Uncured-Labeled Meat Products Produced Using Plant-Derived

Perspective Cite This: J. Agric. Food Chem. XXXX, XXX, XXX−XXX

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Uncured-Labeled Meat Products Produced Using Plant-Derived Nitrates and Nitrites: Chemistry, Safety, and Regulatory Considerations Nicholas Rivera,*,† Marisa Bunning,† and Jennifer Martin‡ †

Department of Food Science and Human Nutrition, Colorado State University, Fort Collins, Colorado 80523, United States Department of Animal Sciences, Colorado State University, Fort Collins, Colorado 80523, United States

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‡

ABSTRACT: Consumers often malign conventional curing agents while concomitantly accepting the natural forms of the same constituents in numerous food products. This paradox ostensibly exceeds all other food-related controversies to date and likely contributes to the rapid expansion of meat products that utilize natural nitrate derivatives. While there is high demand for these products, a fundamental lack of understanding regarding the safety and chemical implications of curing agents, whether derived from synthetic or natural sources, continues to persist. This manuscript elucidates the variations among curing preparations with particular emphasis pertaining to the associated safety, chemical, and regulatory ramifications encompassing these product categories. KEYWORDS: nitrite, nitrate, cured meats, processed meat products, uncured

1. INTRODUCTION

2. OVERVIEW OF NITRITE AND NITRATE FUNCTIONS IN CURING OPERATIONS Nitrites, and less commonly nitrates, are used to impart unique properties to the end-product. These inimitable properties consist of flavor and taste enhancement, pigment fixation, antimicrobial capacity, and prolonged preservation.8−12 In the context of nitrite concentration(s), 10−15 ppm are required to induce pigment fixation for commercial stability, 20−50 ppm are required to retard rancidity, 50 ppm are required to ensure proper flavor development, and 40−80 ppm are required to inhibit the outgrowth of Clostridium botulinum.9,13,14 Nitrite undergoes various fates once added to meat products. These fates have been reported to occur in the following proportions: reaction with heme proteins (5−15%), reaction with nonheme proteins (20−30%), reaction of nitrous acid with free α-amino acids via the Van Slyke reaction to form nitrogen gas (1−5%), reaction with sulfhydryl groups (5−15%), reaction with lipids (1−5%), oxidation back to nitrate (1−10%), and free nitrite (5−20%).12 2.1. Preservative Properties. While a multitude of volatile compounds have been identified in meat products cured with nitrite, nitrite largely influences flavor by preventing lipid oxidation, and correspondingly, the formation of undesirable lipid oxidation byproducts, such as hexanal and 2,4-decadienal.15,16 When these objectionable odorants are generated, they mask the detection of desirable aromas, primarily sulfur-containing components, that are often associated with meat products cured with nitrite.16 By the same token, nitrite is considered to be the most effective agent at preventing oxidative rancidity observed in cooked,

The paradoxical phenomenon existing between consumer perception and processed meat products is arguably unprecedented. Nitrites remain among the top feared food additives, while concentrated nitrate-containing plant sources, such as beetroot juice, are embraced by the same public maligning their presence in meats.1,2 Moreover, consumers often err on the side of distaste for chemical additives in meat products without a comprehensive understanding of their functionalities.3 This inadequate conception has resulted in the development and rapid expansion of meat products processed with plant-derived nitrates.4 Although plant-derived sources are incorporated in lieu of traditional (i.e., synthetic) sources, these compounds are added to achieve equivalent organoleptic outcomes and are indistinguishable at the molecular level.5 However, this information is not always apparent to consumers and access to credible resources regarding meat processing may be limited. Considerable research and decades of empirical evidence have established the antimicrobial capacity of traditional curing agents. While the breadth of experimental and empirical data for plant-derived nitrates is meager in comparison, there is no reason to believe these natural forms would differ from those that are synthetic assuming equal concentrations.6 However, in the U.S., meats processed with plant-derived nitrates as an alternative to synthetic nitrites and nitrates must bear a mandatory “Uncured” label, even though a product labeled as “Uncured” may contain residual nitrite concentrations ranging from zero to levels similar to, and sometimes much greater than, traditionally cured products.7 With this, the “Uncured” declaration may inadvertently suggest significantly lower levels of nitrates and nitrites and, further, different handling requirements than traditionally cured products. © XXXX American Chemical Society

Received: Revised: Accepted: Published: A

March 22, 2019 June 10, 2019 June 25, 2019 June 25, 2019 DOI: 10.1021/acs.jafc.9b01826 J. Agric. Food Chem. XXXX, XXX, XXX−XXX

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Journal of Agricultural and Food Chemistry

Figure 1. Fate of myoglobin in cured meat products: [HNO2], concentrated nitrous acid; NO, nitric oxide; NO2, nitrite; O, oxidized; + O2, oxygenated; − O2, deoxygenated; R, reduced; and Δ, heat. Adapted from ref 9. Copyright 1966 American Chemical Society.

