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Modern Concepts & Developments in Agronomy

Food Safety Issues in Semi-moist/Intermediate Moisture Foods and their Mitigation Using Clean Label Antimicrobials- A Review

Aiswariya Deliephan, Bhadriraju Subramanyam* and Charles G Aldrich

Department of Grain Science and Industry, USA

*Corresponding author: Bhadriraju Subramanyam, Department of Grain Science and Industry, Kansas State University, Manhattan, Kansas 66506, USA

Submission: February 21, 2023;Published: March 10, 2023

DOI: 10.31031/MCDA.2023.12.000791

ISSN 2637-7659
Volume12 Issue 4

Abstract

Semi-moist or intermediate moisturized foods with water activity in the range of 0.60-0.85 are primarily susceptible to mold contamination and mite infestation. Additionally, cross contamination of pathogenic bacteria from food contact surfaces can occur in processing facilities. Synthetic preservatives, fumigants and chemical sanitizers had been traditionally used to mitigate these contaminants; however, they could be potentially unsafe for health and environment in the long term. There is an increasing demand from consumers for natural and clean label antimicrobials to replace these synthetic components. This paper presents a review of food safety issues in semi-moist foods and some of the natural and clean label mitigation strategies to enhance food safety and shelf-life.

Keywords: Intermediate moisture food; Semi-moist food; Antimicrobial; Clean label

Introduction

Semi-moist or intermediate moisture foods have gained more attention worldwide by having features very similar to fresh food products, but with a longer shelf life [1]. By definition, semi-moist foods are shelf-stable food products that have water activities (aw) of 0.60-0.84, with a moisture content ranging from 15-40% and are edible without rehydration [2]. Production of semi-moist foods with properties close to fresh foods yet having extended shelf life to satisfy the demand of the consumer is vitally important for the food industry.

Semi-Moist Foods

Historically, ancient civilizations produced semi-moist/intermediate moisture foods using methods such as sun drying, smoking or roasting over fire, and adding salt to preserve food for winter months [3]. In the current times, foods are processed to semi-moist levels mostly by partial drying (e.g., dried fruit), osmotic drying using humectants (e.g., pickled vegetables), and food formulations using humectants and additives to keep them shelf stable (e.g., cakes, chewy dog treats). Many types of foods that are commercially available, like confectionery and pet foods, are specially formulated to achieve water activity in the semi-moist or semi-moist range (0.60-0.84 aw). Food ingredients are mixed with salt and/or sugar, and additives such as polyols (e.g., propylene glycol) and mold inhibitors (e.g., potassium sorbate) and then, subjected to processing methods such as cooking, extrusion, baking or dehydration to result in a semi-moist final product [4]. This method of formulating foods is fast and energy efficient and offers great flexibility in formulation.

The unique features that make semi-moist foods appeal to consumers include microbial safety, desirable odors, high nutritional values, and Ready to Eat (RTE) characteristics [5]. Some of the popular examples of semi-moist foods consumed in our day-to-day lives are fruit cake, country-style ham, fondants, high sugar cakes, sweetened condensed milk, salted fish, molasses, jams, pet food, dried fruits and nuts, parmesan cheese, chocolate bars, marshmallows, and biscuits. As these semi-moist food products encompass a wide category of foods ranging from cereal-based to meat-based to dairy products to pet foods, research in this area of foods contributes tremendously to the well-being of humans and pets all over the world.

Semi-moist pet foods (e.g., chewy dog treats) are a smaller but significant portion of the manufactured pet food market, and they require the use of humectants and acidification to control water activity and mold growth. Semi-moist pet foods also have a low fiber content and relatively high sugar content, which make them highly palatable for pets and increasingly purchased by pet owners [6]. Semi-moist pet foods are manufactured in a way similar to extruded food, but the water content is maintained at a higher level because of the added humectants. The final moisture content of 25 to 35% is more prone to mold growth and spoilage, which is mitigated by mold or bacterial inhibitors as well as managing the ‘active water’ component of the food [6]. The amount of water activity is a measure of the amount of water available for bacterial growth and the addition of humectants helps to keep this at a low level, which effectively inhibits their growth despite a higher total water content [6]. It is apparent that much effort is put toward producing products that not only meet nutrient targets but that are also safe for their intended purposes. In addition to the care paid to details during the formulation and manufacturing process, companies maintain post manufacturing quality controls that further ensure safety and nutritional adequacy for the products. Post manufacturing quality control consists of nutrient testing post processing to determine nutrient losses, long- and short-term storage of foods to assess microbial stability and shelf-life losses of nutrients, as well as ongoing tracking of product stability in multiple environmental conditions [6].

