Spoilage of canned foods stored at high temperatures, accompanied by gas production, is

4.4.1 Refrigerated Food

Fresh meat can be preserved for more than 60–70 days by vacuum packaging and a strict control of storage temperature. The storage conditions are defined to ensure prevention of toxin production by C. botulinum. However, spoilage was observed as meat softening, formation of odors described as dairy or sulfurous and production of exudates, caused by clostridial species (Broda et al., 1996a; Cavill et al., 2011; Lawson et al., 1994; Mills et al., 2014). This defect, called “blown pack,” can occur sporadically even if no temperature abuse has occurred. Blown pack results of carbon dioxide production by cold-tolerant species, such as Clostridium estertheticum and Clostridium gasigenes. Other species, Clostridium algidicarnis and Clostridium frigidicarnis, produce off-flavors from meat, but without gas formation. For fresh or chilled meats however, spoilage by lactic acid bacteria is more frequently reported.

Surimi, which is a fish-paste obtained from cooking fish pieces with salt, sugar, and starch, is stored for long time at low temperatures. The presence of psychrotolerant spore-formers, exhibiting proteolytic and amylolytic activities, has been described (Coton et al., 2011; Tsuda et al., 2015). The described species were most frequently Bacillus simplex, B. subtilis, and Sporosancina aquimarina.

REPFEDs are exposed to spoilage by spore formers as cooking inactivates vegetative microorganisms. The presence of B. cereus group bacteria, Bacillus pumilus and other related species was shown. These bacteria are not gas-producers but exhibit several enzymatic activities that could result in odors and texture changes (Samapundo et al., 2014).

4.4.2 Canned Food

Heat processing of low-acid canned food was initially designed to inactivate the most resistant spores of C. botulinum. However, F0 values increased over time to inactivate even more resistant spores of species that cause spoilage. Nowadays, provided that packaging is well-sealed and processing controlled, industrially produced canned food remains stable at ambient temperature for years. Observation of spoilage only occurs when canned food is stored at elevated temperature for several days. This could be the case if food is transported overseas by boat or is exposed to elevated temperatures in warehouses. Two main defects are described: flat sour and hard swell. The former results mainly from G. stearothermophilus recovery and outgrowth whereas the latter is the consequence of M. thermoacetica development. These two bacteria are the causative agents of 71% of observed spoilage cases (André et al., 2013). Other defects are due to Thermoanaerobacterium spp. and moderate thermophilic Bacillus spp. Ultra high temperature (UHT) dairy products can be contaminated by highly resistant spores of aerobic bacteria, and G. stearothermophilus, B. subtilis, and B. coagulans were reported as causative agents of flat sour or slimy milk or cream (Burgess et al., 2010; Pujol et al., 2015).

Acid or acidified pasteurized foods are most frequently spoiled by heat-resistant molds such as Byssochlamys fulva or Byssochlamys nivea, or by lactic acid bacteria (Aneja et al., 2014). Spoilage by endospore-forming bacteria, in particular by Alicyclobacillus spp., might be difficult to detect as they do not produce gas, but rather produce a smoky, medicinal, and antiseptic off-odor resulting in volatile phenols formation (Danyluk et al., 2011; Smit et al., 2011). Several moderate acidophilic Bacillus spp., like B. coagulans, are involved in spoilage of tomato concentrates or apple juice (Thompson, 1981).

4.4.3 Cheeses

Late blowing of semi-hard and hard cheeses occurs from dihydrogen production in cheese paste, causing cracks, and slits. This defect is due to lactate, residual sugars, and citrate consumption by clostridial species. These bacteria produce butyric acid, and to a lesser extent acetic and propionic acids. Clostridium tyrobutyricum, C. butyricum, C. beijerinckii, and C. sporogenes are the species the most frequently associated with this spoilage (Brändle et al., 2016; Gómez-Torres et al., 2015; Le Bourhis et al., 2007).

Ricotta is a soft cheese made from heat coagulation of whey proteins. Ricotta pink discoloration was observed and related to B. cereus group, Paenibacillus spp. and clostridial species detection (Sattin et al., 2016).