refrigerated meats, an occurrence termed “warmed-over flavor,” by inhibiting the formation of n-hexanal, trans-4,5epoxy-(E)-2-decenal, and other aldehydes at concentrations of 40 ppm.17 Iron, both free and heme-bound, is the principal prooxidant in meat products.13 Nitrite, or rather nitrite derivatives, prevent iron-induced oxidation by chelating free iron ions and other prooxidants that may both initiate and catalyze lipid peroxidation in addition to blunting the liberation of iron ions through the stabilization of heme pigments.18 Nitrosyl(i.e., nitric oxide ligands) and nitrosoheme (i.e., nonmetal nitric oxide complex) derivatives, such as S-nitrosocysteine, display direct antioxidative potential while nitro−nitroso derivatives may protect cell membranes by stabilizing polyunsaturated fatty acids.18,19 Likewise, nitric oxide encumbers the lipid peroxidation cycle due to its lipophilic nature by reacting with alkyl-, alkoxyl-, and peroxyl radicals.20 As a result, nitrite prevents both primary- and secondary oxidation. 2.2. Pigment Fixation. Pigment fixation involves the metabolic artifact of nitrate and nitritenitric oxidereacting with myoglobin, a sarcoplasmic heme protein. While hemoglobin also participates in pigment formation, the majority is removed subsequent to exsanguination. Corre-

spondingly, muscle pigmentation is largely attributed to the presence of myoglobin.21 To form the desirable pigment(s) commonly associated with cured meat products, nitrite reacts with myoglobin to first form red nitrosylmyoglobin. Once sufficient heat is introduced to the system, the proteinaceous globin moiety of myoglobin is denatured and loses its native conformation while the red nitric oxide porphyrin ring system persists. This denaturation process results in the formation of the characteristic pink color, nitrosylhemochrome, which is sensitive to both light and oxygen.21 If stored improperly, the pigment will quickly degrade as nitric oxide dissociates. Thus, in order to preserve the integrity of this pigment, protective barriers are implemented including opaque films and modified atmosphere packaging. Myoglobin can exist in an oxygenated or deoxygenated state. Deoxymyoglobin is favored at low oxygen partial pressures while high oxygen partial pressures will rapidly oxygenate myoglobin to form red oxymyoglobin causing the meat to “bloom.”22 Both the oxy- and deoxygenated conformation(s) can be further oxidized from ferrous (Fe2+) to ferric (Fe3+). With this shift in oxidation comes a concomitant alteration in pigmentation.9 The purplish-red of deoxymyoglobin or red of oxymyoglobin is consequentially oxidized to brown metmyoglobin. Metmyoglobin occurs in minimal concentrations in B

DOI: 10.1021/acs.jafc.9b01826 J. Agric. Food Chem. XXXX, XXX, XXX−XXX

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spontaneously degrades to form nitric oxide, a highly reactive free radical, that forms antimicrobial oxidants with much greater antimicrobial efficacy than itself, including peroxynitrite, S-nitrosothiols, nitrogen dioxide, dinitrogen trioxide, dinitrogen tetroxide.33 C. botulinum is safeguarded by a robust endospore that is ubiquitously distributed throughout nature, residing in soil, dust particles, and aquatic sediments.39 This pathogen is capable of producing the most acutely lethal substance that has been identified, the botulinum toxin (BTX).40 Groups I (proteolytic) and II (nonproteolytic) are associated with botulism in humans, Group III is associated with botulism in animals, and Group IV has not been shown to pose deleterious effects to either humans or animals.41 Of importance in the food industry are toxin types A, B, E, and less commonly F.42−44 The resiliency of the endospore makes them difficult to destroy while simultaneously preserving the organoleptic properties of the food. Extending this, intrinsic hindrances, such as heating, may promote spore activation and result in germination if improperly cooled in conditions conducive to growth.45 To complete the transition from a spore to a vegetative cell that actively transcribes toxins, activation, germination, and outgrowth must transpire. This proliferation process occurs in the successive steps of germination, spore-swelling, vegetative cell emergence, elongation, and cell division.46 Germination is defined by (I) the loss of refractility, (II) decrease in optical density, (III) loss of heat resistance, and (IV) release of dipicolinic acid (DPA), which comprises approximately 5− 15% dry weight of the intact spore.47−49 While nitrite has a stimulatory effect on germination and permits vegetative cell emergence and elongation to occur, it ultimately inhibits cell division.46 Moreover, the sporicidal effect of nitrite is attributed to its ability to induce germination by causing spores to shed their heat-resistant DPA coat while impeding the outgrowth of persisting spores.50 For repair to occur, a favorable environment must be present. However, damaged spores are more sensitive to the antimicrobial effects of nitrites. These effects are further augmented in acidic conditions and by the osmotic effects of sodium chloride.51