Food Safety Issues in Semi-Moist Foods

Semi-moist food products are below the minimum water activity for most bacteria, which require 0.90aw, but are susceptible to yeast and mold growth which leads to spoilage. Lowering the water activity is an essential processing step and the main microbial hurdle in semi-moist food products. However, setting the aw at a certain level cannot by itself ensure shelf stability. Other factors and properties of food systems should be considered, and often additional measures must be taken into account to achieve the desired stability. Table 1 shows some of the common microorganisms growing in the aw range of semi-moist foods [7].

Microbial stability is also the primary criterion for the viability of a semi-moist food product under development. Inhibiting microbial growth on a given substrate is not achieved exclusively by lowering the aw, but rather, it is a function of all contributing hurdles i.e., aw, pH, temperature, oxidation reduction potential, preservatives, and existing microflora [8]. Numerous microorganisms of significance that cause spoilage have been shown to be able to grow at aw in the range of 0.60 to 0.84 when other conditions are favorable (Table 1). Thus, additional precautions, besides the adjustment of aw, must be sought to inhibit or limit the proliferation of these microorganisms in semi-moist food products.

Table 1: Microorganisms growing in the aw range of semi-moist foods.


The pathogenic microorganisms of major concern in foods are effectively inhibited by the reduction of aw to the intermediate moisture zone (0.60-0.84aw). For example, the growth of Clostridium spp. were prevented by reduced aw regardless of storage temperature and pH [9]. However, because growth could potentially occur during formulation and storage prior to the reduction of aw, good hygienic and manufacturing practices are essential. Bacillus spp. require a minimum aw of 0.89 to 0.90 for growth [10]. At water activities found in semi-moist foods, Salmonella spp. cannot multiply due to a limit for growth of 0.95aw, but their resistance to heat is greatly increased, and they may persist in semi-moist foods for long periods [11]. Listeria monocytogenes Pirie (Listeriaceae: Bacillales), can grow at considerably lower aw with the reported limit of growth at 0.92aw [12,13]. The food pathogen able to grow at even lower aw is Staphylococcus aureus Rosenbach (Staphylococcaceae: Bacillales), which has also been shown to grow at aw above 0.84 to 0.85 if the pH is favorable. Formulation of semi-moist food products at the highest possible moisture content, for improved texture and palatability, requires additional measures for the inhibition of S. aureus. The same is true for molds. The most often encountered molds are Aspergillus and Penicillium spp., which can grow at aw above 0.77 to 0.85. The minimum aw for mycotoxin production by these molds is usually higher. Several xerophilic and xero-tolerant molds can grow at aw down to 0.62 to 0.64. Yeast growth is another potential problem with semi-moist foods. Compared with the most tolerant halophilic bacteria that can grow down to the aw levels of saturated sodium chloride (i.e., aw 0.75), osmophilic yeasts can grow at water activities down to 0.62aw (e.g., Zygosaccharomyces rouxii (Boutroux) Yarrow (Saccharomycetaceae: Saccharomycetales). Good manufacturing practices, pasteurization of mixtures, and use of chemical preservatives, such as sulfites, benzoates, parahydroxybenzoates, sorbates, and diethyl pyrocarbonate, are the usual control measures in semi-moist foods [3].

