Types of traditional greek foods and the

Types of traditional Greek foods and their safety a Laboratory of Microbiology and Biotechnology of Foods, Department of Food Science and Technology, Agricultural University of Athens, 7

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Types of traditional Greek foods and their safety

a Laboratory of Microbiology and Biotechnology of Foods, Department of Food Science and Technology, Agricultural University of Athens, 75 Iera Odos str., Athens GR-11855, Greece

b Center for Meat Safety & Quality and Food Safety Cluster, Department of Animal Sciences, Colorado State University, Fort Collins, CO 80523-1171, USA

a r t i c l e i n f o

Article history:

Received 27 February 2012

Received in revised form

13 May 2012

Accepted 22 May 2012

Keywords:

Cheese

Emulsion-type appetizers

Fermented meats

Food safety

Food pathogens

Table olives

Traditional Greek foods

a b s t r a c t

Greek traditional foods have been evolved over centuries in the country according to local culture and artisanal practices in small scale family-owned installations and constitute a major part of the so-called Mediterranean diet Consumer concern for food safety and high demand for traditional food products is becoming an important challenge for the food industry To this end, safety issues about the hygienic condition and the prevalence of foodborne pathogens for a diversity of popular traditional Greek foods including fermented meat products, cheese, table olives, and emulsion-type appetizers is being reported Until recently, the production of these food commodities presented heterogeneity from area to area and practice to practice resulting in a ﬁnal product with diverse microbiological, physicochemical and sensory characteristics The condition has drastically changed over the last years where the production has shifted from artisanal practice to industrial level under strict processing and hygienic conditions Nowadays, it can be considered that Greek traditional foods have a good safety record

Contents

1 Introduction 32

2 Definition and basics of traditional Greek foods 33

3 Traditional Greek foods 33

3.1 Traditional fermented meats 33

3.2 Greek cheeses 34

3.3 Fermented fruits and vegetables 35

3.4 Emulsion-type Greek appetizers or salads 36

4 How safe are the Greek foods? 36

4.1 Fermented meats 36

4.2 Cheese products 37

4.3 Table olives 37

4.4 Emulsion-type appetizers or salads 38

5 Conclusions 39

References 40

1 Introduction

There are many different cultures within Europe and each one

has its own distinct dietary habits Traditional foods are those that

have been consumed locally or regionally for an extensive period of

time and could be considered as an expression of culture, history,

geography, climate, agriculture, and lifestyle Needed ingredients or recipes of methods for the preparation of such foods have been passed from one generation to the other and becomeﬁnally a part

of the folklore of the country (Trichopoulou, Soukara, & Vasilopoulou, 2007) Traditional foods, apart of being vehicles of culture, could also possess health qualities, since tradition hardly supports foods which are not palatable and healthy A typical example of a dietary pattern with positive health aspects is the Mediterranean diet which is characterized by six components,

* Corresponding author Tel./fax: þ30 210 5294938.

E-mail addresses: gjn@aua.gr , nychas@hol.gr (G.-J.E Nychas).

Contents lists available atSciVerse ScienceDirect

Food Control

j o u r n a l h o m e p a g e : w w w e l s e v i e r c o m / l o c a t e / f o o d c o n t

Food Control 29 (2013) 32e41

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namely, high intake of vegetables, pulses, fruits, olive oil, nuts and

cereals; low intake of saturated lipids; low to moderate intake of

dairy products mainly in the form of cheese and yogurt; low intake

of meat and poultry; moderately high intake ofﬁsh; and moderate

intake of ethanol mostly in the form of wine (Trichopoulou,

Costacou, Bamia, & Trichopoulos, 2003)

For the production of traditional foods, local agricultural

commodities are generally used as raw materials, contributing to

a sustainable environment and employment of rural population

Currently, the combination of healthy and palatable aspects is very

attractive for the food industry and consumers, and consequently

traditional foods could potentially be mass produced and exported

This highlights the necessity for traditional food standardization

and protection of origin and quality through appropriate

legisla-tion This is necessary for the producers and consumers, in order to

protect the quality and identity of the products Moreover, the

country of origin registration of these foods could motivate their

small-scale production in family-owned installations and expand

their export potential (Tregear, Arﬁni, Belleti, & Marescotti, 2007)