living muscles as a result of metmyoglobin reducatse, NADH, and cytochrome b5, reducing Fe3+ to Fe2+.23,24 When in postmortem, active cytochrome enzymes possess the ability to utilize oxygen, which is responsible for the red color on the surface of meats due to the presence of oxymyoglobin.25 It is with the oxidation state of iron in which determines the conformation of myoglobin, and consequentially, the corresponding pigment. More specifically, absorption of visible light via the conjugated double bond system of the chromophoric heme group confers pigment output.22 In the ferrous state, iron can readily bind oxygen at the sixth coordinate position of heme and change conformation by tightening the planar porphyrin ring by 0.26 A.26 When this occurs, the pigment exists as oxymyoglobin. Without a ligand at the sixth position, the pigment exists as deoxymyoglobin. If iron is further oxidized to the ferric state, metmyoglobin forms. The displacement of oxygen with water at the sixth coordinate position of heme iron results in the inability for metmyoglobin to bind oxygen.22,27 To react with nitric oxide and form nitrosylmyoglobin, reduction of metmyoglobin via enzymatic or nonenzymatic means must first transpire.25 If metmyoglobin persists and is in an acidic medium, it may react with nitrous acid in profusion and generate nitrimyoglobin.28 Upon heating, nitrimyoglobin will form green nitrihemin, a reaction cascade termed “nitrite burn.”25 In the case of Parma hams where nitrite nor nitrate is added yet stable, bright-red coloration nevertheless develops; the iron in heme is substituted for zinc to form zinc protoporphyrin IX.29 A comprehensive overview of cured-meat pigment formation is illustrated in Figure 1. 2.3. Antimicrobial Properties. Nitrite is a bacteriostatic agent that prevents the growth of food spoilage organisms and major foodborne pathogens including Listeria monocytogenes, Salmonella enterica serovar Typhimurium, Achromobacter, Aerobacter, Escherichia, Flavobacterium, Bacillus cereus, Micrococcus spp., Clostridium perfringens, and Clostridium botulinum.30 The antipathogenic properties of nitrite inclusion are attributed to (I) perturbed oxygen uptake and oxidative phosphorylation, (II) inhibition of critical enzymes, including aldolase, glyceraldehyde-3-phosphate, and nitrogenases, and (III) formation of bactericidal nitrite derivatives.31−33 The pH of the system greatly influences the corresponding bacteriostatic effect. For example, a one unit decrease in pH from 7.0 to 6.0 results in a 10-fold increase in inhibition against C. botulinum, the primary pathogen of concern in processed meat products, due to the favored formation of nitrous acid.11 Nitrous acid (HNO2) is a weak acid reflected by an aciddissociation constant (pKa) of 3.4.34 Weak acids are characteristically bacteriostatic due to their ability to prolong the duration of the lag phase.35 An increase in system acidity is accompanied by an increase in the concentration of undissociated nitrous acid, which rapidly diffuses through microbial plasma membranes. Upon influx into the cytoplasm, nitrous acid dissociates and is no longer freely permeable. It becomes trapped and acidifies the cell, ultimately preventing organismal growth.36 Additionally, nitrous acid interacts with a myriad of compounds including thiol- and amino groups, myoglobin, ascorbic acid, phenols, and secondary amines.31 These interactions exhibit antimicrobial capacity by reacting with various primary amino acid residues at low pH levels, particularly through interference with sulfur assimilation by obstructing sulfhydryl (R−SH) groups, such as cysteine residues, and through the disruption of iron assimilation by forming iron-complexes.31,32,37,38 Furthering this, nitrous acid

3. TRADITIONAL CURING 3.1. Definition, Unit Operations, and Curing Agents. The term “cure(d)” is applied either as a verb or a noun in the meat industry depending on context. Use as a verb (i.e., “to cure”) denotes the addition of purified nitrites and/or nitrates to a meat product. Use as a noun (i.e., “a cure”) refers to the chemical constituents themselves (i.e., nitrites and/or nitrates). Although “cure” or “curing” may reference sole salt preservation, the term is often reserved for the inclusion of purified nitrites and/or nitrates. Dry curing (e.g., Parma hams) exemplifies this exception as these products must be salt cured and may or may not be manufactured with conventional curing agents as per 9 CFR 319.106.52 “Cured-raw” meats often consist of the entire anatomical muscle groups, such as whole pork hind legs, pork loins and bellies, beef briskets, mutton legs, ostrich breasts, and game meat cuts while “cured-cooked” meats consist of comminuted products of varying geometries that are often placed into molds and/or casings prior to cooking for reconstitution purposes.53 Curing agents are used in processing both cured-raw and cured-cooked meats. Because the curing process may achieve sufficient lethality, products are differentiated by whether they C


