Abstract
Cyclospora cayetanensis is a human-specific protozoan parasite that causes gastrointestinal illness, primarily through the ingestion of contaminated water or fresh produce. This study provides an epidemiological overview of cyclosporiasis in Canada from 2000 to 2022 using data from the Canadian Notifiable Disease Surveillance System, FoodNet Canada, and outbreak investigations. A total of 5337 cases were reported during this period, with the incidence increasing from 0.12 to 1.70 per 100,000 population. Seasonal peaks occurred between May and August of each year, and adults aged 30–59 years were disproportionately affected. Enhanced surveillance data identified international travel, particularly to resorts in Mexico, as a common exposure. National-level investigations occurred annually from 2013 to 2022, and various fresh produce items were identified as items of interest, but few investigations led to the identification of a source of illness. Advancements in molecular diagnostics since 2015 have likely contributed to the observed rise in case detection. This report underscores the burden of cyclosporiasis in Canada and highlights the need for continued surveillance, public health interventions targeting contaminated produce, and travel health messaging to mitigate outbreaks and reduce transmission. It also underscores the importance of real-time genetic typing to identify and differentiate clusters of closely related isolates that are more likely to share a common source.
Introduction
Cyclospora cayetanensis is an enteric protozoan parasite, specific to humans based on the latest scientific evidence, which causes gastrointestinal illness. Symptoms of cyclosporiasis typically include watery diarrhea, nausea, anorexia, cramps, and fatigue. Illness is typically self-limiting after 10–24 days; however, illness can be relapsing. Immunocompromised individuals may have prolonged illness (Arrowood et al, 2022). Infected individuals shed unsporulated oocysts in their feces; under controlled laboratory conditions, these oocysts require 7–15 days to sporulate and become infectious. However, the time and conditions required for sporulation in natural environment are unclear (Ortega and Sanchez, 2010). As a result, the infection does not pass directly from person to person but is transmitted through the ingestion of oocyst-contaminated water or fresh produce.
In Canada, cyclosporiasis is a reportable infection, and cases are reported through the Canadian Notifiable Disease Surveillance System (CNDSS). In the past, diagnosis was traditionally based on the detection of C. cayetanensis oocysts in stool using microscopy. Polymerase chain reaction (PCR)-based detection methods are also available (Li et al., 2020). However, testing methods and protocols vary between jurisdictions in Canada. Recently, genotyping methods have been developed in an effort to differentiate geographic isolates of C. cayetanensis and to link cases to one another and to specific foods (Barratt et al., 2021).
Cyclosporiasis is endemic in tropical and subtropical areas worldwide (Giangaspero and Gasser, 2019). Outbreaks were first reported in Canada and the United States in the mid-1990s (Herwaldt, 2000). A variety of fresh produce items contaminated in the country of origin and imported into North America have been implicated in outbreaks (Dixon et al., 2016; Casillas et al., 2019). In Canada, infections are associated with international travel or domestically acquired through the consumption of imported produce contaminated with oocysts.
This report describes the epidemiology of C. cayetanensis in Canada from 2000 to 2022, based on data collected through national surveillance data and reported outbreak investigations. The goals are to improve the understanding of the epidemiology of the pathogen and to inform control measures to minimize further infections.
Materials and Methods
Data sources
National surveillance data
From 2000 to 2022, a case of cyclosporiasis was defined as a laboratory confirmation of infection through identification of C. cayetanensis oocysts in stool, duodenal/jejunal aspirate or small bowel biopsy, in a person with or without clinical illness (Public Health Agency of Canada, 2009). Since 2000, all laboratory-confirmed cases of cyclosporiasis in Canada meeting the case definition are reportable to the Public Health Agency of Canada (PHAC) through the CNDSS. Data collected through this system include age, sex, month and year of episode date, and province of residence. Episode date is based on a hierarchy of onset date, report date, and date of diagnosis or laboratory test date, depending on the earliest date available. Cases missing episode date information, or for which only the year was reported, were excluded from seasonal trend analyses.
FoodNet Canada data
FoodNet Canada, the integrated sentinel site surveillance network for enteric disease in Canada, is facilitated by the PHAC (Public Health Agency of Canada, 2013). Laboratory-confirmed cases of cyclosporiasis reported within a sentinel site are interviewed with an enhanced standardized questionnaire. Information collected includes clinical, travel, and risk exposure details. FoodNet Canada classifies cases as either endemic (sporadic, domestically acquired), nonendemic (immigration-related), outbreak-related, travel-related (outside of Canada within the incubation period), or lost to follow-up. Outbreak-related cases can be further classified (e.g., outbreak-endemic, outbreak-lost to follow-up). For this analysis, outbreak-endemic cases were included within the overall “endemic” category. Lost to follow-up, including outbreak-lost to follow-up cases, and nonendemic cases were excluded from this analysis.