However, the combination of artisan practices employed in

traditional food manufacturing and the potential for poor hygienic

conditions, prevailing especially in small-scale family-owned

pro-cessing installations, may result in the contamination and survival

of foodborne pathogens that may be present throughout the

distribution chain until the time of consumption The incidence of

foodborne disease in many countries across Europe is increasing,

according to the World Health Organization (WHO) Regional

Director for Europe (WHO, 2003) For instance, foodborne

intoxi-cations such as botulism remain frequent in Eastern Europe and in

most cases are related to traditional ways of preserving foods at

home The highest incidence of botulism was reported in the

Caucasus (Armenia, Azerbaijan and Georgia) and is attributed to the

consumption of home-canned vegetables WHO data also show

that although the incidence of salmonellosis is decreasing in

several countries in Western Europe, the pathogen is still the most

frequently reported cause of outbreaks in the WHO European

Region, responsible for around 75% of the outbreaks Most of these

are due to the consumption of foods of animal origin, particularly

insufﬁciently cooked eggs or foods containing raw eggs, such as

mayonnaise, ice cream or cream-ﬁlled pastries

The aim of the review paper is to provide information about the

hygienic condition and the prevalence of foodborne pathogens in

a diversity of popular traditional Greek foods including fermented

meat products, cheese, table olives, and emulsion-type appetizers

Safety issues with these products are also discussed

2 Deﬁnition and basics of traditional Greek foods

The history of Greek gastronomy is lost through written sources

and indications coming from the greater Aegean area Greek cuisine

has a long tradition and itsﬂavors change according to season and

geographic region Greek cookery, historically a forerunner of

Western cuisine, spread its culinary inﬂuence e via ancient Rome e

throughout Europe and beyond (Wilkins & Hill, 2006) Ancient

Greek cuisine was characterized by its frugality and was founded on

the“Mediterranean triad”: wheat, olive oil, and wine, with meat

being rarely eaten and ﬁsh being more common This trend in

Greek diet continued in Roman and Ottoman times and changed

only recently when technological progress has made meat more

available Wine and olive oil have always been a central part of it

and the spread of grapes and olive trees in the Mediterranean is

associated with Greek colonization The Byzantine cuisine was

similar to the classical cuisine including, however, new ingredients

that were not available before, like caviar, nutmeg and lemons, with

ﬁsh continuing to be an integral part of the diet Byzantine cuisine

beneﬁted from Constantinople’s position as a global hub of the spice trade (Balatsouras, 2004)

The most characteristic and ancient element of Greek cuisine is olive oil, which is frequently used in the dishes It is produced from the olive trees prominent throughout the region, and adds to the distinctive taste of Greek food The basic grain in Greece is wheat, though barley is also grown Important vegetables include tomato, aubergine (eggplant), potato, green beans, okra, green peppers, and onions Honey in Greece is mainly derived from the nectar of fruit trees such as the citrus trees of lemon, orange, bigarade (bitter orange), and from thyme and pine from conifer trees The aromatic, ivory colored resin, mastic, is characteristic of the region as it is grown on the Aegean island of Chios (Dalby, 2001), and is common

in the Greek diet

Greek cuisine uses some ﬂavorings more often than other Mediterranean cuisines do, namely oregano, mint, garlic, onion, and bay laurel leaves Other common herbs and spices include basil, thyme and fennel seed Many Greek recipes, especially in the northern parts of the country, use“sweet” spices in combination with meat, for example cinnamon and cloves in stews (Hanlidou, Karousou, Kleftoyanni, & Kokkini, 2004)

The climate and terrain has tended to favor the breeding of goats and sheep over cattle, and thus traditional beef dishes are uncommon, although this trend has changed in the last years, as beef has become the main meat item for many Greeks Fish dishes are mostly common in coastal regions and on the islands, but also throughout Greece, especially in major cities A great variety of traditional cheese types are also used in Greek cuisine, including Feta, Kasseri, Kefalotyri, Graviera, Anthotyros, Manouri, Metsovone, Mizithra, etc (Balatsouras, 2004)

3 Traditional Greek foods 3.1 Traditional fermented meats The origin of fermented foods is lost in antiquity Fermentation became popular with the dawn of civilization because it not only preserved food but also gave it a variety of tastes, forms, and other sensory attributes (Campbell-Platt, 1994; Caplice & Fitzgerald,

1999; Prajapati & Nair, 2003) Traditional sausages are the most commonly produced fermented meat products in Greece In the past, most Greek rural families prepared them shortly before Christmas, when they slaughtered their home-grown pig(s), from pork meat and fat, chopped and mixed together with salt and seasonings Theﬁrst document referring to meat curing is consid-ered to be that of Homer In Odyssey (about 1000e900 BC) he describes a rather primitive type of sausage as “ smoked goat-paunchesﬁlled with blood and fat offered as an hors d’oeuvre ” The manufacturing methods were of course-and indeed still are in most areas-a craft (Gounadaki, Skandamis, Drosinos, & Nychas,