4.4.4 Bread

Bread ropiness has been described for many years and corresponds to unpleasant odors resembling overripe pineapples, bitter taste, and later on, crumb discoloration and sticky and greasy bread (Thompson et al., 1993). It occurs within 12 hours of cooking and is more frequent in undercooked breads, bran breads, and organic breads. The defect results from amylase activity and from extracellular polysaccharides production. Several Bacillus species are involved in this defect, B. licheniformis, B. subtilis, and B. pumilus being initially described as the most frequent ones (Pepe et al., 2003; Rosenkvist, 1995). A recent study pointed out the high frequency of B. amyloliquefaciens and B. cereus group from spoiled bread of Italian origin (Valerio et al., 2012).

4.4.5 Dry Ingredients

Due to their low water activity, dry ingredients are protected from microbial spoilage. However, a lot of attention was placed on these products as they are ingredients for canned foods and REPFEDs. Dry milk, milk proteins, whey powder, flour, starch, and spices exhibit a high prevalence of spore-formers (Burgess et al., 2010; Guinebretiere et al., 2003; Iurlina et al., 2006; Miller et al., 2015b; Postollec et al., 2012; Rückert et al., 2004; Sadiq et al., 2016; Watterson et al., 2014). The most frequent species, found in dairy powders, with differing proportions depending on the study, are G. stearothermophilus, B. licheniformis, and A. flavithermus.

1.4.1 Bacteria

LAB, encompassing Lactococcus, Lactobacillus, Leuconostoc, Weissella, and Carnobacteria species, as well as Enterococcus are frequently associated with spoilage. Although LAB are generally beneficial for food and are used for the fermentation of a variety of food and raw materials, where they contribute to flavor, texture, and shelf life, some species can play a significant role in food spoilage and decay (Remenant et al., 2015). Undesirable changes caused by LAB include greening of meat and gas formation in cheeses (blowing), pickles (bloater damage), and canned or packaged meat and vegetables. Off-flavors described as mousy, cheesy, malty, acidic, buttery or liver-like may be detected in wine, meats, milk, or juices spoiled by these bacteria. LAB may also produce large amounts of an exopolysaccharide that causes slime on meats and ropy spoilage in some beverages (Rawat, 2015).

In addition to LAB species, other Gram-positive bacteria can play a significant role in food spoilage. One of the most prominent is the psychrotrophic species Brochothrix thermosphacta, known as an important spoiler bacterium of various food matrixes. Enterobacteriaceae can also play a key role in food spoilage due to their ability to metabolize amino acids to malodorous volatile compounds, such as foul-smelling diamines and sulfuric compounds. Gram-negative bacteria with species belonging to the genera Serratia, Hafnia, and Pseudomonas have also often been incriminated. Pseudomonas spp., particularly P. fluorescens, P. putida, and P. fragi, also contribute to a large extent to the spoilage process of food. These are the predominant spoilers of foods stored under aerobic refrigerated conditions, especially aerobically chill-stored beef, seafood, poultry, and milk (Remenant et al., 2015).

There are several sporeformers bacteria which can produce significant economic spoilage of foodstuff (Brown, 2000). Some species can be psychrotrophic which can spoil refrigerated dairy products; others such as Bacillus subtilis are mesophilic and can spoil bakery products, whereas others such as G. stearothermophilus are thermophilic and spoil foods that are canned or in hermetically sealed packages. Clostridia generally spoil foods of low oxygen/reduction potential such as canned or vacuum-packaged foods (Setlow and Johnson, 2013). Several psychrophilic and psychrotolerant species including Clostridium algidicarnis, Clostridium algidixylanolyticum, Clostridium estertheticum, Clostridium frigidicarnis, and Clostridium gasigenes have been implicated in red meat spoilage (softening of the meat, large amounts of drip, offensive odor). Of these species, C. estertheticum (subspecies estertheticum and laramiense) and C. gasigenes additionally produce gas and have been recognized as causative agents of “blown pack” spoilage of vacuum-packed chilled meats at normal storage temperatures (−1.5 to 2°C) (Heyndrickx, 2011). In addition, the acid tolerant species Clostridium barati and Clostridium butyricum have been reported as the causative agents of the spoilage of canned pasteurized mung bean sprouts, stored under acidic conditions (Remenant et al., 2015). Spores of Clostridium tyrobutyricum can cause spoilage of semihard cheeses with long ripening times such as Gouda and Emmenthaler (Heyndrickx, 2011). Spoilage from Clostridium sporogenes produces typically blown or burst packs with a strong putrefactive odor. (Brown, 2000). Spoilage from C. thermosaccharolyticum manifests itself by blown or burst packs with a strong butyric or cheesy odor (Brown, 2000).

