Development of Polyphenolics Extracts from Mexican Crops as Natural Antimicrobial Agents for Postharvest Treatments ^†

Abstract

In the last decade, the use of natural antimicrobial agents, like polyphenolic extracts in postharvest applications, has gained attention. However, a significant challenge lies ahead. Demonstrating these agents’ commercial-scale production feasibility, practical applications, and economic viability compared to traditional agrochemicals is crucial. This review focuses on the achievements and obstacles in using polyphenolic extracts from Mexican crops as natural antimicrobial agents against postharvest phytopathogens and foodborne microorganisms. A comprehensive knowledge of the molecular mechanisms in vitro and in vivo, as well as plant systems, is essential for better results. Toxicity assessments and an evaluation of the impact on fruit quality are needed. Incorporating coating and encapsulation techniques can enhance the effectiveness of extracts. An integrated approach is needed for efficient, cost-effective control throughout the preharvest, harvest, and postharvest phases. Successful commercialization depends on the cost–benefit analysis, infrastructure, raw materials, local needs, and technical facilities, among other factors. Additionally, incorporating strategies related to circular economy can improve plant residue utilization and enhance technological and marketing approaches.

1. Introduction

Mexico is a megadiverse country with a high number of natural resources, ranking fourth in the world for its richness of plant species. However, high food losses, the intensive use of agrochemicals, agro-food waste and the lack of infrastructure for their use and management affect its agro-industrial development [1]. According to the principles of circular economy, the valorization of agro-food waste has garnered growing attention due to its possible use as a source of high biological active compounds (HBACs), with applications in the food, pharmaceutical and cosmetic industries, among others. Furthermore, HBACs are environmentally and human-health-friendly alternatives for the control of pathogens in different contexts. In particular, polyphenols (PPhs) are considered very attractive compounds because they are responsible for the antioxidant and antimicrobial properties of some vegetable extracts [2,3,4]. The postharvest process is focused on food properties (nutritional, taste, aroma, and good appearance) and food safety. Most studies are focused on phytopathogenic microorganisms and foodborne bacteria, which threaten the health of consumers [4]. The present review aims to evidence the success and challenges of research on PPh extracts from Mexican crops as natural antimicrobial against phytopathogens and foodborne microorganisms in postharvest processes.

2. Mexican Crops as Potential Sources of PPhs Extracts Natural Antimicrobial

Among the main crops in Mexico, there are some traditional cultivars that serve as sources of PPh extracts, which are known for their antimicrobial properties. The selection of the following crops (

Table 1. Antimicrobial effect of phenolic extracts of different origins on pathogenic microorganisms (in vitro).

Source	Extract/PPhs Concentration	Pathogen	Concentration	Inhibition	Reference
Foodborne microorganisms
Prickly pear (Opuntia ficus indica (L.) Mill.) (Cladode)	Aqueous PPhs extract 700 mg GAE/100 g	Salmonella typhi Helicobacter pylori Escherichia coli Staphylococcus aureus	3.40 mg/mL 1.37 mg/mL 1.41 mg/mL, 1.41 mg/mL	>50%	[5]
Piper dioica L.merril	Aqueous eugenol extract *	Streptococcus mutans	0.1–1 mg/mL	15.9 mm a 24 h 18.6 mm a 48 h	[6]
Clove (Eugenia caryophyllata Thunb.) Mexican oregano (Lippia berlandieri Schauer)	Alcoholic extracts of eugenol and carvacrol*	Listeria monocytogenes ATCC 19,114 E. coli ATCC 25922		>than non-encapsulated extracts	[7]
Habanero chili pepper (Capsicum chinense)	Habanero Pepper Peel Ethanolic Extract	Candida albicans—ATCC 90,028 C. tropicalis—CI C. glabrata—ATCC2001 C. krusei—ATCC 6258	3000 µg/mL 750 µg/mL 3000 µg/mL 3000 µg/mL	100%	[8]
Phytopathogens
Jackfruit leaf (Artocarpus heterophyllus Lam)	Hydroalcoholic PPhs extract	Alternaria alternate	1 mg/mL **	40%	[3]
Jack ruit leaf (Artocarpus heterophyllus Lam)	Hydroalcoholic PPhs extract	Colletotrichum gloesporioides	1–5 mg/mL **	40–60%	[4]
Pepper (Piper Dioica L. merril)	Nanoencapsulated eugenol *	C. gloesporioides	0.5% (p/p) eugenol nanoformulation	100%	[9]
Cinnamon (Cinnamomum zeylanicum J.Presl)	Methanolic extract	Fusarium spp.	300 ppm	31.8–45.6%	[10]
Xoconostle (Opuntia oligacantha C.F. Först)	Nanoencapsulated emulsion 409.37 mg GAE/Ml	C. gloesporioides		>that non encapsulated extracts	[11]

* pure compound. ** concentration of PPhs.