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Journal of Agricultural and Food Chemistry Table 1. Common Curing Methods53

complete list of approved curing agents are issued in 9 CFR 424.21(c).54 Table 2 recapitulates the most commonly applied additives in traditional curing operations. Nitrate use is limited in traditional curing operations and is often reserved for prolonged release cures, such as long-dried fermented and/or cured air-dried salami, with endogenous nitrate reductase and/ or by the inclusion of nitrate reducing bacteria.55 With this product class, nitrate must first be reduced to nitrite and subsequently to nitric oxide before pigment fixation ensues. Reduction to nitric oxide is catalyzed by the inclusion of cure accelerants, such as ascorbate or erythorbate.

are ready to eat or not ready to eat. An overview of curing methods are outlined in Table 1. The vast majority of traditionally cured meat products are manufactured with sodium nitrite in place of potassium nitrite due to the molecular weight differences between potassium and sodium. When equal mass input is considered, there is less nitrite ion available from potassium nitrite than sodium nitrite. Approximately 30% more potassium nitrite is required to achieve the same effects as sodium nitrite. In addition to nitrites, staple components for the purpose of preservation and organoleptic enhancement include salt, sugar, and phosphates. While these ingredients are the most commonly employed, a D


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Journal of Agricultural and Food Chemistry Table 2. Common Traditional Curing Meat Additives5

*

Functions are primarily executed by the inclusion of nitrite.

3.2. Regulations. The regulations for traditionally cured meat products vary depending on the product type. Permissible concentration limits for curing agents are defined in 9 CFR 424.21.54 Immersion, pumped, and massaged (whole

muscle) maximum ingoing nitrate and nitrite concentrations are 700 and 200 ppm, respectively. Comminuted meat products maximum ingoing nitrate and nitrite concentrations are 1718 and 156 ppm, respectively. Dry cured maximum E


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and although ingoing nitrite concentrations may reach several hundred parts per million, residual levels often occur on the order of 5−15 ppm.1,7,67 For perspective, a hot dog yields approximately 11 ppm nitrite at the point of consumption.1 Currently, the World Health Organization (WHO) has established an acceptable daily intake (ADI) of 0.0−0.07 and 0.0−3.7 mg/kg/day for cumulative daily nitrite and nitrate ingestion, respectively.68 Using the upper extreme of these values, a healthy 60 kg individual can safely consume up to 4.2 mg of nitrite per day. In terms of nitrate ingestion, it is important to note that approximately 80−85% of dietary nitrates are derived from vegetable origin, not from processed meat products.69 The average portion of spinach in a salad can exceed this value alone (239−3872 ppm), and consumers adhering to specific diets, such as the Dietary Approaches to Stop Hypertension (DASH), may surpass the ADI for nitrates by as much as 550% for a 60 kg individual.69 Nitrates, irrespective of origin, are reduced to nitrite by commensal nitrate-reducing bacteria that reside on the dorsal surface of the tongue and possess an absolute bioavailability of ∼100%.69 It is estimated that approximately 25% of dietary nitrates are secreted in saliva and of this ∼20% (5−8% total nitrate intake) is subsequently reduced to nitrite.70 Nitrites present in saliva react in solution with secondary- and tertiary amines, N-substituted amides, carbamates, in addition to other reactants.59 When this occurs, nitrosamines are produced in the gastrointestinal tract. This endogenous formation is postulated to be a major source of human exposure to nitrosamines.71−73 The high acidity environment of the stomach is favorable to endogenous nitrosamine formation.74 This pH effect has been demonstrated by the inability to form nitrosamines in the neutral pH environment of the colon, even in the presence of secondary amines.75 The designation of N-nitroso compounds as carcinogens reinforces consumer demand for curing agents in which can effectively replace nitrites, thereby minimizing exposure to nitrosamines.76 Extensive research has been carried out on this subject to increase technological capabilities. This research has largely focused on technologies such as high-frequency heating, high-pressure processing, and natural antimicrobial agents (e.g., bacteriocins, phytochemicals, and organic acids).5 Examples of these efforts include isolation of the bacterial strain, Staphylococcus sciuri I20-1, which produces a heat-stable antimicrobial compound with antibotulinal activity against both vegetative cells and spores.77 This proteinaceous compound is also inhibitory against certain strains of S. aureus.77 However, the inhibitory effect is thwarted by a resistant S. aureus subpopulation.77 As a result, skepticism regarding its efficacy has prevented complete nitrite replacement.77 Bacterial utilization has also been employed as a nitrite circumvention method in meat products cured without the use of conventional nitrites to induce pigment fixation. Use of nitric oxide producing Lactobacillus fermentum generates adequate pigment fixation in sausages without the direct addition of nitrates or nitrites.78 Efforts to abate nitrate and nitrite exposure in foodstuffs have extended to products beyond cured meats. Agronomy implementations have resulted in the successful cultivation of nitrate-free lettuce and nitrite levels in pickles have been reduced by 97% with the inclusion of nitrite reductasegenerating mushrooms (Boletus edulis).79,80 With a seemingly boundless demand for nitrate and nitrite-free products, it is

