Abstract
Fish and seafood products are some of the most important protein sources in human nutrition. At the same time, these products are perishable and, if left unpreserved, spoil rapidly. Some fish products are heavily cured (salted, dried) and shelf stable at ambient temperature. An increasing number of fish products are preserved by low levels of salt, cooling, packaging in modified atmosphere, and/or addition of low levels of preservatives. The microflora of these products is often complex; however, spoilage is mostly caused by microbial action.
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Introduction
Fish and seafood products are some of the most important protein sources in human nutrition. At the same time, these products are perishable and, if left unpreserved, spoil rapidly. Some fish products are heavily cured (salted, dried) and shelf stable at ambient temperature. An increasing number of fish products are preserved by low levels of salt, cooling, packaging in modified atmosphere, and/or addition of low levels of preservatives. The microflora of these products is often complex; however, spoilage is mostly caused by microbial action.
Production of fish has increased over many years and the increase in the last two decades has mostly been due to a dramatic growth in the aquaculture sector (Fig. 1). Catches from wild fish populations have stagnated at approximately 90–100 million metric tons and today (2005), 40% of the fish used for human consumption are aquaculture-reared species. Also, our processing of fish has changed. The increase in fish production has mostly been utilized as “fresh fish,” whereas cured and canned products have become, proportionally, less popular (Fig. 2).
Global fish production from wild fish catches and from aquaculture (FAO, 2004)
Utilization of fish catches (FAO, 2004)
The raw materials for seafood products are bivalve mollusks, crustaceans, cephalopods, or finfish. These organisms have very different lifestyle and different gross composition, which influence subsequent spoilage patterns. Bivalve mollusks such as oyster accumulate glycogen (Martino & da Cruz, 2004), whereas other fish raw materials are virtually devoid of carbohydrates. Therefore, postmortem pH does not decrease to the same extent as pH in red meats and Shewanella species, which are quite sensitive to low pH can therefore grow and spoil chilled finfish similar to their involvement in spoilage of high-pH meat (Borch, KantMuermans, & Blixt, 1996). Crustacea have a high content of free amino acids, some of which (e.g., arginine and glycine) contribute to the characteristic crustacean flavor (Finne, 1992). Many cephalopods contain ammonia (NH4 +) in quite high concentration (100–300 mM) (Seibel, Goffredi, Thuesen, Childress, & Robison, 2004). Seafood raw materials are, in general, very rich in nonprotein nitrogen (NPN) such as amino acids and trimethylamine oxide, and bacterial metabolism of these compounds is often the cause of spoilage.
Spoilage Concepts
Spoilage of a food product is, in this chapter, a term used to describe that the product is no longer edible based on a sensory assessment. Safety issues are not included in the spoilage or shelf-life considerations. The sensory rejection may be caused by discoloration, physical changes, textural changes, slime or gas formation, or the development of off-flavors and off-odors. Spoilage may arise due to a number of chemical or microbiological changes. Lipid hydrolysis and oxidation are very common causes of spoilage in many fatty fish species and rejection of small uneviscerated species such as anchovies may be caused by “belly burst” in which the enzymes and microorganisms of the digestive tract cause massive gas development (Careche, Garcia, & Borderias, 2002). Protein denaturation and development of “card box” flavor due to changes in the protein and lipid fraction are common causes of spoilage of frozen fish products. However, microbial growth and metabolism is the major cause of spoilage of fresh, lightly preserved, and semi-preserved fish products. Microbial spoilage involves growth of bacteria, yeast, or fungi to high numbers and products of their metabolism give rise to the sensory impressions perceived as spoilage. Visible slime may appear as a result of the formation of extracellular polysaccharides from carbohydrate substrates (Lyhs, Koort, Lundstrom, & Bjorkroth, 2004). Fungal growth on, for example, dried fish is also a very visible spoilage form (Chakrabarti & Varma, 2000) as is the red discoloration that often accompanies spoilage of heavily salted fish (Prasad & Panduranga Rao, 1994). Off-odors and off-flavors arise when low-molecular-weight compounds are degraded by microorganisms. Typical spoilage compounds of seafood products include ammonia from deamination of amino acids, sulfides formed from sulfur-containing amino acids (Herbert & Shewan, 1975), trimethylamine resulting from bacterial reduction of trimethylamine oxide, and esters that may arise from degradation of phospholipids (Table 1).
The microflora on newly caught or produced product is a function of the microorganisms present on the live animal and the microorganisms contaminating during processing. Each seafood processing operation has its own unique microflora reflecting the raw materials and the preservation parameters used (Bagge-Ravn, Yin, Hjelm, Christiansen, Johansen, & Gram, 2003). Only some of the microorganisms will be able to tolerate the product-specific conditions (temperature, packaging, pH, water activity) and proliferate during storage. Those successful will form the spoilage microflora (or microbiota), which simply are the microorganisms present on the product at the point of sensory rejection. Only some of the species present are able to produce the off-odors and off-flavors, which are typical of the spoiling product, and this spoilage potential is typically determined by inoculating pure cultures of bacteria in sterile food systems (Chinivasagam, Bremner, Wood, & Nottingham, 1998; Dalgaard, 1995b; Gram, Trolle, & Huss, 1987; Herbert, Hendrie, Gibson, & Shewan, 1971; Joffraud, Leroi, & Chevalier, 1998; Miller, Scanlan, Lee, & Libbey, 1973). Subsequently, it must be determined if the microorganisms with spoilage potential are capable of producing the amounts of compounds associated with the spoiling product under relevant conditions of storage. This assesses the so-called spoilage activity of the microorganisms. For instance, Vibrio spp., Aeromonas spp., Shewanella spp., and Photobacterium phosphoreum are capable of reducing trimethylamine oxide (TMAO) to trimethylamine (TMA). The latter, fishy smelling compound, is typical of spoiling gadoid fish species. Gadoid species are those fish belonging to the Gadidae family, which includes cod, haddock, whiting, and pollock.
