Review

A Canadian Application of One Health:Integration of Salmonella Data from Various

Canadian Surveillance Programs (2005–2010)

Elizabeth Jane Parmley,1 Katarina Pintar,1 Shannon Majowicz,2 Brent Avery,1 Angela Cook,1

Cassandra Jokinen,1 Vic Gannon,1 David R. Lapen,3 Ed Topp,3 Tom A. Edge,4 Matthew Gilmour,5

Frank Pollari,6 Richard Reid-Smith,1 and Rebecca Irwin1

Abstract

Most bacterial pathogens associated with human enteric illness have zoonotic origins and can be transmitteddirectly from animals to people or indirectly through food and water. This multitude of potential exposureroutes and sources makes the epidemiology of these infectious agents complex. To better understand theseillnesses and identify solutions to reduce human disease, an integrative approach like One Health is needed. Thisarticle considers the issue of Salmonella in Canada and interprets data collected by several Canadian surveillanceand research programs. We describe recovery of Salmonella from various samples collected along the exposurepathway and compare the serovars detected in the different components under surveillance (animal, food,environment, and human). We then present three examples to illustrate how an approach that interprets mul-tiple sources of surveillance data together is able to address issues that transcend multiple departments andjurisdictions. First, differences observed in recovery of Salmonella from different cuts of fresh chicken collected bydifferent programs emphasize the importance of considering the surveillance objectives and how they mayinfluence the information that is generated. Second, the high number of Salmonella Enteritidis cases in Canada isused to illustrate the importance of ongoing, concurrent surveillance of human cases and exposure sources toinformation domestic control and prevention strategies. Finally, changing patterns in the occurrence of ceftiofur-resistant Salmonella Heidelberg in retail meats and humans demonstrates how integrated surveillance canidentify an issue in an exposure source and link it to a trend in human disease. Taken together, surveillancemodels that encompass different scales can leverage infrastructure, costs, and benefits and generate a multidi-mensional picture that can better inform disease prevention and control programs.

Introduction

Enteric pathogens pose a significant disease burden inCanada, causing an estimated 11 million illnesses (Tho-

mas et al., 2008) and costing $3.7 billion dollars annually(Majowicz et al., 2006). Bacteria play a major role in entericdisease (Girard et al., 2006) and are the focus of most entericpathogen surveillance programs. Most bacteria associatedwith human enteric illness are zoonotic, and may be trans-mitted directly to people from animals or indirectly throughfood and water ( Jones et al., 2008). Many potential exposure

routes and sources for infection make determining the epi-demiology of these infectious agents complex (Fig. 1).

Identification of sources and routes of infection is the cor-nerstone of disease prevention and requires an integrated,multiprogram approach, as no single program or jurisdictionis able to inform all aspects of the problem. One Health is aninternationally accepted model that recognizes the inter-relationship between human, animal, economic, and environ-mental health, and proposes a multidisciplinary, cross-sectoralapproach to surveillance and mitigation of complex publichealth problems (Waltner-Toews, 2009; Powdrill et al., 2010).

1Laboratory for Foodborne Zoonoses, Public Health Agency of Canada, Guelph, Ontario, Canada.2School of Public Health and Health Systems, University of Waterloo, Waterloo, Ontario, Canada.3Science and Technology Branch, Agriculture and Agri-Food Canada, Ottawa, Ontario, Canada.4Watershed Stressors and Nutrients, Environment Canada, Burlington, Ontario, Canada.5National Microbiology Laboratory, Public Health Agency of Canada, Winnipeg, Manitoba, Canada.6Centre for Food-borne, Environmental, and Zoonotic Infectious Diseases, Public Health Agency of Canada, Guelph, Ontario, Canada.

FOODBORNE PATHOGENS AND DISEASEVolume 10, Number 9, 2013ª Mary Ann Liebert, Inc.DOI: 10.1089/fpd.2012.1438

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This makes it a suitable approach to address the epidemiologyof enteric illness.

