Listeria, caramel apples and food contact surfaces

The 2014 caramel apple listeriosis outbreak was traced back to cross-contamination between food contact surfaces (FCS) of equipment used for packing and fresh apples. For Washington State, the leading apple producer in the U.S with 79% of its total production directed to the fresh market, managing the risk of apple contamination with Listeria monocytogenes within the packing environment is crucial. The objectives of this study were to determine the prevalence of Listeria spp. on FCS in Washington State apple packinghouses over two packing seasons, and to identify those FCS types with the greatest likelihood to harbor Listeria spp.

Five commercial apple packinghouses were visited quarterly over two consecutive year-long packing seasons. A range of 27 to 50 FCS were swabbed at each facility to detect Listeria spp. at two timings of sampling, (i) post-sanitation and (ii) in-process (three hours of packinghouse operation), following a modified protocol of the FDA’s Bacteriological Analytical Manual method.

Among 2,988 samples tested, 4.6% (n=136) were positive for Listeria spp. Wax coating was the unit operation from which Listeria spp. were most frequently isolated. The FCS that showed the greatest prevalence of Listeria spp. were polishing brushes, stainless steel dividers and brushes under fans/blowers, and dryer rollers. The prevalence of Listeria spp. on FCS increased throughout apple storage time. The results of this study will aid apple packers in controlling for contamination and harborage of L. monocytogenes and improving cleaning and sanitation practices of the most Listeria-prevalent FCS.IMPORTANCE Since 2014, fresh apples have been linked to outbreaks and recalls associated with post-harvest cross-contamination with the foodborne pathogen L. monocytogenes These situations drive both public health burden and economic loss and underscore the need for continued scrutiny of packinghouse management to eliminate potential Listeria spp. niches. This research assesses the prevalence of Listeria spp. on FCS in apple packinghouses and identifies those FCS most likely to harbor Listeria spp. Such findings are essential for the apple packing industry striving to further understand and exhaustively mitigate the risk of contamination with L. monocytogenes to prevent future listeriosis outbreaks and recalls.

Prevalence of listeria species on food contact surfaces in Washington state apple packinghouses, 2021

Applied Environmental Microbiology

Blanca Ruiz-Llacsahuanga 1Alexis Hamilton 1Robyn Zaches 1Ines Hanrahan 2Faith Critzer 3

DOI: 10.1128/AEM.02932-20

3 sick: Another outbreak of listeriosis likely associated with prepackaged caramel apples

On December 1, 2017, PulseNet, the U.S. Centers for Disease Control’s molecular subtyping network for foodborne disease surveillance, identified a cluster of three Listeria monocytogenes clinical isolates with indistinguishable pulsed-field gel electrophoresis (PFGE) pattern combinations. These isolates were closely related to one another by whole-genome multilocus sequence typing within three allele differences (range = 0–3 alleles), indicating that the infections were likely from the same source.

CDC, the Food and Drug Administration (FDA), and state and local health departments initiated a multistate investigation. An outbreak case of listeriosis was defined as an infection with L. monocytogenes, with an isolate that was indistinguishable by PFGE and closely related by whole-genome multilocus sequence typing to the outbreak strain isolated during October–December 2017.

The cases corresponding to the three isolates were identified in Illinois, Iowa, and Michigan. Isolation dates ranged from October 15, 2017, to October 29, 2017. Patients ranged in age from 55 to 71 years (median = 69 years), and all three patients were male. All patients were hospitalized for listeriosis; no deaths were reported. PulseNet was queried routinely for new isolate matches during the investigation, and no additional cases were identified.

Interviews were conducted with all three patients or their surrogates using the standard Listeria Initiative questionnaire (1), which asks about a variety of foods consumed in the month preceding illness onset. Grocery store receipts were collected for the patient in Michigan. Review of reported exposures indicated that all three patients had consumed prepackaged caramel apples purchased from retail establishments in the month preceding illness onset. A case-case analysis was performed comparing exposure frequencies for all food items included in the Listeria Initiative questionnaire for the three outbreak-associated cases with exposure frequencies for 186 sporadic cases of listeriosis from the same states reported to CDC since 2006. Caramel apple consumption was significantly higher among patients included in the outbreak, compared with that among patients with sporadic illnesses (odds ratio = 21.7; 95% confidence interval = 2.3–infinity). None of the interviewed patients had leftover caramel apples in their home for testing.

