Critical Reviews in Biotechnology
ISSN: 0738-8551 (Print) 1549-7801 (Online) Journal homepage: http://www.tandfonline.com/loi/ibty20
Spoilage Yeasts Graham Fleet To cite this article: Graham Fleet (1992) Spoilage Yeasts, Critical Reviews in Biotechnology, 12:1-2, 1-44, DOI: 10.3109/07388559209069186 To link to this article: https://doi.org/10.3109/07388559209069186
Published online: 27 Sep 2008.
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Citing articles: 172 View citing articles
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Critical Reviews in Biotechnology, 12( 112):1-44 ( 1992)
Spoilage Yeasts Graham Fleet Department of Food Science and Technology, The University of New South Wales, Kensington, New South Wales, Australia ABSTRACT: Yeasts are best known for their beneficial contributions to society, and the literature abounds with discussions of their role in the fermentation of alcoholic beverages, bread, and other products. Yeasts also cause spoilage, but, with a few exceptions, this unwanted activity often goes unrecognized and underestimated as a major problem in the food and beverage industries. In some cases, there is only a fine line between what is perceived as either a spoilage or beneficial activity. This review examines the occurrence and growth of yeasts in foods and beverages with respect to their spoilage activities, the biochemistry of this spoilage, and technologies for the enumeration and identification of spoilage yeasts.
KEY WORDS: yeasts, spoilage, foods, properties, spoilage yeasts
I. INTRODUCTION The presence of microorganisms in foods, beverages, and other commodities is significant to the human community for three main reasons: (1) the microorganisms may be pathogenic and pose a risk to public health; (2) they may depreciate the sensory appeal of the product to the point that it is considered spoiled and unacceptable; and (3) some species can effect desired changes in products, as in the production of fermented foods and beverages. Yeasts, as one group of microorganisms, are best known for their positive contributions to society, particularly through their activities in the fermentation of bread, alcoholic beverages, and other products. Yeasts also cause spoilage, but, with the exception of their effects on a few specific commodities, this negative attribute often goes unrecognized and underestimated. The public health significance of yeast contaminants in foods and beverages has been considered negligible. Infections from the few known pathogenic yeasts, such as Candida albicans and Cryptococcus neoformans, are not transmitted through foods. Moreover, humans have been inadvertently consuming high populations of viable yeast cells in fermented foods and beverages for thousands of years without obvious detriment to health (apart from intoxication
from ethanol); however, the public health safety of yeasts in foods may need some rethinking. There are occasional reports of gastroenteritis from foods, wherein yeasts were suspected to be the causative agent. In addition, there is increasing evidence that some individuals develop allergic and other negative reactions to yeast^,^ and this has led to the publication of significant lay literature and the promotion of so-called “yeast free” diet^.^ As a consequence of this increased medical awareness, the inadvertent presence of yeasts in foods, whether they be spoilage species or otherwise, is likely to attract more attention in the future. Many studies have been published on the spoilage of foods and beverages by yeasts, and these have been reviewed comprehensively on several occasions.5-8 The thrust of this literature has been ecological, essentially describing in qualitative terms the main products spoiled and the species of yeasts responsible. Most reviewers have concluded that yeast spoilage is limited to a narrow range of products, especially those of low pH or high sugar concentration, where competition from bacterial growth is restricted. Fleet has reexamined the literature on spoilage yeasts for foods generally9 and for dairy products specifically,1° and concluded that yeasts occur and grow in a greater range of products than previ-
0738-8551192/$.50 0 1992 by CRC Press, Inc.