In Canada, there are several national enteric pathogensurveillance programs that measure disease incidence andtarget some of the possible exposure sources. The PublicHealth Agency of Canada (PHAC) has a suite of nationalenteric disease surveillance programs, each designed to sup-port different public health actions. The Canadian NotifiableDisease Surveillance System (PHAC, 2012a), the National En-teric Surveillance Program (NESP) (PHAC, 2012b), and PulseNet Canada (PHAC, 2012c) focus solely on human cases andprovide data for early outbreak detection and response andnational disease trend monitoring.

Infectious, enteric illness is not exclusively a human prob-lem. To reduce the burden of disease, information is neededabout the presence of pathogens in the full array of expo-sure sources (e.g., foods, animals, drinking water, and recre-ational water). Integrated surveillance programs collectsamples and generate information from multiple componentswith a system (Galanis et al., 2012). Two integrated entericsurveillance programs—the Canadian Integrated Programfor Antimicrobial Resistance Surveillance (CIPARS) and theNational Integrated Enteric Pathogen Surveillance Program(C-EnterNet)—collect data along the farm-to-fork continuumand provide information about exposure routes and sourcesof enteric organisms and antimicrobial resistance (AMR) inCanada.

CIPARS tracks temporal and regional trends in antimicro-bial use (AMU) in humans and animals and AMR in selectedspecies of enteric bacteria recovered from different pointsalong the food chain on a Canada-wide basis (Government ofCanada, 2011a). C-EnterNet was designed to detect changesin human enteric disease and pathogen exposure from food,animal, and water sources. It reports on the prevalence ofenteric pathogens across the exposure spectrum and on inci-

dence rates and risk factors among human cases (travel-related and endemic) (Government of Canada, 2011b). Theseprograms operate together closely, but their designs are in-herently different. Not only do they have different objec-tives but also, CIPARS is focused on the national level andC-EnterNet is focused in sentinel communities and watersheds.

In addition to CIPARS and C-EnterNet, a number of sur-veillance and research initiatives led by other federal gov-ernment departments systematically assess enteric pathogenprevalence in surface waters. These include the National Agri-Environmental Standards Initiative (Edge et al., 2012), theWatershed Evaluation of Beneficial Management Practicesprogram (AAFC, 2013a), the National Water Quality Sur-veillance Research Initiative, and the Sustainable AgricultureEnvironmental Systems initiative (AAFC, 2013b). Generalgoals of these programs are to (1) gain a better understand-ing of spatial and temporal trends associated with entericpathogen prevalence in surface waters across Canada, (2)determine the most important animal sources of these path-ogens, and (3) qualify and quantify their contribution withrespect to human infection. Data generated from these ini-tiatives complement the exposure data collected by CIPARSand C-EnterNet.

Salmonella was chosen as a model pathogen for this analysisbecause it is the second leading cause of bacterial gastroenteritisin Canada (Government of Canada, 2007), and is included in theenvironmental surveillance programs described above (Jokinenet al., 2011; Wilkes et al., 2011; Edge et al., 2012), as well asCIPARS, C-EnterNet, NESP and Canadian Notifiable DiseaseSurveillance System. Although Salmonella is frequently isolatedfrom animals, food, and humans, the attribution of salmonel-losis to sources has yet to be fully elucidated in Canada.

This article is not an exhaustive review of all Salmonella dataavailable in Canada. Our purpose is to demonstrate how in-tegrating surveillance data from programs with different

FIG. 1. Sources and pathways of transmission of Salmonella in Canada.

748 PARMLEY ET AL.

designs and objectives can help develop research hypotheses,evaluate trends, understand the efficacy of interventions, andidentify important data gaps.

Materials and Methods

The sampling design and laboratory methods of CIPARSand C-EnterNet have been described elsewhere (Governmentof Canada—CIPARS, 2011a; Government of Canada—C-EnterNet, 2010a). The main components of these programs,as they pertain to Salmonella over the study period (2005–2010), are shown (Table 1).