Data were obtained for all cyclosporiasis cases reported in any of the FoodNet Canada sentinel sites from 2010 to 2022. This included data from the Quebec site (Région sociosanitaire de la Montérégie, July 2019 to December 2022), the Ontario pilot site (Region of Waterloo, January 2010 to March 2014), the current Ontario site (Middlesex-London Health Unit, August 2014 to December 2022), the Alberta site (Alberta Health Services: Calgary and Central Zones, June 2014 to December 2022), and the British Columbia site (Fraser Health, April 2010 to December 2022). In 2022, the boundaries of the Alberta site changed. The following communities were removed: Southeast Quadrant of Calgary, City of Airdrie, Camrose County, and Wetaskiwin County.
Investigation data
Outbreak Summaries is a Canadian surveillance system used to summarize and share the results of outbreak investigations. The system was established in 2008, and as of 2022, 11 of 13 provinces/territories participate in the program. An initial list of cyclosporiasis investigations since 2008 was extracted on May 24, 2024. Data were supplemented with: (1) a review of national investigation records retained by the Outbreak Management Division of PHAC, (2) a review of literature for Canadian cyclosporiasis outbreaks from 2000 to 2022, and (3) review of the Publicly Available International Foodborne Outbreak Database maintained by PHAC.
Investigations were identified as “event-associated” if all cases were linked to a single event (e.g., conference) or “community-associated” if there was no single event linking the cases. Investigations were classified as solved when a source was identified. However, if no source was identified, but certain food items were of interest without being conclusively linked, the investigation was not considered solved. Episode date was based on a hierarchy of onset date, report date, and date of diagnosis or laboratory test date, depending on the earliest date available.
National-level investigations of cyclosporiasis since 2014 have included all endemic cases of cyclosporiasis with an onset date after May 1st and without travel outside the United States or Canada in the 14 days prior to illness onset.
Data analysis
Data were analyzed using Stata 15 software (College Station, TX). Incidence rates were calculated using Canadian population data obtained from Statistics Canada (2024).
Results
National surveillance data
Since becoming a notifiable disease in 2000, between 28 and 63 (median of 175) laboratory-confirmed cases of cyclosporiasis have been reported annually. The national incidence of cyclosporiasis increased from 0.12 per 100,000 in 2000 to 1.70 per 100,000 in 2022 (Fig. 1). The majority of cases (80.5%) occurred between May and August (Fig. 2). Cases have been reported in 9 of the 10 provinces and all 3 territories. Adults from 30 to 59 years of age had the highest incidence rates, with children under the age of 15 having lower incidence rates (Table 1).
Incidence rate per 100,000 of cyclosporiasis cases reported to the Canadian Notifiable Disease Surveillance System (CNDSS), Canada, 2000–2022.
Number of cyclosporiasis cases reported to the Canadian Notifiable Disease Surveillance System (CNDSS) by month of episode date, 2000–2022 (N = 5272).
Characteristics of Cyclosporiasis Cases Reported to the CNDSS, Canada, 2000–2022
Percentages may not total 100% due to rounding. CNDSS, Canadian Notifiable Disease Surveillance System.
FoodNet Canada data
A total of 169 cases were reported in the FoodNet Canada sites from 2010 to 2022. Of these cases, 24 were lost to follow-up and 1 was immigration-related. These 25 cases were excluded from the analysis, leaving a total of 144 cases.
For the cases included in this analysis, the majority traveled internationally during their incubation period (60.4%; 87/144). Mexico was the most common destination reported by international travel-related cases (63.2%; 55/87) (Table 2). All of the cases reporting travel to Mexico, except one case, had onset dates between May and August. For cases with travel details available, the majority traveled to the Mexican State of Quintana Roo (86.7%; 39/45) and most stayed at a resort during their trip (85.2%; 46/54).
Cases of Cyclosporiasis Reported to FoodNet Canada by Month of Onset Including International Travel, 2010–2022
Percentages may not total 100% due to rounding.
Excludes 24 reported cases that were classified as lost to follow-up; also excludes one case classified as nonendemic (immigration-related).
Includes 37 cases that were part of endemic outbreak investigations.
International travel-related cases, including cases that traveled to the United States.
Investigation data
From 2000 to 2022, 23 investigations of domestically acquired cyclosporiasis were reported in Canada (Table 3). The majority of the investigations were community-associated investigations, 82.6% (19/23), and of these, 21.1% (4/19) were considered solved. All sources identified were contaminated fresh produce (i.e., basil, sugar snap peas, prepackaged salad, cilantro, and parsley). Four (17.4%, 4/23) of the investigations were associated with a specific event or events, with 75.0% (3/4) of these investigations identifying a source of infection (i.e., basil or cool pesto crunch).