1
ously thought. It was also concluded that further advances in understanding the spoilage activities of yeasts would require a more quantitative approach to studying their occurrence and growth in specific products and more detailed investigations of their biochemical transformations. For these reasons, and because the ecological studies have been thoroughly covered,’-I0 the present review gives stronger emphasis to the biochemical and physiological properties of spoilage yeasts. Information on the ecology of spoilage yeasts is updated and presented in overview form to provide the appropriate background and orientation. Because of the importance of being able to accurately determine the populations and identities of spoilage yeasts, recent developments in technologies for conducting these measurements are covered. The discussion is limited to foods and beverages and, in some cases feeds, and does not cover yeast spoilage of pharmaceuticals and health-care products. “J*
-
II. SPOILAGE RECOGNITION AND ECONOMIC IMPLICATIONS Changes in the sensory properties of foods do not become apparent to the consumer until yeasts have grown to populations of lo5 to lo6 cells per gram. These changes are most evident at populations of lo7to los cells per gram. However, unless yeast growth is accompanied by very obvious physical effects such as swelling and explosion of packages or gross alteration to product appearance, spoilage may go unnoticed. Apart from carbon dioxide, the major products of yeast growth in foods are likely to be alcohols, organic acids, and esters.I3A large proportion of the community will have positive associations with the aromas and flavors of these substances through their experiences in consuming fermented foods and alcoholic beverages. Consequently, many consumers may not interpret the unwanted occurrence of such substances in other commodities as spoilage. In the author’s experience, foods obviously affected by yeasts frequently occur at retail and domestic locations. Swollen containers of yogurts, cottage cheese, salads, and coleslaw are often seen in retail outlets and domestic refrig2
erators. Bottles of tomato and other sauces, jams, and syrups that are opened and stored in kitchen cupboards occasionally ferment. Slices of bacon and other varieties of preserved meats can develop surface colonies of yeasts if stored too long in the refrigerator. Similarly, packaged fruit juices, opened and kept in the domestic refrigerator, develop significant yeast populations if not consumed within 5 to 7 d. Various cheeses may quickly develop yeast populations of lo6 to los cells per gram after opening. The average consumer is largely unaware of these circumstances and happily consumes these foods, seemingly without complaint or illness. Most microbiological consultants have experiences with yeast spoilage of products at the industrial scale. This problem is not uncommon, and the financial losses can be quite high. Products often implicated involve fruit pulps, fruit juices, syrups, soft drinks, various sauces, alcoholic beverages, and confectionery products. Fleet’ has mentioned one example of yogurt spoilage by yeasts, in which the cost of the outbreak was in excess of $100,000. For reasons of commercial confidentiality, the incidence and economic cost of industrial outbreaks of yeast spoilage remain unreported. In documenting the costs of such outbreaks, consideration needs to be given to (1) the value of the spoiled product, (2) the cost of recall and disposal, (3) subsequent decreased retailer and consumer purchase of the product because of tarnished reputation, and (4) the legal and insurance fees associated with determining responsibility and awarding compensation. Usually, several parties represented by manufacturers, suppliers of raw materials and packaging, and retailers are involved in these cases.
111. SPOILAGE OF SPECIFIC COMMODITIES A. Meats Literature on the microbial spoilage of meats is dominated by reference to the activities of bacteria.14 Apart from the discussions by Jay’5 and Dalton et al. l6 and the more recent review of Fung
and Liang,'6a very few studies have comprehensively addressed the occurrence, growth, and significance of yeasts in meats and meat products. This lack of interest apparently originates from the widely accepted view that bacteria grow much better and faster on meat substrates than yeast and, consequently, they will have a greater presence and significance. While this view may be correct for fresh meats stored at refrigeration or ambient temperatures, it may not be appropriate for processed meats or fresh meats stored under other conditions. Bacterial growth on such meats may be restricted, thereby allowing increased growth and prevalence of yeasts. The following discussion demonstrates a greater occurrence and significance of yeasts in meats and meat products than previously considered.