ingoing nitrate and nitrite concentrations are 2187 and 625 ppm, respectively.56 The United States Department of Agriculture (USDA) regulates nitrite content by total meat content rather than total formulation or finished product weight.56 Distinct regulations have been enacted for the manufacturing of bacon due to the innate, high-temperature frying conditions, which are conducive to nitrosamine formation.57 Therefore, nitrate use is prohibited in bacon due to the prolonged reduction of nitrate to nitrite. The ingoing target nitrite concentration for bacon has been adjusted accordingly. In bacon manufacturing, pumped or massaged (rind removed) maximum ingoing nitrite concentrations are 120 ppm sodium nitrite or 148 ppm potassium nitrite where the ingoing concentration may be further reduced with an approved partial quality control program or with implementation of sugar and lactic acid culture. Immersion (rind removed) maximum ingoing nitrite concentrations are 120 ppm sodium nitrite or 148 ppm potassium nitrite. Dry cured (rind removed) maximum ingoing nitrite concentrations are 200 ppm sodium nitrite or 246 ppm potassium nitrite. Pumped, massaged, immersion, or dry cured (rind intact) maximum ingoing nitrite concentrations are 108 ppm sodium nitrite or 133.2 ppm potassium nitrite where the maximum upper limit is reduced by 10% to compensate for mass of skinrind as rind does not retain cure solution.56 The USDA Food Safety and Inspection Service (FSIS) permits a ±20% ppm deviation for nitrites and reductants at the time of injecting or massaging due to variability in pumping procedures, such as draining and purging.56

4. FORMATION OF N-NITROSO COMPOUNDS Nitrosamines, or N-nitroso compounds, are formed by secondary amines, tertiary amines, quaternary amines, amino acid residues of tryptophan, histidine, arginine, tyrosine, and cysteine, and/or free iron precursors reacting with a nitrosating agent, most commonly in the form of nitrous anhydride.58−60 Sodium ascorbate and its isomer, sodium erythorbate, curtail nitrosamine formation by potentiating the reduction of nitrite to nitric oxide. In this context, the presence of these strong nucleophiles in the acidic medium of bacon favors nitrosylation of heme to form nitrosylheme over N-nitrosylation.61 Herrmann et al. (2015) demonstrated the efficacy of erythorbic acid in the inhibition of N-nitrosohydroxyproline, N-nitrosoproline, N-nitrosopiperidine, and N-nitrosothiazolidine-4-carboxylic acid in cured sausages.62 However, not all reductants have demonstrated equivalent efficacy, even when possessing similar moieties. The fat-soluble ester of ascorbate and palmitate, ascorbyl palmitate, does not prevent nitrosamine formation.60 Accompanying constituents will also influence this effect. For example, in the presence of 10% fat, ascorbic acid markedly increases N-nitrosodimethylamine (8fold increase), N-nitrosodiethylamine (60-fold increase), and N-nitrosopiperidine (140-fold) levels and constituents in black pepper may facilitate the generation of N-nitroso-2-methylthiazolidine-4-carboxylic acid and N-nitrosopiperidine.63−65 While the International Agency for Research on Cancer (IARC) have cited 24 N-nitroso compounds that extend from Group 1−3 classification, an analysis conducted by the USDA Food Safety and Inspection Service (FSIS) in 2014 determined that pork bacon nitrosamine exposure is not a significant public health risk.66 The etiological factor identified in the production of nitrosamines is a function of residual nitrite concentration, F


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Journal of Agricultural and Food Chemistry Table 3. Common Uncured-Labeled Meat Additives83