Shewanella species can grow under aerobic storage to 108–109 cfu/g and produce the amounts of TMA found in aerobically, iced-stored fish. When the fish is packed in CO2 atmosphere, large amounts of TMA are detected; however, counts of Shewanella remain below 106 cfu/g. Although they have the spoilage potential, they do not possess sufficient spoilage activity. Instead, CO2-tolerant P. phosphoreum grow and produce the TMA formed in packed fish (Dalgaard, 1995b; Dalgaard, Gram, & Huss, 1993).
In some products, the specific spoilage microorganisms are one single group or species, for example, Shewanella baltica in iced cod (Chai, Chen, Rosen, & Levin, 1968; Vogel, Venkateswaran, Satomi, & Gram, 2005), P. phosphoreum in CO2-packed chilled fish (Dalgaard, Mejlholm, Christiansen, & Huss, 1997), or Lactobacillus alimentarius in some marinated herring (Lyhs, Korkeala, Vandamme, & Bjorkroth, 2001). The spoilage patterns of other products may be much more complex and spoilage is brought about by a combination of several microorganisms. Typically, these as single cultures do not give rise to the product spoilage off-odors but only when cocultured (Jorgensen, Huss, & Dalgaard, 2000; Mejlholm, Boknaes, & Dalgaard, 2005).
Fish Substrates of Spoilage
Fish muscle is rich in nonprotein nitrogen and the amino acids, nucleotides, and trimethylamine oxide serve as microbial substrates or electron acceptors. The products of microbial metabolites result in the spoilage of the products (Table 1). Trimethylamine oxide is a small odorless compound which accumulates in finfish, elasmobranches, cephalopods, and some bivalves (Sadok, Uglow, & El-Abed, 2003; Seibel & Walsh, 2002). In finfish, it is mostly found in marine gadoid fish species but can also be formed in other species. It was believed for many years that the compound was not produced in freshwater fish species; however, it has been detected in both Nile perch and tilapia (Anthoni, Borresen, Christophersen, Gram, & Nielsen, 1990). The role of TMAO in fish is not known but it is generally believed that it acts as a compatible solute balancing the effects of salt levels in the marine environment, deep pressure, or high concentrations of urea found in elasmobranches (Seibel & Walsh, 2002; Yancey, Clark, Hand, Bowlus, & Somero, 1982), where it stabilizes protein folding (Yancey, 2005). Several bacterial species may use TMAO as an electron acceptor in an anaerobic respiration and the reduced compound, trimethylamine (TMA), is the most prominent compound giving rise to “fishy” odor. TMAO/TMA is a redox couple and its presence in fish ensures a positive redox potential of approximately 200 mV as opposed to red meat where the Eh is negative. The Eh decreases to negative values when TMAO is reduced to TMA (Huss & Larsen, 1980; Yancey, 2005).
The ability to use TMAO as an electron acceptor gives obligately respiratory microorganisms an advantage when oxygen becomes limited. Ringo, Stenberg, and Strom (1984) suggested that the complete Krebs’ cycle was used when Shewanella respired using TMAO and that amino acids such as cysteine were used as substrates, resulting in the parallel formation of hydrogen sulfide (H2S). More recent studies have determined that the metabolism is slightly more complex and that TMAO reduction involves only part of the TCA cycle (Scott & Nealson, 1994).
Sulfurous odors arise from bacterial degradation of l-cysteine and l-methionine. The volatiles consist of an array of compounds including hydrogen sulfide, methyl mercaptan, and dimethyl sulfide (Herbert & Shewan, 1975). Some sulfurous off-odors give rise to more fruity or onion-like off-odors. The fruity off-odors also consist of esters and are typically formed from degradation of monoamine–monocarboxylic amino acids (Castell & Greenough, 1959) but also low-molecular-weight fatty acids can act as substrates for bacterial production of fruity off-odors (Reddy, Bills, & Lindsay, 1969).
Bacterial decarboxylation of amino acids gives rise to the formation of the so-called biogenic amines (Table 2), some of which are off-odorous. These compounds have mainly been of interest due to their role in food safety being the cause of histamine poisoning; however, they have also been used as indicators of spoilage in a number of products.
Seafoods are products rich in protein and it is often stated that proteolytic bacteria are important for the spoilage process. However, the pool of free amino acids is more than sufficient to support bacterial growth and acts as substrates for the off-odors and off-flavors formed. In a series of classical experiments, Lerke and coworkers (Adams, Farber, & Lerke, 1964; Lerke, Adams, & Farber, 1963; Lerke, Adams, & Farber, 1965; Lerke, Farber, & Adams, 1967) inoculated spoilage bacteria into fish juice and separated it into a high-molecular-weight fraction (protein) and a low–molecular-weight fraction (amino acids and TMAO). In the LMW fraction, off-odors and spoilage compounds identical to the spoiling fish developed, whereas no off-odors were formed in the HMW fraction (Table 3).
The odor, flavor, and color of fish are influenced by its feed; however, little is known about the influence of fish feed on subsequent spoilage patterns. This is becoming an issue as an increasing amount of fish raw material is produced in aquaculture. Replacing 50% of fish meal in a typical trout diet with vegetable protein had no influence on subsequent growth of bacteria on iced fillets or on spoilage rates (Ozogul, Ahmad, Hole, Ozogul, & Deguara, 2006).