Apart from the above-mentioned food safety and spoilage issues of bacteria, molds and yeasts, another important issue for semi-moist foods during storage is infestation by mites. Mites are small arachnids (arthropods) that feed on stored food products causing economic losses and may also cause allergies to humans and pets [14]. They also act as vectors of other pathogens [15]. Storage mites (e.g., Acarus siro Linnaeus (Acaridae: Sarcoptiformes) and Tyrophagus putrescentiae Schrank (Acaridae: Sarcoptiformes) feed on mold that grows on food [16]. Storage mites thrive in environments where there is moisture or increased humidity but are most frequently found in dry semi-moist food items such as flour, grains, dried fruits, cereal, and semi-moist dog and cat foods.

Molds and mycotoxins affecting semi-moist foods

Fungi are widely distributed in the environment and are frequent contaminants of food and animal feed. They appear as spoilage-causing organisms under reduced values of water activity in intermediate (0.75-0.90 aw) and low moisture (<0.75aw) foods, and foods with low pH values <4.0 (acidic foods). The minimum water activity limits for the growth of some of the common mold species found in semi-moist foods are summarized in Table 2 [17].

Table 2:Minimum water activity limits for the growth of common mold species found in semi-moist foods.


The most common species of fungi isolated from human foods belong to the genera Aspergillus, Penicillium, Fusarium, Alternaria, Cladosporium, Mucor, Rhizopus, Eurotium and Emericella [18,19]. Species of genera Aspergillus, Penicillium and Eurotium are storage fungi that can develop at ≤0.85 aw, so they can be isolated from spices, dried fruits and vegetables, pumpkin seeds, sunflower seeds, stored cereals, and similar products that are under the categories of intermediate or low moisture foods [20]. Species of the genera Fusarium and Alternaria are ‘field’ fungi and their development requires higher moisture content in the substrate and lower temperatures [20]. These species are usually found in cereal grains and cereal products. Also, they are common causes of illness in fruits and vegetables in the field, in addition to species of the genera Sclerotina, Bortrytis, Monilia, Rhizopus, Mucor and Penicillium. Fungi are common contaminants of meat and milk products during storage, with species of genera Penicillium, Aspergillus, Cladosporium, Geotrichum, Mucor, Sporotrichum, Trichoderma commonly isolated from these food groups [20]

Growth of fungi in food leads to food spoilage, causing economic losses due to food waste. On the other hand, toxin-producing species of genera Aspergillus (A. carbonarius, A. flavus, A. ochraceus, A. oryzae, A. parasiticus, A. versicolor), Penicillium (P. nordicum, P. expansum, P. viridicatum, P. verrucosum), Fusarium ( F. culmorum, F. graminearum, F. oxysporum, F. verticillioides, F. proliferatum), Alternaria ( A. alternata, A. solani, A. brassicae, A. tenuissima, A. tomato) as well as teleomorphs of the class Ascomycetes (Petromyces alliaceus, Emericella nidulans, etc.) can biosynthesize toxic secondary metabolites namely mycotoxins. Examples of mycotoxins are aflatoxins, ochratoxin A, sterigmatocystin, patulin, fumonisins, zearalenone, deoxynivalenol, alternariol, alternariol monomethyl ether, and tenuazonic acid [18,19]. Intake of mycotoxins by animals and humans causes intoxication called mycotoxicosis. Mycotoxicosis leads to acute and chronic toxicity (cytotoxicity, hepatotoxicity, neurotoxicity, teratogenicity, mutagenicity, and carcinogenicity) [21]. At a cellular level, mycotoxins react with nucleic acids and inhibit the biosynthesis of macromolecules DNA and RNA, or act on structures and functions of biological membranes or impair the energy metabolism [22,23].

Molds and mycotoxins also affect pet food. A study by Beuno et al. [24] identified commonly occurring molds in 21 pet foods. These included dry dog kibbles across 8 commercial brands produced in Argentina. Molds were comprised mainly of Aspergillus, followed by Rhyzopus and Mucor spp., and A. flavus was found in 14 of 60 pet food samples purchased in Portugal [25]. In another study Scudamore et al. [26] identified significant growth of Aspergillus spp. in commercial pet food with 20-25% moisture content after 4 weeks of incubation. Although the presence of toxigenic fungi does not necessarily result in mycotoxin production, preventing fungal growth in pet food can certainly minimize the risk of mycotoxicosis. Fungal contamination can lead to economic losses associated with nutrient and palatability reduction, and the presence of mycotoxins affects both animal and human health [27]. Aspergillus flavus is the most reported in pet food and responsible for the production of aflatoxins.

