Assessment of the Chemical Hazards in Herbs Consumed in Europe: Toxins, Heavy Metals, and Pesticide Residues ^†

Abstract

The increasing global interest in herbs and spices necessitates a thorough examination of the chemical hazards associated with their consumption. The objective of this work was to provide an understanding of the current state and prevalence of chemical contaminants (toxins, heavy metals, and pesticide residues) in herbs and spices consumed in Europe, facilitating informed decision-making in public health and regulatory frameworks Through an extensive literature search, contamination levels of chemical hazards among different herbs and spices were evaluated. The European Rapid Alert System for Food and Feed (RASFF) has shown 1133 notifications for spices and herbs in the last 10 years (2013–2023). Focusing on the chemical hazards associated with the consumption of these products, mycotoxins (especially aflatoxins and ochratoxin A) and plant-derived compounds with potential health implications (e.g., pyrrolizidine alkaloids) were the most often notified. Nevertheless, besides these naturally occurring compounds, other deliberated added substances such as artificial unauthorized dyes (e.g., Sudan I, II, III, and IV) that can pose a human health risk have been identified. Finally, environmental contaminants could also be present in herbs and spices. Pesticide residues (e.g., chlorpyrifos, carbendazim, and bifenthrin) have been notified, and studies in terms of their persistence and adherence to regulatory limits and heavy metals were also investigated, focusing on cadmium, lead, and mercury due to the bioaccumulation abilities of plants. Other environmental contaminants, such as dioxins and dioxin-like polychlorinated biphenyls (dl-PCBs) and polycyclic aromatic hydrocarbons (PAHs), were considered for this study. In conclusion, this work contributed to identifying gaps and challenges in regulatory practices and to the dialog on the safety and quality of herbs and spices, offering a holistic perspective on toxins, heavy metals, and pesticide residues and fostering collaboration between all stakeholders to advance in public health protection in Europe.

1. Introduction

Wild edible plants (WEPs) have been recognized throughout history as part of the human diet, especially in those regions that have experienced food scarcity shortages, crop failure, and other adversities such as seasonal variations, diseases, climatic events, and social or political conflicts, participating in the social and cultural heritage [1,2,3,4]. WEPs encompass a wide variety of plants and botanical elements, such as herbs, forbs, vines, sedges, rushes, grasses, shrubs, trees, and ferns (Figure 1) [3]. The flavor capacity of both spices and herbs has been used for decades in traditional cuisine and has been introduced in the food industry for the purpose of processed food elaboration [1].

Nutritionally, WEPs serve as a source of both macronutrients and micronutrients, with carbohydrates constituting the primary macronutrient (ranging from <1% to 83%), while mineral content can reach up to 25% [5,6]. WEPs are rich in bioactive compounds that can provide substantial health benefits. Many species are particularly valued for their high levels of antioxidants, polyphenols, flavonoids, vitamins, and minerals, all of which contribute to their diverse biological effects [7,8,9]. For example, Sparganium minor is noted for its high total polyphenol content, which can reach up to 258 mg per 100 g of edible parts, enhancing its antioxidant capacity. These nutraceutical compounds have been associated with the prevention of chronic degenerative diseases, positioning WEPs as beneficial additions to the diet for promoting overall health and wellness [10].

Additionally, WEPs are highly regarded for their unique flavor profiles and aromatic qualities. Essential oils and secondary metabolites such as terpenes (e.g., cariophyllene, pinene, limonene, and linalool), alkaloids (e.g., caffeine and nicotine), and flavonoids (e.g., quercetin, kaempferol, hesperidin, and apigenin) contribute to the aroma and flavor of these plants, making them highly sought-after in both traditional and contemporary culinary practices [11,12]. For example, plants such as wild garlic (Allium vineale), nettles (Urtica dioica), and dandelions (Taraxacum officinale) are often used to enhance the flavor of dishes, providing both distinct sensory characteristics and potential health benefits [12]. As consumers increasingly seek natural and sustainable alternatives to synthetic flavors, these natural flavor compounds are becoming more popular within the food industry [1].

However, the supply chain of WEPs is vulnerable, so they can be subjected to chemical contamination within one or more stages of it [1,8]. The presence of chemical compounds in WEPs can be due to different factors. In contrast, although WEPs are characterized for innumerous phytochemicals with great bioactivities, some of them also have toxic chemicals such as alkaloids, toxic proteins, terpenes, polycyclic compounds, or oxalates [2]. Additionally, the use of pesticides for crop treatment with the aim to prevent, repel, or mitigate invasive and harmful organisms leads to the presence of these compounds in WEPs, which is mainly due to their ubiquitous presence [13,14,15]. Therefore, it is fundamental to assess and measure the toxicity and frequency of these compounds in WEPs. The European Rapid Alert System Feed and Food (RASFF) is a consumer-friendly internet tool that provides the latest information on food recall notices, which includes the chemical hazards found in WEPs [16].

The objective of this work was to provide an understanding of the status and prevalence of chemical contaminants (toxins and pesticide residues) in herbs and spices consumed in Europe, facilitating informed decision-making in public health and regulatory frameworks.