Reported Investigations of Domestically Acquired Cyclosporiasis in Canada, 2000–2022
Distribution of cases within Canada. Investigation was considered single province if all cases were located in a single province. If cases were located in two or more provinces, location was reported as multiple provinces.
Investigations were considered community if the illness occurred within the general population (i.e., not limited to a particular event); event-based investigations occurred when illness was linked to a specific event.
A source of illness was conclusively identified, and the investigation was considered solved.
Food item(s) was considered an item of interest in investigation but evidence was not conclusive, so the investigation was considered unsolved.
Data are not available.
The first investigation coordinated at the national level, with cases in two or more provinces, was reported in 2008. From 2013 to 2022, an investigation with cases in multiple provinces occurred each year from April–May to September–October. These investigations each had large numbers of cases (25–399), and the median age of cases ranged from 46 to 56 years. These investigations involved a collaboration of local, provincial, and national public health professionals. One (1/10) was solved, identifying a prepackaged salad and imported cilantro and parsley from Mexico as a source of infections. A community outbreak in 2014 with cases in multiple provinces included six cases that attended the same catered event. A cohort analysis was conducted and identified blackberries and blueberries as items of interest.
The percent of endemic cases was less than half of the total number of cases reported with onsets between May and August prior to 2019; since that time, the percent of endemic cases has increased (Table 4).
Cases of Cyclosporiasis Reported to the CNDSS, 2014–2022, with Episode Dates Between May and August Compared with the Number of Endemic Cases Reported
Percentages may not total 100% due to rounding. CNDSS, Canadian Notifiable Disease Surveillance System.
% is the percentage of cases reported to CNDSS between May and August out of the total number of cases reported to CNDSS that year.
Cases reported as part of national investigations with no travel reported outside of Canada or the United States during the 14 days prior to illness onset, with onset dates between May and August.
% is the percentage of endemic cases reported between May and August out of the number of cases reported to CNDSS between May and August that year.
Includes six cases reported as part of a provincial investigation with onset dates in August (Whitfield et al., 2017).
Discussion
Surveillance trends
The national incidence rate has been steadily increasing since 2000, with the exception of a large drop in cases in 2021. The yearly number of reported cases is likely an underestimate of the true burden of disease; 654 reported illnesses in 2022 represent an estimated total burden of 35,471 cases of cyclosporiasis in Canada (Thomas et al., 2013). Incidence rates by province or territory show considerable variation, with the highest rates being reported in Ontario and British Columbia; this may be due in part to variations in testing practices.
The change in reported incidence rate is likely reflective of changes in disease occurrence as well as changes and surveillance practices. The change in laboratory testing practices may also account for some of the variation in incidence rates among provinces and territories. Traditional diagnostic methods involve fixing stool specimens on microscope slides and examining for C. cayetanensis oocysts under the microscope, which can be challenging and requires a high level of expertise. In recent years, there has been a shift to multiplex molecular assays for numerous pathogens, including C. cayetanensis. These assays provide rapid results and high-throughput testing (Almeria et al., 2023). Between 2015 and 2022, six provinces/territories moved to molecular testing for cyclosporiasis, which may have resulted in increased incidence rates (internal communication). Between 2000 and 2020, the national case definition for a confirmed case of cyclosporiasis required the identification of C. cayetanensis oocysts, but some provinces and territories included the detection of Cyclospora spp. by PCR in their provincial/territorial case definitions during this time frame. The switch to molecular testing has been demonstrated to lead to an increased incidence rate for other parasites (Johnson et al., 2020). In 2023, the national case definition was officially changed to include detection of C. cayetanensis oocysts or nucleic acid (Public Health Agency of Canada, 2024a).
Data collected by FoodNet Canada showed that 60% of cases, excluding those classified as lost to follow-up and nonendemic, traveled internationally within their incubation period. Data on international travel is not routinely collected for other national surveillance programs, but estimates from investigation data suggest that 55% of cases with onsets between May to August had no travel reported outside of Canada or the United States. However, this is in line with other studies which found that 63% of cases in British Columbia and 50% of cases in Ontario were associated with international travel (Taylor et al., 2010; Public Health Ontario, 2017). In contrast, the United States reported a smaller percentage, 18.8%, associated with international travel from 2011 to 2015 (Casillas et al., 2019).
There was considerable variation in the number of travel and endemic cases by year. The time frame of this study includes the COVID-19 pandemic (2020–2022) when international travel was restricted. A decrease in the proportion and incidence rates of cases classified as international travel-related was observed due to the COVID-19 pandemic in 2020 and 2021 and associated public health measures, including travel restrictions. This has been shown to impact the reported incidence rate of a number of other enteric infections as well (Dougherty et al., 2023). Changes in care-seeking behavior might have also impacted the number of reported cases in 2021 and 2022.