Aflatoxins are a group of mycotoxins produced by Aspergillus spp., mainly A. parasiticus and A. flavus [28]. They are common fungal contaminants of corn, peanuts, cottonseed, tree nuts, wheat, and rice. Aflatoxins B1, B2, G1, and G2 are the four naturally occurring forms of aflatoxins, with aflatoxin B1 the most potent, prevalent, and carcinogenic [29]. Aflatoxins are hepatotoxic and carcinogenic. Dogs are extremely sensitive to this group of toxins, with the liver being their main target [30]. Dogs exposed to 0.5-mg of aflatoxin/kg of body weight typically die within days, exhibiting vomiting, depression, polydipsia, polyuria, and hepatitis [31].

In the US aflatoxicosis related illnesses in dogs and Aspergillus flavus contaminated dog food recalls were reported in 2005. More recently, in 2020, 28 deaths and 8 illnesses were reported in dogs that consumed the recalled Sportmix™ pet food product that was contaminated with aflatoxin [32]. Pet food recalls by Sunshine Mills also happened in 2020, due to aflatoxin contamination from corn that was used as ingredient in the pet food [33]. Currently the FDA has an established action level of 20ppb for aflatoxin in pet foods. Many of the recalled products contained >400ppb aflatoxin. Thus, there is a need to control or reduce toxigenic A. flavus contamination.

Mite infestation in semi-moist foods

Mites are common pests of stored cereals and oilseed. Storage mites belonging to the Glycyphagidae and Acaridae families including Tyrophagus, Acarus, Lepidoglyphus and Glyciphagus are considered to be important pests in stored foods and a source of environmental allergens for humans and pets like dogs with atopic dermatitis [34,35]. These mites are often found in stored hay, straw, grain, and dry feed stuffs. In the UK, surveys have detected their presence in over 80% of stores, with Acarus siro, Lepidoglyphus destructor, Tyrophagus longior, and Tyrophagus putrescentiae in order of predominance [36,37]. Surveys from other parts of the world have found L. destructor, T. putrescentiae and Tyrophagus spp. to be the predominant species, with A. siro occurring less frequently than in temperate regions [38-40].

Among astigmatid mites, Tyrophagus putrescentiae is a cosmopolitan species commonly encountered infesting a large number of semi-moist and low moisture foods including food grains and stored food with a high fat and protein content, such as dried eggs, dried bananas, cheeses, ham, fishmeal, wheat spillage, oats, flour, and different kinds of nuts [41,42]. It causes serious economic losses as well as reducing nutrient content and germination ability [43]. In addition, the mite is responsible for allergic diseases among farmers and food industry workers handling heavily infested stored products [41] which can cause acute enteritis and systemic anaphylaxis [44] when contaminated food is ingested. The mite also acts as a carrier of bacteria and toxigenic fungi such as Aspergillus spp. in stored grain kept under warm and moist conditions [45]. When food products, including pet food, are stored at homes by consumers, they are susceptible to mite infestation from house dusts which can harbor some storage mites. Brazis et al. [46] observed that two out of ten different brands of sealed commercial dog foods contained storage mites, and upon storage at optimal temperatures and humidity, nine out of ten products contained storage mites. T. putrescentiae is a small mite species (0.28- 0.41mm) with a translucent body and virtually colorless chelicerae and limbs. The mite’s life cycle requires 2-3 weeks under ideal environmental conditions (23 °C and a relative humidity of 87%). According to Bahrami et al. [47], typical development times for eggs, larvae, and the two nymphal stages are 2, 3 and 5 days, respectively, at a temperature of 25 °C and 70%RH. There are different reports on longevity of adult mites depending on temperature, relative humidity, and food source [48]. The lifespan of the mites reared on wheat germ at 25 °C and 85% RH was about 60 days. In terms of food impact on longevity, it was up to 120 days for mites reared on wheat germ, 80 days on pumpkin seeds, 75 days on powdered milk and 25 days on rolled oats. A female mite reared on wheat germ or yeast can produce 500 eggs [48].