1. Fresh Red and Poultry Meats
Retail samples of minced or ground meat contain variable populations of yeasts that range Yeasts readfrom lo2to lo7cells per gram.'6,35-40 ily proliferate in comminuted meats during refrigerated storage, but their final populations (lo6 to lo7 cells per gram) remain insignificant compared to those of bacteria. Packaging under an atmosphere of carbon dioxide, but not nitrogen, may restrict their Although yeasts play only a minor role in the spoilage of ground meats, their presence at lo6 to lo7cells per gram may be significant to consumers who suffer yeast allergies. The species most frequently isolated from refrigerated, comminuted meats include Candida zeylanoides, C. lipolytica, C . famata (sporogenous equivalent, Debaryomyces hansenii), C. sake, and Cryptococcus Zaurentii var. Zaurentii (Table 1). Long-term frozen storage of either lamb,41 beef,6 p o ~ l t r y ,or~ offal ~*~~ can give a yeast-dominated spoilage flora that produces spoilage off-flavors. Under these conditions, low temperature and reduced water activity of the meat surface combine to restrict bacterial growth, allowing yeasts to multiply from initial populations of 10 to lo3 cells per square centimeter to lo6 to lo7 cells per square centimeter. For both lamb4] and poultry,3o the dominant species at spoilage were Cryp. laurentii var. laurentii and C . zeylanoides (Table 1). Both species are lipolytic and this property could account for their ability to spoil the meats. Spoilage of frozen meats by yeasts is probably more common than presently thought. Further research is required to determine the frequency of this problem and to confirm the role of yeasts in producing off-flavors and taints in these products.
Freshly slaughtered cuts of beef, '7-23 lamb,24-26 ~ ~ alIigato?l ,~~ meats, as Pork, '6.27728 p o ~ l t r y ,and well as offal r n e a t ~ ,harbor ~ ~ - ~low ~ populations (10' to lo3 cells per gram or square centimeter) of yeasts. There is limited growth of yeasts on these meats during refrigerated (4"to 5°C) storage, but the maximum populations formed rarely exceed lo5 to lo6 cells per gram or square centimeter. The effect of packaging environment on this growth requires more study, but it seems that it is not encouraged by vacuum packaging and may be restricted by packaging under an atmosphere of carbon dioxide. 18-22.26.27 Overall, yeast populations on fresh and refrigerated carcasses or cuts of carcasses represent only 5 to 10% of the total microbial flora and are insignificant in the spoilage process when compared with bacteria. However, conditions that suppress bacterial growth on fresh meats, such as addition of an2. Processed Red and Poultry Meats tibiotics or acidulents such as lactic, citric, and acetic acids, will encourage yeast growth during In contrast to fresh meats, retail samples of refrigerated tora age.^^.^^ Because of their low processed delicatessen-type meats are frequently populations and general insignificance, the specontaminated with quantitatively significant popcies of yeasts associated with fresh meats have ulations (105 to lo7 cells per gram) of yeasts.4245 not been the subject of detailed taxonomic study. Specific studies have been conducted with fresh The most frequently encountered species are those and fermented sausages,16,46-51 bacon,52 frankof Candida and RhodotoruZa and, to a lesser exf u r t e r ~corned , ~ ~ beef,42various cured h a r n ~ , ~ ~ - ~ * tent, Saccharomyces and Debaryomyces (Table and haggis.59There is little doubt that yeasts proliferate in these products during refrigerated stor1). 3
TABLE 1 Yeast Species Most Frequently Isolated from Meat Products Product
Yeast species
Fresh red and poultry meats
Candida spp., Rhodotorula spp., Debaryornyces spp., Trichosporon (not adequately studied) Cryptococcus laurentii, C. infirmo-miniatus, Candida zeylanoides, Trichosporon pullulans Cryptmomus laurentii ,a Candida zeylanoides a Candida lipolytica,a C. zeylanoides, C. larnbica, C. sake, Cryptococcus laurentii, Debaryornyces hansenii, Pichia rnembranaefaciens Debaryomyces hansenii, a Candida spp.” Rhodotorula
Frozen lamb Frozen turkey Ground/minced meat
Processed meats (frankfurters, sausages, hams, bacon) Fish Shrimp Shellfish Crabmeat
a
SPP.
Debatyomyces spp., Candida spp., Rhodotorula spp., C. /ipo/yticaa Candida spp., Rhodotorula spp., Trichosporon spp. Rhodotorula rubra, a Candida spp. Rhodotorula spp., Candida spp., Cryptococcus spp., Trichosporon spp.
16, 75, 76 41
30 i6,37,3a
16, 17, 45, 51, 52, 55, 77 66-68.
