Professional Documents
Culture Documents
A Review
1. Introduction, 199
2. Taxonomy of yeasts in dairy products, 199
3. Milk, 201
4. Cream, butter, other non-fermented products, 201
5. Yogurt, 202
6. Cheese, 203
6.1 General occurrence of yeasts, 203
6.2 Yeast spoilage of cheese, 204
6.3 Contribution of yeasts to cheese maturation, 204
7. Other fermented dairy products, 207
8. Further research, 207
9. References, 207
1. Introduction
Yeasts are commercially significant in foods because they cause spoilage or conduct desirable fermen-
tations (Rose & Harrison 1970; Reed & Peppler 1973). Infections arising from the few, known patho-
genic yeasts, such as Candida albicans or Cryptococcus neoforrnans (Hurley et al., 1987) are not
transmitted through foods. Consequently, the public health significance of yeasts in foods has been
considered by most health authorities to be minimal, if not negligible. However, this attitude may
need revision. In summaries of statistics on food-borne disease in Canada, Todd (1983) noted cases
where yeasts were suspected of causing food poisoning. The allergic reactions of consumers to foods
and their contaminants are of increasing concern to health authorities, and yeasts have been men-
tioned in this connection (Taylor 1980; Anon. 1984).
Although the fermentative and spoilage activities of yeasts are well known in many food and
beverage commodities, little consideration has been given to the specific occurrence and significance
of yeasts in dairy products. Indeed, recent reviews on the microbiology of milk and dairy products
(Robinson 1981; Cousin 1982; Law & Mabbitt 1983; Bishop & White 1986) deal mostly with bac-
teria and make scant reference to yeasts. Consequently, one is left with the general impression that
yeasts are of little economic significance to the modern dairy industry. This review focuses attention
on the occurrence and importance of yeasts in dairy products, highlighting their involvement in the
spoilage of some products and their beneficial role in the fermentation of others. Ingram (1958),
Walker & Ayres (1970), Peppler (1976) and Walker (1977) have reviewed the spoilage of foods by
yeasts, in general, and these contributions include significant reference to dairy products. Marth
(1978) discusses some specific aspects of yeasts in dairy products.
3. Milk
Although milk is the raw material of most dairy products, surprisingly few studies have been con-
ducted on the specific occurrence of yeasts in either raw or pasteurized milks. Often, information on
yeasts is reported as an appendage to more detailed bacteriological studies. Generally, the available
information shows that yeasts occur in both raw (Foster et al. 1957; Ingram 1958; Randolph et al.
1973; Engel 1986a) and pasteurized (Jones & Langlois 1977; Fleet & Mian 1987; Vadillo et al. 1987)
milks, but at low, insignificant populations. Populations less than lo3 cells/ml are mostly reported
but, occasionally, counts as high as lo4 cells/ml can occur. Such yeasts rarely grow in milk during
refrigerated storage and are quickly overgrown by psychrotrophic bacteria (Cousin 1982; Bishop &
White 1986). However, yeast growth might occur in milk where bacterial growth has been inhibited
by residual antibiotics. Also, yeasts might develop in milk as secondary flora, after bacterial growth
and spoilage. Sweetened condensed milks are particularly prone to gassy fermentation by yeasts
because bacterial growth is restricted by the high sugar concentration and low water activity of this
product (Walker & Ayres 1970).
The taxonomy of yeasts found in milk has attracted little attention. Early studies, reviewed by
Walker & Ayres (1970), suggest the frequent occurrence of pigmented yeasts of the genus Rho-
dotorula. Engel (1986a) reported a prevalence of Candida curvata in samples of raw milk. In a survey
of 26 samples of pasteurized milks, Fleet & Mian (1987) described, in descending order of frequency,
the isolation of C . famata, Kluy. marxianus, Cryptococcusflavus and C . diJ7uens. In addition, they
showed that these species, as well as Saccharomyces cerevisiae, could grow to 108-109 cells/ml when
they were inoculated and incubated in UHT-treated milk. While the growth of Candida, Kluy-
oeromyces and Cryptococcus species could be explained in terms of their ability to utilize either milk
lactose, protein or fat, this explanation would not apply to S . cerevisae, which lacks these properties.
Further studies are required to determine the substrates that S . cerevisiae utilizes for its growth in
milk (Fleet & Mian 1987).
Although there are many possible environmental sources of yeast contamination of raw milk, this
is not so for pasteurized milks. The frequent occurrence of yeasts in pasteurized milks suggests that
they have some degree of tolerance to the pasteurization process (Fleet & Mian 1987; Vadillo et al.
1987), but this possibility requires investigation.
