Product recalls are an unwelcome event among food manufacturers. In recent years, recalls for undeclared allergens have become the number-one reason for food product recalls. Often, the U.S. Food and Drug Administration (FDA) and/or the U.S. Department of Agriculture's Food Safety and Inspection Service (USDA-FSIS) classify recalls for undeclared allergens as Class 1 recalls because the products contain residues of undeclared priority food allergens that have been associated with severe allergic reactions, including fatalities.
Class 1 recalls are defined as situations where there is a reasonable probability that the use of or exposure to a food product will cause serious adverse health consequences or death to humans. Residues of most of the so-called "Big 8" (and soon-to-be "Big 9," with the recent addition of sesame seeds) allergenic foods are considered as a basis for Class 1 recalls. The Big 8 allergenic foods are milk, eggs, fish, crustacean shellfish (e.g., shrimp, crab, lobster), peanuts, soybeans, tree nuts (walnuts, cashews, etc.), and wheat. Residues of these Big 8 priority allergenic foods are almost always considered as a basis for Class 1 recalls.
Occasionally, when the undeclared residues are from wheat or involve ingredients with very low levels of detectable allergenic protein (e.g., soy lecithin), the recalls are classified as Class 2 recalls. With the recent passage of the FASTER Act by the U.S. Congress, FDA will soon add sesame seeds to the list of priority allergenic foods. Presumably, the presence of undeclared sesame seed residues will be considered as a basis for a Class 1 recall also because severe reactions, including death, have been attributed to inadvertent ingestion of sesame seed residues by sesame-allergic consumers.
While food allergen recalls are unwelcome, potentially valuable lessons can be learned from these unfortunate events. Good manufacturing practices (GMPs) have evolved from corrective actions taken to prevent allergen recalls. FDA evaluated the root causes of allergen recalls in Food Safety Magazine in 2014,1 and these root causes likely remain relevant. In 2014, packaging errors—including use of the incorrect package or label, terminology errors, or failure to carry forward allergen information from an ingredient to the final label—were prominent root causes of allergen recalls.
Terminology errors may have decreased in the ensuing years, although this is not certain. Terminology errors mostly involve failures to properly declare ingredients from allergenic sources in plain English language, as required by the Food Allergen Labeling and Consumer Protection Act of 2004 (FALCPA). For example, butter or flour might be listed as ingredients without clear declaration that butter is derived from milk or flour is derived from wheat. Cross-contact is another prominent causative factor in food allergen recalls.1 Cross-contact is defined as the unintentional incorporation of food allergen residues into a food that is not labeled as containing those allergens. Cross-contact can occur through use of shared manufacturing equipment, shared facilities, or other manufacturing practices.
As noted, FDA and USDA-FSIS consider all recalls involving undeclared priority allergen residues, with the exception of wheat residues in some cases by FDA, to be the basis for Class 1 recalls. The level of allergen residues in the packaged food product is not taken into consideration in most cases. The causative factors involved in food allergen recalls are not created equal.1 Packaging and labeling errors can, and often do, lead to high and risky levels of allergen residues in the affected food products. The use of undeclared rework or the incorrect ingredient can similarly lead to high levels of allergen residues. In contrast, cross-contact situations involving shared equipment or facilities often involve comparatively low levels of undeclared allergen residues that are sometimes detectable only in the first products made after an allergen changeover. However, if allergen residues are detected in a product, a Class 1 recall is often the result.
Products with undeclared allergen residues that result in consumer complaints are clearly the most serious scenarios. Of course, careful investigation is often required to ensure that the affected consumers have identified the correct product if several products are consumed in a meal occasion. As expected, FDA and USDA-FSIS do devote effort when consumer complaints are involved with a product. The goal for packaged food companies to avoid allergen recalls is to ensure that detectable levels of allergen residue will not be found in a product unless the ingredient is labeled or has a precautionary allergen label when residues are detectable, even after implementation of GMPs.