Taxonomy of an Important Fish Spoilage Bacterium
The understanding of the bacteriology of seafood spoilage was brought about by studies in a 20-year period from 1950 to 1970 by Castell (Castell & Anderson, 1948), by Lerke’s group (Adams et al., 1964; Lerke et al., 1963, 1965, 1967), and by the microbiology team at Torry Research Station led by James Shewan (Castell & Anderson, 1948; Shaw & Shewan, 1968; Shewan, 1977). It was discovered, relatively early, that the “total bacterial count” was not a parameter that could indicate spoilage or remaining shelf life of fresh fish (Castell, Anderson, & Pivnick, 1948; Huss, Dalsgaard, Hansen, Ladefoged, Pedersen, & Zittan, 1974). However, the spoilage off-odors and off-flavors were produced by very specific bacteria, and the most noticeable were the fishy and sulfidy odors of spoiling gadoid fish species produced by Gram-negative, psychrotrophic bacteria capable of producing hydrogen sulfide and reducing trimethylamine oxide. The specific microorganisms associated with chill storage fish spoilage were originally grouped as Achromobacter, which was a compilation of Gram-negative, nonfermentative, rod-shaped bacteria, several of which today have been reclassified as Acinetobacter, Moraxella, Psychrobacter, and Shewanella. In 1941, Long and Hammer (Long & Hammer, 1941) reclassified the bacterium as Pseudomonas and due to its role in fish spoilage, the species became Pseudomonas putrefaciens. The research team at Torry Research Station classified pseudomonads into four groups (I, II, III, IV) (Shewan, Hobbs, & Hodgkiss, 1960) and the fish spoilage bacterium belonged to group IV. This bacterium was moved to the Alteromonas genera because of different GC contents between Ps. putrefaciens (43–53%) and the majority of pseudomonads (58–72%). Molecular approaches once again led to the bacterium’s name being changed. Colwell and coworkers (Macdonell & Colwell, 1985) sequenced the 5S rRNA gene of several marine bacteria and determined that the bacterium belonged to a completely new genus named Shewanella. Recently, results of 16S rRNA gene sequence analyses of genera from this group led to a proposal for a new family Shewanellaceae (Ivanova, Flavier, & Christen, 2004), which contains about 30 Shewanella spp. The number of new Shewanella species is constantly increasing. In 1998, Ziemke, Hofle, Lalucat, and Rossello-Mora (1998) characterized a large number of Shewanella isolates from the Baltic Sea using DNA–DNA hybridization, 16S rRNA gene sequencing, and phenotypic testing. They concluded that strains classified as Shewanella putrefaciens were a diverse group and belonged to two different species, one being S. putrefaciens and a new one being S. baltica. Recent studies (Vogel et al., 2005) have revealed that the H2S-producing bacteria that develop during iced storage of cod and plaice are indeed S. baltica strains. Although it is not possible to know whether bacterial isolates from former studies are S. baltica or S. putrefaciens or even some of the new psychrotrophic Shewanella species such as S. hafniensis or S. morhaue (Satomi, Vogel, Gram, & Venkataraman, 2006; Shewan et al., 1960), one must assume that several of these probably today would be classified as S. baltica. Recent studies of low-temperature-stored garfish and tuna have also identified the H2S-producing bacteria of the spoilage microflora as S. baltica (Dalgaard, Madsen, Samieian, & Emborg, 2006; Emborg, Laursen, & Dalgaard, 2005).
Microbiology of Freshly Caught Fish
The muscles of healthy fish are sterile and microorganisms reside at the surfaces such as skin, gills, and gastrointestinal tract of finfish. The level of microorganisms vary depending on the area of catch; however, the skin typically contains 104 cfu/cm2, the gills 106 cfu/g, and the digestive tract up to 108 cfu/g (Austin, 2002). The level of microorganisms in the digestive tract may vary from 104 to 109 cfu/g (Spanggaard et al., 2000). Most of the microbiota are culturable under standard laboratory conditions; however, the digestive tract may contain high levels of anaerobic microorganisms (Huber, Spanggaard, Appel, Rossen, Nielsen, et al., 2004) requiring special culture conditions.
A wide array of different bacterial species can be found on fish; however, the dominant microbes are genera or species typical of the aquatic environment, including pseudomonads, coryneforms, and bacteria belonging to the Acinetobacter/Moraxella group (Table 4). In some studies of tropical fish species, Gram-positive bacteria dominate the microbiota; however, the bacterial flora mostly consists of Gram-negative species. The microbiota on the skin surface is often dominated by aerobic, nonfermentative microorganisms, whereas a higher proportion of fermentative bacteria are present on the gills and in the gastrointestinal tract (Spanggaard et al., 2001). The bacteria that subsequently become important in spoilage of fresh finfish are present only in small proportions. Vogel et al. (2005) determined that the number of H2S-producing bacteria varied between 101 and 103 and constituted between 0.1 and 10% of the total bacterial count. After 3 weeks of storage, the counts had increased to 108–109 and H2S-producing bacteria constituted 2–30% of the viable count. In the warm summer months, several of the H2S-producing bacteria were mesophilic Shewanella algae, which is a human pathogen. These bacteria quickly disappeared upon iced storage and the psychrotrophic H2S-producing bacteria subsequently dominated the spoilage bacterial community.
Product Categories and Spoilage
The principal spoilage microorganisms and microbial spoilage processes are described in this chapter. The seafood products are grouped in categories having somewhat similar microbial ecology – and hence, similar spoilage processes. Table 5 provides examples of typical shelf lives of some seafood products.
Raw, Fresh Seafood
Bivalve Mollusks
As mentioned, oysters have a relatively high content of glycogen and spoilage is characterized by the growth of lactic acid bacteria, the formation of lactic acid, and a concurrent decrease in pH. The pH of fresh oysters is approximately 6 and spoiled oysters have pH values of 4.9–5.3 (Aaraas et al., 2004; Cook, 1991). Other studies have noted an increase in bacteria such as Ps. putrefaciens (Brown & McMeekin, 1977) or Pseudoalteromonas (Romero, Gonzalez, & Espejo, 2002) during spoilage and this is more likely to cause development of amine compounds. It is often stated that bacteria will not grow when mollusks are stored live; however, Lorca, Pierson, Flick, and Hackney (2001) determined that counts of halotolerant bacteria (such as Vibrio spp.) increased from approximately 105 to 108 cfu/g over a 10-day storage period. The increase was seen at storage temperatures of 7, 13, and 21°C.
Crustaceans
Fresh shrimp are often stored in ice for a few days to facilitate loosening of the shell, known as ripening (Hoegh, 1989). This process is autolytic and partly caused by the increase in pH which loosens the shrimp shell proteins that have a low pI (Hoegh, 1989). The content of ammonia increases steadily during iced storage to 1.5 g/kg after 7–8 days of storage. This is primarily a result of autolytic proteases and is accompanied by a concurrent increase in free amino acids (Hoegh, 1989).