5. Yogurt
Yogurt is a fermented milk product that, traditionally, was prepared by allowing milk to sour at
4 W 5 " C . Modern yogurt production is a well-controlled process that utilizes ingredients of milk,
milk powder, sugar, fruit, flavours, colouring, emulsifiers and stabilizers, and pure cultures of lactic
acid bacteria to conduct the fermentation. Although fruit and flavoured yogurts are now very
popular, plain yogurts, that contain no non-milk ingredients, are still prepared. Details of the pro-
duction (Humphreys & Plunkett 1969; Robinson & Tamine 1986), composition (Robinson & Tamine
1975; Kroger 1976) and microbiology (Davis 1975; Bottazzi 1983) of yogurts are well reviewed.
Yeasts are not involved in the fermentation for producing yogurt, but they are a major cause of
spoilage of the final product. When they are produced under conditions of good manufacturing
practice, yogurt should contain less than 10 yeast cells/g (but preferably less than 1 cell/g) and, if
refrigerated at 5°C or less, they should not undergo spoilage by yeasts (Davis 1970, 1975). In these
cases, a shelf-life of 4 weeks is expected and is limited by factors other than yeasts. Yogurt which is
contaminated with an initial load of 100 or more yeast cells/g will probably spoil as the yeast cells
multiply. Spoilage becomes evident when the yeast population reaches 105-106 cells/g, and is first
seen as a swelling of the yogurt package due to gas production by yeast fermentation. Eventually, the
package ruptures and the yogurt acquires a yeasty, fermentative flavour and odour, and gassy
appearance (Suriyarachchi & Fleet 1981; Green & Ibe 1987). Occasionally, yeast colonies are seen on
the under surface of the package lid.
There are two main mechanisms by which yogurts become contaminated with yeasts. First, they
may originate from contaminated ingredients such as fruits, nuts and honey which, in most oper-
ations, are added to the fermented yogurt base just before packaging. Second, yeasts may develop on
the surfaces of production equipment, such as mixing vessels and filling machines, that have been
poorly cleaned and sanitized (Davis 1975; Suriyarachchi & Fleet 1981). Usually, yogurt base is free of
yeasts because the ingredients may already have been mixed and heated to approximately 90°C for
30min. Growth of yeasts during fermentation of the mix is most unlikely because high concentrations
of starter cultures of lactic acid bacteria are used, and because the fermentation temperature of
4 W Y C is restrictive to the growth of most yeast species. Contamination of the starter culture with
Kluy. marxianus could pose a potential risk, however, as this yeast can grow at 4 W Y C and ferment
lactose (Kreger-van-Rij 1984).
It is not uncommon to find yeast populations of lo3 cells/g or more in retail samples of either plain
or fruit yogurts. In many cases, counts of 106-107 cells/g have been recorded (van Uden & Carmo
Sousa 1957; Green & Ibe 1987; Fleet & Mian 1987). Surveys of retail yogurts in the U K (Davis 1974,
1975) and Canada (Arnott et al. 1974) found that 2&30% of samples had yeast counts exceeding
lo3 cells/g. Similar surveys in Portugal (van Uden & Carmo Sousa 1957), Australia (Suriyarachchi &
Fleet 1981 ; Fleet & Mian 1987) and Nigeria (Green & Ibe 1987) revealed a much higher incidence of
contamination, with some 60% of samples having counts exceeding lo4 cells/g. Lesser degrees of
contamination were reported for retail yogurts in the USA (Kroger 1976; Hankin & Shields 1980)
and the Netherlands (Hup & Stadhouders 1972). Yogurts purchased in Spain (Garcia & Fernandez
1984) and Saudi Arabia (Salji et al. 1987) also exhibited contamination with yeasts, but quantitative
statistics were not reported.
Identification of the yeast species found in yogurts has been undertaken in a few studies. Lactose
fermenting strains of Torulopsis spp. (Soulides 1956), C . pseudotropicalis (van Uden & Carmo Sousa
1957) and Kluy. bulgaricus (Dubois et al. 1980) have been implicated in the spoilage of plain yogurts.
Torulopsis candida, T. versatilis, C . pelliculosa, C. intermedia and Hansenula anomala were the species
most frequently isolated from retail yogurts in the United Kingdom (Tillbury et al. 1974). Candida
lusitaniae, C . krusei and Kluy. fragilis were the main species isolated from 100 samples of yogurts
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Yeasts in dairy products 203
produced in Lagos, Nigeria (Green & Ibe 1987). In a survey of 169 samples of yogurts retailed in
Sydney, the species most frequently isolated in descending order were: C. famata, Kluy. marxianus, S .
