North American Cyclospora outbreaks

My aunt got sick from Cyclospora in some basil-based thingy in Florida, in 2005.

She was sick for weeks.

On June 12, 1996, Ontario’s chief medical officer, Dr. Richard Schabas, issued a public health advisory on the presumed link between consumption of California strawberries and an outbreak of diarrheal illness among some 40 people in the Metro Toronto area. The announcement followed a similar statement from the Department of Health and Human Services in Houston, Texas, who were investigating a cluster of 18 cases of Cyclospora illness among oil executives.

Dr. Schabas advised consumers to wash California berries “very carefully” before eating them, and recommended that people with compromised immune systems avoid them entirely. He also stated that Ontario strawberries, which were just beginning to be harvested, were safe for consumption. Almost immediately, people in Ontario stopped buying strawberries. Two supermarket chains took California berries off their shelves, in response to pressure from consumers. The market collapsed so thoroughly that newspapers reported truck drivers headed for Toronto with loads of berries being directed, by telephone, to other markets.

However, by June 20, 1996, discrepancies began to appear in the link between California strawberries and illness caused by the parasite, Cyclospora, even though the number of reported illnesses continued to increase across North America. Texas health officials strengthened their assertion that California strawberries were the cause of the outbreak, while scientists at the U.S. Centers for Disease Control and Prevention (CDC) and the Food and Drug Administration (FDA) said there were not yet ready to identify a food vehicle for the outbreak. On June 27, 1996, the New York City Health Department became the first in North America to publicly state that raspberries were also suspected in the outbreak of Cyclospora.

By July 18, 1996, the CDC declared that raspberries from Guatemala — which had been sprayed with pesticides mixed with water that could have been contaminated with human sewage containing Cyclospora — were the likely source of the Cyclospora outbreak, which ultimately sickened about 1,000 people across North America. Guatemalan health authorities and producers have vigorously refuted the charges. The California Strawberry Commission estimates it lost $15 million to $20 million in reduced strawberry sales.

Cyclospora cayetanensis is a recently characterised coccidian parasite; the first known cases of infection in humans were diagnosed in 1977. Before 1996, only three outbreaks of Cyclospora infection had been reported in the United States. Cyclospora is normally associated with warm, Latin American countries with poor sanitation.

One reason for the large amount of uncertainty in the 1996 Cyclospora outbreak is the lack of effective testing procedures for this organism. To date, Cyclospora oocysts have not been found on any strawberries, raspberries or other fruit, either from North America or Guatemala. That does not mean that cyclospora was absent; it means the tests are unreliable and somewhat meaningless. FDA, CDC and others are developing standardized methods for such testing and are currently evaluating their sensitivity.

The initial, and subsequent, links between Cyclospora and strawberries or raspberries were therefore based on epidemiology, a statistical association between consumption of a particular food and the onset of disease. For example, the Toronto outbreak was first identified because some 35 guests attending a May 11, 1996 wedding reception developed the same severe, intestinal illness, seven to 10 days after the wedding, and subsequently tested positive for cyclospora. Based on interviews with those stricken, health authorities in Toronto and Texas concluded that California strawberries were the most likely source. However, attempts to remember exactly what one ate two weeks earlier is an extremely difficult task; and larger foods, like strawberries, are recalled more frequently than smaller foods, like raspberries. Ontario strawberries were never implicated in the outbreak.

Once epidemiology identifies a probable link, health officials have to decide whether it makes sense to warn the public. In retrospect, the decision seems straightforward, but there are several possibilities that must be weighed at the time. If the Ontario Ministry of Health decided to warn people that eating imported strawberries might be connected to Cyclospora infection, two outcomes were possible: if it turned out that strawberries are implicated, the ministry has made a smart decision, warning people against something that could hurt them; if strawberries were not implicated, then the ministry has made a bad decision with the result that strawberry growers and sellers will lose money and people will stop eating something that is good for them. If the ministry decides not to warn people, another two outcomes are possible: if strawberries were implicated, then the ministry has made a bad decision and people may get a parasitic infection they would have avoided had they been given the information (lawsuits usually follow); if strawberries were definitely not implicated then nothing happens, the industry does not suffer and the ministry does not get in trouble for not telling people. Research is currently being undertaken to develop more rigorous, scientifically-tested guidelines for informing the public of uncertain risks.

But in Sarnia (Ontario, Canada) they got a lot of sick people who attended the Big Sisters of Sarnia-Lambton Chef’s Challenge on May 12, 2010.