A seasonal pattern to endemic and travel cases was observed, with most cases occurring between May and August. The same seasonality has been observed in both travel and domestic cases in the United States (Casillas et al., 2019). A similar seasonality has been observed in Honduras and Mexico, with most cases occurring during May or June through August, corresponding to the rainy season in these countries (Kaminsky et al., 2016; Orozco-Mosqueda et al., 2014).
The most common travel destination reported by cyclosporiasis cases was Mexico. Studies from other countries have also reported cyclosporiasis to be linked to travel to Mexico (Marques et al., 2017). Mexico is a popular destination for Canadian travelers (Statistics Canada, 2016).
Investigations
National investigations of domestically acquired cyclosporiasis have occurred annually from 2013 to 2022. In the past, national investigations were hampered by the lack of genetic typing methods to understand the genetic relationship among cases. Genetic testing methods have been developed and used retrospectively to analyze C. cayetanensis isolates associated with national investigations (Yanta et al., 2022). These authors found multiple genetic clusters in the national investigations, suggesting that multiple sources of infection account for the increase we see each year in Canada from May to August. Prospective genetic typing in real time has been ongoing at the National Microbiology Laboratory (PHAC) during the summer Cyclospora season since 2020. This work has the potential to aid in outbreak investigations by identifying and differentiating smaller clusters of isolates that are closely related genetically and, therefore, more likely to be from the same source. The revised national case definition for cyclosporiasis recommends untreated or unfixed specimens be submitted to support PCR-based methodologies and downstream molecular surveillance (Public Health Agency of Canada, 2024a).
Many innovative investigation techniques and strategies have been used in Canada to investigate cyclosporiasis outbreaks. These include the review and analysis of import data for fresh produce to understand the country of origin for products of interest and how these can vary over the outbreak time period. In addition, public health professionals have proactively collected consumption data from the public on specific high-risk food items (e.g., blackberries, cilantro) to have real-time reference values available for comparison purposes. These data were collected using short online surveys that appear when individuals visit a specific website. This was first done by British Columbia in 2018 and was subsequently done at the national level in 2019 (Taylor and Galanis, 2020). In this study, a review of investigations shows that it is beneficial to prioritize clusters of cases with similar exposures (e.g., restaurants or events). Investigations associated with specific events were solved 75% (3/4) of the time compared with community investigations in which only 21.1% (4/19) were solved.
Continued surveillance and outbreak investigations are key to implementing public health interventions targeting contaminated produce to mitigate transmission. From 1996 to 1999, annual outbreaks of cyclosporiasis in North America were attributed to the consumption of fresh raspberries imported from Guatemala. Following the implication of this specific product, public health professionals in the United States were able to take regulatory action on the importation of this product in 1998, preventing further outbreaks in that country. A similar ban on imports of fresh raspberries from Guatemala between March and August was put into place in Canada the following year (Herwaldt, 2000; Canadian Food Inspection Agency, 2013). In addition, outbreaks of cyclosporiasis in Texas in 2012, 2013, and 2014 were traced back to fresh cilantro from Puebla, Mexico, leading to an import alert in the United States from April to August of each year (Casillas et al., 2019). In response, Mexico developed the System for the Reduction of Contamination Risks, a voluntary system for producers. Canada permits the import of fresh cilantro certified under this system (Canadian Food Inspection Agency, 2020).
This description of the epidemiology of Cyclospora is subject to several limitations. Reported illness is an underrepresentation of the true burden of disease due to underreporting and variations in diagnostic practices across jurisdictions. Additionally, the transition to molecular testing methods complicates comparison of incidence rates over time and among provinces and territories. Finally, follow-up procedures, such as how exposure periods are defined, vary among and within provinces and territories in Canada, leading to potential inconsistencies in how travel-related cases are classified.
Conclusions
Data from various surveillance programs and outbreak investigations give us a more comprehensive picture of the epidemiology of cyclosporiasis in Canada. Data show that both travel-associated and endemic cases account for a considerable and growing number of cases each year in Canada. This trend should continue to be monitored, and separate public health actions or messaging may be needed to reduce the risk of exposure to C. cayetanensis in Canada and among international travelers. There also appears to be a considerable burden of illness associated with domestic exposures, suggesting the need for continued surveillance of imported fresh produce.
Footnotes
Acknowledgments
The authors would like to thank the local and provincial public health organizations, including those within the FoodNet Canada sentinel sites, for their contributions to national surveillance programs and investigations.
Authors’ Contributions
V.M.: Conceptualization, formal analysis, writing—original draft, and writing—review and editing. R.J. and D.D.: Formal analysis, writing—original draft, and writing—review and editing. B.D. and R.G.: Writing—review and editing.
Disclosure Statement
No competing financial interests exist.
Funding Information
No funding was received for this article.