cerevisiae, C. stellata and C. difjluens (Suriyarachchi & Fleet 1981; Fleet & Mian 1987). Each of the
species was able to establish good growth (populations exceeding lo7cells/g) when they were inocu-
lated into freshly prepared plain and fruit yogurts and incubated at either 20"C, 15°C or 5' C. At 5"C,
best growth was exhibited by C. famata and C. dfluens which reached 106-107cells/g by 9 days
(Fleet & Mian 1987). These authors concluded that the growth and predominance of particular
species in yogurts is related to ability of the species to: (1) grow at the low temperatures ( < 10°C) of
yogurt storage; (2) produce lipolytic and proteolytic enzymes to hydrolyse milk fat and protein; (3)
ferment lactose or sucrose which are the main carbohydrates of either plain or flavoured yogurts
respectively; and (4) assimilate lactic and citric acids which are the main organic acids in yogurt. The
most prevalent yeasts in yogurts, C. famata and Kluy. marxianus, were positive for many of these
properties (Fleet & Mian 1987).
Control over the occurrence and growth of yeasts in yogurts is straightforward, and embraces the
general principles of good manufacturing practice. The critical points to monitor are: (1) proper
mixing and heating of ingredients before fermentation; (2) absence of yeasts in the starter culture of
lactic acid bacteria; (3) absence of yeasts (not detectable in 1.0 g) in fruit and other ingredients added
to the fermented yogurt base; (4) regular, effective cleaning and sanitation of processing equipment;
and (5) rapid cooling of the final product to 5 ° C and maintenance of this temperature throughout
retailing (Davis 1975; Suriyarachchi & Fleet 1981). In some countries, the use of sorbate or benzoate
preservatives may be permitted, but it is noteworthy that two of the main yeasts, C.famata and Kluy.
marxianus, found in yogurts are tolerant of these substances at concentrations of 500 mg/l (Fleet &
Mian 1987).
6. Cheese
The occurrence of yeasts in cheese is not unexpected because of the low pH, low moisture content,
elevated salt concentration and refrigerated storage of these products. It is not widely recognized,
however, that yeasts can be a major component of cheese microflora. The significance of this presence
needs stronger emphasis, and depends on the particular style of cheese. In some cheeses, yeasts
contribute to spoilage, but in others they make a positive contribution to flavour development
during the stage of maturation. The chapters in the book by Fox (1987) provide good overviews of
the chemistry, physics and microbiology of the different types of cheeses.
The literature on the isolation of yeasts and moulds from foods in general, contains scattered
references to the occurrence of yeasts in many samples of soft, semi-soft and hard cheeses. In some
samples, yeast counts as high as 107-108 cells/g have been reported (Koburger 1971; Hup & Stad-
houders 1972; Anagnostakis & Hankin 1975; Koburger & Farhat 1975; Henson et al. 1982; Brodsky
et al. 1982; Williams 1986; Jarvis & Shapton 1986; Banks & Board 1987). More specific surveys have
confirmed this frequent occurrence. In a survey of imported European and North American cheeses,
Nakase & Komagata (1977) found that 5 of 12 samples had yeast counts of 106-108 cells/g. Debary-
omyces hansenii and Candida lipolytica were the species most frequently isolated (Nakase et al. 1977).
Retail samples of Burgos and Villalon cheeses produced in Spain had yeast counts of 103-105cells/g
(Chavarri et al. 1985). Eleven of 50 samples of the Greek cheese, Kopanisti had yeast populations of
105-106 cells/g. The predominant species, Pichia memhranaefaciens and P . fermentans were recovered
from 80% and 24%, respectively, of the samples (Tzanetakis et al. 1987). Fleet & Mian (1987) report-
ed that 48% of 23 samples of Australian cheddar cheese had yeast counts in the range 104-106 cells/g.
Thirty seven Yn of 19 cottage cheeses contained yeasts at 105-107cells/g. The most frequently isolated
species from both cheese types were C. famata (38% of samples), Kluy. marxianus (19%) and C .
difjluens (14%). These authors demonstrated the ability of yeasts to grow in cheddar and cottage
cheeses during storage at 5°C for 10 days. In a comprehensive survey of 256 samples of blue-veined
cheeses, representing mostly Danablue, Roquefort and Gorgonzola varieties, de Boer & Kuik (1987)
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204 G.H . Fleet
recorded a very high incidence of yeasts. Eighty seven o/o of Gorgonzola samples and 77% of Roque-
fort samples contained yeast populations exceeding lo6 cells/g, with some samples having 107-108
cells/g. Debaryomyces hansenii was the most frequently occurring species, but isolates of Kluy. marx-
ianus, S. cereuisiae and Yarrowia lipolytica were also obtained. a similar, large survey of Brie and
Camembert cheeses purchased in Holland revealed that 60% of samples had yeast populations
greater than lo6 cells/g. Yarrowia lipolytica, D. hansenii, Kluy. marxianus and several Candida species
were the predominating yeasts (Nooitgedagt & Hartog 1988).