Michael T. Osterholm, PhD, who has a lot of titles and once called me at 5 a.m. to tell me I was an asshole (maybe not the exact words, but the sentiment) and chair of the Holstein Blue-Ribbon Panel on the Prevention of Foodborne Cyclospora Outbreaks writes that the 1996 cyclosporiasis outbreak in the United States and Canada associated with the late spring harvest of imported Guatemalan-produced raspberries was an early warning to public health officials and the produce industry that the international sourcing of produce means that infectious agents once thought of as only causing traveler’s diarrhea could now infect at home. The public health investigation of the 1996 outbreak couldn’t identify how, when, where, or why the berries became contaminated with Cyclospora cayetanensis.

The investigation results were published in the New England Journal of Medicine in 1997. I was asked to write an editorial to accompany the investigation report.2 In my editorial, I noted the unknowns surrounding the C. cayetanensis contamination. The 1997 spring harvest of Guatemalan raspberries was allowed to be imported into both the United States and Canada—and again, a large outbreak of cyclosporiasis occurred. As in the 1996 outbreak, no source for the contamination of berries was found. Later in 1997, the Food and Drug Administration (FDA) prohibited the importation of future spring harvests of Guatemalan raspberries until a cause for the contamination could be demonstrated and corrective actions taken. While the FDA did not permit the 1998 importation of the raspberries into the United States, the berries continued to be available in Canada. Outbreaks linked to raspberries occurred in Ontario in May 1998. When the U.S. Centers for Disease Control and Prevention (CDC)-led investigative team published its 1997 outbreak findings in the Annals of Internal Medicine, 3 I was again asked to write an accompanying editorial.4 As I had done in my previous editorial, I highlighted how little we know about the factors associated with the transmission Cyclospora on produce and how to prevent it.

Unfortunately, the state of the art for preventing foodborne, produce-associated cyclosporiasis had changed little since the 1996 outbreak despite the relatively frequent occurrence of such outbreaks.

Thirty-four years after that first Guatemalan raspberry-associated outbreak — and a year after produce-associated cyclosporiasis outbreaks that were linked to U.S.-grown produce — there has been a major leap in prevention, yet the outbreaks still happen.

 Foodborne outbreaks of cyclosporiasis have been reported in the United States since the mid-1990s and have been linked to various types of imported fresh produce, including raspberries, basil, snow peas, mesclun lettuce, and cilantro; no commercially frozen produce has been implicated to date. U.S. foodborne outbreaks of cyclosporiasis that occurred before 2000 were summarized previously, as were the major documented outbreaks in 2013 and 2014. Foodborne outbreaks during the 18-year period of 2000–2017 are summarized here.

The table provides information about 39 reported foodborne outbreaks of cyclosporiasis that occurred in the United States during 2000–2017; the total case count was 1,730. No outbreaks were reported in 2003, 2007, or 2010. Overall, a median of two outbreaks were reported per year, with a median of 19 cases per outbreak (range, 3 to 582 cases). Although the outbreaks occurred during 8 different months (December through July), the peak months were May, June, and July. As indicated in the table, a food vehicle of infection was identified (or suspected) for 17 of the 39 outbreaks.

Identifying the particular food item/ingredient that caused an outbreak of cyclosporiasis can be very challenging—for example, if fresh produce was served as a garnish or topping or if several types of produce were mixed together. CDC and other agencies are working to develop and validate molecular typing methods that could distinguish among different strains of the parasite Cyclospora cayetanensis that causes cyclosporiasis. In the future, such tools could help link cases of cyclosporiasis to each other and to particular types of produce, which could help public health officials investigate and prevent cases and outbreaks of Cyclospora infection.