2007) The sausage mixture was stuffed in casings prepared from the small intestine of pigs and they were subsequently placed in cool rooms with sufﬁcient aeration to allow for drying and consumed within a few weeks or in some places over the summer,

a period in which substantial weight loss (ca 30%) occurred and

“fresh” sausages became semi-dried products Today, although home production still occurs in the traditional way, large quantities are produced throughout the year at butchers’ shops and by meat processing companies (Papagianni, Ambrosiadis, & Filiousis, 2007) Traditional Greek sausages are produced with lean meat and fat and the addition of salt (1.6e2.5%), phosphates, nitrites, mono-sodium glutamate and ascorbic acid or its salt, sugar and various seasonings Lean or semi-lean pork and beef meat, pork bellies and pork fat can be used as raw materials The sausage mixture is then stuffed in natural casings but the products must be kept chilled

E.Z Panagou et al / Food Control 29 (2013) 32e41 33

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until consumption This product is characterized as fresh and

non-cooked and may be partially dried or smoked, fat should not exceed

35% The product should be cooked before consumption The pH in

the surface layer of the sausages varies between 4.67 and 6.09, and

the awvalue is ca 0.96 (Ambosiadis, Soultos, Abrahim, & Bloukas,

2004) The physicochemical, sensory and microbiological qualities

of traditional Greek sausages have been characterized in two

studies (Ambrosiadis et al., 2004;Drosinos et al., 2005), indicating

that lactic acid bacteria are the dominant group of microorganisms,

while identiﬁcation of isolates showed high counts of Lactobacillus

plantarum and L plantarum/pentosus (Drosinos et al., 2005)

3.2 Greek cheeses

Greece has a long tradition in producing a variety of dairy

products, among which cheeses have a dominant position, as the

country possesses the second place, after France, in cheese

consumption worldwide (FAO, 2005) Undoubtedly, the most

important and famous Greek cheese with worldwide acceptance is

Feta with an average annual consumption of about 12 kg per capita

Feta is a protected designation of origin (PDO) soft white cheese

ripened in brine, manufactured from ewes’ milk or a mixture of

ewes’ and goats’ milk, in which the proportion of the latter is not

higher than 20e30% (Manolopoulou et al., 2003) The most suitable

period for Feta cheese production is from January to May

depending on milk availability, as this is the milking season for

sheep and goats Traditionally, this type of cheese is produced in

small family-owned dairy installations with basic equipment with

unpasteurized or pasteurized milk, following a craft and empirical

process However, this situation has drastically changed and today

Feta cheese is produced almost exclusively with pasteurized milk in

well-equipped dairy factories around the country, using

commer-cial lactic acid cultures (Anifantakis, 1991) Various starters have

been successfully used, such as Lactococcus lactis and Lactobacillus

bulgaricus in a ratio of 1:3, producing Feta cheese of‘excellent’ or

‘ﬁrst’ quality (Sarantinopoulos, Kalantzopoulos, & Tsakalidou,

2002) The milk is renneted at 32C and coagulation takes place

in 40e45 min The resulting curd is cut (2 cm thick slices),

trans-ferred into vats with perforated inner walls and bottom, and

pressed by a weight equal to that of the curd Cheese blocks

(23 12 6 cm) are then dry-salted for 5 days at 16C and left for

10 more days at the same temperature During this period a slime of

surface-growing bacteria is developed, which is considered to

contribute greatly to cheese ripening Later the cheese blocks are

put into barrels or tin containers of 14 kg with brine (6e7% salt) in

order to continue ripening at 2e5 C The Feta cheese may be

consumed after ripening for at least two months (

Litopoulou-Tzanetaki, Tzanetakis, & Vafopoulou-Mastrojianaki, 1993) Similar

to Feta is the White cheese, in which the milk comes exclusively

from cows Both products have a maximum permitted moisture

content of 54% and a minimum fat content in dry matter of 46%

(Zerﬁridis, 2001)

Other popular traditional cheeses of economic and nutritional

importance are whey cheeses, namely Mizithra, Anthotyros and

Manouri, manufactured commercially from the whey of Feta or

hard cheeses (e.g Kefalotyri, Graviera) They are protected

desig-nation of origin (PDO) cheeses, with a maximum permitted

mois-ture content of 60e70%, and a minimum fat content in dry matter of

50e70%, depending on cheese type (Kandarakis, 1986; Samelis,

Kakouri, Rogga, Savvaidis, & Kontominas, 2003) These cheeses

are usually consumed fresh within a few days or weeks of their

production Their production is based on denaturation and

coagu-lation of the water-soluble whey proteins following heating at high

temperatures (>85C), where the curd is typically collected as

a surface pellicle from the coagulating whey system (Samelis et al.,

2003) To enhance the content of cheese in protein and fat, it is common practice to supplement the whey with different concen-trations of milk and milk fat prior to heating (Kandarakis, 1986) Due to thermal treatment of the whey, the indigenous microbiota is inactivated and starter cultures are not usually added during the process Consequently, this type of cheese is practically free of microorganisms provided that strict hygienic conditions are met However, subsequent handling of the curd results in post-processing contamination with a variety of spoilage bacteria (Kalogridou-Vassiliadou, Tzanetakis, & Litopoulou-Tzanetaki, 1994;