Psychrotrophic bacteria increase during storage (Cann, 1973). The spoilage flora may contain a large proportion of Moraxella or Acinetobacter (Surendran, Mahadeva Iyer, & Gopakumar, 1985; Vanderzant, Cobb, Thompson, & Parker, 1973), but other studies have revealed that pseudomonads and alteromonads dominate (Shamshad, Kher, Riaz, Zuberi, & Qadri, 1990). Pseudomonas fragi and Shewanella putrefacienshave been identified as the primary spoilage agents of chill-stored shrimp, with Ps. fragi spoiling iced-stored shrimp and S. putrefaciens being the dominant microorganism in shrimp stored in ice slurry (Chinivasagam, Bremner, Thrower, & Nottingham, 1996). Naturally, spoiling prawns are characterized by amines, sulfides, and esters and both Ps. fragi and S. putrefaciens produced sulfides, whereas amines were mostly formed by S. putrefaciens and the spoilage esters mainly by Ps. fragi (Chinivasagam, Bremner, et al., 1998).
Indole has been suggested as a spoilage indicator for shrimp and prawn; however, this is not a universal compound in all species. Indole is produced by bacteria that degrade tryptophan. Levels may, in some species, increase to above 100 μg/100 g and some regulatory agencies use 250 μg/100 g as the spoilage limit. Indole production is mainly an issue of high-temperature storage and is likely caused by members of Enterobacteriaceae; however, indole is not formed in all species (Mendes, Goncalves, Pestana, & Pestana, 2005), not even at elevated temperatures in severely spoiled product (Table 6). Sensory rejection of crustacea may also be caused by the formation of black spots (melanosis). Melanin is formed from tyrosine and it has been suggested that this is a bacterial process as several spoilage pseudomonads can oxidize tyrosine (Chinivasagam, Bremner, & Reeves, 1998). This process is normally prevented or controlled by dipping the shrimp in sulfites or other reducing components.
Cephalopods
The shelf life of iced-stored squid is slightly shorter than that of most finfish and the product is rejected in 8–12 days (Albanese, Cinquanta, Lanorte, & Di Matteo, 2005; Paarup et al., 2002; Vaz-Pires & Barbosa, 2004). Spoilage is characterized by ammoniacal off-odors and the rapid onset of ammonia production at relatively low cell densities suggested that spoilage is mainly autolytic and not caused by bacterial growth (Vaz-Pires & Barbosa, 2004). Paarup et al. (2002) determined that the spoilage microflora was dominated by Pseudoalteromonas that reached 107 cfu/g. This bacterium may contribute to late ammonia formation. Trimethylamine also develops during iced storage (Paarup et al., 2002) but it is not known which microbes are responsible for its production.
Finfish
Storage of finfish at ambient temperature leads to rapid growth of mesophilic Gram-negative bacteria belonging to Vibrionaceae or Enterobacteriaceae (Len, 1987; Liston, 1992). These bacteria reduce TMAO to TMA and produce several sulfides and shelf life is short, typically less than 24 h. Cooling, mostly in flaked or crushed ice, is the most common and most effective method for preservation of fresh finfish. The initial biochemical changes in the fish muscle are autolytic and related to the breakdown of ATP. These changes, however, do not have a major impact on sensory quality. Lipid hydrolysis and oxidation may proceed in fatty fish species and contribute to the development of unpleasant off-flavors and off-odors. However, the most offensive off-odors and flavors leading to spoilage at a low temperature are a consequence of bacterial action. As temperature decreases, the microbiota of the product changes and at 0–2°C, the spoilage microflora which reach 108–109 cfu/g after 2–4 weeks is mostly dominated by pseudomonads and shewanellae (Fig. 3, Table 7) even though other psychrotrophic microbes sometimes also grow. Some studies have reported the growth of the Gram-positive bacterium Brochothrix thermosphacta in iced finfish (Grigorakis, Alexis, Gialamas, & Nikolopoulou, 2004; Lalitha et al., 2005) but their numbers are two orders of magnitude lower than numbers of Shewanella (Koutsoumanis & Nychas, 1999). Photobacterium phosphoreum may also grow during aerobic low-temperature storage of some fish species, and together with shewanellae and pseudomonads constitute the spoilage microflora (Dalgaard et al., 2006). The specific importance of each of these three groups in the actual spoilage process has not been described.
The dominance of pseudomonads and shewanellae has been seen in warm tropical freshwater fish and in fish caught in cold, marine waters (Gram, Wedell-Neergaard, & Huss, 1990; Koutsoumanis & Nychas, 1999). Growth of these psychrotrophic bacteria in marine fish is accompanied by the production of TMA caused by Shewanella metabolism. Pseudomonas spp. dominate the spoilage of iced freshwater finfish (Chytiri, Chouliara, Savvaidis, & Kontominas, 2004; Gelman, Glatman, Drabkin, & Harpaz, 2001; Gram, 1989) and the spoilage off-odors are typically more fruity or onion-like. Remaining shelf life of iced gadoid species can be predicted based on numbers of H2S-producing bacteria because their numbers correlate closely with sensory rejection (Fig. 4; Jorgensen, Gibson, & Huss, 1988).
Changes in total bacterial count and in H2S-producing bacteria during storage of haddock fillets at 1°C. At day 0 and 10, H2S-producing bacteria account for 3 and 29% of the total bacterial count, respectively (Chai et al.,1968)
Growth of H2S-producing bacteria in iced cod and the rejection based on sensory evaluation (Jorgensen et al., 1988)
Temperature is the most important factor influencing shelf life of fresh finfish. Shelf life of iced cod is approximately 14–16 days (Jorgensen et al., 1988), whereas increasing the temperature to 5°C shortens the shelf life to 6–7 days.