Table: Summary of U.S. foodborne outbreaks of cyclosporiasis, 2000–2017
Year(s)* Month(s)* Jurisdiction(s)* No. of cases† Food vehicle and source, if identified‡
2000 May Georgia 19 Raspberries and/or blackberries (suspected)
2000 June Pennsylvania 54 Raspberries
2001 January–February Florida 39
2001 January New York City 3
2001–02 December–January Vermont 22 Raspberries (likely)
2002 April–May Massachusetts 8
2002 June New York 14
2004 February Texas 38
2004 February Illinois 57 Basil (likely)
2004 May Tennessee 12
2004 May–June Pennsylvania 96 Snow peas from Guatemala ⁂
2005 March–May Florida 582 ¶ Basil from Peru
2005 May South Carolina 6
2005 April Massachusetts 58
2005 May Massachusetts 16
2005 June Connecticut 30 Basil (suspected)
2006 June Minnesota 14
2006 June New York 20
2006 July Georgia 3
2008 March Wisconsin 4 Sugar snap peas (likely) ⁂
2008 July California 45 ¶ Raspberries and/or blackberries (likely)
2009 June District of Columbia 34
2011 June Florida 12
2011 July Georgia 88**
2012 June–July Texas 16
2013†† June Iowa, Nebraska, and neighboring states 162 Bagged salad mix from Mexico
2013†† June–July Texas 38 Cilantro from Mexico
2013 July Wisconsin 8 Berry salad (suspected)
2014 June Michigan 14
2014‡‡ June–July Texas 26 Cilantro from Mexico
2014 July South Carolina 13
2015 May–July Georgia, Texas, and Wisconsin 90 Cilantro from Mexico
2016 June–July Texas 6¶¶ Carrots or green cabbage (suspected)
2017 May Florida 6 Berries (suspected)
2017 May–July Texas 38*** Scallions (i.e., green onions)
2017 June Michigan 29
2017 June Tennessee 4†††
2017 June Connecticut 3
2017 July Florida 3‡‡‡

* The entries in the first three columns refer to the known or likely year(s), month(s), and jurisdiction(s) in which the exposure(s) to Cyclospora occurred.

† The case counts include laboratory-confirmed and probable cases of cyclosporiasis. By definition, each outbreak included at least two linked cases, at least one of which was laboratory confirmed.

‡ A food vehicle is specified only if a single ingredient or commodity was identified in an outbreak investigation.

¶ Cases that occurred in Canadian travelers to the United States were not included.

** An additional 10 probable cases were associated with this outbreak but were not counted in the table: nine of these cases were in residents of states in which cyclosporiasis was not a reportable condition, and the other case was in a patient whose state of residence was unknown.

†† For additional details, see summary information about the outbreak investigations in 2013. For the purposes of this table, the exposure month(s) and case counts are limited to those explicitly linked in the investigations to the food item specified in the last column.

‡‡ For additional perspective, see summary information about outbreak investigations in 2014. For the purposes of this table, the exposure months and the case count for the outbreak in Texas are limited to those explicitly linked in the investigations to the food item specified in the last column.

¶¶ An additional nine suspected cases were identified in persons associated with this outbreak but were not counted in the table because of reporting issues (e.g., insufficient case data).

*** An additional three probable cases were identified in persons associated with this outbreak but were not counted in the table because of reporting issues (e.g., insufficient case data).

††† An additional two probable cases were identified in persons associated with this outbreak but were not counted in the table because of reporting issues (e.g., insufficient case data).

‡‡‡ One additional probable case was identified in a person associated with this outbreak but was not counted in the table because of a reporting issue.

⁂ More information to help distinguish among types of peas can be found herepdf icon.

Table: Summary of U.S. foodborne outbreaks of cyclosporiasis, 2000–2017
Year(s)* Month(s)* Jurisdiction(s)* No. of cases† Food vehicle and source, if identified‡
2000 May Georgia 19 Raspberries and/or blackberries (suspected)
2000 June Pennsylvania 54 Raspberries
2001 January–February Florida 39
2001 January New York City 3
2001–02 December–January Vermont 22 Raspberries (likely)
2002 April–May Massachusetts 8
2002 June New York 14
2004 February Texas 38
2004 February Illinois 57 Basil (likely)
2004 May Tennessee 12
2004 May–June Pennsylvania 96 Snow peas from Guatemala ⁂
2005 March–May Florida 582 ¶ Basil from Peru
2005 May South Carolina 6
2005 April Massachusetts 58
2005 May Massachusetts 16
2005 June Connecticut 30 Basil (suspected)
2006 June Minnesota 14
2006 June New York 20
2006 July Georgia 3
2008 March Wisconsin 4 Sugar snap peas (likely) ⁂
2008 July California 45 ¶ Raspberries and/or blackberries (likely)
2009 June District of Columbia 34
2011 June Florida 12
2011 July Georgia 88**
2012 June–July Texas 16
2013†† June Iowa, Nebraska, and neighboring states 162 Bagged salad mix from Mexico
2013†† June–July Texas 38 Cilantro from Mexico
2013 July Wisconsin 8 Berry salad (suspected)
2014 June Michigan 14
2014‡‡ June–July Texas 26 Cilantro from Mexico
2014 July South Carolina 13
2015 May–July Georgia, Texas, and Wisconsin 90 Cilantro from Mexico
2016 June–July Texas 6¶¶ Carrots or green cabbage (suspected)
2017 May Florida 6 Berries (suspected)
2017 May–July Texas 38*** Scallions (i.e., green onions)
2017 June Michigan 29
2017 June Tennessee 4†††
2017 June Connecticut 3
2017 July Florida 3‡‡‡

By July 18, 1996, the CDC declared that raspberries from Guatemala — which had been sprayed with pesticides mixed with water that could have been contaminated with human sewage containing Cyclospora — were the likely source of the Cyclospora outbreak, which ultimately sickened about 1,000 people across North America. Guatemalan health authorities and producers have vigorously refuted the charges. The California Strawberry Commission estimates it lost $15 million to $20 million in reduced strawberry sales.