Contaminants from food contact surfaces

Although the water activity range of semi-moist foods are mostly unfavorable for the growth of pathogenic bacteria, contaminated food contact surfaces can transmit and perpetuate pathogens to foods including semi-moist foods in industrial and domestic food handling environments, thereby creating food safety issues through cross contamination. Exposure to pathogens on surfaces may take place either directly by contact with contaminated objects or indirectly via aerosols originating from the surface. Various bacteria of public health significance, including Salmonella, E. coli, and Listeria, can survive on hands, sponges, clothes, utensils, and currency for hours or days [49]. Pathogenic bacteria may remain on equipment surfaces even after disinfection procedures are applied, increasing the risks associated with the transmission of diseases [50]. Not only bacteria, but mold spores from the environment may also remain on equipment surfaces, on the floor of food manufacturing facilities, on automobile tires etc. and eventually find their way to contaminate foods. Therefore, domestic and industrial food handling environments can be important sources of foodborne pathogens and spoilage organisms including bacteria and molds. Further complicating biological hazard control on these surfaces is the potential formation of biofilms. Biofilms are formed when individual bacterial cells adhere and embed in an extracellular polymeric substance on surfaces such as processing equipment providing a defense mechanism [51]. Pathogenic bacteria, including Salmonella spp. and Listeria monocytogenes, may form biofilms in processing environments [51]. Their extracellular polymeric matrix is difficult to penetrate for sanitizing, for example, Salmonella spp. has been shown to maintain their presence on dry surfaces for up to 4 weeks through a biofilm [52].

Application of Clean-Label Components

According to an annual poll conducted by the Center for Food Integrity, consumers have less confidence in the safety and quality of the food supply and are demanding more all-natural and minimally processed foods with less synthetic chemical additives [53]. Consumers also have increased interest in organic foods because they are often viewed to be healthier, better tasting, or fresher than conventional products [54]. However, though free of synthetic chemicals, organic and all-natural foods are not exempt from bacterial and fungal contamination and may require the addition of antimicrobials to ensure their safety. All-natural, cleanlabel antimicrobials including those derived from plants, animals and bacteria have been shown to be effective at increasing the safety of food products by destroying or limiting the growth of pathogens and spoilage organisms [55,56].

Mold inhibitors

The most commonly used chemical preservatives to prevent mold spoilage in semi-moist foods include: (i) propionates (calcium or sodium propionate), (ii) sorbates (sorbic acid and potassium sorbate), (iii) benzoates, (iv) parabens (methyl and propyl), and (v) acetic acid [57]. Calcium and sodium propionate are the neutral salts of propionic acid. Propionate is a naturally occurring byproduct of the Propionibacterium spp. found in Swiss cheese. Due to their lack of activity against yeast, propionates are the most widely used antimicrobial and mold inhibitor in yeast-raised baked foods [57]. Propionic acid is industrially produced by the hydro-carboxylation of ethylene and the aerobic oxidation of propionaldehyde [58]. Calcium propionate and sodium propionate are produced by the acid-base reaction of calcium carbonate and sodium hydroxide with propionic acid. Sorbic acid, and its sodium and potassium salts, are effective against yeasts and molds. Consequently, since these products can inhibit yeast fermentation, sorbates are applied to semi-moist food products as encapsulates sprayed onto the product as an aerosol or incorporated into packaging material. Sorbic acid was first isolated from the berries of Mountain Ash (Sorbus spp.) trees [59] and is commercially prepared by synthetic procedures, such as the condensation of crotonaldehyde and ketene [60]. Benzoates (sodium benzoate) are inhibitory to yeast and mold and most commonly used to delay spoilage of high acid fillings, fruits and jams [57]. Sodium benzoate is manufactured by the neutralization of benzoic acid with sodium hydroxide [61]. Benzoic acid naturally occurs in cranberries, prunes and cinnamon. Parabens are related to benzoic acid-esters of para-hydroxybenzoic acid. Because they share benzoic acid’s ability to inhibit yeast and mold activity, parabens are typically used in cereal and potatobased snacks [57].