74
63-65 9, 72, 73 70, 71
Indicates species associated with reports of spoilage; see also more extensive Tables in Jay‘” and Fung and Liang.’”
age, especially if they have been vacuum packaged.42,49*50 Yeasts in vacuum-packaged corned beef, for example, increased from lo3to 1O7 cells per gram during storage for 15 d at 5°C.42Similar increases were reported during the refrigerated storage of British fresh sausage.I6 While such growth appears significant, the final population of yeasts may represent only 10% or less of the total flora. Packaging under carbon dioxide or nitrogen can prevent this yeast growth .47-49*s3 The species of yeasts associated with processed meats are listed in Table 1. By far, Deburyomyces hansenii and its asporogenous form, C. fumatu, are the most frequently isolated species. In a survey of 200 Italian salami sausages, for example, Grazia et al.51reported 82% of the 821 yeast isolates as D. hansenii. Unfortunately, most of the studies listed in Table 1 do not report quantitative population data for the species isolated. The significance of yeasts in processed meats will depend upon the product, but this subject requires more detailed investigation. In some products, yeasts cause spoilage. For example, they may cause slimes and discoloration on the surfaces of frankfurters and sausages, and gas4
Ref.
swelling of packaged, sliced meat^.^^','^ Other less obvious but negative effects include the production of off-flavor and taints, the production of metabolites such as acetaldehyde that can neutralize the preservative effects of sulfur dioxide, and the utilization of sodium nitrite that is added as a curing agent and preservative. 16,2s However, yeast growth may be desirable during the production of fermented sausages.mq61According to Grazia et al.,” the occurrence of D. hunsenii in Italian salamis has a positive effect on product quality.
3. Seafoods Yeasts occur in aquatic environments at populations of lo2 to lo3 cells per milliliter. This population, as well as the species present, varies with proximity to land masses and the degree of pollution.62 It is not unexpected, therefore, that the surfaces and intestinal contents of freshly caught ~ h r i r n p s , ~various ~ - ~ ’ fish specie^,^^-^^ c r a b ~ , ~and ~ * ~~h’e l l f i s h ’ ~harbor * ~ ~ yeasts. Such studies are too few and incomplete to draw general conclusions about the association of yeasts
with seafoods, but it seems that the populations of yeasts in freshly caught products are usually
ISSN: 0738-8551 (Print) 1549-7801 (Online) Journal homepage: http://www.tandfonline.com/loi/ibty20
Spoilage Yeasts Graham Fleet To cite this article: Graham Fleet (1992) Spoilage Yeasts, Critical Reviews in Biotechnology, 12:1-2, 1-44, DOI: 10.3109/07388559209069186 To link to this article: https://doi.org/10.3109/07388559209069186
Published online: 27 Sep 2008.
Submit your article to this journal
Article views: 362
View related articles
Citing articles: 172 View citing articles
Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=ibty20
Critical Reviews in Biotechnology, 12( 112):1-44 ( 1992)
Spoilage Yeasts Graham Fleet Department of Food Science and Technology, The University of New South Wales, Kensington, New South Wales, Australia ABSTRACT: Yeasts are best known for their beneficial contributions to society, and the literature abounds with discussions of their role in the fermentation of alcoholic beverages, bread, and other products. Yeasts also cause spoilage, but, with a few exceptions, this unwanted activity often goes unrecognized and underestimated as a major problem in the food and beverage industries. In some cases, there is only a fine line between what is perceived as either a spoilage or beneficial activity. This review examines the occurrence and growth of yeasts in foods and beverages with respect to their spoilage activities, the biochemistry of this spoilage, and technologies for the enumeration and identification of spoilage yeasts.
