**4. Discussion**

As there is no curative treatment for food allergies, and allergen avoidance is the mainstay of management, the presence of undeclared allergens in food implies a significantly dangerous risk for allergic patients. The avoidance of food allergens is onerous for patients and families and often fails, with 10% of patients on average experiencing at least one allergic reaction per year [16]. In their study, Fleischer et al. established that 87.4% of allergic reactions to foods in preschool-aged children were mainly caused by accidental exposure. Among causes of accidental reactions, unintentional ingestion (e.g., purely accidental due to forgetfulness, reduced supervision, not checking a product, etc.), label-reading errors, cross-contamination, errors in preparation, and manufacturer's labeling errors were found. The severity grade of these allergic reactions varied considerably, both among individuals and the allergens involved. Of all of the allergic reactions registered by the authors, 70.1% involved mild symptoms (skin, and/or oral symptoms, and/or upper-respiratory symptoms, but not all three organ systems); 18.4% involved moderate symptoms (skin, oral, upper-respiratory, or gastrointestinal symptoms); and 11.4% involved severe reactions (lower-respiratory symptoms; cardiovascular symptoms; or a combination of skin, oral, upper-respiratory, and gastrointestinal symptoms). These results reveal the impact of individual sensitivity to a particular allergen [17].

Although food-related anaphylaxis is relatively common, and all allergens are likely to cause severe reactions, fatalities remain rare, with a reported range of approximately 0.03 to 0.3 deaths per million people per year in the general population, and are very rare in infants and young children [18]. However, the vast majority of fatal allergic reactions were due to peanuts, tree nuts, seafood, and cow's milk [19]. Moreover, the consumption of non-prepackaged foods, served in catering establishments, self-service stores, bakeries, restaurants, etc., is frequently involved. This could probably be associated with a lack of direct allergen information on these kinds of products and the high risk of cross-contamination [20].

Despite the efforts made by the European Union to increase controls and consumers' information through labeling, including in community legislation regarding the mandatory declaration of allergens in food products, the results of the present study show that the risk due to the presence of undeclared allergens continues to be a problem for these patients. Previous studies have already highlighted that the presence of undeclared allergens was one of the main causes of food safety incidents/recalls [21]. An analysis of global recalls from previous years (from 2008 to 2018) also placed milk as the most frequently undeclared allergen, along with multiple allergens and gluten [22]. According to our results, this trend has persisted over time. However, contrary to what was observed in our results, nuts were not listed among the top allergens with the highest incidence in analyses of previous years and of non-EU countries [23,24]. Data from different countries and continents (RASFF vs. CDC, New Zealand, Australia, etc.), as well as the allergen-monitoring increase throughout the world in recent years, associated with the development of specific regulatory legislation, could explain the observed differences.

Previous studies also established cereal and bakery products as the most common food categories associated with the undeclared presence of milk, followed by confectionery [22]. However, this has changed over the four years of the study period since, from our results, it can be observed that milk allergens were more common in the recalls of prepared dishes than in those of confectionery. In any case, prepared dishes have already been identified by previous analyses as frequent causes of recalls [24]. The obtained results are worrying since both categories, derived from cereals and prepared dishes, are likely to be frequently

consumed by children and adolescents, and they lead the list of products with the most prevalent allergens for this population.

FA patients often consume food products that self-report to be allergen-free (e.g., dairyfree) on their labels, trusting in their safety. However, the results exposed a concerning presence of undeclared allergens in a wide variety of those foods. This fact was especially striking in prepared meals and bakery products classified as "gluten-free". The evidence regarding the threshold limit of gluten concentration in food is also unclear. The consumption of about 200 mg gluten per day is clearly associated with the development of intestinal mucosal abnormalities after only 4 weeks in patients with celiac disease. However, it has been demonstrated that individual sensitivity to gluten varies among people with celiac disease, and the daily-intake limit should lie between 10 and 100 mg [25]. The length of exposure to gluten is also a determinant factor. For example, some authors have found that the ingestion of 10 or 50 mg gluten per day was associated with the worsening of the villous height/crypt depth ratio in most patients after 3 months [26]. In any case, under these premises, the high gluten amounts reported in some notifications (from 20 to more than 1600 mg/kg) highlight the obvious risk for some people with celiac disease and gluten intolerance, as the maximum limit ingestion must not exceed the 10 mg per day to avoid detrimental effects, such as significant histological abnormalities in some patients. According to European legislation, the statement "gluten-free" may only be made when the food as sold to the final consumer contains no more than 20 mg/kg of gluten, and the statement "very low gluten" may only be made where the food, consisting of or containing one or more ingredients made from wheat, rye, barley, oats, or their crossbred varieties, which have been specially processed to reduce the gluten content, contains no more than 100 mg/kg of gluten in the food as sold to the final consumer [10]. According to the painful limit of exposure, the serving portion of these products, and the quantity of gluten found, Table 4 shows examples of the potential allergen intake through the consumption of these products. It must be remarked that, in most of them, the estimated intake doses exceeded the limit of 10 mg in a serving portion.