is the most common vehicle for nitrate inclusion as it contains approximately 3 150 ppm nitrate and does not detract from the desired organoleptic characteristics associated with traditionally cured meat products.82 Another common component in uncured-labeled meat products is sea salt. Both nitrates and nitrites are naturally occurring in sea salt, albeit in low concentrations. These concentrations have been reported to range from 0.3−1.7 ppm and 0.0−1.2 ppm for nitrate and nitrite, respectively, and are inconsequential in regard to imparting the curing functions observed with customary quantities.83 Sodium chloride is an auspicious antimicrobial agent due to its hypertonic nature and osmotic effect, which is capable of inducing plasmolysis. In sufficient concentrations (i.e., 9−10.5%), sodium chloride alone has been shown to inhibit growth and toxin production of C. botulinum.84 When a water activity of 0.89 is achieved, the growth of spoilage- and pathogenic bacteria, S. enterica serovar Typhimurium, L. monocytogenes, S. aureus, and E. coli 0157:H7, ceases.85 Sodium chloride concentration may be effectively lowered to 5.8% and 4.9% with the introduction of 75 and 150 ppm nitrite, respectively.84 However, because typical salt concentrations in cured meat products range from 2−3% total weight, the practicality of sodium chloride as a sole inhibitor is not feasible when considering the concentrations required. Moreover, lipid oxidation, and consequentially, the deterioration of the foodstuff, may be accelerated due to the prooxidant activity of sodium chloride.86 This necessitates the incorporation of supplementary antibotulinal additives as well as introducing various hurdles to reduce sodium chloride to edible concentrations. Adding 1−2% sugar to the brine also serves as a complementary antimicrobial hurdle by influencing osmotic pressure, and hence, reducing the water activity.87 Sugar is primarily incorporated both for organoleptic enhancement and

likely the marketplace will continue to observe an expansion of clean-label, nitrate and nitrite-free alternatives.

5. ALTERNATIVE CURING 5.1. Definition and Ingredients. Uncured-labeled meats are held to the same constraints as traditionally cured meats and must adhere to the requirements for standard of identity representation with the exception being the products do not need to contain nitrates or nitrites. In essence, any ingredient, except for those outlined in 9 CFR 424.21(c), are permissible for use in uncured-labeled products so long as they are deemed safe and do not conflict with standard of identity.47 Table 3 outlines the most commonly applied additives in alternative curing curing operations. The addition of such ingredients may preclude these products from bearing label statements such as “Natural” (i.e., does not contain artificial flavor or flavoring, coloring agents, chemical preservatives, or any artificial/ synthetic ingredient as outlined in 21 CFR 101.22) or “Organic” (i.e., must comply with USDA Organic Foods Production Act of 1990).81 Due to the inability to incorporate traditional curing agents in uncured-labeled meat products, nitrates derived from plants have been elected as an alternative source. These ingredients are often selected for their multifunctional properties. This is exemplified by exploiting vegetable juice powders for both their desirable flavor profile and elevated nitrate content. While nitrate-containing vegetable powders are commonplace for producing uncured-labeled meat products, input quantities may be limited due to distinctive flavor and pigment profiles. These limitations may be further hindered due to the variability in nitrate concentration(s) across vegetable sources and further by the anatomical region of the plant. Nitrate content may range from 80 ppm in tomato fruit to 9 040 ppm in the leaves of turnip greens.82 Ultimately, celery juice powder G


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O157:H7, and S. enterica serovar Typhimurium.89 Additional studies have corroborated this finding using natural nitrates and preconverted nitrites with supplementary antimicrobial agents (i.e., blended-cultured sugar, vinegar, cherry, lemon, and vinegar powder) when compared to synthetic sodium nitrite in inhibiting the growth of L. monocytogenes.90 However, without these auxiliary antimicrobial integrations, L. monocytogenes proliferation was similar to that of nitrate/nitrite-free meat products. From a regulatory perspective, the USDA has classified plant-derived nitrates as antimicrobial or flavoring/seasoning agents (9 CFR 317.2(f)(1)(i)(B) and 9 CFR 381.118(c)(2)) rather than as curing agents per 9 CFR 424.21(c).91,92 When traditional curing agents are substituted with plant-based alternatives, 9 CFR 317.17 states normal cured products “to which nitrate or nitrite is permitted or required to be added” may be manufactured without the use of synthetic nitrates or nitrites if the descriptive name is preceded by the term “Uncured” provided the product is similar in size, flavor, consistency, and general appearance to the traditional product. These regulations further declare products prepared without synthetic nitrates or nitrites must bear a “No Nitrate or Nitrite Added” statement with the exception of products that contain a high brine concentration of greater than or equal to 10%.