Briefly, CIPARS monitors AMR in Salmonella isolated fromhumans, animals, and animal-derived food sources acrossCanada. Laboratory-confirmed human Salmonella isolates aresubmitted to the National Microbiology Laboratory as part ofreference requests, surveillance programs, surveys or out-break investigations. Isolates are characterized to the serovarlevel and selected serovars are phage typed and tested forAMR.

CIPARS isolates Salmonella from samples collected alongthe food chain including (1) fecal samples from grower-finisher swine herds from the major pork-producing prov-inces in Canada; (2) cecal samples from chickens and pigs atslaughter, and (3) retail chicken and pork purchased in BritishColumbia, Saskatchewan, Ontario, Quebec, New Brunswick,Prince Edward Island, and Nova Scotia. All recovered

Salmonella undergo further testing to determine serovar (someare phage typed) and antimicrobial susceptibility. CIPARSalso characterizes Salmonella isolates recovered from veteri-nary diagnostic and animal feed samples. Because no infor-mation is available about how many samples were collectedand tested, these data are not included herein.

Between 2005 and 2010, C-EnterNet operated in one sen-tinel site (Region of Waterloo, Ontario); in 2010, it expanded toa second site (Fraser Health Authority, British Columbia).Within each site, C-EnterNet tests for Salmonella in threesources: manure from farms (dairy, beef, swine, and broilerpoultry operations), retail meats (chicken, beef, and pork),and surface water. Human cases of salmonellosis identified bylocal public health are administered a standard, comprehen-sive questionnaire to evaluate all potential exposures (riskfactors) and to classify cases as international travel-related orendemic (both sporadic [non–outbreak related] and outbreakrelated). Isolates are characterized to the serovar level andsubsequently both phage type and pulsed-field gel electro-phoresis patterns are obtained.

Health Canada, Environment Canada, and Agriculture andAgri-Food Canada support systematic environmental moni-toring of Salmonella in watersheds across Canada through theNational Agri-Environmental Standards Initiative (Edge et al.,2012) and Watershed Evaluation of Beneficial ManagementPractices/National Water Quality Surveillance Research In-itiative/ Sustainable Agriculture Environmental Systems

Table 1. Canadian Integrated Program for Antimicrobial Resistance Surveillance (CIPARS)and National Integrated Enteric Pathogen Surveillance Program (C-EnterNet) Surveillance

Components for Salmonella (Years Captured)

Surveillance component Species C-EnterNet CIPARS

Sentinel Site 1—Region of Waterloo, Ontario,Canada (population estimate = 500,000)

Canada-wide (populationestimate = 33,000,000)

Diagnostic Human X X

(2005–2010) (2005–2010)All animal species · X

(2005–2010)Farm Swine X X

(2005–2010) (2007–2010)Chicken X ·

(2007–2010)Cattle (beef) X ·

(2007–2010)Cattle (dairy) X ·

(2006–2010)Abattoir Swine · X

(2005–2010)Chicken · X

(2005–2010)Retail meat Pork X X

(2005–2010) (2007–2010)Chicken X

bX

a,b

(2005–2010) (2005–2010)Beef X ·

(2005–2010)Surface water — X ·

(2005–2010)Surveillance programs Feed and ingredients · ·

(2005–2010)

aIn 2007, CIPARS changed the method of bacterial isolation from retail chicken.bCIPARS collects retail chicken legs with skin and C-EnterNet collects retail chicken breasts without skin.

ONE HEALTH IN ACTION: SALMONELLA IN CANADA 749

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programs (AAFC, 2013a; AAFC 2013b).Collectively, between2005 and 2010, Salmonella data were generated for fiveCanadian watersheds, each with different upstream pollu-tion pressures: (1) Bras d’Henri (Quebec), (2) South NationRiver (Eastern Ontario), (3) Grand River (Southern Ontario),(4) Oldman River (Alberta), and (5) Sumas River (BritishColumbia). The methods used for site identification, samplecollection (Edge et al., 2012), Salmonella isolation ( Jokinen et al.,2010), and serotyping and phage typing ( Jokinen et al., 2011)have been described previously.