) was based on their native origin in Mexico (Habanero chili pepper, allspice, prickly pear), commercial importance (cinnamon), their impact on agricultural development in various Mexican states (broccoli and jackfruit), and the attention they have received from the Mexican and international scientific communities. In addition, a brief description of each crop is provided below:

2.1. Alslpice (Piper Dioica L. Merril)

Allspice is native to Mexico and Central America and has been domesticated and naturalized in various tropical countries. In Mexico, it is ecologically distributed on the slope of the Gulf of Mexico, from the north of Puebla and Veracruz to the south of the Yucatan, relating some similar climatic and edaphic characteristics [12]. Its national production is channeled mainly to the international market. Allspice production in the country is located within two contexts: growing allspice as an alternative crop via traditional backyard agriculture with family and manual labor and a lack of support and technology; and another more sophisticated international trade system [13]. According to the authors, the fruit contains 1.89% ± 0.94 of essential oil. The eugenol content in the leaves and fruit varies from 38.23 to 46.52%, with respect to its origin and location.

2.2. Broccoli (Brassica Oleracea var. Italica)

Broccoli is an annual crop, which falls within the cruciferous family and the genus Brassica oleracea. In Mexico, Guanajuato accounts for over 67% of the national broccoli production, alongside other contributing states [14]. Within broccoli, HBACs have been empirically proven to exert antimicrobial properties. These compounds encompass vitamin C, carotenoids, PPhs, glucosinolates, sulforaphane, and enzymes such as peroxidases and lyases, among others. Diverse extraction techniques facilitate the isolation of these NA agents. For instance, ethyl acetate and chloroform ethyl acetate extracts have exhibited discernible activity against Escherichia coli and Candida albicans, respectively. Furthermore, aqueous extracts derived from lyophilized broccoli have demonstrated efficacy against Bacillus cereus, Streptococcus faecalis, Staphylococcus aureus, Listeria monocytogenes, Salmonella typhimurium, Pseudomonas aeruginosa, E. coli, Shigella sonnei, and C. albicans [15]. Notably, the presence of NAs is not confined solely to the broccoli florets, but extends to their agro-industrial byproducts, such as stems and leaves. Specifically, aqueous extracts derived from broccoli stems, at a concentration ratio of 1:20 w/v, have demonstrated antimicrobial activity against L. monocytogenes, with a minimum inhibitory concentration (MIC) of 102.4 mg/mL [16].

2.3. Cinnamon (Cinnamomum Zeylanicum J.Presl)

The Cinnamomum genus includes C. zeylanicum and C. cassia, spices that are widely used worldwide and belong to the Lauraceae family. In Mexico, cinnamon bark serves various purposes, with its prominent role as an aromatic ingredient in foods. It also has application in ethnobotanical medicine due to its antimicrobial properties, as well as its antioxidant and antimutagenic capabilities [17]. C. cassia contains a higher coumarin concentration, up to 1% [18]. This characteristic is linked to the fact that isocoumarin, a secondary metabolite found in cinnamon, is hepatotoxic to humans. The European Food Safety Authority (EFSA) regulates the tolerable daily intake (TDI) of coumarin, setting limits between 0.1 mg and 2.0 mg/kg of body weight for general food products.

2.4. Habanero Chili Pepper (Capsicum Chinense Jacq.)

Habanero chili pepper represents an integral part of Mexican cultural tradition and identity, having left its mark on Mexican cuisine for at least eight centuries [19]. In addition, it holds substantial economic importance; in 2019, global production reached approximately 42 million tons [1]. The increase in demand for habanero peppers and their products has led to a growth in waste generation (peduncles, stems, and leaves) [20]. Different researchers have explored the HBAC profile of habanero chili pepper. Mokhtar et al. [21] evaluated the in vitro antimicrobial activity of pepper PPhs and capsaicinoids against thirteen pathogenic bacteria. The principal PPhs present are caffeic acid, quercetin, rutin, kaempferol, coumarin, and narangin. Vuerich et al. [22] analyzed the antifungal activity of the pepper’s ethyl acetate extract against some of the major fungal and Oomycetes pathogens of grapevine; the total concentration of PPhs in the oleoresin accounted for 268.5 ± 15.4 mg g⁻¹ (dw), with vanillic acid (65%) being the predominant compound, followed by protocatechuic acid (13%), both of which are hydroxycinnamic derivatives. Habanero chili and its by-products present interesting alternatives as potential sources of PPh extracts to be used as natural antimicrobial agents for postharvest treatments.