Packed, Fresh Fish
Spoilage of aerobic chill-stored fish is mainly caused by the growth of pseudomonads and shewanellae which are respiratory bacteria and it could be expected that removal of the oxygen-containing atmosphere either by vacuum packing or by CO2 packaging would result in extension of shelf life. However, Shewanella species are capable of anaerobic respiration using TMAO as an electron acceptor (Jorgensen & Huss, 1989; Pitt & Hocking, 1999; Ringo et al., 1984; Scott & Nealson, 1994) and the CO2-tolerant marine bacterium P. phosphoreum also grows well in vacuum-packed fish at low temperatures (Dalgaard et al., 1993). Therefore, vacuum packing does not result in a marked extension of the sensory shelf life of many marine fish species. Freshwater fish and some tropical species do not carry these two spoilage bacteria in high amounts and vacuum packing is likely to select for a microflora dominated by lactic acid bacteria (Hussain, Ehlermann, & Diehl, 1976; Pedersen & Snabe, 1995); however, little is known about the effect on shelf life. Concern has been raised that vacuum packing would increase the risk of botulism because Clostridium botulinum type E would be able to grow and produce toxin if temperatures were above 3°C. However, no case of botulism has ever been attributed to fresh, packed fish. First, no toxin was detected in a survey of 1,100 commercial packages of vacuum-packed fresh fish (Lilly & Kautter, 1990) and second, type E toxin is heat labile and would likely be inactivated in cooked product (Ohye & Scott, 1957).
One would assume that packaging in a CO2-containing atmosphere would cause a dramatic extension of chilled shelf life because CO2 has a marked inhibitory effect on respiratory bacteria such as shewanellae and pseudomonads. Red meat typically spoils due to the growth and metabolism of pseudomonads and packaging in CO2 extends chilled shelf life from days to months, with the microflora becoming dominated by lactic acid bacteria (Borch et al., 1996). The shelf life of marine fish species packaged in a CO2 atmosphere is only marginally extended as compared to nonpackaged product and in gadoid species, significant amounts of trimethylamine are produced (Dalgaard et al., 1993; Debevere & Boskou, 1996; Ruiz-Capillas, Saavedra, & Moral, 2003). This is due to the growth and metabolism of the CO2-tolerant marine bacteria P. phosphoreum (Dalgaard et al., 1993; Debevere & Boskou, 1996; Emborg, Laursen, Rathjen, & Dalgaard, 2002) and remaining shelf life of CO2-packaged cod can be modeled based on numbers of P. phosphoreum (Dalgaard, 1995a). Photobacterium phosphoreum grows to 107–108 cfu/g during low-temperature storage of packed fish and the amounts of TMA produced far exceeds the amounts formed during spoilage of nonpacked fish. This is due to very high production of TMA per cell of P. phosphoreum (Dalgaard, 1995b).
CO2 packaging of fish that do not contain P. phosphoreum extends shelf life to some degree. Photobacterium phosphoreum is sensitive to freezing and a freezing step before CO2 packaging eliminates the bacteria and extends shelf life of the packaged product (Dalgaard, Munoz, & Mejlholm, 1998; Emborg et al., 2002). Also, the shelf life of freshwater fish or tropical water fish that do not naturally harbor P. phosphoreum may be extended by packaging either under vacuum (Merivirta, Koort, Kivisaari, Korkeala, & Bjorkroth, 2005) or in a CO2 atmosphere (Gimenez & Dalgaard, 2004; Reddy, Villanueva, & Kautter, 1995). The elimination of P. phosphoreum from packaged fish often leads to a dominance by lactic acid bacteria and B. thermosphacta which can reach 107–108 cfu/g (Emborg et al., 2002; Lannelongue, Finne, Hanna, Nickelson, & Vanderzant, 1982), which is similar to patterns observed for stored, packaged red meats (Borch et al., 1996; Dainty & Mackey, 1992). A bacterium belonging to Enterobacteriaceae has also been detected as a major part of the spoilage microflora in CO2-packaged tuna fish (Emborg et al., 2005). This bacterium and P. phosphoreum are both capable of forming large amounts of histamine at low temperatures (2°C) (Emborg et al., 2005, 2002). The production of biogenic amines is in several fish species believed to be a consequence of elevated temperatures that allow mesophilic Morganella morganii to grow and decarboxylate amino acids (Lehane & Olley, 2000). Amine production is of special interest in scombroid fish species which are rich in histidine, the precursor of histamine. Photobacterium phosphoreum may produce histamine (van Spreekens, 1987) at refrigeration temperatures but the finding of other M. morganii-like psychrotolerant histamine producers is novel. Histamine production in Sri Lankan tuna fish packed in CO2 and N2 and stored at 2°C began at day 3 and increased to more than 1,000 ppm on day 9 (Emborg et al., 2005). In garfish stored aerobically at 0°C, only low concentrations of histamine were detected and only after sensory rejection; however, at 5°C, more than 1,000 ppm were formed both in aerobically stored and CO2-packaged garfish (Dalgaard et al., 2006). Histamine formation parallels TMA formation and, hence, is a similar spoilage indicator.
Cured Seafood
Curing of fish refers to a wide variety of preservation principles combining salting, acidification, fermentation, and addition of preservatives such as sorbate, benzoate, lactate, and acetate. Although the proportion of the fish catch that is used for cured products is decreasing (Fig. 2), still at least 10 million tons are preserved in this manner. As the degree of preservation is “increased” compared to fresh fish, there is a change in the spoilage microflora toward fermentative Gram-negative bacteria, lactic acid bacteria, and yeast (Gram, 2005).
Salted, Cold-Smoked Fish
Especially salmon, but also to some extent trout, cod, and halibut are processed as lightly salted, cold-smoked products. The salt concentration is typically between 3 and 6% (as water-phase salt) and the cold-smoking process never increases above 28–30°C. Fish proteins denature at higher temperatures and the fish would obtain a “cooked” appearance as in hot-smoked products. The process may also rely on a combination of drying and addition of liquid smoke (Siskos, Zotos, & Taylor, 2005). Cold-smoked products are typically packaged under vacuum and retail distributed at refrigeration temperature. Often the products are held under frozen storage before display at retail. If products are stored aerobically, spoilage occurs more rapidly and visible colony growth of pseudomonads and yeast cells can be seen. Packaging of salmon and other fatty fish species also serves the purpose of eliminating oxidation of the lipid fraction as rancidity otherwise becomes a major off-odor.