State and local officials collected records at two of the three retail locations where caramel apples had been purchased. All three retailers sold the same brand of caramel apples (brand A). The product was packaged in a plastic clamshell containing three caramel apples, each on a stick. Caramel apples were seasonal products that were only available for a short period in the fall at two of the retail locations. However, the retail location where the Illinois patient purchased caramel apples had the product in stock at the time of the investigation. Eight packages of caramel apples were collected for testing by the Illinois Department of Public Health, but L. monocytogenes was not detected in any samples. It was not known whether the tested caramel apples were from the same lots as those consumed by the ill persons in this outbreak.

During an inspection at the caramel apple production facility, FDA reviewed records and practices and collected environmental samples for testing. No significant food safety concerns were observed. None of the environmental swabs yielded L. monocytogenes. Environmental swabs collected at a single whole apple supplier yielded L. monocytogenes, but it was not the outbreak strain. Traceback activities did not implicate a specific lot or supplier of whole apples used in brand A caramel apple production during the period of interest.

No additional outbreak-associated illnesses were identified during the investigation. In light of the limited shelf life of the product (reported by the production facility to be 15 days), it was unlikely that caramel apples consumed by ill persons in this outbreak would have still been available for purchase or in persons’ homes at the time of the investigation. Because there was no evidence to suggest an ongoing risk to the public, no public warning was issued by federal or state agencies.

Although the outbreak strain of L. monocytogenes was not isolated from caramel apples or their production environment, the epidemiologic evidence indicated that caramel apples were the suspected vehicle in this outbreak. All outbreak-associated ill persons consumed a specific brand of a relatively uncommon food product in the month before their illness onset, and all were infected with indistinguishable L. monocytogenes strains. Caramel apples were previously implicated in a large multistate outbreak of listeriosis during 2014–2015, caused by contamination of whole apples (2). Ready-to-eat food processors, including those that make caramel apples, could consider the introduction and persistence of L. monocytogenes in food production environments as a potential hazard and mitigate that risk through appropriate environmental monitoring and preventive controls (3). Further research into the control of L. monocytogenes in fresh produce, including fresh apples, might help identify prevention strategies to reduce or eliminate the pathogen in some ready-to-eat foods.


Notes from the field: Outbreak of listeriosis likely associated with prepackaged caramel apples



Jessica R. Marus, MPH1; Sally Bidol, MPH2; Shana M. Altman3; Oluwakemi Oni, MPH4; Nicole Parker-Strobe, MPH2; Mark Otto, MSPH5; Evelyn Pereira, MPH5; Annemarie Buchholz, PhD5; Jasmine Huffman1,6; Amanda R. Conrad, MPH1; Matthew E. Wise, PhD1

1Division of Foodborne, Waterborne, and Environmental Diseases, National Center for Emerging and Zoonotic Infectious Diseases, CDC; 2Michigan Department of Health and Human Services; 3Illinois Department of Public Health; 4Iowa Department of Public Health; 5Food and Drug Administration, Silver Spring, Maryland; 6Oak Ridge Institute for Science and Education, Oak Ridge, Tennessee.

All authors have completed and submitted the ICMJE form for disclosure of potential conflicts of interest. No potential conflicts of interest were disclosed.

Listeria in caramel apples changes apple safety focus

Chuck Robinson of Produce Retailer writes the Listeria outbreak connected to caramel apples in late 2014 and early 2015 gave the produce industry a slap to remind it to remain vigilant about food safety.

caramel.appleDiscussion of the outbreak dominated the first day of the seventh annual Center for Produce Safety Research Symposium on June 28-29.

That outbreak was traced to one apple supplier, Bidart Bros., Bakersfield, Calif. Only commercially produced, prepackaged whole caramel apples were involved.

There were 35 people from 12 states reported infected, according to the Centers for Disease Control and Prevention. Seven of them died before the case was closed, three of them linked to listeriosis.

Since the outbreak, the apple industry has changed focus from E. coli and compliance with Food Safety Modernization Act regulations to address listeria’s threat to the industry, said Ines Hanrahan, project manager for the Washington Tree Fruit Research Commission, Wenatchee.

In general, more attention to details is required to maintain sanitation, she said, including getting rid of standing water and daily cleaning zones that come into contact with food. Brushes need to be cleaned more frequently and dunk tanks must be cleaned and the water changed more often.