We used several approaches to analyze the surveillancedata presented herein. First, measures of Salmonella preva-lence and rates of disease between 2005 and 2010 are pre-sented. Salmonella recovery and serovars detected acrossvarious surveillance and research programs and sectors weresummarized using Excel 2000 (Microsoft Office 2000) anddescriptive statistics were calculated using Excel and EpiInfo� 6 (Centers for Disease Control and Prevention). Second,three retrospective narratives were used to illustrate howCIPARS and C-EnterNet Salmonella data supported action.Environmental and land-use information were used to helpidentify potential sources of Salmonella in these systems.

Results

Quantitative results

Between 2005 and 2010, NESP reported 37,925 humanSalmonella cases (PHAC, 2012b). During this period, CIPARSrecovered Salmonella from 23% (470/2050) of farm swinesamples, 43% (942/2199) of abattoir swine samples, and 2%(69/4598) of raw pork chops at retail. In comparison, 23%(1198/5140) of abattoir chicken samples and 32% (1760/5483)of raw chicken thighs were Salmonella positive (Fig. 2).

Within C-EnterNet Sentinel Site 1, 691 laboratory-confirmedhuman cases of Salmonella were reported (2005–2010). Ofthese, 193 (28%) were international travel–related and 498

(72%) were endemic (domestically acquired); 51 (10%) ofendemic cases were outbreak-related, and 447 (90%) weresporadic cases. Endemic, sporadic cases are the focus of C-EnterNet surveillance efforts. During this time period, C-En-terNet recovered Salmonella from 53% (200/376) of manuresamples from broiler chicken farms, 10% (45/432) from beef(cow–calf), 12% (80/643) from dairy cattle, and 30% (216/712)from swine (farrow to finish). At retail, Salmonella was re-covered from 30% (295/995) of raw chicken breasts, 0.5% (5/984) of raw ground beef, and 2% (19/983) of raw pork chops(Fig. 2).

Across all species and sources within both integrated sur-veillance programs, the most common serovars identifiedwere Salmonella enterica serovar Enteritidis, Salmonella Ty-phimurium, and Salmonella Heidelberg (Fig. 3). NESP re-ported the same top three serovars between 2005 and 2010(PHAC, 2012b). Across the main agricultural food commod-ities (chickens, pigs, beef, and dairy cattle), a wide variety ofserovars was detected but the serovar distribution differed:Salmonella Heidelberg and Salmonella Kentucky were commonin all poultry sources; Salmonella Typhimurium emerged as apredominant serovar across all porcine sources, and bovinesource distributions were mixed.

Environmental monitoring programs collected sampleswithin multiple tributaries across Canada; for simplicity, theresults are aggregated at the watershed level. Salmonellaprevalence varied between watersheds, from 6% (125/1975)in the South Nation River to 20% (127/622) in the GrandRiver, as well as within watersheds (Table 2). Prevalence inthe Grand River was consistently three times higher than inthe South Nation River watershed, likely as a result of dif-ferent point and nonpoint source pollution drivers (Wilkeset al., 2011; Government of Canada, 2011b). Across all fivewatersheds, the two most common serovars were SalmonellaTyphimurium and Salmonella Thompson. Between water-sheds, differences in serovar distributions were noted. For

Table 2. Annual Salmonella Prevalence in Five Canadian Watersheds by Year (2005–2010)

Watershed 2005 2006 2007 2008 2009 2010 Total

Sumas River (British Columbia)No. samples 80 83 163No. positive 8 15 23% Positive 10 18 14

Oldman River (Alberta)No. samples 134 203 155 110 602No. positive 15 11 8 9 43% Positive 11 5 5 8 7

South Nation (Ontario)No. samples 495 430 63 264 390 333 1975No. positive 28 48 3 11 16 19 125% Positive 6 11 5 4 4 6 6

Bras d’Henri (Quebec)No. samples 72 125 50 70 317No. positive 13 11 1 2 27% Positive 18 9 2 3 9

Grand River (Ontario)No. samples 42 140 134 100 112 94 622No. positive 2 28 13 33 28 23 127% Positive 5 20 10 33 25 25 20

752 PARMLEY ET AL.

example, Salmonella Kentucky was never detected in theOldman River, Sumas River, or the Bras d’Henri watershedsbut was commonly found in the two Ontario watersheds(Fig. 3).