**Table 4.** Examples of estimated gluten-intake dose via "gluten-free" products according to their serving portions and notifications of undeclared gluten amounts.

The use of certain types of allergen-related labeling claims to attract consumers is a widespread practice among manufacturers, but a lack of control over potential allergens is often observed. In the case of patients allergic to milk or eggs, "vegan" products, such as soy or oat beverages, represent a suitable and safe alternative, such that they are frequently consumed by them. However, the results exposed that 64.9% of the notifications related to these types of products included undeclared allergens of animal origin (milk or eggs). The results are in accordance with those founded by Bedford et al. (2017). In their study, the authors observed that 50% of chocolates labeled "dairy-free" or "lactose-free", as well as 25% of those labeled "vegan", tested positive for milk, all with concentrations >1000 ppm [27].

Regarding milk as an allergen, current legislation only considers it mandatory to highlight the term "milk" to clearly differentiate it from the rest of a list of ingredients; however, it would be appropriate to review this legislation. When possible, labels should discern between the presence of lactose and milk proteins, instead of using only the term "milk" without more precise details; doing so would provide more practical information to patients, allowing them to make more convenient purchase choices according to their pathology, whether that be a milk protein allergy, lactose intolerance, or even if they are galactosemic. This discernment should also be systematically implemented in RASFF notifications to provide more accurate information for those patients. Although it varies a great deal according to the individual, as is the case with all food allergens, the threshold dose that induces symptoms in 5% of patients allergic to milk is less than 30 mg of milk proteins [28]. This low threshold dose implies an important risk for allergic consumers. It should also be remarked that, according to this symptomatic dose and the range of undeclared milk detected, a serving portion of 200 g of the product could imply, in some cases, a lactoprotein intake of 500 mg, almost 17 times higher than the dosage limit.

In contrast, regarding lactose, the EFSA Panel on Dietetic Products, Nutrition and Allergies concluded that symptoms of lactose intolerance have been described after the intake of less than 6 g of lactose in some subjects. However, the vast majority of subjects with lactose maldigestion could tolerate up to 12 g of lactose as a single dose with no (or only minor) symptoms. Additionally, it has been concluded that higher doses might be tolerated if they are distributed throughout the day [29]. It is relevant that even the highest amounts of undeclared lactose found (1.56 g/100 g) do not exceed the tolerance limit for intolerant patients. However, undeclared lactose also implies a serious risk for patients with galactosemia. For them, the threshold dose of lactose and galactose is lower, and strict lactose avoidance is required. It has been suggested to disallow all foods with a galactose content of >20 mg/100 g [30]. With all of this being the case, many of the undeclared lactose products about which notifications were emitted represented a severe danger for these patients.

In EU legislation, the claim "lactose-free" has only been defined for infant and followon formula (≤10 mg/100 Kcal). Notwithstanding, some EU member states have set threshold levels at the national level for the use of the terms "lactose-free" or "low lactose" for foodstuffs other than those intended for infants. Unfortunately, a common level has not been adopted among these EU member states, and the lactose threshold level in "lactosefree" products varies between "absence of lactose and galactose" and 100 mg/100 g of the final product [29]. The lack of a common criterion adopted by all EU member states causes management and trade between countries difficult for manufacturers and can easily lead to notifications being emitted.

On the other hand, vegan patterns have globally risen during the last several years, including in FA pediatric patients [31,32]. Among the different motivations of plant-based dieters, the aversion to animal products due to moral and ethical reasons is highlighted [33]. In this context, the presence of undeclared allergens of animal origin, such as eggs, milk, fish, or seafood, in "vegan-claimed products" threatens the freedom of choice of this population and may pose a moral challenge to them.

Cross-reactivity is another problem of undeclared allergens in products. For example, a 75% cross-reactivity between soy as a primary food allergy and peanuts as a cross-reactive food has been observed [34]. If an allergic consumer were to ingest a product free of the primary trigger allergen, but it contains the cross-reactive undeclared allergen, it could imply a risk for their health.