KEY WORDS: yeasts, spoilage, foods, properties, spoilage yeasts
I. INTRODUCTION The presence of microorganisms in foods, beverages, and other commodities is significant to the human community for three main reasons: (1) the microorganisms may be pathogenic and pose a risk to public health; (2) they may depreciate the sensory appeal of the product to the point that it is considered spoiled and unacceptable; and (3) some species can effect desired changes in products, as in the production of fermented foods and beverages. Yeasts, as one group of microorganisms, are best known for their positive contributions to society, particularly through their activities in the fermentation of bread, alcoholic beverages, and other products. Yeasts also cause spoilage, but, with the exception of their effects on a few specific commodities, this negative attribute often goes unrecognized and underestimated. The public health significance of yeast contaminants in foods and beverages has been considered negligible. Infections from the few known pathogenic yeasts, such as Candida albicans and Cryptococcus neoformans, are not transmitted through foods. Moreover, humans have been inadvertently consuming high populations of viable yeast cells in fermented foods and beverages for thousands of years without obvious detriment to health (apart from intoxication
from ethanol); however, the public health safety of yeasts in foods may need some rethinking. There are occasional reports of gastroenteritis from foods, wherein yeasts were suspected to be the causative agent. In addition, there is increasing evidence that some individuals develop allergic and other negative reactions to yeast^,^ and this has led to the publication of significant lay literature and the promotion of so-called “yeast free” diet^.^ As a consequence of this increased medical awareness, the inadvertent presence of yeasts in foods, whether they be spoilage species or otherwise, is likely to attract more attention in the future. Many studies have been published on the spoilage of foods and beverages by yeasts, and these have been reviewed comprehensively on several occasions.5-8 The thrust of this literature has been ecological, essentially describing in qualitative terms the main products spoiled and the species of yeasts responsible. Most reviewers have concluded that yeast spoilage is limited to a narrow range of products, especially those of low pH or high sugar concentration, where competition from bacterial growth is restricted. Fleet has reexamined the literature on spoilage yeasts for foods generally9 and for dairy products specifically,1° and concluded that yeasts occur and grow in a greater range of products than previ-
0738-8551192/$.50 0 1992 by CRC Press, Inc.
1
ously thought. It was also concluded that further advances in understanding the spoilage activities of yeasts would require a more quantitative approach to studying their occurrence and growth in specific products and more detailed investigations of their biochemical transformations. For these reasons, and because the ecological studies have been thoroughly covered,’-I0 the present review gives stronger emphasis to the biochemical and physiological properties of spoilage yeasts. Information on the ecology of spoilage yeasts is updated and presented in overview form to provide the appropriate background and orientation. Because of the importance of being able to accurately determine the populations and identities of spoilage yeasts, recent developments in technologies for conducting these measurements are covered. The discussion is limited to foods and beverages and, in some cases feeds, and does not cover yeast spoilage of pharmaceuticals and health-care products. “J*
-
II. SPOILAGE RECOGNITION AND ECONOMIC IMPLICATIONS Changes in the sensory properties of foods do not become apparent to the consumer until yeasts have grown to populations of lo5 to lo6 cells per gram. These changes are most evident at populations of lo7to los cells per gram. However, unless yeast growth is accompanied by very obvious physical effects such as swelling and explosion of packages or gross alteration to product appearance, spoilage may go unnoticed. Apart from carbon dioxide, the major products of yeast growth in foods are likely to be alcohols, organic acids, and esters.I3A large proportion of the community will have positive associations with the aromas and flavors of these substances through their experiences in consuming fermented foods and alcoholic beverages. Consequently, many consumers may not interpret the unwanted occurrence of such substances in other commodities as spoilage. In the author’s experience, foods obviously affected by yeasts frequently occur at retail and domestic locations. Swollen containers of yogurts, cottage cheese, salads, and coleslaw are often seen in retail outlets and domestic refrig2
erators. Bottles of tomato and other sauces, jams, and syrups that are opened and stored in kitchen cupboards occasionally ferment. Slices of bacon and other varieties of preserved meats can develop surface colonies of yeasts if stored too long in the refrigerator. Similarly, packaged fruit juices, opened and kept in the domestic refrigerator, develop significant yeast populations if not consumed within 5 to 7 d. Various cheeses may quickly develop yeast populations of lo6 to los cells per gram after opening. The average consumer is largely unaware of these circumstances and happily consumes these foods, seemingly without complaint or illness. Most microbiological consultants have experiences with yeast spoilage of products at the industrial scale. This problem is not uncommon, and the financial losses can be quite high. Products often implicated involve fruit pulps, fruit juices, syrups, soft drinks, various sauces, alcoholic beverages, and confectionery products. Fleet’ has mentioned one example of yogurt spoilage by yeasts, in which the cost of the outbreak was in excess of $100,000. For reasons of commercial confidentiality, the incidence and economic cost of industrial outbreaks of yeast spoilage remain unreported. In documenting the costs of such outbreaks, consideration needs to be given to (1) the value of the spoiled product, (2) the cost of recall and disposal, (3) subsequent decreased retailer and consumer purchase of the product because of tarnished reputation, and (4) the legal and insurance fees associated with determining responsibility and awarding compensation. Usually, several parties represented by manufacturers, suppliers of raw materials and packaging, and retailers are involved in these cases.