Qualitative results: Retrospective narratives

Detecting Salmonella on grocery store (i.e., retail) chick-en. CIPARS and C-EnterNet use similar sampling designsfor retail meat surveillance and have used the same laboratorymethods since 2007 (Government of Canada, 2010b). How-ever, there are two important differences between CIPARSand C-EnterNet retail chicken meat sampling designs: (1)C-EnterNet samples chicken breast meat but CIPARS sampleschicken legs and thighs, and (2) C-EnterNet incubates a 50-gpiece of chicken (to enumerate the bacterial contaminationlevels), whereas CIPARS incubates the whole chicken piece.

Between 2005 and 2007, C-EnterNet purchased skin-onchicken breasts. In 2008 sampling shifted to skinless chickenbreasts, to reflect human consumption practices (Nesbitt et al.,2008). No difference in Salmonella prevalence was observedbetween skin-on and skinless chicken breasts (Cook et al.,2012). Between 2005 and 2010, Salmonella was recovered from30% (295/995) of chicken breasts purchased by C-EnterNet.

In 2007, CIPARS modified their incubation technique usedto isolate Salmonella from retail chicken after C-EnterNetdemonstrated higher Salmonella recovery. The original labora-tory method (2005–2006) resulted in 11% (172/1558) of chickentesting positive for Salmonella; after adopting the modifiedtechnique (2007–2010), Salmonella recovery was 40% (1588/3925). When CIPARS and C-EnterNet used the same incuba-tion methods (2007–2010), the proportion of Salmonella-positiveC-EnterNet chicken meat samples was significantly lower thanthe proportion of CIPARS samples (odds ratio = 1.51 [95%confidence interval: 1.24, 1.83]). When Salmonella recovery fromC-EnterNet chicken meat samples was compared to the On-tario-specific CIPARS samples (46%; 543/1191), the differenceremained significant (odds ratio = 1.85 [1.49, 2.30]).

The most likely explanation for the difference in recoverybetween the two programs is that C-EnterNet incubates 50 gof chicken meat, whereas CIPARS incubates the entire piece ofchicken. In support of this hypothesis, C-EnterNet enumera-tion data show that when a given chicken breast tests positive,few Salmonella colony-forming units are detected (Govern-ment of Canada, 2011b). The discordance in recovery high-lights the different objectives of the two programs. WhereCIPARS aims to recover enough isolates to assess AMRtrends, C-EnterNet’s primary objective is to measure patho-gen prevalence.

Salmonella Enteritidis. Since 2005, the number of Salmo-nella Enteritidis cases among Canadians has been in-creasing (Nesbitt et al., 2012); it is now the most commonlyreported serovar from human cases in Canada. NESP collectsaggregate data from provincial laboratories to identify na-tional and cross-jurisdictional trends in human infections.These isolates represent laboratory-confirmed cases and haveminimal epidemiological information associated with eachisolate (e.g., no travel information). However, these nationaldata provide important information that can be used to betterunderstand the emergence of this serovar and potential routesand sources of exposure. While local and regional differences

are critical to the epidemiology, national information can helpidentify important linkages with environmental and behav-ioral drivers of infection.