to provide a carbon source for nitrate-reducing bacteria. The plant-derived nitrates used in the production of some uncuredlabeled products require bacteria mediated conversion via nitrate reductase enzymes. For adequate nitrate reduction to occur, an incubation temperature of 38−42 °C for a duration determined by the product diameter is required.8 To circumvent the time intensive and variant process required for nitrate reduction to occur, this incubation step has been largely substituted for preconverted vegetable juice powders. Flavor companies now routinely provide a certificate of analysis with concentrations standardized to 15,000−20,000 ppm nitrite.5 Cure accelerants, including natural acidulants and reductants, consist of vinegar, lemon juice solids, and/or acerola cherry powder. However, acidification of these meat products is not desired due to depressed moisture holding capacity, which is unable to be restored by common water-binding enhancers, such as phosphates.83 The abundance of ascorbic acid in acerola cherry functions as a strong reducing agent but does not sufficiently influence pH. In terms of reduction capacity, 0.28% cherry powder has been shown to reduce nitrite by 50%.83 The USDA may approve lactate salts in uncured-labeled products categorized as “Natural” if use as a flavoring agent, rather than as a preservative, can be justified.83 5.2. Food Safety Implications and Regulations. While uncured-labeled products can achieve the same organoleptic outcomes as traditionally cured products, the food safety effects may not be as easily reproducible. Although the concentrations required for inhibiting pathogenic growth using conventional curing agents have long been ascertained, similar studies using plant-derived nitrates have only recently been reported.6 King et al. (2015) demonstrated preconverted, standardized nitrite derived from plant sources may achieve similar inhibition of C. perf ringens during chilling when compared to synthetic sources if equivalent ingoing concentrations are utilized.6 However, when nitrite concentrations are not held equal, pathogenic proliferation may be greater in both no cure (i.e., free from all nitrates) and naturally cured (i.e., plant-derived nitrates) meat products when compared to those that are traditionally cured.7 Furthermore, pathogen growth rates may be highly variable within the same naturally cured product category.7 This intravariability becomes particularly discernible when residual nitrite concentrations are considered. Jackson et al. (2011) elucidated this phenomenon by testing residual nitrite concentrations in commercial frankfurters and observed a range of 3.34−65.69 and 6.83−7.83 ppm for naturally cured and traditionally cured products, respectively.7 These findings serve as a food safety forewarning: the variability in residual nitrite concentration(s) poses potentially deleterious effects due to the inability to suppress pathogen growth at low concentrations and the potential to participate in nitrosamine formation at high concentrations. In 2018, FSIS addressed this issue by regulating the minimum concentration of nitrate and nitrite in these products (FSIS Directive 7120.1). Maximum limits for these compounds are provided in 9 CFR 424.21.54,88 To attenuate remaining food safety concerns, ongoing research efforts have attempted to emulate the antipathogenic effects of traditional curing agents through the medium of natural antibacterial composites. These research efforts have established the efficacy of preconverted, nitrite-containing celery juice powder with a starter culture as being comparable to sodium nitrite in inhibiting L. monocytogenes, E. coli

6. DISCUSSION Due to the verbiage, contemporary labeling is prone to generate confusion at the consumer level. Although plantderived nitrates and preconverted nitrites are incorporated to execute the same biochemical functions as synthetic forms used in traditional curing operations−an explicit distinction must be present on the label. This terminology was adopted prior to the introduction of plant-based nitrate preparations. The intent of this legislation was to prevent ambiguity by differentiating truly uncured (i.e., nitrate- and nitrite-free) products from those that were traditionally cured due to distinct organoleptic differences. However, subsequent manufacturing with plant-derived nitrates resulted in perceptively indistinguishable products. The coinciding and resultant overlap of uncured-labeled meat products (i.e., those completely devoid of nitrate and nitrite from plant-derived or synthetic origin and those containing plant-derived nitrates and/or nitrites) may contribute to the perceived confusion that emanates from the consumer basis. To address this, industry stakeholders have petitioned the USDA to reconsider the labeling of uncured meat products and to add nitrates derived from vegetables to the list of approved curing agents.93 When all factors are taken into consideration, it would appear logical to label these products as “Cured” or to remove the “Uncured” label requirement. If manufacturers, consumers, and/or regulatory agencies wish to permit differentiation between products prepared with plantderived vs traditional curing agents, resulting products could be allocated into three classification types that could easily be distinguished by consumers: (I) traditionally cured products produced with synthetic nitrates and nitrites, (II) cured products produced with plant-derived nitrates and preconverted nitrites (further addition of the “Natural” or “Organic” label could be ascribed if all aspects of production qualify for the given designation), and (III) uncured products containing no added nitrates or nitrites, which would retain the “Uncured” label. H