Cyclospora cayetanensis is a recently characterised coccidian parasite; the first known cases of infection in humans were diagnosed in 1977. Before 1996, only three outbreaks of Cyclospora infection had been reported in the United States. Cyclospora is normally associated with warm, Latin American countries with poor sanitation.

One reason for the large amount of uncertainty in the 1996 Cyclospora outbreak is the lack of effective testing procedures for this organism. To date, Cyclospora oocysts have not been found on any strawberries, raspberries or other fruit, either from North America or Guatemala. That does not mean that cyclospora was absent; it means the tests are unreliable and somewhat meaningless. FDA, CDC and others are developing standardized methods for such testing and are currently evaluating their sensitivity.

The initial, and subsequent, links between Cyclospora and strawberries or raspberries were therefore based on epidemiology, a statistical association between consumption of a particular food and the onset of disease. For example, the Toronto outbreak was first identified because some 35 guests attending a May 11, 1996 wedding reception developed the same severe, intestinal illness, seven to 10 days after the wedding, and subsequently tested positive for cyclospora. Based on interviews with those stricken, health authorities in Toronto and Texas concluded that California strawberries were the most likely source. However, attempts to remember exactly what one ate two weeks earlier is an extremely difficult task; and larger foods, like strawberries, are recalled more frequently than smaller foods, like raspberries. Ontario strawberries were never implicated in the outbreak.

Once epidemiology identifies a probable link, health officials have to decide whether it makes sense to warn the public. In retrospect, the decision seems straightforward, but there are several possibilities that must be weighed at the time. If the Ontario Ministry of Health decided to warn people that eating imported strawberries might be connected to Cyclospora infection, two outcomes were possible: if it turned out that strawberries are implicated, the ministry has made a smart decision, warning people against something that could hurt them; if strawberries were not implicated, then the ministry has made a bad decision with the result that strawberry growers and sellers will lose money and people will stop eating something that is good for them. If the ministry decides not to warn people, another two outcomes are possible: if strawberries were implicated, then the ministry has made a bad decision and people may get a parasitic infection they would have avoided had they been given the information (lawsuits usually follow); if strawberries were definitely not implicated then nothing happens, the industry does not suffer and the ministry does not get in trouble for not telling people. Research is currently being undertaken to develop more rigorous, scientifically-tested guidelines for informing the public of uncertain risks.

But in Sarnia (Ontario, Canada) they got a lot of sick people who attended the Big Sisters of Sarnia-Lambton Chef’s Challenge on May 12, 2010.

Michael T. Osterholm, PhD, who has a lot of titles and once called me at 5 a.m. to tell me I was an asshole (maybe not the exact words, but the sentiment) and chair of the Holstein Blue-Ribbon Panel on the Prevention of Foodborne Cyclospora Outbreaks writes that the 1996 cyclosporiasis outbreak in the United States and Canada associated with the late spring harvest of imported Guatemalan-produced raspberries was an early warning to public health officials and the produce industry that the international sourcing of produce means that infectious agents once thought of as only causing traveler’s diarrhea could now infect at home. The public health investigation of the 1996 outbreak couldn’t identify how, when, where, or why the berries became contaminated with Cyclospora cayetanensis.

The investigation results were published in the New England Journal of Medicine in 1997. I was asked to write an editorial to accompany the investigation report.2 In my editorial, I noted the unknowns surrounding the C. cayetanensis contamination. The 1997 spring harvest of Guatemalan raspberries was allowed to be imported into both the United States and Canada—and again, a large outbreak of cyclosporiasis occurred. As in the 1996 outbreak, no source for the contamination of berries was found. Later in 1997, the Food and Drug Administration (FDA) prohibited the importation of future spring harvests of Guatemalan raspberries until a cause for the contamination could be demonstrated and corrective actions taken. While the FDA did not permit the 1998 importation of the raspberries into the United States, the berries continued to be available in Canada. Outbreaks linked to raspberries occurred in Ontario in May 1998. When the U.S. Centers for Disease Control and Prevention (CDC)-led investigative team published its 1997 outbreak findings in the Annals of Internal Medicine, 3 I was again asked to write an accompanying editorial.4 As I had done in my previous editorial, I highlighted how little we know about the factors associated with the transmission Cyclospora on produce and how to prevent it.