Although these are effective mold inhibitors, they are considered to be ‘synthetic’ chemical additives. In recent times, consumers have preferred natural, clean label ingredients in their foods. Thus, there has been growing research to investigate cleanlabel mold inhibiting components to improve shelf life of semimoist foods. Table 3 summarizes some of the previous research that investigated natural/clean label ingredients to inhibit mold growth in semi-moist foods [20,62-108] Table 3.

Table 3:Natural/clean label ingredients inhibit mold growth in semi-moist foods.


When it comes to the mode of action of natural mold inhibitors, the chemical structure of the natural plant essential oil components and their antifungal properties are found to be related. The presence and position of the hydroxyl group in the molecule, the presence of the aromatic ring, solubility in fats and spatial orientation affect the antifungal activity [74,75]. Compounds containing aromatic rings include phenolic compounds and are characterized by high antimicrobial activity [76,77]. Also, the presence of an alkyl group on the benzene ring of phenols or guaiacol [78], acetate groups (for example, geranyl-acetate has a stronger antimicrobial activity than geraniol, and bornyl-acetate than borneol) [79], oxygen in monoterpenes and their carbonylated compounds [80] enhance the antifungal activity of the components. Phenolic components (carvacrol, thymol, eugenol etc.) exhibit the strongest antifungal and antimycotoxigenic activity, followed by alcohols, aldehydes, ketones, esters and hydrocarbons [81]. A possible mechanism of action for plant essential components on the growth of fungi has been reported in several studies. It is generally accepted that the essential oil components act on the functionality and the structure of the cell membrane [82]. Low concentrations result in changes in the cell’s structure, inhibiting respiration and changing the permeability of the cell membrane, whereas high concentrations lead to severe membrane damage, loss of homeostasis and cell death [83]. Conner et al. [84] suggested that the antifungal activity is the product of essential oil components’ interaction with enzymes responsible for energy production and the synthesis of structural compounds of the cell. On the other hand, Omidbeygi et al. [85] suggested that the essential oil components pass through the cell membrane, integrate with membrane enzymes and proteins of membranes, causing a loss of macromolecules from the interior of the cell, and thereby leading to changes in the cell and ultimately to its death.

Control of mite infestation

Traditionally, control of mite infestation in stored foods depends on chemical methods such as fumigation with methyl bromide, spraying with organophosphorus compounds, or treatment with pesticides like benzyl benzoate and repellents like DEET (N, N-diethyl-m-toluamide) because ecological control methods with high humidity and temperature cause alterations in food quality. Residual pesticides are mainly used to treat the structure of buildings, and some are applied directly to the food commodity. Methyl bromide, though an effective fumigant used to control storage mites like T. putrescentiae, has been phased out in industrialized nations across the world, including the US, due to its ozone-depleting nature. Numerous efficacy tests have been performed with experimental and formulated acaricides against mold mites in the context of agricultural and industrial settings [86-90]. They leave behind some residue on the treated commodity, and repeated use of these chemicals have resulted in the development of resistance by the mites [91]. These chemicals have had undesirable effects on non-target organisms and have led to environmental and human health concerns [92]. These problems have highlighted the need for the development of new strategies for targeted storage mite control, preferably using safe, non-toxic, and natural compounds.

Some of the previous research studies have investigated natural/ clean label components to inhibit T. putrescentiae infestation, which are summarized in Table 4 [93,94,63].

Utilizing mitigation strategies along with good sanitation practices in the industry and storage spaces help in developing effective integrated pest management for mites in these areas.

Table 4:Natural/GRAS (Generally Recognized as Safe) ingredients evaluated in food substances to mitigate T. putrescentiae infestation.