Alicyclobacillus species have been recognized to spoil acidic products. Spoilage is sometimes associated with a slight increase in turbidity and white sediment at the bottom of packages, but the most important fault is taint of strong medicinal or antiseptic flavor caused mainly by the production of guaiacol, but also by 2,6-dibromophenol and 2,6-dichlorophenol. Affected products are pasteurized fruit juices (mainly apple and orange) and fruit juice blends, but there have also been reports of spoiled carbonated fruit drinks, berry juice containing iced tea, and diced canned tomatoes (Heyndrickx, 2011).

The polysaccharides produced by microorganisms during their growth can also cause food spoilage. An example is the contamination of certain fermented beverages (cider or wine) by Leuconostoc species giving the product an oily consistency (Baron and Gautier, 2016).

For the most part, the spoilage organisms discussed have been harmless bacteria that pose no threat to human health. However, in certain situations, the bacteria responsible for food spoilage may, in fact, be pathogenic. The pathogenic species, B. cereus, has been linked to spoilage and human illness in fluid milk products. Clostridium perfringens can comprise a large portion of the spoilage flora under anaerobic storage conditions. In addition, Enterobacteriaceae, including pathogenic Salmonella spp. and E. coli, can dominate the spoilage microflora under aerobic and anaerobic storage conditions. Vibrio spp. are commonly present on seafood products harvested from warm water climates. These organisms tend to dominate the microflora of seafood products that are abused at temperatures more than 20°C. In particular, the human pathogen Vibrio parahaemolyticus has been shown to be the predominant spoilage organism in shrimp held at temperatures of 24°C or greater (Benner, 2014). Moreover, biogenic amines can be produced in meat and fish by several members of this group while others produce off-odors or colors in beer (Obesumbacterium), bacon and other cured meats (Proteus, Serratia), cheeses (several genera), cole slaw (Klebsiella), and shell eggs (Proteus, Enterobacter, Serratia) (Rawat, 2015).

1.4.2 Yeasts

Species of Zygosaccharomyces and related genera are usually the yeasts that colonize and spoil high sugar and high salt products (Blackburn, 2006). The Zygosaccharomyces genus consists of six species, of which Z. bailii, Z. bisporus, and Z. rouxii are the most relevant to the spoilage of foods and beverages. These yeasts are characterized by fermentative spoilage of products such as fruit juices, fruit concentrates, syrups, sauces, alcoholic beverages, honey, jams, and confectionary. The fermentative nature of Zygosaccharomyces metabolism produces carbon dioxide that is of concern if the food product is in a sealed container, as the increase in gas can cause the container to leak or, in extreme cases, explode. Haze or sediment can occur in beverages as cellular biomass accumulates, and in some cases, surface biofilms can form. Taste modification can occur by the production of secondary metabolites with sensorial impacts on the food or beverage and include acetic acid, esters, and higher alcohols (Howell, 2016).

Saccharomyces are best known for their positive contributions to food and beverage production, but they also can have deleterious effects including circumstances when the same species spoil the very commodities they produce (Blackburn, 2006). In particular, end products such as CO2 and ethanol, as well as minor compounds like acids, esters, ketones, aldehydes, alcohols, and sulfur compounds drastically change the aroma and flavor of a spoiled substrate (Howell, 2016).

Candida species make up one-quarter of all known yeasts and their heterogeneity means that they are responsible for the spoilage of a wide range of foods (Blackburn, 2006). Dekkera produces distinctive off-taints with secondary metabolism, where phenolic and mousy flavors can spoil the aroma and desirability of the wine (Howell, 2016). Several yeasts such as H. uvarum and C. krusei are able to produce significant amounts of acetic acid during spoilage of beverages, particularly wine (Howell, 2016). Yarrowia lipolytica is associated with surface discoloration of cheese, where catabolism of the amino acid tyrosine gives the pigmented compound melanin. Surface spoilage of uncooked and cooked meats (such as chicken or turkey) has been also observed, where the extracellular proteolytic and lipolytic activities result in spoilage aromas (Howell, 2016). Of particular importance is the growth of D. hansenii in fermented dairy products with the removal of lactic acid (Howell, 2016). The growth of Schizosaccharomyces pombe removes malic acid from fruit juices, which increases the pH and dramatically affects the taste and stability of the juice (Howell, 2016).