The shelf life of vacuum-packaged, cold-smoked fish varies between species and factories and depends to some extent on the degree of drying, smoking, and the amount of salt added (Leroi & Joffraud, 2000). The sensory shelf life varies between 3 and 9 weeks (Jorgensen, Dalgaard, & Huss, 2000); however, the longer shelf lives may not be acceptable from a safety perspective as, for instance, Listeria monocytogenes and sometimes C. botulinum may be able to grow in this product (Gram, 2001a, 2001b). Recently, consumption of a packed cold-smoked salmon product 3 days after “use-by-date” was linked to a case of botulism (Dressler, 2005). The total bacterial count is reduced slightly by the cold-smoking process and is between 101 and 104 cfu/g in the freshly produced product (Dondero, Cisternas, Carvajal, & Simpson, 2004; Hansen, Drewes Rontved, & Huss, 1998; Leroi, Joffraud, Chevalier, & Cardinal, 1998).
The total bacterial count of vacuum-packaged, cold-smoked fish increases during refrigerated storage (4–5°) and the spoilage microflora is often dominated by lactic acid bacteria or a combination of lactic acid bacteria and fermentative Gram-negative bacteria (Enterobacteriaceae or P. phosphoreum) (Hansen et al., 1998; Leisner, Millan, Huss, & Larsen, 1994; Leroi et al., 1998; Lyhs, Bjorkroth, Hyytia, & Korkeala, 1998). Lactic acid bacteria counts typically increase to 106–108 cfu/g during a few weeks of refrigerated storage (Fig. 5) (Jorgensen, Dalgaard, et al., 2000a; Leroi & Joffraud, 2000). The spoilage pattern of cold-smoked fish is complex and no single bacterial species has been identified as being responsible for the spoilage. Although autolytic changes may cause some textural changes, the actual spoilage is of bacterial origin (Hansen, Gill, Rontved, & Huss, 1996). Several types of lactic acid bacteria may become dominant in cold-smoked fish; some studies revealed that the microflora is dominated by carnobacteria (Paludan-Muller, Dalgaard, Huss, & Gram, 1998) and in other trials different Lactobacillus species are dominant. Based on phenotypic characteristics, the lactobacilli have been identified as Lb. curvatus, Lb. sakei, and Lb. plantarum,with each of three processing plants having their own composition of the flora (Hansen & Huss, 1998). The odor profile of spoiled cold-smoked fish varies and a range of potentially odorous volatile compounds are produced during spoilage, including alcohols, aldehydes, esters ketones, and phenols (Jorgensen, Huss, & Dalgaard, 2001). Only some compounds were produced in quantities exceeding an odor threshold and trimethylamine and 3-methylbutanal were both believed to contribute to the spoilage odor profile (Jorgensen et al., 2001). Several of the bacteria that can be isolated from the spoilage microflora of cold-smoked fish produce spoilage off-odors either as pure cultures or as mixed cultures (Joffraud et al., 1998; Stohr, Joffraud, Cardinal, & Leroi, 2001). However, it has not been possible to correlate these odor profiles directly to the profile of the spoiling product.
Changes in aerobic count, lactic acid bacteria, H2S-producing bacteria, and yeasts and molds in cold-smoked salmon stored under vacuum at 8°C (Leroi et al., 1998)
Cold-smoked fish products are high-value delicatessen products which are traded globally, and an objective chemical “spoilage index” would be valuable in quality and shelf-life determinations (Leroi, Joffraud, Chevalier, & Cardinal, 2001). It has been demonstrated that the production of biogenic amines may be indicative of spoilage, although the amines themselves apparently do not contribute to the spoilage profile (Jorgensen, Huss, et al., 2000). Several different combinations of biogenic amines can be found at the point of spoilage (Table 8) (Jorgensen, Dalgaard, et al., 2000) and some are likely to be the result of metabolism by mixed bacterial communities. For instance, most spoilage bacteria produce only low concentrations (max 10 μg/10 g) of putrescine when grown as single cultures (Jorgensen, Huss, et al., 2000). The spoiling product is characterized by much higher putrescine concentrations and cocultures of lactic acid bacteria and Gram-negative bacteria give rise to the concentrations equivalent of the spoiling product. A similar metabiosis is seen in spoilage of vacuum-packed meat (Dainty, Edwards, Hibbard, & Ramantanis, 1986; Edwards, Dainty, & Hibbard, 1985). Putrescine is formed by ornithine decarboxylation which is common in several Gram-negative bacteria. The pool of ornithine may be replenished by lactic acid bacteria that use arginine deiminase to convert arginine to citrulline and ornithine carbamoyltransferase to convert citrulline to ornithine (Jorgensen, Huss, et al., 2000).
Other Lightly Preserved Seafood Products
A number of other delicatessen seafood products are similar to the cold-smoked fish in preservation profile and, hence, in spoilage microbiology. For instance, cooked shrimp may be packaged in modified atmosphere and distributed at refrigeration temperature (Mejlholm et al., 2005) or brined before packaging (Dalgaard et al., 2003). These products contain 2–3% NaCl (water-phase salt) and are preserved with either lactic acid or a combination of citric, sorbic, and benzoic acid. The shelf life is 2–3 weeks and the spoilage microflora is dominated by lactic acid bacteria accompanied by B. thermosphacta that grow to 107–108 cfu/g (Mejlholm et al., 2005). Single bacterial cultures did not produce the odor profile typical of the spoiling product, but a coculture of Carnobacterium maltaromaticum and B. thermosphacta produced the typical “wet dog” off-odors.