2. Materials and Methods

This study assessed chemical hazards in herbs and spices consumed in Europe by conducting a literature review and analyzing RASFF data from 2013 to 2023. An extensive search of peer-reviewed journals, review articles, and authoritative reports was conducted using databases such as PubMed, Scopus, SciencieDirect, Google Scholar, and Web of Science, focusing on contaminants such as mycotoxins, unauthorized colorants, pesticide residues, heavy metals, and environmental pollutants. Relevance of first (Q1) and second (Q2) quartile articles was selected to ensure inclusion of high-quality, reliable data and cutting-edge research. Relevant studies were evaluated for contamination levels, detection methods, and regulatory compliance. Additionally, data collected by the European Food Safety Authority (EFSA) played a critical role in providing comprehensive and up-to-date information on the prevalence and risks of these contaminants, thereby increasing the robustness of the study findings.

3. Chemical Hazards Associated with Wild Edible Plants

The global interest in herbs and spices necessitates a thorough examination of the chemical hazards associated with their consumption. This is particularly crucial as some potential toxic compounds can be found in these plants, such as alkaloids or residues from pesticides. Aside from the natural toxins present in herbs and spices, the presence of pesticide residues raises significant concerns. Between 2013 and 2023, RASFF had 135 notifications for chlorpyrifos and 104 notifications for ethylene oxide. Ethylene oxide (EtO) was used for treating herbs and spices, despite being banned since 1997 due to its high carcinogenic activity (Figure 2A) [17]. Out of the total alerts in herbs and spices, 89 correspond to spices and 120 to herbs. The notified alerts were distributed into the following four families: Lamiaceae (82), Apiaceae (60), Solanaceae (17), and Piperaceae (50). Both literature data and RASFF showed that pepper (50) and oregano (39) were the products most contaminated. Thus, the three most hazardous risks in WEPs are natural toxins like alkaloids, pesticide residues, and the improper use of banned substances like EtO (Figure 2B) [18]. These potential risks are discussed in detail in the section below.

3.1. Pyrrolizidine Alkaloids

Regarding alkaloids (PAs), pyrrolizidine is one of the most frequently toxic compounds detected. It is classified as a pro-toxin that needs to be bioactivated to exert toxicity [19,20]. In 2011, the EFSA concluded that 1,2-unsaturated PA must be considered as a probable genotoxic carcinogen for which a tolerable daily intake (TDI) cannot be established. Instead, EFSA adopted the Margin of Exposure (MOE) approach. Based on the available data, an MOE of 1:10,000 was calculated for an exposure of 7 ng/kg bw per day. For an adult weighing 70 kg, this corresponds to a daily exposure of about 500 ng PA [21]. This alkaloid-type compound can be found in different WEPs, including Senecio spp., Petasites spp., Symphytum spp., and Arnebia benthamii spp. [20,22]. PAs are involved in the chemical defense of plants and are dispersed in many distantly related angiosperms. However, they share homospermidine synthase (HSS), which is the first specific enzyme in PA biosynthesis in all these lineages. HSS uses spermidine and putrescine as substrates to catalyze the formation of homospermidine, an intermediate that has been shown to be exclusively incorporated into the necine base fraction, the characteristic bicyclic ring system of PAs [23]. PAs are mainly synthesized in roots but can also be found in certain young leaves. These compounds are mainly stored as N-oxides, which are highly soluble in water and can be transported to other plant organs [24]. Depending on the esterification of hydroxyl groups, PAs can exist as monoesters or diesters. Diesters are formed by esterification of two carboxyl groups of a dicarboxylic acid. There are two main types: 1,2-unsaturated PAs (retronecine, heliotridine, or otonecine), which are known to be toxic, and less toxic saturated PAs (platynecine) [25]. Hydrolysis, N-oxidation, and oxidation are the three main pathways for the metabolic activation of pyrrolizidine compounds.

The mechanism of action of their toxicity is rapid absorption, although kidneys and lungs are also affected [19]. The intake of PAs has been associated with liver damage, being a leading cause of hepatic veno-occlusive disease (VOD), which can lead to liver cirrhosis and failure. Additionally, it can also cause pulmonary hypertension, cardiac hypertrophy, degenerative kidney lesions, or even death [19,25]. Pneumotoxic, genotoxic, cardiac hypertrophy, and carcinogenic effects were also shown upon ingestion of these compounds [26].

3.2. Pesticides: Chlorpyrifos and Ethylene Oxide

Chlorpyrifos (CPS) is used as an insecticide for grain, fruit, and vegetable crop treatment. This compound induces toxicity by generating free radicals and altering enzymatic and non-enzymatic antioxidant defenses [27]. Furthermore, this organophosphate pesticide is reported to interfere with the signals from the neurotransmitter of acetylcholine [28]. According to human epidemiological studies, long-term–low-level exposure to CPS (Ach) can lead to chronic neurotoxicity, including deficits in memory, cognition, and syntactic reasoning [29]. As a matter of fact, the European Commission formally confirmed that chlorpyrifos and chlorpyrifos–methyl are no longer authorized since January 2020, being the maximum residue levels (MRLs) lowered to 0.01 mg/Kg for all food and feed across the European Union [30].

