HeimanKE, ModyRK, JohnsonSD, GriffinPM, Hannah GouldL. Escherichia coli O157 Outbreaks in the United States, 2003–2012. Emerg Infect Dis, 2015; 21:1293–1301.
21.
HermanKM, HallAJ, GouldLH. Outbreaks attributed to fresh leafy vegetables, United States, 1973–2012. Epidemiol Infect, 2015; 143:3011–3021.
22.
HosmerDW, LemeshowS, SturdivantRX. Applied Logistic Regression. 3rd ed. Hoboken, NJ: John Wiley and Sons, 2013:528.
23.
HrudeySE, PaymentP, HuckPM, GillhamRW, HrudeyEJ. A fatal waterborne disease epidemic in Walkerton, Ontario: Comparison with other waterborne outbreaks in the developed world. Water Sci Technol, 2003; 47:7–14.
24.
InvikJ, BarkemaHW, MassoloA, NeumannNF, CeyE, CheckleyS. Escherichia coli contamination of rural well water in Alberta, Canada is associated with soil properties, density of livestock and precipitation. Can Water Resour J, 2019; 44:248–262.
25.
JalavaK, OllgrenJ, EklundM, SiitonenA, KuusiM. Agricultural, socioeconomic and environmental variables as risks for human verotoxigenic Escherichia coli (VTEC) infection in Finland. BMC Infect Dis, 2011; 11:275.
26.
JarosP, CooksonAL, CampbellDM, BesserTE, ShringiS, MackerethGF, et al.A prospective case-control and molecular epidemiological study of human cases of Shiga toxin–producing Escherichia coli in New Zealand. BMC Infect Dis, 2013; 13:1.
27.
JohnsonRP, HoltslanderB, MazzoccoA, RocheS, ThomasJL, PollariF, et al.Detection and prevalence of verotoxin-producing Escherichia coli O157 and non-O157 serotypes in a Canadian watershed. Appl Environ Microbiol, 2014; 80:2166–2175.
28.
KarmaliMA.Emerging public health challenges of Shiga toxin–producing Escherichia coli related to changes in the pathogen, the population, and the environment. Clin Infect Dis, 2017; 64:371–376.
29.
KimJ, JungI. Evaluation of the gini coefficient in spatial scan statistics for detecting irregularly shaped clusters. PLoS One, 2017; 12:1–13.
30.
KlumbCA, ScheftelJM, SmithKE. Animal agriculture exposures among Minnesota residents with zoonotic enteric infections, 2012–2016. Epidemiol Infect, 2020; 148:e55.
31.
KoroME, AnandanS, QuinlanJJ. Microbial quality of food available to populations of differing socioeconomic status. Am J Prev Med, 2010; 38:478–481.
32.
KrolikJ, MaierA, ThompsonS, MajuryA. Microbial source tracking of private well water samples across at-risk regions in southern Ontario and analysis of traditional fecal indicator bacteria assays including culture and qPCR. J Water Health, 2016; 14:1047–1058.
33.
KulldorffM.A spatial scan statistic. Commun Stat Theory Methods, 1997; 26:1481–1496.
34.
KulldorffM, HuangL, KontyK. A scan statistic for continuous data based on the normal probability model. Int J Health Geogr, 2009; 8:58.
35.
KulldorffM, Information Management ServicesI. SaTScanTM v 9.6: Software for the Spatial and Space-Time Scan Statistics. 2018. Available at: www.satscan.org Accessed November3, 2020.
36.
LockingME, O'BrienSJ, ReillyWJ, WrightEM, CampbellDM, CoiaJE, et al.Risk factors for sporadic cases of Escherichia coli O157 infection: The importance of contact with animal excreta. Epidemiol Infect, 2001; 127:215–220.
37.
Luna-GuevaraJJ, Arenas-HernandezMMP, Martínez De La PeñaC, SilvaJL, Luna-GuevaraML. The role of pathogenic E. coli in fresh vegetables: Behavior, contamination factors, and preventive measures. Int J Microbiol, 2019;2019 [Epub ahead of print]; DOI: 10.1155/2019/2894328..
38.
MacDougallL, MajowiczS, DoréK, FlintJ, ThomasK, KovacsS, et al.Under-reporting of infectious gastrointestinal illness in British Columbia, Canada: Who is counted in provincial communicable disease statistics?. Epidemiol Infect, 2008; 136:248–256.
39.
MajowiczSE, EdgeVL, FazilA, McNabWB, DoréKA, SockettPN, et al.Estimating the under-reporting rate for infectious gastrointestinal illness in Ontario. Can J Public Health, 2005; 96:178–181.
40.
MajowiczSE, ScallanE, Jones-BittonA, SargeantJM, StapletonJ, AnguloFJ, et al.Global incidence of human Shiga toxin–producing escherichia coli infections and deaths: A systematic review and knowledge synthesis. Foodborne Pathog Dis, 2014; 11:447–455.
41.
MichelP, WilsonJB, MartinSW, ClarkeRC, McEwenSA, GylesCL. Temporal and geographical distributions of reported cases of Escherichia coli O157:H7 infection in Ontario. Epidemiol Infect, 1999; 122:193–200.
42.
Mughini-GrasL, van PeltW, van der VoortM, HeckM, FriesemaI, FranzE. Attribution of human infections with Shiga toxin–producing Escherichia coli (STEC) to livestock sources and identification of source-specific risk factors, The Netherlands (2010–2014). Zoonoses Public Health, 2018; 65:e8–e22.
43.
PaphitisK, PearlDL, BerkeO, McEwenSA, Trotz-WilliamsL. Detection of spatial, temporal and space-time Salmonella Heidelberg and Salmonella Typhimurium clusters in Ontario in 2015, and comparisons to known outbreaks. Zoonoses Public Health, 2020; 67:617–628.