The stronger focus requires bigger cleaning crews and more time allotted to cleaning, she said. Training and rewards for improvement also are demanded.

“It’s about the people cleaning the brushes every day understanding why they are cleaning the brushes,” Hanrahan said.

The advent of whole genome sequencing, which provides more detailed and precise data for identifying outbreaks than the current standard technique, will mean more outbreaks will be detected, warned Martin Wiedmann, a food safety professor for Cornell University, Ithaca, N.Y. The produce industry must be prepared.

As the caramel apple-linked outbreak shows, the industry should realize what is happening in the field is of secondary importance, he said.

“I think we need to focus on our processing and packing facilities,” Wiedmann said.

There were many reasons at the outset of the investigation to not expect apples to be the outbreak source, said Kathleen Glass, associate director of the Food Research Institute at the University of Wisconsin-Madison. Reasons include the fact that the apples were sanitized and then dipped in hot caramel, which would seem likely to kill listeria. Also, the fruit is acidic, which would discourage listeria growth.

“You put all these factor together, and you don’t think apples are going to be a likely source of Listeria monocytogenes,” Glass said.”

However, the stems and calyxes of the fruit can harbor listeria, and pushing wooden stick through the calyx into the core also pushed listeria there.

“I’m really kind of surprised we hadn’t seen this sort of problem before,” Glass said.

Pat Kennelly, chief of the food safety section of the food and drug branch of California Department of Public Health, said problems were widespread at the Bidart Bros. packing facility. His staff’s investigation began well after the facility had closed operations for the season on Oct. 31.

“Given the level of contamination we found a month after operations had ceased, I can’t imagine what we would have found if we had tested when it was in operation,” Kennelly said.

It’s the stick: Listeria grows on caramel apples at room temp

A 2014 multistate listeriosis outbreak was linked to consumption of caramel-coated apples, an unexpected and previously unreported vehicle for Listeria monocytogenes. This outbreak was unanticipated because both the pH of apples (<4.0) and the water activity of the caramel coating (<0.80) are too low to support Listeria growth.

caramel.appleIn this study, Granny Smith apples were inoculated with approximately 4 log10 CFU of L. monocytogenes (a cocktail of serotype 4b strains associated with the outbreak) on each apple’s skin, stem, and calyx. Half of the apples had sticks inserted into the core, while the remaining apples were left intact. Apples were dipped into hot caramel and stored at either 7°C or 25°C for up to 11 or 28 days, respectively. Data revealed that apples with inserted sticks supported significantly more L. monocytogenes growth than apples without sticks under both storage conditions.

Within 3 days at 25°C, L. monocytogenes populations increased >3 log10 in apples with sticks, whereas only a 1-log10 increase was observed even after 1 week for caramel-coated apples without sticks. When stored at 7°C, apples with sticks exhibited an approximately 1.5-log10 increase in L. monocytogenes levels at 28 days, whereas no growth was observed in apples without sticks. We infer that insertion of a stick into the apple accelerates the transfer of juice from the interior of the apple to its surface, creating a microenvironment at the apple-caramel interface where L. monocytogenes can rapidly grow to levels sufficient to cause disease when stored at room temperature.

No growth of L. monocytogenes occurred on refrigerated caramel apples without sticks, whereas slow growth was observed on refrigerated caramel apples with sticks. In contrast, significant pathogen growth was observed within 3 days at room temperature on caramel apples with sticks inserted. Food producers should consider interfaces between components within foods as potential niches for pathogen growth.

Growth of Listeria monocytogenes within a Caramel-Coated Apple Microenvironment

doi: 10.1128/mBio.01232-15; 13 October 2015; mBio; vol. 6; no. 5; e01232-15

Kathleen A. Glass, Max C. Golden, Brandon J. Wanless, Wendy Bedale, Charles Czuprynski

US apple industry questions FDA’s response on caramel apple outbreak

Tom Karst of The Packer writes that in a presentation to the U.S. Apple Association’s Outlook and Marketing Conference Aug. 20, the Food and Drug Administration’s Roberta Wagner took questions from the audience about pending food safety rules and the fallout from the foodborne illness outbreak in late 2014 linked to Listeria monocytogenes in caramel apples.

caramel.appleOne audience member asked Wagner, associate director for Food Safety Modernization Act Operations at FDA, about the agency’s unclear messages about whether whole apples were involved. He asked her if whole fresh apples were implicated in the outbreak.