The 2011 Food Safety Modernization Act (FSMA) requires the implementation of hazard-based preventive controls for allergen residues. Clearly, effective labeling, packaging, and cross-contact controls will aid in the prevention of food allergen recalls. The authors wish to share examples of several past food allergen recall events to highlight the importance of root cause analysis and the implementation of corrective action in the promulgation of GMPs. We will not reveal the identities of the companies involved in these recalls, and have altered product descriptions (except for the spice recalls that were widely publicized at the time of those recalls) to prevent readers from easily guessing the identities of these companies. Some of these recalls occurred many years ago and led to corrective actions and best practices that have prevented future similar recalls within those companies.
In our view, the sharing of root causes and corrective actions is educational for other companies. Unfortunately, the FDA Recall Enterprise System (RES) does not always reveal the root cause or corrective actions involved in food allergen recall episodes and, thus, opportunities for other companies to learn from these unfortunate events are lost.
Recall Episode 1: Egg Residue in Canned Pasta
A manufacturer of retorted pasta products received several consumer complaints implicating a particular SKU of canned pasta in the causation of adverse reactions in egg-allergic children. The particular SKU was a new product that had been recently added to the company's portfolio. The symptoms involved in these adverse reactions were consistent with the symptoms of a food allergy reaction. The product did not divulge the presence of egg in the ingredient list.
An analysis of several containers of retained product from the implicated lot did not reveal the presence of detectable egg residue. The pasta in this product was obtained from a pasta supplier. The manufacturer of the implicated product decided to conduct an inspection of the pasta supplier's facility. In the course of that inspection, a location was discovered where a line transporting egg noodles crossed over a line transporting this company's non-egg product. The inspector was able to discern that egg noodles would periodically drop from the noodle line into the non-egg pasta. Subsequently, a tote of the finished non-egg pasta ingredient was found to contain several egg noodles on visual inspection. Since these noodles were discrete particulates, they were not likely present in every container of the manufacturer's retorted product. Thus, the presence of egg evaded detection when only a few containers were selected for egg analysis.
The line crossover was identified as the root cause, and a shield was placed over the non-egg line to prevent egg noodles from dropping into the non-egg pasta. Another aspect of this event revealed that parents of egg-allergic children specifically purchased this retorted pasta product because it did not declare eggs as an ingredient, which enhanced the likelihood of consumer complaints in circumstances where egg cross-contact occurred.
Recall Episode 2: Peanut in Ice Cream
An ice cream manufacturer received a consumer complaint implicating chocolate ice cream as the causative product involved in an allergic reaction of a peanut-allergic consumer. The ice cream manufacturer made several dozen SKUs of ice cream flavors, including several that contained peanut as an intentional ingredient—peanut butter swirl and an SKU with chocolate-coated peanut inclusions.
The company employed several GMPs including scheduling of peanut SKUs as the final products made before clean-in-place (CIP) sanitation, the use of adenosine triphosphate (ATP) test strips, and peanut-specific lateral flow devices (LFDs) to assess the effectiveness of CIP runs by testing of final rinse water, and the use of like-into-like rework practices. Despite these approaches, analysis using quantitative peanut enzyme linked immunosorbent assay (ELISA) methods in an external laboratory revealed the presence of detectable peanut residues in the chocolate ice cream.
Several containers of chocolate ice cream were analyzed and found to contain similar, moderately high levels of undeclared peanut. This finding offered an important clue to the root cause because a CIP cleaning failure would typically lead to higher levels in the first product made after the cleaning, with diminishing levels thereafter. Also, cleaning failures would typically lead to low levels of detectable allergen even in the initial products, except in the unexpected situation where CIP was not conducted.
A review of rework records at the manufacturing facility clearly and astonishingly showed that peanut butter swirl ice cream had been incorporated into the chocolate ice cream. The use of rework as an ingredient explains why consistent and moderately high levels of peanut residues were detected in the chocolate ice cream. Further investigation revealed that a key employee had interpreted the like-into-like as permitting the use of any flavor in rework that would not affect the color or flavor of the chocolate ice cream.