Lioliou, Litopoulou-Tzanetaki, Tzanetakis, & Robinson, 2001), rendering, thus, whey cheeses susceptible to rapid bacterial dete-rioration, particularly under abuse storage temperatures For this reason, the shelf-life of whey cheeses is rather limited ranging from less than 7 days under aerobic conditions to 20e30 days when vacuum packaging is employed (Dermiki, Ntzimani, Badeka, Savvaidis, & Kontominas, 2008), unless dried like Mizithra Spread acid-curd soft white cheeses like Galotyri and Katiki are another category of traditional Greek PDO cheeses, with

a maximum permitted moisture content of 75% and minimum fat content in dry matter of 40% for both types (Katsiari, Kondyli, & Voutsinas, 2008) Galotyri is considered as one of the oldest traditional cheeses in Greece and is popular in the regions of its origin, namely Epirus and Thessaly (Anifantakis, 1991) The cheese

is white, spread acid-curd with a pH value of ca 4.0 It is charac-terized by pleasant organoleptic characteristics, acid taste and

a mild aroma It is produced from raw or pasteurized ewes’ or goats’ milk or their mixture at various proportions with or without the supplement of starter cultures and rennet (Rogga et al., 2005) There is a National Individual Standard for this cheese (General Chemical State Laboratories, 1988, p 8401) which was further amended (Anonymous, 1994, pp 60e61) according to which the use of cows’ milk and/or milk powder or concentrates, as well as the addition of milk proteins, casein salts, coloring substances, or preservatives other than sodium chloride (common salt) are not allowed Based on traditional processing, the raw milk is boiled and subsequently placed in clay jars for approximately 24 h at ambient temperature Afterward, salt is added at a concentration of ca 3e4% (w/v) and the milk is left for 2 days with periodic stirring to undergo a natural acidiﬁcation Occasionally, rennet or yogurt culture may be added prior to salting to facilitate milk coagulation and acidiﬁcation The curd is transferred to clean cheese cloth which is then hung from a rafter in the store room for curd draining

at 15C for ca 6 h After draining, the curd is taken out on a clean board, mixed well with dry salt (1.5%, w/w) and sealed tightly in containers which are then placed in a cold storage room (<4C) for

up to two months for ripening (Katsiari et al., 2008)

Katiki is a creamy white acid-curd soft cheese with a mild sour and salty taste made from goats’ milk or a combination of goats’ and ewes’ milk, which is popular in Greek and other Mediterranean markets It is a traditional PDO soft cheese produced primarily in the area of Domokos in Central Greece The product belongs to the so-called ‘unripened soft cheeses’, which are consumed fresh within a few days from manufacture According to the traditional cheese-making practices employed by most small dairies in the area, the raw milk after being pasteurized and cooled to ca 25C, is inoculated with a mesophilic starter culture of lactic acid bacteria to facilitate coagulation and acidiﬁcation Occasionally, a small amount of rennet may be added when the pH reaches a value of 6.0e6.2 After 24 h, the curd is transferred to clean cheese cloth for draining When the moisture of cheese is ca 72%, salt is added, mixed to produce a homogeneous cheese mass, packaged and stored at 4C Theﬁnal characteristics of the product are: moisture, 75%; fat-in-dry-matter, 40%; protein, 8.8%; salt, 1.5e2%; pH, 4.3e4.5 (Panagou, 2008)

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Other traditional Greek cheeses of wide acceptance are Kasseri,

Kefalotyri and Graviera, all of protected designation of origin in the

EU Kasseri cheese is produced from sheeps’ milk or from a mixture

of sheeps’ and up to 20% goats’ milk It belongs to the so-called

“semi-hard” cheeses with maximum moisture 40% and minimum

fat-in-dry-matter 40%, for the ﬁrst grade cheese The annual

production in Greece amounts to ca 21,000 tons (Zerﬁridis, 2001)