Meat products are rarely degraded by proteolysis by spoilage yeasts, as most do not produce extracellular proteases. There are some notable exceptions, e.g., Y. lipolytica, Rhodotorula, and Cryptococcus spp. in meat products cured with nitrates, spoilage with Pichia and Cryptococcus spp. can lead to metabolism of sodium nitrate and sodium nitrite (Howell, 2016). In sauerkraut, a pink discoloration is induced by Rhodotorula spp. (Campos et al., 2015).

1.4.3 Molds

Although the range of molds is immense there are a specific and rather limited number of genera and species that are spoilage hazards for each kind of food. The Zygomycetes, popularly known as the “pin molds” are often seen as rapid growers following a “hit and run” strategy for the foods that they spoil. The Penicillia and Aspergilli are common spoilage molds with the latter generally growing more rapidly and at higher temperatures or lower water activities than the former. Other types of molds are significant in food spoilage, but many molds may be present on, or isolated from, foods in which they never or rarely cause spoilage (Blackburn, 2006).

However, molds are also responsible for the formation of undesired mycotoxins that are small (molecular weight of ~700 DA) secondary metabolites produced by several fungi belonging mainly to the genera Aspergillus, Penicillium, Fusarium, and Alternaria. Some mycotoxins appear to be produced in response to environmental changes, usually due to the onset of stress conditions. The most significant mycotoxins, from both public health and agronomic perspectives, include aflatoxins, trichothesenes, fumonisins, ochratoxin A, patulin, tremogenic toxins, and ergot alkolids (Miescher Schwenninger et al., 2011).

3.1 Gas production and VOCs

Blown-pack spoilage (BPS) is a common type of spoilage observed in meats and meat products. BPS is characterized by abundant gas production that causes package distension, usually accompanied by foul odors, unacceptable discoloration, and textural changes (Clemens, Adam, & Brightwell, 2010), and VOCs also contribute to package distension and/or off-odors (Remenant, Jaffrès, Dousset, Pilet, & Zagorec, 2015) (Fig. 2). Generally, the major gas components in blown packs are CO2, H2, and VOCs, including aldehydes, alcohols, ketones, hydrocarbons, hydrogen sulfide, dimethyl sulfide, and organic acids (Adam, Flint, & Brightwell, 2010; Moschonas, Bolton, Sheridan, & McDowell, 2010). Different microbial species release different VOCs during meat spoilage, collectively leading to decreased quality. For example, butanol and butyric acids are main indicators of the BPS caused by clostridia. Hernandez-Macedo et al. (2012) analyzed the gas and VOCs compositions of vacuum-packed beef, finding that CO2 had the highest concentration in blown packs (generally 70%–95%), and 1-butanol, benzaldehyde, acetic acid were the main VOCs. According to Li et al. (2020), Pseudomonas spp.(30.46%), Enterobacter spp. (20.76%), Pantoea spp. (13.38%), Serratia spp. (12.63%), and Rahnella spp. (10.15%) predominated during meatball storage, and the BPS group had a CO2 abundance (78.53%) that was nearly twice that of the normal group. Specific spoilage species, of Clostridium spp., lactic acid bacteria (LAB), and Enterobacteriaceae, may drive BPS. Numerous Clostridium species are associated with the spoilage of chilled, vacuum-packed fresh meat, such as Clostridium algidicarnis, Clostridium algidixylanolyticum, Clostridium estertheticum, Clostridium frigidicarnis, Clostridium gasigenes, and Clostridium putrefaciens (Adam et al., 2010; Iacumin & Comi, 2021). LAB, such as Lactobacillus brevis, Leuconostoc mesenteroides, Lactobacillus pentosus, and other species such as Hafnia alvei and Klebsiella pneumonia, have also been implicated in the BPS of vacuum-packaged chilled meats (Gaenzle, 2015; Chaves, Silva, Sant'Ana, Campana, & Massaguer, 2012).

3.2 Slime and softening

Slime and softening on meat surfaces that affect consumer choice mainly result from the effects of three factors: i) Colonies and extracellular polysaccharides following mass microbial reproduction and secretion form a continuous slime layer, which protects the growth of microorganisms (Katiyo, de Kock, Coorey, & Buys, 2020). ii) During storage, endogenous enzymes and extracellular enzymes secreted by microorganisms decompose protein, fat, and other nutrients in meat to generate putrefactive substances, such as amines, indoles, organic acids, and ketones (Pellissery, Vinayamohan, Amalaradjou, & Venkitanarayanan, 2020; Stanborough et al., 2018). iii) Meat tissues are damaged by extracellular enzymes and the released interior material combines with the microbial biofilm to form part of the slime (Wickramasinghe, Ravensdale, Coorey, Dykes, & Chandry, 2021). The meat texture depends on the integrity of muscle fibers, and degradation of specific proteins (myofibrillar, collagen, and elastin) represents the main cause of meat softening (Petruzzi, Corbo, Sinigaglia, & Bevilacqua, 2017; Schreuders, Schlangen, Kyriakopoulou, Boom, & Jan van der Goot, 2021), which usually accompanies slime formation (Fig. 2).