The Scandinavian speciality “gravad” fish is also a lightly preserved product similar to cold-smoked fish. Fillets are sprinkled with salt, sugar, herbs (typically dill), and spices and left under slight pressure for 1–2 days at refrigeration temperature. The product is stored aerobically or vacuum packaged (Leisner et al., 1994; Lyhs, Bjorkroth, & Korkeala, 1999; Lyhs, Lahtinen, et al., 2001). The aerobic count increases in vacuum-packed product to approximately 108 cfu/g over 2–3 weeks and the microflora is dominated by lactic acid bacteria and also H2S-producing bacteria, which may increase to 106 cfu/g (Lyhs, Lahtinen, et al., 2001). The dominant lactic acid bacteria are Lactobacillus sakei, Lb. curvatus, and Carnobacterium piscicola (now C. maltaromaticum) (Lyhs, Korkeala, & Bjorkroth, 2002).
Barrel-salted lumpfish roe (as described below) is used in a desalted type of product in which the salt concentration is adjusted to 4% and pH is reduced with lactic acid to approximately 5.5 (Basby, Jeppesen, & Huss, 1998a). This product is packed in airtight containers and distributed at refrigeration temperature. Spoilage which manifests itself with off-odors characterized as sulfidy, sour, or rotten is caused by bacterial growth (Basby, Jeppesen, & Huss, 1998b). Lactic acid bacteria increased to 107–108 cfu/g and Enterobacteriaceae were detected at levels between 105 and 106 cfu/g. When assessing spoilage potential, only M. morganii strains produced off-odors in a heat-treated roe (Basby, Jeppesen, & Huss, 1998c). Although not tested, it is likely that spoilage in this product is brought about by an interaction between the lactobacilli and the Gram-negative bacteria present.
Semipreserved Seafood Products
Several fish products are preserved by NaCl, acid, and preservatives like benzoic acid, sorbic acid, lactate, acetate, and/or nitrate. Some of the products are based on raw fish such as Scandinavian marinated herrings, the German rollmops, or the anchovies of Southern Europe. Other types of products such as brined shrimp are based on cooked raw materials.
The raw materials for marinated herring are either barrel-salted herring stored for 6–12 months or fillets that are acid-brined for 2–3 weeks. Subsequently, the fish is drained and covered in a brine (or marinade) with salt, acetic acid, sugar, and preservatives. The products are left to ripen and stored at 5–10°C. Often these products are microbiologically stable; however, when spoilage occurs, it is typically due to the growth of acetic acid-tolerant lactic acid bacteria (Lyhs et al., 2004; Lyhs, Korkeala, et al., 2001) or yeasts (Somners, 1975). Spoilage can be characterized by gas formation produced by heterofermentative lactobacilli such as Lb. alimentarius (Lyhs, Korkeala, et al., 2001). Spoilage may also be manifest by slime or ropiness which is caused by the growth of Leuconostoc species (Lyhs et al., 2004) or halophilic Gram-negative rod-shaped bacteria (Magnusson & Moeller, 1985). pH is an important parameter in preventing the growth of spoilage lactobacilli and yeasts (Fig. 6).
Growth of lactic acid bacteria and yeasts in brine of marinated herring is dependent on pH (Jessen, 1987)
Ripened anchovies are prepared by salting partially gutted (or nongutted) fresh anchovies. By tradition, the product is packaged in cans but these are not heat sterilized and must be held at refrigeration temperature. Microbial counts decrease during the ripening process to less than 104 cfu/g (Pons-Sanchez-Cascado, Veciana-Nogues, & Vidal-Carou, 2003). Biogenic amines increase during the ripening process but do not reach hazardous levels under controlled salt and storage conditions (Pons-Sanchez-Cascado et al., 2003). Total volatile bases increase during ripening (Pons-Sanchez-Cascado, Veciana-Nogues, Bover-Cid, Marine-Font, & Vidal-Carou, 2005) but this is believed, as the herring ripen, to be caused by enzymes from the gut and is not a consequence of bacterial action. The microflora rapidly becomes dominated by halophilic bacteria but their counts remain relatively low (104–105 cfu/g) (Perrez Villarreal & Pozo, 1992).
Similar to the herring and anchovy products, some types of fish roe are also barrel salted (at 15–25% NaCl) for months before further processing to caviar products. Caviar is produced from a number of fish species of which the most famous is sturgeon, but also a number of other species such as cod and lumpfish are used (Bledsoe, Bledsoe, & Rasco, 2003). Some of these products retain high levels of salt during subsequent marketing but others are desalted before marketing. Yet others are processed directly to lower levels of salt, i. e., 5–8% NaCl (water phase salt) (Bledsoe et al., 2003). Very little is known about spoilage of these products and microbiological studies have mainly addressed food safety issues related to potential for growth of C. botulinum and L. monocytogenes.
Heavily Salted Fish
Some fish, including gadoid species, are sometimes preserved exclusively by heavy salting. This process eliminates all of the spoilage bacteria described in the products above and the product is shelf stable at ambient temperature for a long time. However, the use of poor-quality salt can lead to a very characteristic type of spoilage called pinking. This is due to the growth of red-pigmented halophilic bacteria (Lamprecht, 1988; Prasad & Panduranga Rao, 1994; Prasad & Seenayya, 2000) that are strongly proteolytic causing a softening of the muscle and rotten off-odors. Pink is a traditional term for visible growth of extremely halophilic Gram-negative bacteria, such as Halobacterium salinarium, that belong to the family Halobacteriaceae. Most are nonmotile and obligate aerobes. Also, especially in tropical countries, this type of product may spoil due to fungal growth visible on the salted fillets or fish (Santoso, Gandjar, Sari, & Sembiring, 1999). Several different filamentous fungi have been isolated from spoiled, salted fish (Pitt & Hocking, 1999). Fungal spoilage of salted fish from temperate or subtropical climates differs from that of tropical salted fish with respect to genera and species (Pitt & Hocking, 1999) (Table 9). The spoilage described as “dun” is the visible appearance of brown colonies (1–2 mm in diameter). This is a caused by the growth of the fungus Wallemia sebi, an obligate aerobe.
Heated Seafood Products
Seafood raw materials are heated or cooked and result in a number of products such as hot-smoked fish, pasteurized crab meat, sous vide-cooked fillets, and fully canned products. Typically, the temperatures used are sufficient to result in substantial reduction of any microorganism present and it is either postprocess contamination that introduces spoilage microorganisms or spores surviving heat treatment that give rise to vegetative cells with spoilage potential.