111. SPOILAGE OF SPECIFIC COMMODITIES A. Meats Literature on the microbial spoilage of meats is dominated by reference to the activities of bacteria.14 Apart from the discussions by Jay’5 and Dalton et al. l6 and the more recent review of Fung
and Liang,'6a very few studies have comprehensively addressed the occurrence, growth, and significance of yeasts in meats and meat products. This lack of interest apparently originates from the widely accepted view that bacteria grow much better and faster on meat substrates than yeast and, consequently, they will have a greater presence and significance. While this view may be correct for fresh meats stored at refrigeration or ambient temperatures, it may not be appropriate for processed meats or fresh meats stored under other conditions. Bacterial growth on such meats may be restricted, thereby allowing increased growth and prevalence of yeasts. The following discussion demonstrates a greater occurrence and significance of yeasts in meats and meat products than previously considered.
1. Fresh Red and Poultry Meats
Retail samples of minced or ground meat contain variable populations of yeasts that range Yeasts readfrom lo2to lo7cells per gram.'6,35-40 ily proliferate in comminuted meats during refrigerated storage, but their final populations (lo6 to lo7 cells per gram) remain insignificant compared to those of bacteria. Packaging under an atmosphere of carbon dioxide, but not nitrogen, may restrict their Although yeasts play only a minor role in the spoilage of ground meats, their presence at lo6 to lo7cells per gram may be significant to consumers who suffer yeast allergies. The species most frequently isolated from refrigerated, comminuted meats include Candida zeylanoides, C. lipolytica, C . famata (sporogenous equivalent, Debaryomyces hansenii), C. sake, and Cryptococcus Zaurentii var. Zaurentii (Table 1). Long-term frozen storage of either lamb,41 beef,6 p o ~ l t r y ,or~ offal ~*~~ can give a yeast-dominated spoilage flora that produces spoilage off-flavors. Under these conditions, low temperature and reduced water activity of the meat surface combine to restrict bacterial growth, allowing yeasts to multiply from initial populations of 10 to lo3 cells per square centimeter to lo6 to lo7 cells per square centimeter. For both lamb4] and poultry,3o the dominant species at spoilage were Cryp. laurentii var. laurentii and C . zeylanoides (Table 1). Both species are lipolytic and this property could account for their ability to spoil the meats. Spoilage of frozen meats by yeasts is probably more common than presently thought. Further research is required to determine the frequency of this problem and to confirm the role of yeasts in producing off-flavors and taints in these products.