“I can tell you the statistic we are showing are only for caramel apples,” she said.

According to the Centers for Disease Control and Prevention, 35 people were sickened, 34 hospitalized and three died as a result of the outbreak linked to caramel apples.

“One of the research areas we need to (address) is why caramel apples and not apples?” she said.

Another conference attendee noted that foreign governments blocked imports of whole fresh apples.

“What is the FDA going to do so we hopefully curb that in the future?” he said.

Wagner said the FDA can’t control actions by other governments, but that the FDA will work with agriculture officials in other countries to defuse any concerns.

Listeria monocytogenes linked to whole apples used in commercially produced, prepackaged caramel apples – United States, 2014-2015

To be presented at the U.S. Centers for Disease Control and Prevention’s 64th Annual Epidemic Intelligence Service (EIS) conference April 20-23 in Atlanta.

caramel.appleBackground: Listeria monocytogenes (Lm) infection is the third leading cause of death from foodborne illness in the United States. Lm isolates undergo pulsed-field gel electrophoresis (PFGE) and whole genome sequencing (WGS) to identify disease clusters. In November 2014, two multistate clusters of Lm infections with distinct PFGE patterns were detected. Due to geographic and temporal overlap and a case with co-infection, they were investigated together to identify the source and prevent illnesses.

Methods: Cases were defined as illnesses with highly related Lm strains by WGS reported to PulseNet, the national molecular subtyping network for foodborne disease surveillance, with onset from 10/17/2014 to 2/12/2015. Information was collected on foods consumed in the weeks before illness onset using hypothesis-generating questionnaires and open-ended interviews. Case-patient food exposures were compared with data from listeriosis patients with genetically unrelated Lm using Fisher’s exact test. Traceback was performed to identify the suspect food source. WGS was performed on all case-patient, produce, and environmental isolates.

Results: Thirty-five cases from 12 states and 1 from Canada were identified; 34 patients were hospitalized and seven died. Three cases of meningitis occurred among healthy children. Twenty-eight (90%) of 31 patients reported consuming prepackaged caramel apples (multiple brands) compared with 1 (2.8%) of 36 patients with unrelated Lm isolates (p<0.001). Environmental and produce samples from a common apple supplier were highly related to clinical isolates by WGS. Three caramel apple producers and the apple supplier issued voluntary recalls.

Conclusions: Whole apples used in prepackaged caramel apples were the outbreak source. This is a new vehicle for Lm infections. Research is needed to understand factors specific to caramel apple production to prevent further contamination and illness.

7 dead, 28 sick: Listeria tainted apples appear in Thailand, no ban

Thai authorities have confirmed the existence of listeriosis-associated apples imported from the U.S. to Thailand, advising the public to thoroughly wash fruits and vegetables before consumption.

caramel.appleThe Director-General of the Department of Medical Science (DMSC) Apichai Mongkol have addressed the warning issued from the U.S. Food and Drug Administration (FDA) about the recall of the apples from Bidart Bros. as the FDA have confirmed a contamination of Listeria in the apples.

Produce contaminated by Listeriosis have been confirmed in Thailand at the Laem Chabang port in Rayong province through a cargo vessel, as warned in the FDA’s document.

Two strains of Listeria monocytogenes were confirmed in the Bidart Bros apple processing plant near Bakersfield, California, the FDA said.

“Those same strains were also found in Bidart Bros. apples collected from a retailer,” the FDA said in a statement on Friday.

Multistate outbreak of Listeriosis linked to commercially produced, prepackaged caramel apples

As the number of illnesses increased to 32 from Listeria in caramel apples, clues emerged regarding the source of the original contamination.

caramel.appleThe U.S. Centers for Disease Control and Prevention reports:

◦       Three voluntary recalls of commercially produced, prepackaged caramel apples have been announced by Happy Apples, California Snack Foods, and Merb’s Candies after hearing from Bidart Brothers, an apple supplier, that there may be a connection between Bidart Brothers apples and this listeriosis outbreak.

◦       Investigators are continuing to work to identify if any other brands or types of commercially produced, prepackaged caramel apples may be linked to illnesses.

◦       CDC continues to recommend that U.S. consumers do not eat any commercially produced, prepackaged caramel apples, including plain caramel apples as well as those containing nuts, sprinkles, chocolate, or other toppings, until more specific guidance can be provided.