The use of peanut-containing rework was identified as the root cause of this recall. Corrective actions included more specific and detailed employee training on preventive allergen controls and implementation of a new rework policy (exact-into-exact), where rework was only allowed to be incorporated into the same SKU of product from which it had been generated.
Recall Episode 3: Peanut Residue in Spice Mix
The manufacturer of a seasoning mix product was alerted to the presence of undeclared peanut in the seasoning by a customer who conducted routine allergen testing of the branded retail seasoning mix. Testing of retained packets of the seasoning mix and its individual components was immediately initiated. The peanut allergen testing revealed the presence of high levels of undeclared peanut in the ground cumin used as an ingredient of the mix. The ground cumin had been imported from Turkey.
Due to the very high levels of peanut found in the cumin, the manufacturer suspected intentional adulteration; however, such allegations are difficult to prove. Other spice mix companies that were customers of the same Turkish supplier were also found to have received and distributed seasoning mixes and ground cumin with high levels of undeclared peanut. Initially, no consumer complaints were received, but several complaints ultimately were linked to products associated with the implicated cumin. Hundreds of product recalls ensued.
The root cause was the presence of undeclared peanut in cumin obtained from a specific supplier. The corrective action was the cessation of the import of ground cumin from the particular Turkish supplier. Some affected companies began to source ground cumin from U.S. suppliers that imported whole cumin seeds and ground the spice in U.S. facilities.
The initial manufacturer of the seasoning mix could be lauded for having a best practice that allowed quick identification of cumin as the source of the undeclared peanut. This company kept records of all of its products, a GMP employed by many companies that aids immensely in recall investigations; however, this company also kept records of the individual ingredients that went into the seasoning mix. In our experience this practice is less common, but it had immeasurable benefits in this episode.
Recall Episode 4: Peanut Traces in Cumin
The detection of peanut-adulterated ground cumin from one importer and the implication of several suppliers of seasoning mixes (Recall Episode 3 above) caused many companies to begin testing cumin and cumin-containing seasoning mixes for peanut residues. Fortunately, to our knowledge, high levels of detectable peanut residues have not been found in ground or whole cumin. However, low levels of peanut residues (<25 ppm and often <10 ppm) were periodically found in cumin.
Since cumin is a very pungent spice, its use in formulated food products is self-limited. Thus, these low levels of peanut in cumin were unlikely to present any risk to peanut-allergic consumers. However, the presence of detectable peanut residues in cumin prompted several companies to recall or discard product. The source of these low-level peanut residues in cumin proved difficult to identify, as multiple suppliers were impacted.
About 90% of the world's cumin is imported from India, and a reasonable share of that cumin is harvested by small-scale farmers. The cumin-growing region of India is also home to peanut farms. An observation was made by inspectors in India that many of these farmers were reusing burlap bags that may have been previously used for peanuts or peanut meal. Peanuts in India are sometimes processed into peanut oil, leaving behind peanut meal that farmers might transport in burlap bags to feed cows; those same bags might be later used to carry cumin.
This root cause was never fully documented, but several spice manufacturers began supplying the farmers with new burlap bags. This practice coincided with fewer cumin or cumin-containing spice mixes testing positive for peanut residues. This episode reveals the complexities associated with supply chain vigilance for undeclared allergen residues.
Recall Episode 5: Almond Residue in Paprika
In the EU, retail paprika samples were recalled for the presence of undeclared almond. Recalls were also announced in Canada. To our knowledge, consumer complaints were never linked to almond residues in paprika. Like cumin, paprika is a highly pungent spice, and its use levels in consumer ready-to-eat food products is self-limited. However, the levels of undeclared almonds in the ground paprika were moderately high.
The source of the ground paprika was a Middle Eastern supplier. This supplier had no almonds in its facility, although the supplier indicated that it used shared equipment to grind both paprika and mahaleb, a popular Middle Eastern spice made from the pits of a variety of mahaleb cherries. Almonds and cherries belong to the same botanical family (the rose family), and the small seeds contained inside cherry pits resemble almonds, although smaller in size.