Unfortunately, the state of the art for preventing foodborne, produce-associated cyclosporiasis had changed little since the 1996 outbreak despite the relatively frequent occurrence of such outbreaks.

Thirty-four years after that first Guatemalan raspberry-associated outbreak — and a year after produce-associated cyclosporiasis outbreaks that were linked to U.S.-grown produce — there has been a major leap in prevention, yet the outbreaks still happen.

Foodborne outbreaks of cyclosporiasis have been reported in the United States since the mid-1990s and have been linked to various types of imported fresh produce, including raspberries, basil, snow peas, mesclun lettuce, and cilantro; no commercially frozen produce has been implicated to date. U.S. foodborne outbreaks of cyclosporiasis that occurred before 2000 were summarized previously, as were the major documented outbreaks in 2013 and 2014. Foodborne outbreaks during the 18-year period of 2000–2017 are summarized here.

The table provides information about 39 reported foodborne outbreaks of cyclosporiasis that occurred in the United States during 2000–2017; the total case count was 1,730. No outbreaks were reported in 2003, 2007, or 2010. Overall, a median of two outbreaks were reported per year, with a median of 19 cases per outbreak (range, 3 to 582 cases). Although the outbreaks occurred during 8 different months (December through July), the peak months were May, June, and July. As indicated in the table, a food vehicle of infection was identified (or suspected) for 17 of the 39 outbreaks.

Identifying the particular food item/ingredient that caused an outbreak of cyclosporiasis can be very challenging—for example, if fresh produce was served as a garnish or topping or if several types of produce were mixed together. CDC and other agencies are working to develop and validate molecular typing methods that could distinguish among different strains of the parasite Cyclospora cayetanensis that causes cyclosporiasis. In the future, such tools could help link cases of cyclosporiasis to each other and to particular types of produce, which could help public health officials investigate and prevent cases and outbreaks of Cyclospora infection.

Table: Summary of U.S. foodborne outbreaks of cyclosporiasis, 2000–2017
Year(s)* Month(s)* Jurisdiction(s)* No. of cases† Food vehicle and source, if identified‡
2000 May Georgia 19 Raspberries and/or blackberries (suspected)
2000 June Pennsylvania 54 Raspberries
2001 January–February Florida 39
2001 January New York City 3
2001–02 December–January Vermont 22 Raspberries (likely)
2002 April–May Massachusetts 8
2002 June New York 14
2004 February Texas 38
2004 February Illinois 57 Basil (likely)
2004 May Tennessee 12
2004 May–June Pennsylvania 96 Snow peas from Guatemala ⁂
2005 March–May Florida 582 ¶ Basil from Peru
2005 May South Carolina 6
2005 April Massachusetts 58
2005 May Massachusetts 16
2005 June Connecticut 30 Basil (suspected)
2006 June Minnesota 14
2006 June New York 20
2006 July Georgia 3
2008 March Wisconsin 4 Sugar snap peas (likely) ⁂
2008 July California 45 ¶ Raspberries and/or blackberries (likely)
2009 June District of Columbia 34
2011 June Florida 12
2011 July Georgia 88**
2012 June–July Texas 16
2013†† June Iowa, Nebraska, and neighboring states 162 Bagged salad mix from Mexico
2013†† June–July Texas 38 Cilantro from Mexico
2013 July Wisconsin 8 Berry salad (suspected)
2014 June Michigan 14
2014‡‡ June–July Texas 26 Cilantro from Mexico
2014 July South Carolina 13
2015 May–July Georgia, Texas, and Wisconsin 90 Cilantro from Mexico
2016 June–July Texas 6¶¶ Carrots or green cabbage (suspected)
2017 May Florida 6 Berries (suspected)
2017 May–July Texas 38*** Scallions (i.e., green onions)
2017 June Michigan 29
2017 June Tennessee 4†††
2017 June Connecticut 3
2017 July Florida 3‡‡‡

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About Douglas Powell

A former professor of food safety and the publisher of barfblog.com, Powell is passionate about food, has five daughters, and is an OK goaltender in pickup hockey. Download Doug’s CV here. Dr. Douglas Powell editor, barfblog.com retired professor, food safety 3/289 Annerley Rd Annerley, Queensland 4103 dpowell29@gmail.com 61478222221 I am based in Brisbane, Australia, 15 hours ahead of Eastern Standard Time