C-EnterNet is the only federally supported program that isable to routinely separate endemic from travel-related humancases. Among 259 Salmonella Enteritidis isolates from SentinelSite 1, 91 (35%) were travel-related, and 168 (65%) were en-demic. Of the endemic cases, 39 (23%) were outbreak-relatedand 129 (77%) were sporadic. CIPARS and C-EnterNet datademonstrate that Salmonella Enteritidis is frequently recov-ered from a variety of animal species along the farm-to-forkcontinuum and is particularly common among chickensamples: 14% (246/1760) of CIPARS and 9% (26/295) ofC-EnterNet Salmonella isolates from retail chicken wereSalmonella Enteritidis) (Fig. 3). The phage types recoveredmost often from chicken sources are the same as those ob-served among endemic human Salmonella Enteritidis cases:PT 13, 13a, and 8 (Nesbitt et al., 2012). Salmonella Enteritidiswas rarely isolated from three watersheds. This serovar re-presented less than 3% (4/159 and 3/132) of Salmonella iso-lates from Ontario watersheds and 9% (4/47) of isolates fromthe Quebec watershed, suggesting that water is not the pre-dominant source of this pathogen.

CIPARS data provide an additional layer of information tothe Salmonella Enteritidis story. In Canada, 18% (1008/5691) ofhuman Salmonella Enteritidis isolates (2005–2009) demon-strated resistance to one or more antimicrobial agents tested;lower levels of resistance were observed among animal andfood isolates collected during the same period (Nesbitt et al.,2012). Although the levels of resistance are low currently, it isimportant to continue to monitor resistance to ensure that re-commended treatments remain effective. CIPARS data showthat resistance can emerge quickly: in 2005, 69% (33/48) ofSalmonella Kentucky isolates from chicken at slaughter and 77%(10/13) of isolates from retail chicken were fully susceptible toall antimicrobials tested (Government of Canada, 2007). By2006, just 33% (26/80) of slaughter chicken isolates and 19% (4/21) of retail chicken isolates were fully susceptible (Govern-ment of Canada, 2009).

Although the majority of human Salmonella Enteritidiscases are sporadic, outbreaks provide unique opportunities toinvestigate exposure pathways. Among six Salmonella En-teritis outbreaks documented in Canada between 2003 and2009, three were associated with eggs or chicken (Nesbitt et al.,2012). Internationally, chicken and eggs have also beenidentified as important risks for sporadic disease (Molbak andNeimann, 2002; Kimura et al., 2004; Marcus et al., 2007; Collardet al., 2008; Voetsch et al., 2009). Unfortunately, neither CI-PARS nor C-EnterNet routinely captures Salmonella data fromthe layer sector. To begin to fill this gap, CIPARS sampledspent layer hens at slaughter (2009–2011). Forty-two percent(117/279) of samples tested positive for Salmonella; 15 Salmo-nella Enteritidis isolates were identified (CIPARS unpublisheddata, 2012). CIPARS also supported research to estimate Sal-monella prevalence at egg-breaking stations: 2% (5/300) ofsamples were positive for Salmonella Enteritidis (Governmentof Canada, 2011a). Both programs continue to broaden theirsampling to incorporate additional potential exposure sour-ces: in 2010, C-EnterNet expanded their retail meat-samplingprogram to include ground poultry meat and preparedchicken nuggets and in 2011, CIPARS added chicken nuggetsand ground turkey to their retail sampling protocol.

ONE HEALTH IN ACTION: SALMONELLA IN CANADA 753

Salmonella Heidelberg. Salmonella Heidelberg is the thirdmost common Salmonella serovar recovered from Canadians,representing 10% (3876/37,925) of all Salmonella isolates(PHAC, 2012b). Salmonella Heidelberg is more commonlyisolated from people in Canada than in the United States[CDC, 2009]) and is more often isolated in North Americathan other regions of the world (WHO, 2006). C-EnterNet datasupport this finding; just one travel-related case of SalmonellaHeidelberg was identified between 2005 and 2010. CIPARSand C-EnterNet animal and food data demonstrate that thisserovar is frequently isolated from chickens on farm, atslaughter, and at retail (Fig. 3).