Pseudomonas fragi, P. fluorescens, and Pseudomonas aeruginosa can produce slime on meat and products during storage (Martin, Murphy, Ralyea, Wiedmann, & Boor, 2011; Wang et al., 2021). Extracellular enzymes secreted by Pseudomonas species have strong protease activities against the myofibrillar and myomatrix proteins, which helps bacteria penetrate into meat to obtain new nutrition sources, which increases slime formation and meat softening (Katiyo et al., 2020). A. salmonicida quickly formed slime in chicken breast meat, which was characterized by strong proteolytic activity against myofibrillar proteins and dextran production (Wang, Zhang, et al., 2017). Meanwhile, some LAB species, such as Leuconostoc gelidum, Leuconostoc carnosum, and L. mesenteroides, produced slime by fermenting sugars in meat products and degrading nitrogen-containing compounds (Comi, Andyanto, Manzano, & Iacumin, 2016; Vihavainen & Bjorkroth, 2007). In addition, Serratia, Micrococcus, Shewanella, and Brochothrix species are also related to slime production and softening during meat spoilage (Pellissery et al., 2020). The amounts of slime are determined by packaging, processing methods, the relative humidity, and the temperature, among other factors. With anaerobic packaging, aerobic microorganisms are replaced by slow-growing facultative anaerobic microorganisms that have high potential for producing thick slime (Gram et al., 2002; Pothakos, Devlieghere, Villani, Bjorkroth, & Ercolini, 2015).

3.3 Discoloration and luminescence

Microorganisms are the main cause of meat discoloration in association with protein discoloration and pigment accumulation (Fig. 2). Metabolites produced by microbial growth may lead myoglobin to greenization, usually associated with H2O2 and H2S. For example, Weissella viridescens, Leuconostoc spp., and Pseudomonas putida can cause the greening of frankfurters and other pickled vacuum-packed meats (Smolander et al., 2002; Zhang, Jiang, Guo, Bai, & Zhao, 2020). Various organisms can secrete fat-soluble pigments and produce colored spots on meat surfaces, such as Enterococcus casseliflavus in canned luncheon meat; other microorganisms (including Serratia marcescens, P. aeruginosa, and Flavobacterium) can also cause pigment accumulation depending on various factors, such as the temperature, packaging conditions, and fat oxidation (Tomasevic, Djekic, Font-i-Furnols, Terjung, & Lorenzo, 2021).

Besides the excessive phosphorous contents from animal feeds, meat luminescence mainly results from contamination with luminescent bacteria during processing, storage, transportation, and in retail locations. Luminescent bacteria can release fluorescence between 450 and 500 nm, which is augmented by intracellular luciferases that can be observed with the naked eye under dark conditions. Photobacterium are commonly isolated from marine habitats (Yoshizawa, Wada, Kita-Tsukamoto, Yokota, & Kogure, 2009), but have recently also been identified in chilled meats as part of the spoilage microbiota (Hauschild, Hilgarth, & Vogel, 2020; Hilgarth, Fuertes, Ehrmann, & Vogel, 2018). Various Vibrio and Shewanella species with high luminescence potential have been identified in meat products (Höll, Hilgarth, Geissler, Behr, & Vogel, 2019). Remarkably, the presence of luminescent bacteria in meat-related products, which were traditionally detected from aquatic food, could be partly explained by two hypotheses. One is the microbial cross-contamination during food processing, because the meat and the aquatic products are usually separately manufactured by the same equipment, lines or in a same processing place (factory and household kitchen)(Singh, Walia, & Farber, 2019); in addition, the aquatic materials are commonly used as fundamental ingredients for meat products. Another marked reason is the improvements of detection techniques, since that the culture-dependent protocols have replaced by culture-independent strategies. Although the harmfulness of luminescent substance itself to humans may unknown (Doulgeraki et al., 2012), it is not recommended to consume luminescent meat.