The cheese has a whiteeyellow color, a rind of the same color, and it

is characterized byﬁrm texture with the presence of few holes

uniformly distributed in the mass of the cheese Its ripening period

is at least 3 months The cheese is distinguished for its pleasant

taste andﬂavor and is consumed as table cheese or used for pizza

production, similar to Mozzarella cheese (Arvanitoyannis &

Mavropoulos, 2000) Kefalotyri is manufactured from sheeps’ or

goats’ milk or a mixture of them (Anifantakis, 1991) The name

refers to the “head-shaped” appearance of the cheese

(Kalantzopoulos, 1993) Around 3600 tons of cheese are consumed

in Greece on an annual basis The cheese is characterized by hard

texture, salty taste, and strongﬂavor It is a hard rind cheese of

whiteeyellow color Small gas holes and bigger slit holes exist in

the mass of cheese The chemical constituents of theﬁnal product

are: moisture, 36%; fat, 28%; fat-in-dry-matter, 45%; pH, 5.6; salt

content, 4% Graviera is a popular Greek yellow hard cheese with

a high fat content (30e33%, w/w) and a relatively low salt content

(2.0e3.5%, w/w) It is produced mainly from ewes’ milk, which is

acidiﬁed by a mixed culture of mesophilic (1% L lactis ssp lactis or L

lactis ssp cremoris) and thermophilic (0.1% Streptococcus

thermo-philus and Lactobacillus helveticus) organisms The curds are cooked

to approximately 50 C and, after whey drainage, molded and

pressed at an increasing pressure The cheeses are salted by

frequent application of dry salt to the surface for 2e3 weeks and

ripened for 3e4 months (Fox & McSweeney, 2003)

3.3 Fermented fruits and vegetables

Olives, a common fermented fruit in Greece, are one of the oldest

food crops in the Mediterranean basin the cultivation of which

dates back to the Late Bronze Age (Riley, 2002) They are probably

the most economically important fermented vegetable food in the

Western world Today, although the olive producing areas of the

world are extended as far as Australia, South Africa, Chile and Peru,

almost 98% of olive trees grown in the world are located around the

Mediterranean (Kiritsakis & Markakis, 1987) The average world

production reached around 1,823,000 tons in the year 2006/2007,

the majority of which is produced in the European Union (w50%),

namely Spain, Italy, and Greece (IOC, 2009)

There are three basic commercial preparations in the

interna-tional markete Spanish style green olives, naturally black olives

(Greek style), and black ripe olives (California style)e for which

processing procedures are well-established in the literature

(Garrido-Fernández, Fernández Díez, & Adams, 1997) Spanish-style

green olives are initially subjected to a debittering treatment with

a dilute solution of sodium hydroxide (1.8e2.0, w/v) to hydrolyze

the bitter constituent oleuropein, followed by a washing step to

remove the excess of alkali Olives are then immerged in brine

(6e8%, w/v, NaCl) where they undergo a spontaneous fermentation

mainly by lactic acid bacteria (Balatsouras, 1990) Theﬁnal product

can be marketed as plain olives or olives with different stufﬁng

material (e.g almond, pimiento, etc.) Naturally black olives are

directly placed in brine right after harvest, with a salt concentration

ranging from 8 to 10%, or slightly lower A natural fermentation

takes place for which a complex microﬂora of Gram-negative

bacteria, lactic acid bacteria and yeasts is responsible (Tassou,

Panagou, & Katsaboxakis, 2002) Theﬁnal fermented product can

be marketed as plain, depitted, or sliced olives in brine

Frequently, theﬂavor of olives is enhanced by the addition of various herbs and spices Black ripe olives are obtained from fruits harvested when not fully ripe, which have been blackened by oxidation and have been debittered by alkaline treatment These olives are not subjected to fermentation and consequently must be preserved in hermetically sealed containers that have been previ-ously subjected to heat sterilization to ensure microbiological control (Garrido-Fernández et al., 1997)

Another commercial preparation of naturally black olives of rather minor importance is the so-called dry-salted olives The fruits are harvested fully ripe or over-ripe and are placed in concrete tanks together with coarse salt in a proportion of 40% (w/ w) Due to osmotic dehydration, olives lose water and other solutes, including much of the bitter constituent oleuropein, and become, thus, gradually debittered andﬁnally eatable (Panagou, 2006)

In Greece, almost 90,000 to 100,000 tons of raw olives are processed to produce primarily Spanish-style green olives as well

as naturally black olives Most fermented olives (w90%) are distributed throughout the marketing chain“in bulk” i.e., in plastic containers of various sizes, and only a small amount is packed in hermetically sealed glass or tin containers and then subjected to thermal treatment (pasteurization) The product can be found in retail outlets in both types; however, olives sold in bulk have generally a lower price and are greatly preferred by consumers If the fermentation process is adequate, the physicochemical char-acteristics of theﬁnal product e particularly pH, titratable acidity, and salt contente can ensure the microbiological safety and good keeping quality of the product The minimum requirements for these characteristics should comply with the trade standards for table olives in international trade established by the International Olive Council (IOC, 2004)

Cucumbers are one of the most important raw vegetable materials used for fermentation in Greece Cucumber fermentation,

a typical vegetable brine-salted fermentation, is considered to take place in four stages, namely initiation, primary fermentation, secondary fermentation, and post-fermentation (Bamforth, 2005)