Since 2003, the national scope of CIPARS enabled identifi-cation of regional differences in the prevalence of ceftiofur-resistant Salmonella Heidelberg in retail chicken and humans(Dutil et al., 2010). Ceftiofur is an extended-spectrum cepha-losporin widely used in veterinary medicine and is closelyrelated to ceftriaxone (used in humans). Since cross-resistanceis high, the use of ceftiofur in animal agriculture is a humanhealth concern; ceftiofur is not approved for use in poultry inCanada.

Antimicrobial use is considered the major determinant ofAMR, and changes in ceftiofur resistance in Quebec appear tobe associated with changing use practices (Dutil et al., 2010).As an integrated system, CIPARS was able to evaluate thesuccess of an intervention. When ceftiofur use was voluntarilybanned in Quebec, CIPARS identified a decrease in thenumber of ceftiofur-resistant Salmonella Heidelberg isolatesfrom chicken and humans. Subsequently, with a partial returnto use, CIPARS identified an increase in ceftiofur resistance.

The national design of CIPARS allowed for elucidationof regional differences in the presence of AMR in this serovar.The C-EnterNet platform complements this national per-spective by enabling more detailed investigation at thecommunity level to better understand the drivers of resis-tance. Addition of AMR testing of C-EnterNet isolates couldbe used to test research hypotheses about AMR throughcommunity-level studies of the relationship between practiceson farm, in the environment, along the food chain, and inhuman medicine.

Discussion

Enteric disease and AMR are complex public health issues.Established integrated surveillance programs help identifysources of infection and routes of transmission. This infor-mation helps identify serovar differences, data gaps, andpotential points of intervention to reduce human and animaldisease and AMR emergence.

Within a bacterial genus, different species and serovarsbehave differently in time, space, and across host species.Certain serovars are more common in one animal species thananother (Fig. 3), and different Salmonella Enteritidis phagetypes are seen in different sources. The ability of bacteria toevolve and occupy novel ecological niches adds furthercomplexity. Understanding the epidemiology of entericpathogens requires a One Health approach, which is flexibleand recognizes the changing relationships between patho-gens, hosts, and the natural and socioeconomic environmentsthat we share.

Surveillance is a mixture of imperfect subsystems that,when combined, are greater than the sum of their individual

parts. Surveillance is critical to the policy-making process,providing evidence needed to target interventions to improvefood and water safety and ultimately reduce the burden ofdisease. Policies and interventions have impact at multiplescales, ranging from the individual, to the community, to theworld as a whole. In Canada, where enteric disease and theassociated exposure sources fall under different jurisdictions,successful public health action requires various levels of sur-veillance data to support jurisdiction-specific policies andinterventions. A community-focused surveillance programcannot feasibly capture the national picture, nor can a broad,national program capture the complex inter-relationships atthe local level.

The surveillance data presented herein inform a multidi-mensional picture of the complex relationships between en-teric pathogens, host and reservoir species, the naturalenvironment, and the health of humans and animals. Theseprograms do not capture information for every part of thesystem, but together they offer long-term capacity to betterunderstand the system and identify points for intervention.One Health is not a short-term approach. Understanding andreducing human and animal disease are long-term goals thatrequire consideration of the complex interactions along theexposure-to-disease continuum.

Salmonella infections are common around the world,but disease incidence and serovar distribution vary. In theUnited States, the three most common serovars are SalmonellaEnteritidis, Salmonella Typhimurium, and Salmonella Newport(CDC, 2011); in Canada, Salmonella Enteritidis and SalmonellaTyphimurium are also the most common serovars associatedwith human infections, but Salmonella Heidelberg was thethird and Salmonella Newport was the sixth most commonlyreported serovar (PHAC, 2012b). These differences demon-strate that surveillance data from one country cannot be di-rectly applied to another.