2.5. Jackfruit (Artocarpus Heterophyllus Lam.)

Jackfruit is exhibiting applications in traditional medicine, agriculture and industry in some geographical areas, and in Mexico its major economic impact has been in Nayarit state [23]. It is one of the most common evergreen trees found in the tropical regions, and must periodically be pruned to facilitate fruit harvest. A considerable volume of this biomass (about 10,500 tons/ha of leaf per year) has a high phytochemical and protein content. Regarding the recovery of PPh extracts, some advantages of emerging solid–liquid techniques such as high hydrostatic pressure, ultrasound-assisted extraction, and microwave-assisted extraction have been demonstrated by Mexican authors. Extracts containing mainly flavonoids, tannins, glycosides, phenolic and organic acids, with antimicrobial action against different foodborne and phytopathogenic microorganisms, have been tentatively identified [3,4].

2.6. Prickly Pear (Opuntia ficus indica (L.) Mill.)

Opuntia is a diverse family that predominates in the arid and semi-arid regions of the Americas. About 1400–1800 cacti species have been described in the world, and Mexico is the country with the greatest diversity (850 species, 84% endemic) [24]. PPhs in different parts (fruit, cladode, and pulp) of prickly pear are known to contribute to its antioxidant and antimicrobial activities. Studies have indicated that cladode possesses a higher quantity of phenolics compared with that observed in fruit and pulp. Gallic acid is the most abundant phenolic compound (66.19 μg/g) [5].

3. Antimicrobial Properties vs. Antioxidant Effect of PPhs

The antioxidant capacity of these crops depends on the variability in the concentration and composition of PPhs and other phytochemicals, and their mechanisms of action. High antioxidant capacities related to the action of scavenging hydroxyl radicals measured by ABTS and DPPH methods have been exhibited [4]. The relationship between the antimicrobial action of PPhs and antioxidant capacity has barely been analyzed during postharvest studies [3,4]. In fact, PPhs favor an increase in the permeability of the cellular wall and membrane, causing their disintegration and delaying lipid peroxidation and free radical scavenging [4]. Furthermore, the antimicrobial action of PPhs is associated with the presence of a free hydroxyl group, bonded to a C6 aromatic ring as a system for electron delocalization. It provokes the modification of the microbial membrane and has a key role in the inactivation of microbial enzymes. These changes disturb cellular respiration and may cause cell death [25]. At the same time, potassium ion leakage and a reduction in H₂O₂ decomposition is observed, and highly reactive oxygen species promote oxidative damage and act as proton exchangers. This causes the collapse of the proton motive force and eventually leads to cell death [26]. For instance, the antioxidant activity of prickly pear and the minimum inhibitory concentration (MIC) responses had a significant negative correlation with each other [5].

4. Challenges in Research and Use of NAs in Postharvest Systems

NA technologies will present a major challenge in the coming decades, and some technical problems must be analyzed [27]. In fact, the standardization of commercial NAs depends on various factors, such as the variety and cultivation conditions, climatic factors, plant maturity and agronomic practices, the part of the plant used, methods of extraction and conservation, and the techniques used for chemical characterization [28].

Meanwhile, some technical problems can be considered as opportunities to develop the industrial applications of NAs in postharvest processes and the commercialization [4,27,29,30,31,32] of methods for pathogen and metabolite identification; studying the mechanisms of pathogens and NA compounds will promote the compound’s registration and improve the use of these technologies. Furthermore, in vivo practices, whether conducted under semi-controlled or real conditions, must consider the composition of the microbiota in fruits and vegetables. Additionally, research on the relationship between physiological changes in food products and genetic control will enhance the optimization of treatments. On the other hand, it is crucial to investigate the impact of nanotechnology on preservation strategies and safety [4,27,29,30,31,32]. In fact, micro and nanocapsules have been employed as effective components in coatings, edible films, and PPh formulations. Various methods, utilizing either natural biopolymers or synthetic polymeric materials, have been employed based on their specific use. They improve the physicochemical properties of the capsules or fibers to guarantee their technofunctional properties and applications [9,11,31,32]. For successful technological development, the selection of efficient emerging methods is needed. Furthermore, the implementation of multipurpose biorefineries is proposed, accompanied by the evaluation of their feasibility according to the cost of materials, energy sustainability and their environmental impact, and considering the principles of the circular economy. The production of NAs is a trigger for agro-food waste revaluation, so it is essential to identify and strengthen the research lines that enhance their study and applications, especially from endemic sources. Furthermore, support for primary producers in aspects of training and infrastructure must be ensured.

5. Conclusions

The Mexican agroindustry is challenged with technologically ensuring the management and use of large volumes of agro-food waste. This involves the development of agricultural programs at the local, regional and national level based on viable crops and the redesign of linkage strategies with other industries. The production of HBVCs is a trigger for the revaluation of this biomass, so it is essential to identify and strengthen their investigation and application, especially from endemic sources. Some technical problems can be considered as opportunities to develop the industrial applications of NAs in postharvest processes and commercialization. Greater attention should be given to the development of nanotechnologies, due to their socioeconomic impact. Furthermore, the implementation of multipurpose biorefineries is proposed, accompanied by the evaluation of their feasibility according to the cost of materials, their energy sustainability and environmental impact, considering the principles of the circular economy.