◦       Although caramel apples are often a fall seasonal product, contaminated commercially produced, prepackaged caramel apples may still be for sale at grocery stores and other retailers nationwide or may be in consumers’ homes.

• As of December 30, 2014, a total of 32 people infected with the outbreak strains of Listeria monocytogenes have been reported from 11 states.

◦       Thirty-one ill people have been hospitalized and six deaths have been reported. Listeriosis contributed to three of these deaths and it is unclear whether it contributed to an additional two deaths. The sixth death was unrelated to listeriosis.

◦       Ten illnesses were pregnancy-related (occurred in a pregnant woman or her newborn infant), with one illness resulting in a fetal loss.

◦       Three invasive illnesses (meningitis) were among otherwise healthy children aged 5–15 years.

◦       The Public Health Agency of Canada (PHAC) has identified 2 cases of listeriosis in Canada with the same PFGE patterns as seen in the US outbreak.

listeria4JoNel Aleccia of The Seattle Times reports that all of the retailers said they were issuing recalls after learning that Bidart Bros., a Bakersfield, Calif., apple producer, had voluntarily recalled fresh apples because they may be contaminated with listeria. In a letter to suppliers dated Dec. 22, company president Leonard A. Bidart said the firm had consulted with the federal Food and Drug Administration and California public health officials.

“Out of an abundance of caution tempered by our deep concern for public safety, we are instituting a recall of the processor apples we shipped to you during the 2014 season,” the letter said. However, no formal notification of the Bidart recall has been issued by the FDA or the California Department of Public Health.

In the Northwest, the Bidart move forced the recall of about 220 cases of prepackaged caramel apples distributed by Pacific Coast Fruit Company, said Ted Hendryx, executive vice president.

5 dead, 29 sick: Prepackaged caramel apples as a source of Listeria, what was the source?

The U.S. Centers for Disease Control and Prevention has updated its information on listeria in caramel apples outbreak, as the first lawsuit was filed.

  • caramel.appleCDC is collaborating with public health officials in several states and with the U.S. Food and Drug Administration (FDA) to investigate an outbreak of Listeria monocytogenes infections (listeriosis) linked to commercially produced, prepackaged caramel apples. Listeria can cause a serious, life-threatening illness.
  • The information CDC has at this time indicates that commercially produced, prepackaged caramel apples may be contaminated with Listeria and may be causing this outbreak.
  • Out of an abundance of caution, CDC recommends that U.S. consumers do not eat any commercially produced, prepackaged caramel apples, including plain caramel apples as well as those containing nuts, sprinkles, chocolate, or other toppings, until more specific guidance can be provided.
  • Although caramel apples are often a fall seasonal product, contaminated commercially produced, prepackaged caramel apples may still be for sale at grocery stores and other retailers nationwide or may be in consumers’ homes.
  • This investigation is rapidly evolving. New information will be provided as it becomes available.
  • As of December 22, 2014, a total of 29 people infected with the outbreak strains of Listeria monocytogenes have been reported from 10 states.
  • All 29 ill people have been hospitalized and, five deaths have been reported. Listeriosis contributed to three of these deaths and it is unclear whether it contributed to a fourth. The fifth death was unrelated to listeriosis.
  • Nine illnesses were pregnancy-related (occurred in a pregnant woman or her newborn infant).
  • Three invasive illnesses (meningitis) were among otherwise healthy children aged 5–15 years.
  • To date, 20 (87%) of the 23 ill people interviewed reported eating commercially produced, prepackaged caramel apples before becoming ill.
  • At this time, no illnesses related to this outbreak have been linked to apples that are not caramel-coated and not prepackaged or to caramel candy.
  • Investigators are working quickly to determine specific brands or types of commercially produced, prepackaged caramel apples that may be linked to illnesses and to identify the source of contamination.
  • This investigation is rapidly evolving, and new information will be provided as it becomes available.

The family of a California woman whose death was linked to the prepackaged caramel apples is suing the Safeway grocery chain for selling her the product.

listeria4The lawsuit filed in Santa Cruz County Superior Court Monday alleges that 81-year-old Shirlee Jean Frey bought caramel apples from a Safeway in Felton a few days before Halloween. She died on Dec. 2 after suffering from a listeria infection.

Frey’s family said health officials confirmed she was sickened with the same strains of listeria as four others whose deaths were linked to the caramel apples.

Safeway responded by pulling caramel apples off shelves as precaution.