Hot-Smoked Fish
The hot-smoking process is very similar to the cold smoking described above in that the fish are typically salted to 3–6% NaCl (water phase salt). However, the smoking process typically takes place at higher temperatures (50–80°C) which results in “cooking” of the fish flesh. Several species, such as herring and mackerel, are hot smoked but recently salmon has also become popular as a hot-smoked product. Hot smoking is also a common preservation technology in many developing countries. The hot-smoking process of mackerel can involve a drying step (30°C) and heating step at 50 and 80°C. The entire process usually requires 3 h. Larger and heavier fish require longer smoking (cooking) time.
Lightly salted, hot-smoked fish can be stored aerobically and bacterial growth limits shelf life of the product (Karnop, 1980). Also, fungal growth is quite common and is a shelf-life-limiting factor (Efiuvwevwere & Ajiboye, 1996). The fungi isolated are typically identified as Aspergillus or Penicillium species (Lilabati, Vishwanath, & Shymkesho Singh, 1999). If the product is vacuum packaged immediately after smoking under hygienic conditions, there is virtually no change in microbial levels during subsequent storage. The product becomes dry and somewhat tasteless, but microbial spoilage is not apparent.
Sous Vide-Cooked Fish
The “sous vide” (under vacuum) technology involves heating of the product typically at less-than-boiling temperature (65–75°C) followed by storage of the product at refrigeration temperature. The technique has been developed to improve sensory quality of several types of cooked food. Due to risk from C. botulinum, e.g., survival of spores and subsequent growth and toxin production, it has been recommended that sous vide fish products be heated to at least 90°C for 10 min. To control L. monocytogenes, heating to an internal temperature of 70°C for 2 min must be done (ACMSF, 1992). Several types of bacteria grow during subsequent chill storage and length of lag phase and extent of growth depend on the severity of the preceding heat treatment; however, sensory rejection does not appear to be a consequence of bacterial metabolism (Gonzalez-Fandos, Villarino-Rodriguez, Garcia-Linares, Garcia-Arias, & Garcia-Fernandez, 2005) and shelf lives range from 3 to 5 weeks (Gonzalez-Fandos et al., 2005; Nyati, 2000). Sporadically, Ben Embarek (1994) found that sous vide-cooked cod developed very strong putrid off-odors after storage at 5°C. Spore-forming, Gram-positive bacteria were isolated from these samples; however, their identity (Bacillus or Clostridium) was never determined (Ben Embarek, 1994).
Crab products are important especially to the US market. Crabs are harvested around the world. Some species are dissected before cooking, whereas others are cooked as whole animals. Subsequently the meat is removed from the shell (Cockey & Chai, 1991). Although cooking leaves the flesh sterile, subsequent picking and handling recontaminates the product. Spoilage of canned crab has, as with spoilage of sous vide cod, been caused by sporeformers (Cockey & Chai, 1991).
Fully Canned Products
Some species of fish are often processed and distributed as fully canned products. This is typical of tuna, mackerel, and salmon. These products are shelf stable if correctly processed and microbiological spoilage is not an issue. The use of raw materials of poor quality may result in the presence of biogenic amines in the canned products. The amines are heat stable and will not be inactivated even during canning (Luten et al., 1992)
Miscellaneous
Frozen Fish
Almost 20% of the global fish production is preserved by freezing (Fig. 2) and storage at −18 to −20°C. Growth of bacteria is stopped at these temperatures and sensory rejection is caused by nonmicrobial changes in the protein and lipid fractions of the fish flesh. Spoilage bacteria may grow in the raw fish if stored above 0°C before freezing and this may be reflected in the quality of the frozen product.
Filamentous fungi may grow in these products if stored at elevated freezing temperatures (−10 to −5°C). Many bacteria may, to some extent, survive frozen storage and if the product is thawed, grow and cause a normal type of spoilage. As mentioned above, P. phosphoreum is very sensitive to freezing and a freezing step before thawing and storage in CO2 atmosphere may increase the shelf life of CO2-packaged fish at refrigeration temperature quite substantially (Boknes, Osterberg, Nielsen, & Dalgaard, 2000; Dalgaard et al., 2006; Emborg et al., 2002).
Surimi
Surimi is a product prepared from either deboned meat or fillets. It consists mainly of muscle protein fibers that have been washed several times. Surimi is also prepared by mechanical deboning but is reduced essentially to muscle protein fibers by repeated washing. Some studies have reported that the microflora on surimi is similar to the microflora of fresh fish and consists of Moraxella, pseudomonads, and Corynebacterium (Himelbloom, Brown, & Lee, 1991), with counts of approximately 106 cfu/g (Matches, Raghubber, Yoon, & Martin, 1987). Bacteria grow very well in surimi and surimi-based products; however, these are mostly stored frozen, hence bacterial growth is not a problem (Elliott, 1987).
Dried Fish
The water activity of fully dried or salted and dried fish is so low that no bacteria can grow. However, fungal growth is a major problem, specifically in developing countries and spoilage is caused by Aspergillus and Penicillium species (Chakrabarti & Varma, 2000), but a range of other fungi may also be isolated from these products (Santoso et al., 1999). Aspergillus niger, Aspergillus flavus, and Penicilliumspp. are among the dominant fungi in salted, dried fish (Chakrabarti & Varma, 2000) and A. niger also appear to dominate in dried fish (Atapattu & Samarajeewa, 1990). Not only does visible fungal growth spoil the product per se, but filamentous fungi may also produce mycotoxins, hence constituting a health risk. Aflatoxin has been detected in smoked freshwater fish from Africa (Jonsyn & Lahai, 1992).
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Gram, L. (2009). Microbiological Spoilage of Fish and Seafood Products. In: Sperber, W., Doyle, M. (eds) Compendium of the Microbiological Spoilage of Foods and Beverages. Food Microbiology and Food Safety. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-0826-1_4
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