Freshly slaughtered cuts of beef, '7-23 lamb,24-26 ~ ~ alIigato?l ,~~ meats, as Pork, '6.27728 p o ~ l t r y ,and well as offal r n e a t ~ ,harbor ~ ~ - ~low ~ populations (10' to lo3 cells per gram or square centimeter) of yeasts. There is limited growth of yeasts on these meats during refrigerated (4"to 5°C) storage, but the maximum populations formed rarely exceed lo5 to lo6 cells per gram or square centimeter. The effect of packaging environment on this growth requires more study, but it seems that it is not encouraged by vacuum packaging and may be restricted by packaging under an atmosphere of carbon dioxide. 18-22.26.27 Overall, yeast populations on fresh and refrigerated carcasses or cuts of carcasses represent only 5 to 10% of the total microbial flora and are insignificant in the spoilage process when compared with bacteria. However, conditions that suppress bacterial growth on fresh meats, such as addition of an2. Processed Red and Poultry Meats tibiotics or acidulents such as lactic, citric, and acetic acids, will encourage yeast growth during In contrast to fresh meats, retail samples of refrigerated tora age.^^.^^ Because of their low processed delicatessen-type meats are frequently populations and general insignificance, the specontaminated with quantitatively significant popcies of yeasts associated with fresh meats have ulations (105 to lo7 cells per gram) of yeasts.4245 not been the subject of detailed taxonomic study. Specific studies have been conducted with fresh The most frequently encountered species are those and fermented sausages,16,46-51 bacon,52 frankof Candida and RhodotoruZa and, to a lesser exf u r t e r ~corned , ~ ~ beef,42various cured h a r n ~ , ~ ~ - ~ * tent, Saccharomyces and Debaryomyces (Table and haggis.59There is little doubt that yeasts proliferate in these products during refrigerated stor1). 3
TABLE 1 Yeast Species Most Frequently Isolated from Meat Products Product
Yeast species
Fresh red and poultry meats
Candida spp., Rhodotorula spp., Debaryornyces spp., Trichosporon (not adequately studied) Cryptococcus laurentii, C. infirmo-miniatus, Candida zeylanoides, Trichosporon pullulans Cryptmomus laurentii ,a Candida zeylanoides a Candida lipolytica,a C. zeylanoides, C. larnbica, C. sake, Cryptococcus laurentii, Debaryornyces hansenii, Pichia rnembranaefaciens Debaryomyces hansenii, a Candida spp.” Rhodotorula
Frozen lamb Frozen turkey Ground/minced meat
Processed meats (frankfurters, sausages, hams, bacon) Fish Shrimp Shellfish Crabmeat
a
SPP.
Debatyomyces spp., Candida spp., Rhodotorula spp., C. /ipo/yticaa Candida spp., Rhodotorula spp., Trichosporon spp. Rhodotorula rubra, a Candida spp. Rhodotorula spp., Candida spp., Cryptococcus spp., Trichosporon spp.
16, 75, 76 41
30 i6,37,3a
16, 17, 45, 51, 52, 55, 77 66-68.
74
63-65 9, 72, 73 70, 71
Indicates species associated with reports of spoilage; see also more extensive Tables in Jay‘” and Fung and Liang.’”
age, especially if they have been vacuum packaged.42,49*50 Yeasts in vacuum-packaged corned beef, for example, increased from lo3to 1O7 cells per gram during storage for 15 d at 5°C.42Similar increases were reported during the refrigerated storage of British fresh sausage.I6 While such growth appears significant, the final population of yeasts may represent only 10% or less of the total flora. Packaging under carbon dioxide or nitrogen can prevent this yeast growth .47-49*s3 The species of yeasts associated with processed meats are listed in Table 1. By far, Deburyomyces hansenii and its asporogenous form, C. fumatu, are the most frequently isolated species. In a survey of 200 Italian salami sausages, for example, Grazia et al.51reported 82% of the 821 yeast isolates as D. hansenii. Unfortunately, most of the studies listed in Table 1 do not report quantitative population data for the species isolated. The significance of yeasts in processed meats will depend upon the product, but this subject requires more detailed investigation. In some products, yeasts cause spoilage. For example, they may cause slimes and discoloration on the surfaces of frankfurters and sausages, and gas4
Ref.
swelling of packaged, sliced meat^.^^','^ Other less obvious but negative effects include the production of off-flavor and taints, the production of metabolites such as acetaldehyde that can neutralize the preservative effects of sulfur dioxide, and the utilization of sodium nitrite that is added as a curing agent and preservative. 16,2s However, yeast growth may be desirable during the production of fermented sausages.mq61According to Grazia et al.,” the occurrence of D. hunsenii in Italian salamis has a positive effect on product quality.
3. Seafoods Yeasts occur in aquatic environments at populations of lo2 to lo3 cells per milliliter. This population, as well as the species present, varies with proximity to land masses and the degree of pollution.62 It is not unexpected, therefore, that the surfaces and intestinal contents of freshly caught ~ h r i r n p s , ~various ~ - ~ ’ fish specie^,^^-^^ c r a b ~ , ~and ~ * ~~h’e l l f i s h ’ ~harbor * ~ ~ yeasts. Such studies are too few and incomplete to draw general conclusions about the association of yeasts
with seafoods, but it seems that the populations of yeasts in freshly caught products are usually