The Salmonella Heidelberg and Salmonella Enteritidis storiesdemonstrate that regional differences in pathogen prevalenceand AMR also exist. In order for interventions to effectivelyprevent and control future disease, these regional differencesneed to be recognized. While exposure routes may be local-ized, it is impossible to make linkages to primary drivers ifsurveillance and research are done only in the local contextand in isolation.

We highlighted the utility of integrated enteric pathogensurveillance at different scales by focusing on three Salmonellastories. The differences observed in Salmonella recovery fromchicken legs and breasts underscore the need to investigatepotential reasons for this difference and help fuel research toaddress the following: (1) Which meat products are mostcommonly consumed by Canadians? (2) What factors driveconsumer choices? and (3) Are different AMR patterns re-covered from different cuts of meat?

The Salmonella Enteritidis story illustrates the importance ofongoing surveillance of human cases and exposure sources toinform domestic control strategies. This is particularly true forthis serovar because source attribution is limited by the lowdiscriminatory power of available molecular techniques. C-EnterNet data identified international travel as an importantrisk factor for certain Salmonella Enteritidis phage types andboth programs (C-EnterNet and CIPARS) identified poultryas an important exposure source. Although the same Salmo-nella Enteritidis phage types are observed in broiler chicken

754 PARMLEY ET AL.

and humans, most of the current and proposed policies inCanada (Keery, 2010; DeWinter et al., 2011) focus on eggs.This is likely due to historical and international data linkingSalmonella Enteritidis outbreaks with eggs and may not fullyinclude the current data available about this serovar inbroiler chicken meat. Similar data from the United Statesalso support the important role of domestically producedchicken in the epidemiology of Salmonella Enteritidis (Chaiet al., 2012).

The ceftiofur-resistant Salmonella Heidelberg story dem-onstrates the ability of integrated surveillance to identify aconcurrent issue in an exposure source and human diseaseand how integrated surveillance can be used to evaluate thesuccess of an intervention. This issue would not have beenidentified without the broad CIPARS lens and illustrates howlocation can influence risk. It further highlights that theplanned expansion of C-EnterNet to more sentinel sites andincorporation of AMR testing into the C-EnterNet frameworkwill have benefits. CIPARS was designed to capture AMUand AMR data but, to date, collection of AMU data, particu-larly from livestock sectors, has been limited, reducing ourability to correlate use with emerging AMR patterns. CIPARSand C-EnterNet are working together to support surveillanceand research activities to explain how and why antimicrobialagents are used, what drives the prescribing practice of vet-erinarians and medical doctors, what influences producer andpractitioner decisions to use drugs, and what proportion ofresistant infections may be related to travel. C-EnterNet hasadded questions to their standardized questionnaire aboutAMU and efforts are under way to test all C-EnterNet isolatesfor AMR.

Conclusions

Analyzing data from various surveillance and monitoringprograms together provides an effective way to gain a moreholistic understanding of enteric disease and AMR in Canada.Collectively, the work of CIPARS and C-EnterNet along withthe findings from environmental monitoring programs isgreater than the sum of their individual parts. Together theyact synergistically to provide a multidimensional picture ofthe complex relationships between enteric pathogens, theenvironment, and the health of humans and animals. CIPARSand C-EnterNet, in conjunction with other governmententeric-pathogen monitoring programs, represent One Healthin action in Canada.

Acknowledgments

We thank all of the field workers for sample collection andlaboratory technicians working in Provincial Public HealthLaboratories and PHAC, Environment Canada (EC), andAgriculture and Agri-Food Canada (AAFC) laboratories fortheir technical assistance. Financial support for CIPARS isprovided by the PHAC, Health Canada, AAFC, and theCanadian Food Inspection Agency. Financial support forC-EnterNet is provided by the PHAC.

Disclosure Statement

No competing financial interests exist.

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Address correspondence to:Elizabeth Jane Parmley, PhD

Laboratory for Foodborne ZoonosesPublic Health Agency of Canada

160 Research Lane, Suite 103Guelph, Ontario, Canada N1G 5B2

E-mail: Jane.Parmley@phac-aspc.gc.ca

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