Sanitization of food contact surfaces

Preventive measures utilized by the food industry to decontaminate and sanitize food contact surfaces have included coating of surfaces to limit the establishment of vegetative cells or biofilms [109]. Huss et al. [110] and Schumacher et al. [111] demonstrated that liquid decontamination of animal food manufacturing equipment appears effective but were not very practical or easy to implement. Generally, a water activity level >0.87aw is required for growth of most bacterial pathogens of concern including Salmonella, so introducing a water-based sanitizer would raise the aw to levels that allow for Salmonella growth. Chlorine and chlorine derivatives have been used as a broad-spectrum bactericidal, fungicidal, sporicidal, tuberculocidal, and virucidal control within food manufacturing facilities. Hypochlorite and sodium chlorite can be effective detergents and sanitizers and are known to penetrate biofilms developed by Salmonella [112,113]. However, hypochlorite solutions may produce the carcinogens bischloromethyl ether when in contact with formaldehyde [114], and trihalomethane when in contact with hot water. Because of their potential impact on human health, chlorine and its derivatives must be rinsed from surfaces prior to manufacturing food for consumption by humans or pet animals. Quaternary ammonium compounds are known to be effective sanitizers of fungi, bacteria, and non-enveloped viruses. Their true advantage is their ability to effectively sanitize Salmonella spp. biofilms and because the presence of organic matter is not as inhibitory to their action as it is to other sanitizers [115]. These compounds have been demonstrated to reduce Salmonella spp. by 2 to 3 CFU/cm2 log on galvanized steel [113]. Research has also demonstrated their effectiveness to sanitize stainless steel contaminated with Listeria [116,117] and rubber contaminated with Salmonella [117].

Due to their effectiveness and positive consumer perception of being chemical-free and non-toxic, acid-anionic clean-label sanitizers like acetic, benzoic, and propionic acids have been favored as antimicrobials in food processing facilities. Their mode of action includes acidifying the cytoplasm and disrupting cell membrane organization, which is highly effective for Salmonella destruction in food manufacturing facilities [118,119]. Due to their effectiveness and relative safety, organic acid salts have also been used as surface treatment of foods to prevent microbial growth and as a preservative in finished foods [120,121]. For example, sodium bisulfate, a dry GRAS acidulant, has been demonstrated to prevent Salmonella cross-contamination when used as a coating on pet food kibbles [122] and reduce Shiga Toxin-Producing Escherichia Coli (STEC) loads in wheat during tempering [123]. Recent research has utilized antimicrobial properties of medium chain fatty acids for reduction of Salmonella Typhimurium in animal feed [124] and pet food [125]. Other fatty acids have been used for inclusion in poultry diets for salmonellosis control. Believed antimicrobial modes of action include disruption of the cell membrane and other essential functions [126]. Cochrane [124] demonstrated efficacy of medium chain fatty acids on the reduction of porcine epidemic diarrhea virus. Deliephan et al. [127] demonstrated efficacy of organic acid mixtures containing hydroxy-4-methylthio-butanoic acid (HMTBa) on the reduction of Salmonella on food contact surfaces, and on the reduction of Salmonella and STEC when used as a coating on pet food kibbles [128]. Similarly, 3-hydroxy-3-methylbutyric acid (HMB) was also shown to mitigate Salmonella when coated on pet food kibbles [129]. There has been growing interest in investigating novel food-safe sanitizers to decontaminate food contact surfaces in manufacturing facilities.

Conclusion

This paper reviewed the important food safety issues that affect semi-moist or intermediate moisture foods in the human food and pet food industry, and the application of natural clean-label components in mitigating them. Consumers are increasingly aware of the risks associated with the use of synthetically manufactured additives and preservatives in the food industry. Clean label ingredients have been found to be effective in inhibiting pathogen and spoilage organisms; however, some gaps exist in optimization of dosage levels in foods without compromising on sensory attributes. More systematic research is required to further explore and fully utilize the potential of clean label ingredients for enhancing food safety and consumer acceptance of semi-moist foods.

Acknowledgement

This paper is contribution number 23-207-J of the Kansas Agricultural Experiment Station.

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