6.2 Y E A S T S P O I L A G E OF C H E E S E
Ingram (1958) and Walker & Ayres (1970) have reviewed early studies that describe the spoilage of
Cheddar and Swiss cheeses by yeasts. The main defects attributable to yeast activity were fruity, bitter
or yeasty off-flavours and gassy, open texture. Such problems are now less frequently reported and,
presumably, this is due to better understanding and control by the cheesemaker. Nevertheless, they
still occur. Ikemiya & Yasumi (1973) reported good growth of D . hansenii on the surface of processed
cheese. A fermented, yeasty flavour defect in Australian Cheddar cheese was recently reported by
Horwood et al. (1987) and attributed to the activity of an unidentified species of Candida. Kluy-
ueromyces marxianus, originating from the whey, has been implicated in the gassy spoilage of Parme-
san cheese (Romano et al. 1989). Assessment of cheese spoilage by yeasts is complicated by subjective
judgements on whether yeast activity during maturation is detrimental or beneficial to product
quality. Over-ripening during maturation could be interpreted as spoilage. Thus, continued lactose
fermentation by yeasts a t this stage could lead to increased acidity, gassiness and fruity flavours, and
continued hydrolysis of protein and fat could contribute to bitter and rancid flavours as well as a
softening of product texture.
There is little doubt that yeasts can spoil cottage cheese or similar types of unripened soft cheeses
such as quarg (Roth et al. 1971; Hankin et al. 1975; Guiraud & Galzy 1976; Brocklehurst & Lund
1985; Engel 1986b; Engel et al. 1987). Yeast populations of 106-107 cells/g frequently develop during
refrigerated storage of the final product, leading to flavour and odour defects, gassiness and the
appearance of surface colonies. Torulopsis sphaerica, C. lipolytica, Sporobolomyces roseus, Cryp. lau-
rentii, Kluy. marxianus, C. ualida and P . membranaefaciens have, on different occasions, been impli-
cated in this spoilage. The mechanism of yeast contamination and methods for controlling this
problem are similar to those described for yogurt.
It is very likely that the soft, brined cheeses, such as Feta and Domiati, are prone to yeast spoilage
but the microbiology of these products has received little attention (Haddadin 1986; Abd El-Salam
1987). Ghoniem (1968) briefly reported the occurrence of yeasts in Domiati cheese and suggested their
role in the production of gassy and flavour defects.
6.3 C O N T R I B U T I O NO F Y E A S T S T O C H E E S E M A T U R A T I O N
The growth of yeasts during the maturation (ripening/curing) stages of some cheese varieties is not
widely appreciated, although it has been known for some time and is acknowledged in recent reviews
on the microbiology of cheesemaking (Marth 1978; Law 1982; Vedamuthu & Washam 1983). It is
considered that these yeasts contribute either directly or indirectly to the development of cheese
flavour and texture but, in most cases, the chemical and biochemical mechanisms involved are not
clearly understood. Generally, these yeasts are vaguely described as part of the secondary, associated
or adventitious flora of cheesemaking (Law 1982; Vedamuthu & Washam 1983). In almost all cases,
they originate as contaminants of the cheesemaking process and are not added as a starter culture. A
most likely source of the yeasts is the milk, as evident from the data given in Section 3, but other
sources of contamination include process equipment, starter cultures of lactic acid bacteria, rennet
(Martinez et al. 1986), salt and any added fungal cultures.
8. Further research
Knowledge about the general occurrence and growth of yeasts in dairy products remains incomplete.
More comprehensive ecological surveys are needed to determine the diversity of yeast presence in
dairy products, and to establish the occurrence of any specific yeast-product associations. Such
studies must have a strong taxonomic focus to accurately describe the species present, and a strong
quantitative emphasis to provide data about the potential for yeast growth during production and
retailing of the product.
The biochemical mechanisms by which yeasts affect the sensory quality of dairy products are
poorly understood. Further research is required to determine the biochemical and physiological
properties of the main yeast species found in dairy products. Such information will provide a better
understanding of the factors that affect the growth of these species in dairy products, and of the
mechanisms by which their metabolic activities affect product quality. Thus, little information is
known about the flavour and aroma volatiles produced by Kluy. marxianus when it ferments lactose.
Similarly, little is known about the nature of the proteolytic and lipolytic enzymes produced by Kluy.
marxianus or D. hansenii, and how these enzymes act on milk proteins and fat.
Finally, the deliberate use of selected yeast species in the maturation of cheese or in the production
of other fermented dairy products requires serious exploration, and could give rise to a new starter
culture technology for the dairy industry.
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