44.
Pardhan-AliA, WilsonJ, EdgeVL, FurgalC, Reid-SmithR, SantosM, et al.A descriptive analysis of notifiable gastrointestinal illness in the Northwest Territories, Canada, 1991–2008. BMJ Open, 2012; 2:1–10.
45.
PearlDL, LouieM, ChuiL, DoréK, GrimsrudKM, LeedellD, et al.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; 134:699–711.
46.
PearlDL, LouieM, ChuiL, DoréK, GrimsrudKM, MartinSW, et al.A multi-level approach for investigating socio-economic and agricultural risk factors associated with rates of reported cases of Escherichia coli O157 in humans in Alberta, Canada. Zoonoses Public Health, 2009; 56:455–464.
47.
PedersenRM, NielsenMTK, MöllerS, EthelbergS, SkovMN, KolmosHJ, et al.Shiga toxin–producing Escherichia coli: Incidence and clinical features in a setting with complete screening of patients with suspected infective diarrhoea. Clin Microbiol Infect, 2018; 24:635–639.
48.
PiresSM, MajowiczS, GillA, DevleesschauwerB. Global and regional source attribution of Shiga toxin–producing Escherichia coli infections using analysis of outbreak surveillance data. Epidemiol Infect, 2019; 147:e236.
49.
Pogreba-BrownK, O'ConnorP, MatthewsJ, BarrettE, BellML. Case-case analysis of Campylobacter and Salmonella—using surveillance data for outbreak investigations and monitoring routine risk factors. Epidemiol Infect, 2018; 146:1916–1921.
50.
PollariF, ChristidisT, PintarKDM, NesbittA, FarberJ, LavoieMC, et al.Evidence for the benefits of food chain interventions on E. coli O157:H7/NM prevalence in retail ground beef and human disease incidence: A success story. Can J Public Health, 2017; 108:e71–e78.
51.
ReynoldsC, CheckleyS, ChuiL, OttoS, NeumannNF. Evaluating the risks associated with Shiga-toxin–producing Escherichia coli (STEC) in private well waters in Canada. Can J Microbiol, 2020; 66:337–350.
SchlagerS, LepuschitzS, RuppitschW, AbleitnerO, PietzkaA, NeubauerS, et al.Petting zoos as sources of Shiga toxin–producing Escherichia coli (STEC) infections. Int J Med Microbiol, 2018; 308:927–932.
Statistics Canada. Table 17-10-0005-01 Population Estimates on July 1st, by Age and Sex. 2016a. Available at: https://www.doi.org/https://doi.org/10.25318/1710000501-eng Accessed October29, 2020.
56.
Statistics Canada. Forward Sortation Area Boundary File. Geographic Files and Documentation: 92-179-X. 2016b. Available at: https://www.150.statcan.gc.ca/n1/en/catalogue/92-179-X
57.
Statistics Canada. Census Profile. Profile of a Community or Region: 98-316-X2016001. 2016c. Available at: https://www.150.statcan.gc.ca/n1/en/type/data?geoname=A0011#tables
58.
TadesseS, EnqueselassieF, HagosS. Spatial and space-time clustering of tuberculosis in Gurage Zone, Southern Ethiopia. PLoS One, 2018; 13:1–14.
59.
ThomasMK, MurrayR, FlockhartL, PintarK, PollariF, FazilA, et al.Estimates of the burden of foodborne illness in Canada for 30 specified pathogens and unspecified agents, Circa 2006. Foodborne Pathog Dis, 2013; 10:639–648.
60.
ValcourJE, CharronDF, BerkeO, WilsonJB, EdgeT, Waltner-ToewsD. A descriptive analysis of the spatio-temporal distribution of enteric diseases in New Brunswick, Canada. BMC Public Health, 2016; 16:1–14.
61.
ValcourJE, MichelP, McEwenSA, WilsonJB. Associations between indicators of livestock farming intensity and incidence of human Shiga toxin–producing Escherichia coli infection. Emerg Infect Dis, 2002; 8:252–257.
62.
VargaC, JohnP, CookeM, MajowiczSE. Spatial and space-time clustering and demographic characteristics of human nontyphoidal Salmonella infections with major serotypes in Toronto, Canada. PLoS One, 2020; 15:1–19.
63.
VargaC, MiddletonD, WaltonR, SavageR, TigheM-K, AllenV, 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.
64.
VargaC, PearlDL, McEwenSA, SargeantJM, PollariF, GuerinMT. Evaluating area-level spatial clustering of Salmonella. Enteritidis infections and their socioeconomic determinants in the greater Toronto area, Ontario, Canada (2007–2009): A retrospective population-based ecological study. BMC Public Health 2013;13:, 1078.
65.
VargaC, PearlDL, McEwenSA, SargeantJM, PollariF, GuerinMT. 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. BMC Public Health, 2015; 15:247.
66.
WangL, HuW. Immigrant health, place effect and regional disparities in Canada. Soc Sci Med, 2013; 98:8–17.
67.
WeisentJ, RohrbachB, DunnJR, OdoiA. Detection of high risk campylobacteriosis clusters at three geographic levels. Geospat Health, 2011; 6:65–76.
68.
WhitfieldY, JohnsonK, HobbsL, MiddletonD, DharB, VrbovaL. Descriptive study of enteric zoonoses in Ontario, Canada, from 2010–2012. BMC Public Health, 2017; 17:1–7.
69.
WhitneyBM, MaineroC, HumesE, HurdS, NiccolaiL, HadlerJL. Socioeconomic status and foodborne pathogens in Connecticut, USA, 2000–20111. Emerg Infect Dis, 2015; 21:1617–1624.
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