Conversely, EtO is a colorless direct alkylating gas agent that has been traditionally used as a fumigant in spices in bulk. It can react with cellular components, such as nucleic acids, and prevent cellular metabolism and reproduction [31]. Since it is a highly toxic compound, its use has been banned since 1997, even though it can still be found in food products. According to RASFF, several serious and potentially serious notifications have been established regarding the presence of EtO in herbs and spices, including paprika powder, garam masala, or herbal supplements [32].

Regarding the toxicity associated with these compounds, it is important not only to establish maximum limits in both herbal and spice products but to develop methods to detect their presence in a rapid and effective manner so consumers’ health could be guaranteed. Figure 3 provides an overview of the key differences and main characteristics of PAs, chlorpyrifos, and EtO, focusing on their respective toxicological profiles, uses, and regulatory status.

4. Strategies for Safeguarding Public Health

Guaranteeing consumers’ safety is crucial, so the control of chemical hazards throughout the food chain must be effective. To do this, strategies for the identification and mitigation of these compounds should be developed.

Developing a methodology that establishes a classification of the chemical compounds based on their frequency can be helpful. In this way, a risk-based monitoring program was developed prioritizing the risks of chemical hazards present in paprika, black pepper, basil, thyme, and parsley. This prioritization method classifies chemical hazards in three categories (low, medium, and high frequency), which enables an efficient allocation of monitoring budgets [1]. Regarding mitigating strategies, adsorptive removing processes have been suggested for the pesticides’ elimination. For instance, a superior adsorptive membrane composed of cellulose acetate with different contents of metal–organic frameworks was used for the elimination of chlorpyrifos. The maximum adsorptive capacity was achieved with 60% MIL-53-NH2@CA membrane with 356.34 mg of chlorpyrifos/g [28]. Detection and identification of chemical hazards is also an important approach for safeguarding public health. In this way, a biosensor using a nano-matrix with human serum albumin and Pd-doped nanotubes was constructed for the rapid detection of CPS. This biosensor showed great sensitivity, being able to detect CPS concentrations from 0.5 pM to 500 nM. Furthermore, the biosensor showed good reproducibility, selectivity, and stability [33]. A multiresidue method for the identification of pesticides (including CPS) present in dried herbs was developed and validated by using ultra-performance liquid chromatography–mass spectrometry (UHPLC-MS/MS), showing a limit of quantification (LOQ) ranging from 0.005 to 0.100 mg/Kg and a recovery ranging from 70 to 120% [34]. For pyrrolizidine alkaloids, mass spectrometry (MS) has been traditionally used, although high-resolution MS such as time-of-flight or orbitrap are excellent qualitive methods. For the quantitative analysis, both selective and multiple reaction monitoring based on quadrupole mass spectrometry are the current primary used, showing excellent selectivity, sensitivity, and specificity. For the improvement of analytical efficiency, pre-treatment methodologies have emerged, being solid phase extraction the one with better results when coupled with MS detectors combined with chromatography [35]. The application of ultrasound-assisted dispersive phase extraction was studied for the pyrrolizidine alkaloids present in herbs. The extraction method was coupled to liquid chromatography–tandem mass spectrometry, showing a rapid, simple, and highly efficient methodology, with recoveries ranging from 61 to 128% and LOQ set at 1 μg/kg [36]. In another study, a microextraction method was combined with UHPLC coupled to tandem mass spectrometry analysis for the identification of pyrrolizidine alkaloids present in aromatic herbs. Different large-pore mesostructured silicas, non-modified and modified with amino groups (NH2), were used, and results showed better efficiency in the mesostructured silicas (LP-MS-NH2) [37]. A rapid estimation method that does not need corresponding standards was also developed. By using ultra-high performance liquid chromatography–quadrupole time-of-flight mass spectrometry (UHPLC-QTOF-MS), the measurement of pyrrolizidine alkaloids present in herbs was achieved in a rapid, selective, and sensitive manner [38].

Overall, these studies provide suitable information regarding new strategies for the chemical hazard’s identification and mitigation in WEPs, being helpful in public health safeguarding.

5. Conclusions

WEPs have historically been an important part of the human diet, especially in areas where food is scarce. They offer a diverse range of plants rich in nutrients and health benefits, but their susceptibility to chemical contamination poses risks to consumers. Chemical hazards such as alkaloids and pesticide residues need to be thoroughly investigated and monitored due to their potential health risks. The establishment of maximum limits for these compounds and the development of effective detection methods are essential.

Strategies along the entire food chain are needed to protect public health. Prioritizing the monitoring of high-risk products through risk-based programs, using pesticide removal methods, and developing sensitive detection technologies are critical steps. Recent studies have provided new insights and promising strategies for identifying and mitigating chemical hazards in WEPs to ensure a safer diet for all. Implementation of these strategies will ensure the safety and integrity of WEP products consumed in Europe and beyond.