At the onset of the process, the pH of the brine is ca 5.5 and fermentable carbohydrates, mainly reducing sugars (glucose and fructose), are present As a result, a rapid growth of several Gram-positive and Gram-negative bacteria as well as yeasts occurs This stage can last as long as 7 days during which, lactic acid bacteria and yeasts prevail over undesirable bacteria, mainly due to acidi-ﬁcation of the brine medium This stage is usually completed primarily by L plantarum and secondarily by Pediococcus pentosa-ceus and Lactobacillus brevis Leuconostoc mesenteroides strains are most of the times inhibited by the higher salt concentration, although heterofermentative species are not desired during this type of fermentation (Harris, 1998) Secondary fermentation by fermentative yeasts can occur only when fermentable carbohy-drates have remained in the brine from the previous stage (Franco, Pérez-Díaz, Johanningsmeier, & McFeeters, 2012) Finally, post-fermentation depends on the storage conditions Speciﬁcally, open fermentation vessels facilitate the growth of oxidative yeasts, fungi and bacteria, while anaerobic vessels do not allow the growth

of these microorganisms Several factors, including initial microbial load, growth rates, salt and acid tolerances account for this microbial sequence (Daeschel, Andersson, & Fleming, 1987) In some cases, the predominance of L plantarum may result in excessive concentration of lactic acid that renders the product unﬁt for direct consumption and might inﬂuence its texture as well (Passos, Ollis, Fleming, Hassan, & Felder, 1993) This issue could be resolved by inoculating the brines with a mixed population of L plantarum and fermentative yeasts in order to divert a portion of the fermentable carbohydrates into non-acidic metabolic products (Daeschel, Fleming, & McFeeters, 1988)

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3.4 Emulsion-type Greek appetizers or salads

The consumption of the so-called delicatessen creamy

appe-tizers or salads, as they are called in Greece, has markedly increased

in the last two decades in both Europe and the USA (Tassou,

Samaras, Arkoudelos, & Mallidis, 2009) Their production is based

on a variety of recipes but they are mainly oil-in-water emulsions

consisting of a mayonnaise, starch, yogurt, cheese or vinaigrette

type base, supplemented with particles or animal or vegetable

origin These products are ready for consumption without any

further preparation or cooking (Smittle, 2000) Among these,

traditional Greek deli-type salads are gaining wide consumer

acceptance in both the domestic and international markets, and

a systematic effort has been initiated to standardize their

commercial production by local and international companies

Preservation of these products is not based on thermal treatment to

control microbes, because it will reduce the physical integrity of the

product and result in substantial organoleptic deterioration

(Beuchat, Ryu, Adler, & Harrison, 2006) Consequently, preservation

depends on a combination of intrinsic factors to control or

elimi-nate microorganisms (Micels & Koning, 2000) The shelf life of

these products ranges from 2 to 3 months under refrigerated

storage and relies on the use of acetic acid (vinegar) in the aqueous

phase, reducing pH to 3.6e4.5 Additional intrinsic factors

contributing to the microbiological stability are the low water

activity (aw) due to the presence of high sugar or salt concentration

(e.g 10 and 6%, respectively) as well as the use of chemical

preservatives, namely sorbic and benzoic acid (Manios, Skiadaresis,

Karavasilis, Drosinos, & Skandamis, 2009) Cheese-based salads

such as Tyrokafteri (spicy cheese salad) and Tyrosalata (cheese

salad) are very popular Greek creamy appetizers, the typical

composition of which is shown inTable 1

A food of similar manufacturing technology and composition is

aubergine salad, which is an item produced industrially with

addition of boiled aubergine puree, salt 1e2%, garlic 0.4%, and acetic

acid 0.2e0.4% to reduce pH to ca 4.1 Home-made aubergine salad

is made of eggplants, garlic, and extra virgin olive oil Eggplants are

initially baked at 180C for 15 min to soften their tissue, and then the inner parenchyma of each eggplant is removed and mixed with the other ingredients Finally lemon juice is added to reduce pH to

ca 4.0 Occasionally, different amounts of oregano essential oil are added to enhanceﬂavor and increase the microbiological stability

of theﬁnal product (Skandamis & Nychas, 2000)

Another popular delicacy ofﬁshery origin is tarama salad (cod roe paste) prepared either homemade or industrially The home-made product consists of salted cod roe, bread crumbs or mashed potato, olive oil, lemon juice or spices and is normally kept refrig-erated On an industrial scale, red pigment and chemical preser-vatives, mainly sodium benzoate and sorbic acid, are also added to inhibit the growth of yeasts and fungi associated with food spoilage

A typical composition of commercially available tarama salad consists of dried and salted cod roe (8%), soybean oil (65%), bread, onion, potatoﬂour, lemon juice, spices, sodium benzoate (0.005%), and sorbic acid (0.075%) (Mexis, Chouliara, & Kontominas, 2009)