The fact that 51.1% of the notifications of undeclared allergens had their origin in companies themselves highlights the efforts made by operators to control allergens. However, the proper management of allergens in the food industry implies a great challenge and a cost increase for them. Gupta et al. (2017) estimated this production cost increase as being between 10 and 30% [35]. To control this hazard, manufacturers routinely develop and implement independent allergen control plans to minimize the risk of product contact

with food allergen contaminants and prevent recall events due to undeclared allergens. These plans typically specify practices for the safe handling and storage of raw materials, employee training, facility and equipment design, cleaning procedures, and production scheduling. Recalls due to food allergen cross-contact, cleaning procedures, equipment and premises design, and employee training were ranked by companies as the greatest allergen management expenses. In addition, companies may use precautionary allergen labeling (PAL), such as "may contain" on packaging, to label products for which there is a risk of cross-contact with food allergens during production. However, PAL usage remains voluntary and unregulated, and it currently presents consumers with considerable challenges due to its inconsistent use. The European Commission should also direct its efforts to address the inconsistent usage of PALs, promoting the harmonization of language used in PALs, and improving PAL status to quantified PAL statements, as previously suggested by other authors [36]. It would be helpful in communicating risks for both manufacturers and consumers, so that they can make informed choices when purchasing food products.

Food producers must continue increasing their efforts to improve food allergen management in order to reduce the presence of undeclared allergens in their products. For example, to reach this objective, they can follow and apply available guidance, such as *Guidance on Food Allergen Management for Food Manufacturers* [37]. Furthermore, it would also be highly recommended to implement international standards, such as voluntary food security and quality certifications, for example, International Food Standards version 6.1 [38] or BRGCS's Gluten-Free Certification Program (GFCP) [39]. Currently, scientific advances have allowed the development of technological alternatives, such as irradiation or high hydrostatic pressure, in which, in addition to preserving nutrients, freshness, and organoleptic characteristics, they alter the structure of the proteins causing allergies, reducing their allergenicity [40,41]. However, these kinds of technologies are still under development, and their costs are very high, so they cannot be used by many companies. In the current scene, food manufacturers should improve food allergen management in their practices by focusing on empowering employees through more knowledge about food allergens and allergies, as well as through the use of new digital tools such as big data, as previously proposed by Jia and Evans (2021) [42].

The management of food allergies and dietary avoidance presents several challenges for pediatric dietitians and other healthcare providers [43]. Health professionals who assess FA patients should include nutrition therapy to ensure the adequate intake of nutrients as well as nutritional education with comprehensive information about allergenic ingredients for their avoidance [31,44]. The American Academy of Pediatrics established as a critical issue the improving of the education and training of all stakeholders for recognizing and managing, as well as preventing, allergic reactions. This work includes updating, creating, and implementing various guidelines and educational programs [45]. In this line, educational programs should be based on three basic aspects:

1. Learning which foods, due to their composition, may contain the trigger allergen.

2. Understanding how to read labels to find out if the trigger allergen is present, including "contains traces of" or "may contain" statements. In this sense, it is also essential to note that unpackaged products, packaged directly in store or those sold in the form of self-service (e.g., bread and pastries offered in supermarkets) are very prone to crosscontamination with various allergens. However, despite it being mandatory to inform customers about the allergens present, the absence of a label on products and the high risk of cross-contamination cause their consumption by allergic patients to be unrecommended.

3. Learning resources containing information about undeclared allergens in food labeling, as well as those products more likely to contain them according to the trigger allergen. On this point, it would be useful to provide information about official resources and webpages that share food allergen alerts, such as RASFF.

It would be helpful to provide patients with summarized and visual information about those products that most frequently present undeclared allergens, such as that shown in Table 5.


**Table 5.** Summary of the main allergens that affect the pediatric population, and main risk food category.

As it has been demonstrated that labeling is not a sufficient guarantee, and that there may be undeclared allergens, a useful reference tool for allergic patients and their families is the RASFF consumers' portal. Launched in June 2014, this website is a consumer-friendly internet tool that provides the latest information on food recall notices. It also includes public health warnings issued by food safety authorities and food companies. By using this free tool, EU consumers could identify food that has been flagged in the system, allowing them to make more safety choices. There, users obtain access to practical information on product recalls and public health warnings in any given EU country. Additionally, they could also consult the institutional websites of the member states. The RASFF consumers' portal and most websites provide food alert information on any food hazards, including undeclared allergens. Some of them are shown in Table 6.

**Table 6.** Examples of institutional websites of European Union countries that provide practical undeclared allergen information (product recalls and other public health warnings).



## **Table 6.** *Cont.*

In this respect, free mobile applications, such as HRana from the Croatian Ministry of Agriculture, are very useful for consumers in general, and for allergic patients in particular. This application enables citizens to receive information within 24 h on warnings regarding food, animal feed, and objects, as well as materials that come into direct contact with food which are sold in the Croatian and/or EU markets. Information that the Ministry of Agriculture updates in real time is sent to citizens via an application notification that displays food-related warnings and additional information on the non-compliant product (product name and image, shelf life, type of health risk, action taken by competent institutions, distribution status, etc.), as well as information on the food business operator that markets the product [60].