Subsequent analysis revealed that mahaleb residues would test positive in the almond ELISA methods, and mass spectrometric analysis revealed that the residues in the ground paprika had come from cherry pits and not almonds. Canada rescinded its recalls for undeclared almond in paprika. Allergen ELISA methods are typically quite specific; however, in the case of botanical cousins such as almond and mahaleb cherries, cross-reactivity is possible.
The root cause of these recalls was a faulty analytical method. The corrective action involved the use of a more specific analytical method to distinguish between almonds and cherry pits. Due to the close relationship between almonds and mahaleb cherries, the proteins from these two foods are likely to be highly homologous, suggesting that ingestion of mahaleb might cause reactions in almond-allergic individuals. This comment is speculative and unproven. However, from a regulatory perspective, cherries are not almonds and, therefore, are not covered by FALCPA labeling requirements.
Recall Episode 6: Manufacturer Disposal of Milk-Tainted Cereal
This example did not result in a recall, but it did result in thorough product disposal by the manufacturer. A breakfast cereal manufacturer used shared processing and packaging equipment for the processing of one cereal product with milk and another with no milk-derived ingredients. The company wished to confirm that its allergen cleaning protocol was effective in removing allergen residues.
Some of the shared equipment was dry cleaned without the use of water, while at least one piece of equipment could be wet cleaned. After manufacturing the milk-containing cereal, the allergen cleaning protocol was completed, and the non-milk product was manufactured. Analysis revealed detectable milk-containing product in packages of cereal from the initial part of the manufacturing run of the non-milk product. The milk residue levels were low but still detectable.
After extensive investigation, the manufacturer realized that droplets from the wet washing procedure were transferring onto the roll stock plastic packaging used as the inner liner for the boxes of cereal. Corrective actions involved moving the packaging equipment further away and shrouding it during allergen cleaning.
These recall examples highlight the complexity of effective food allergen control management. Recalls have occurred due to equipment design flaws, poor rework policies, inadequate employee training, supply chain issues, faulty analytical methods, failed vigilance of the supply chain, and even intentional adulteration of ingredients.
These failures are disruptive when they occur and are identified. However, identification of the root causes of recalls can and has led to the implementation of improved manufacturing practices that serve to prevent similar recalls from occurring or reoccurring. We can learn from our mistakes. The food industry is encouraged to identify root causes and corrective actions for the benefit of other companies so that the frequency of food allergen recalls can be diminished.
- Gendel, S. M., J. Zhu, N. Nolan, and K. Gombas. "Learning From FDA Food Allergen Recalls and Reportable Foods." Food Safety Magazine (April/May 2014). https://www.food-safety.com/articles/4312-learning-from-fda-food-allergen-recalls-and-reportable-foods
Steve Taylor, Ph.D., is Professor Emeritus affiliated with the Food Allergy Research and Resource Program in the Department of Food Science and Technology at the University of Nebraska–Lincoln, having retired from full-time activities in July 2019. He was also a Founding Director of the Food Allergy Research and Resource Program (FARRP) at the University of Nebraska. FARRP, established in 1995, is a food industry-funded consortium with more than 100 global member companies. In retirement, Dr. Taylor remains involved in outreach to the food industry on food allergies and sensitivities both through FARRP and as Principal Consultant of Taylor Consulting LLC.
Joseph Baumert, Ph.D., is a Professor in the Department of Food Science and Technology at the University of Nebraska–Lincoln, and Director of the Food Allergy Research and Resource Program (FARRP). His research focuses on the development and improvement of immunochemical methods for detection of food allergens and the development of quantitative risk assessment models for food allergen exposure assessment. Dr. Baumert's extension and outreach focuses on assisting the industry with food allergy risk assessment, risk management, and allergen training.
Melanie Downs, Ph.D., is an Assistant Professor affiliated with the Food Allergy Research and Resource Program (FARRP) in the Department of Food Science and Technology at the University of Nebraska–Lincoln. Her research focuses primarily on the proteomics of allergenic foods, including the identification, characterization, and detection of food allergens using mass spectrometry. In addition to research, Dr. Downs also works with the food industry on a number of aspects of food allergen management.