4 How safe are the Greek foods?

4.1 Fermented meats Meat fermentation may be viewed as a process that takes potentially hazardous raw materials and through a two-stage process of fermentation and ripening, develops an inhibitory ecosystem for most bacterial pathogens Indeed fermentation/ ripening is transforming the perishable and hazardous raw mate-rials into products with extended keeping quality and reduced risk

of causing illness The overall antimicrobial effect elicited in fer-mented meats is the sum of multiple hurdles of microbial (organic acids and ethanol) or non-microbial (reduced aw, nitrites, nitrates, spices, phenolics, and heating temperature) origin However, the manufacturing of traditional fermented products is characterized

by considerable variability in raw materials, operation units, fermentation, and/or ripening conditions This in turn is reﬂected in theﬁnal pH and awof the produced traditional sausages, which have been reported to vary from 4 to 7 and from<0.60 to >0.95, respectively (Gounadaki et al., 2007; Gounadaki, Skandamis, Drosinos, & Nychas, 2008;Skandamis & Nychas, 2007)

The combination of naturalﬂora, and in some cases the appli-cation of starter cultures, was a “triumphal” step in the manufacturing of traditional fermented products, because it assured safer products, especially those with short ripening time Among the antimicrobial factors associated with lactic acid bacteria, such as bacteriocins, hydrogen peroxide, CO2, diacetyl, low redox potential, crowding low pH, and organic acids (Gounadaki

et al., 2007,2008; Skandamis & Nychas, 2007), the main factors are organic acids and low pH Commonly, the level of organic acids, mainly lactic acid, produced by lactic acid bacteria during fermentation exceeds 100 mM (1% v/v), whereas the ultimate pH is often in the range of 4.0e4.5 Another feature that is required so that lactic acid bacteria may elicit their antimicrobial activity is their numerical superiority over any pathogens present Greek traditional sausages have been reported to have lower pH value, lower concentration of biogenic amines than similar products from South European countries e.g France, Italy and high populations of Enterococcus These organisms have been shown to inhibit in vitro growth of Listeria monocytogenes, which suggests possible contri-bution to the safety of the end product, and possibly the value of these strains as protective cultures (Paramithiotis, Kagkli, Blana, Nychas, & Drosinos, 2008) These organisms have a long history

of safe use, although they are not included in the generally recog-nized as safe list (Latorre-Moratalla et al., 2008;Talon et al., 2007) However, despite the increase in safety level conferred by lactic acid bacteria and the indigenous microbial population in general, as

Table 1

Typical composition and physicochemical characteristics of Tyrokafteri (spicy

cheese salad) and Tyrosalata (cheese salad) Based on Manios et al (2009)

Appetizer Composition pH a w Fat (%)

Tyrosalata Water 20% 4.3e4.5 0.901 27.0

Feta cheese

Vegetable oil

Milk powder

Vinegar

Modiﬁed starches

Dried egg yolk

Salt

Sugar

Mustard

Spices/seasonings

Stabilizer (E413, E415)

Sorbic acid (E202)

Tyrokafteri Water 20% 4.2e4.4 0.910 27.1

Feta cheese

Vegetable oil

Milk powder

Vinegar

Modiﬁed starches

Dried egg yolk

Salt

Sugar

Mustard

Spices/seasonings

Chili green pepper (6%)

Stabilizer (E413, E415)

Sorbic acid (E202)

Trang 6

well as by the manufacturing process itself, there are still emerged

or “developed” pathogens that are capable of combating the

inhibitory environment of fermented meats ecosystems The

dominant pathogens that have been reported to be presently

capable of surviving during storage of fermented sausages include

Salmonella, enterohemorrhagic Escherichia coli (EHEC),

Staphylo-coccus aureus, and L monocytogenes (Skandamis & Nychas, 2007)

Therefore, knowledge of the ability of pathogens to survive and

proliferate in fermented traditional Greek meats is an important

prerequisite in order to achieve the food safety objectives related to

these speciﬁc food ecosystems in a reliable and consistent manner

It is expected that survival responses of pathogens will vary

depending not only on the manufacturing process and product

characteristics, but also on whether inoculation is carried out in the

meat batter or theﬁnal products, because the pathogens will be

exposed to different stresses (Gounadaki et al., 2008) Thus, in order

to conduct reliable exposure assessment reports related to

fer-mented products, there is a need for challenge testing A review of

the reports on the survival/growth of the major pathogens in

a variety of fermented dry or semi-dry sausages including Greek

traditional sausage is presented bySkandamis and Nychas (2007)

However, published results on fermented sausages related to

a European research project have indicated that Greek sausages

have good safety records (Skandamis & Nychas, 2007)