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(13) Sindelar, J. J.; Milkowski, A. L. Sodium Nitrite in Processed Meat and Poultry Meats: A Review of Curing and Examining the Risk/Benefit of Its Use. American Meat Science Association White Paper Series, No. 3; November 2011. (14) Aberle, E. D.; Forrest, J. C. Principles of Meat Science; Kendall Hunt, 2001. (15) Donald, B.; Gray, J. I.; Gibbins, L. N. Role of nitrite in cured meat flavor: Antioxidant role of nitrite. J. Food Sci. 1980, 45, 893− 897. (16) Thomas, C.; Mercier, F.; Tournayre, P.; Martin, J.-L.; Berdagué, J.-L. Effect of nitrite on the odourant volatile fraction of cooked ham. Food Chem. 2013, 139, 432−438. (17) KERLER, J.; GROSCH, W. Odorants contributing to warmedover flavor (WOF) of refrigerated cooked beef. J. Food Sci. 1996, 61, 1271−1275. (18) Igene, J. O.; Yamauchi, K.; Pearson, A. M.; Gray, J. I.; Aust, S. D. Mechanisms by which nitrite inhibits the development of warmedover flavour (WOF) in cured meat. Food Chem. 1985, 18, 1−18. (19) Shahidi, F. Prevention of Lipid Oxidation in Muscle Foods by Nitrite and Nitrite-Free Compositions. In ACS Symposium Series; American Chemical Society, 1992. (20) Skibsted, L. H. Nitric oxide and quality and safety of muscle based foods. Nitric Oxide 2011, 24, 176−183. (21) Suman, S. P.; Joseph, P. Myoglobin chemistry and meat color. Annu. Rev. Food Sci. Technol. 2013, 4, 79−99. (22) Suman, S. P.; Joseph, P. Myoglobin chemistry and meat color. Annu. Rev. Food Sci. Technol. 2013, 4, 79−99. (23) Bekhit, A. E. D.; Faustman, C. Metmyoglobin reducing activity. Meat Sci. 2005, 71, 407−439. (24) Livingston, D. J.; McLachlan, S. J.; La Mar, G. N.; Brown, W. D. Myoglobin: cytochrome b5 interactions and the kinetic mechanism of metmyoglobin reductase. J. Biol. Chem. 1985, 260, 15699−15707. (25) Damodaran, S.; Parkin, K. L. Fennema’s Food Chemistry; CRC Press, 2017. (26) Sugawara, Y.; Matsuoka, A.; Kaino, A.; Shikama, K. Role of globin moiety in the autoxidation reaction of oxymyoglobin: effect of 8 M urea. Biophys. J. 1995, 69, 583−592. (27) Faustman, C.; Cassens, R. G. The biochemical basis for discoloration in fresh meat: a review. J. Muscle Foods 1990, 1, 217− 243. (28) Yong, H. I.; Han, M.; Kim, H.-J.; Suh, J.-Y.; Jo, C. Mechanism Underlying Green Discolouration of Myoglobin Induced by Atmospheric Pressure Plasma. Sci. Rep. 2018, 8, 9790. (29) Wakamatsu, J.; Nishimura, T.; Hattori, A. A Zn−porphyrin complex contributes to bright red color in Parma ham. Meat Sci. 2004, 67, 95−100. (30) Krause, B. L.; Sebranek, J. G.; Rust, R. E.; Mendonca, A. Incubation of curing brines for the production of ready-to-eat, uncured, no-nitrite-or-nitrate-added, ground, cooked and sliced ham. Meat Sci. 2011, 89, 507−513. (31) O’Leary, V.; Solberg, M. Effect of sodium nitrite inhibition on intracellular thiol groups and on the activity of certain glycolytic enzymes in Clostridium perfringens. Appl. Environ. Microbiol. 1976, 31, 208−212. (32) Weiss, J.; Gibis, M.; Schuh, V.; Salminen, H. Advances in ingredient and processing systems for meat and meat products. Meat Sci. 2010, 86, 196−213. (33) Brunelli, L.; Crow, J. P.; Beckman, J. S. The comparative toxicity of nitric oxide and peroxynitrite to Escherichia coli. Arch. Biochem. Biophys. 1995, 316, 327−334. (34) Lundberg, J. O.; Weitzberg, E.; Gladwin, M. T. The nitrate− nitrite−nitric oxide pathway in physiology and therapeutics. Nat. Rev. Drug Discovery 2008, 7, 156−167. (35) Lambert, R. J.; Stratford, M. Weak-acid preservatives: modelling microbial inhibition and response. J. Appl. Microbiol. 1999, 86, 157−164. (36) Lambert, R. J.; Stratford, M. Weak-acid preservatives: modelling microbial inhibition and response. J. Appl. Microbiol. 1999, 86, 157−164.

In summary, the organoleptic, preservative, and antimicrobial properties imparted by nitrites and nitrates in processed meat products are unparalleled by any other identified constituent(s) to date. This has posed inherent difficulties in removing them while retaining the anticipated, desirable outcomes. From both a manufacturers’ and consumers’ standpoint, nitrates and nitrites are indispensable, regardless of the source. Ergo, complete omission of synthetic or plantderived nitrates and/or nitrites is unlikely to transpire. With this, it is the opinion of the authors that elimination of the current “Uncured” labeling policy for meats processed with nitrates and/or preconverted nitrites derived from plant origin would result in increased transparency to consumers and complement existing USDA FSIS regulations pertaining to cured and uncured meat products.

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. ORCID

Nicholas Rivera: 0000-0002-9905-7618 Notes

Disclaimer: The views expressed in this article represent the views of the authors and do not represent the official views of the authors’ company, university, program, or agency. The authors declare no competing financial interest.

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Uncured-Labeled Meat Products Produced Using Plant-Derived

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