4.2 Cheese products

Although cheese has been characterized as one of the safest food

products by some authors (Kousta, Mataragas, Skandamis, &

Drosinos, 2010), in 2006 the consumption of contaminated

cheese accounted for 0.4% of the total foodborne outbreaks in

Europe (EFSA, 2008) Cheeses are ready-to-eat food products that,

for the most part, do not undergo any further treatment to ensure

their safety prior to consumption Contamination of cheese with

foodborne pathogens may originate from various sources including

raw milk, brine,ﬂoor and packaging material, cheese vat, cheese

cloth and curd cutting knives, cold room and production room air

(Temelli, Anar, Sen, & Akyuva, 2006) It is also characteristic that the

majority of traditional Greek cheeses are usually produced in small

dairies, with different production processes that are dependent on

the geographical location, resulting in a range ofﬁnal products with

considerable variability in terms of microbiological and

physico-chemical attributes (Freitas & Malcata, 1999)

In a recent survey undertaken in the area of Athens

(Papadopoulou, 2007), 70 commercially available cheese samples

were investigated microbiologically, including white brine cheeses

(Feta, cow cheese, goat cheese), whey cheeses (Mizithra,

Antho-tyros, Manouri), and spread cheeses (Katiki, Galotyri) Main

emphasis was given on the presence of foodborne pathogens, i.e., L monocytogenes, Salmonella spp., S aureus, E coli, and Aeromonas hydrophila, as well as on the characterization of the total mesophilic bacteria, lactic acid bacteria, Lactococcus spp., Enterococcus spp., Pseudomonas spp., Brochothrix thermosphacta, Enterobacteriaceae, and yeasts/moulds From the obtained samples, 27 were sold in sealed retail packages of 500 g, whereas the remaining 43 were marketed in bulk Results showed that the prevailing microbial association in all samples consisted of lactic acid bacteria at levels exceeding 7 log CFU/g in most cases (Tables 2and3) Enterococci were not detected in 35% of brine cheeses, 25% of whey cheeses, and 16% of spread cheeses Enterobacteriaceae were undetectable in 86%

of brine cheese samples, but in whey and spread cheeses their population exceeded 7 log CFU/g in 19e20% of the surveyed samples No moulds were detected; however, yeasts were found in all samples in populations ranging from 2 to 6 log CFU/g The occurrence of Pseudomonas spp was high as the microorganism was found in 75%, 94%, and 85% of brine, whey, and spread cheeses, respectively Br thermosphacta was enumerated in higher pop-ulations in 69% of whey cheeses (2e6 log CFU/g), followed by brine cheeses (21% of samples at 2e5 log CFU/g), and spread cheeses (29%

of samples at 2e3 log CFU/g) The occurrence of Listeria spp was high (40%) in the surveyed samples but only one sample of whey cheese (Manouri) was presumptive positive for L monocytogenes Salmonella spp and S aureus were not detected in any cheese sample E coli was found in 7% of the examined samples at levels varying from 3.0 to 5.3 log CFU/g Aeromonas spp was detected in 13% of cheese samples, however no sample was presumptive for

A hydrophila As expected, cheeses sold in bulk contained higher populations compared with cheeses in packages Moreover, whey cheeses supported higher population densities than brine and spread cheeses in most cases This could be due to the higher pH and moisture content and lower salt concentration of whey cheeses 4.3 Table olives

Table olive processing relies on the microbiota naturally present

on the fruit surface, water, and fermentation plants This may be

a sufficient reason for variations in the flavor of the final product, as well as economic losses due to spoilage In Greece, about 90% of processed olives are marketed in bulk and they are freely available

to consumers in open containers, stored at ambient temperature, exposed to a high risk of contamination from the environment Contamination of olives may be due to harvesting the crop directly from the soil, poor hygiene and unsanitary procedures byﬁeld and processing personnel, inadequate cleaning and sanitizing of pro-cessing equipment, and failure to wash the olives prior to brining Fermented olives have an extended shelf-life (between 1 and 2

Table 2

Population a (log CFU/g) of different microbial groups and pH values of cheese samples sold in packages.

Feta cheese Goat Cheese Cow cheese Mizithra Anthotyros Manouri Katiki Total mesophilic bacteria 7.5 0.3 7.5 0.5 7.0 0.1 8.0 0.1 8.0 0.1 8.0 0.4 7.0 0.5 Lactic acid bacteria 7.6 0.2 7.5 0.5 7.7 0.7 8.0 0.1 8.0 0.1 8.0 0.2 8.0 0.1 Lactococcus spp 7.5 0.2 7.3 0.3 6.6 0.3 7.3 0.3 8.0 8.0 0.6 6.8 0.8

Br thermosphacta 4.0 1.0 <2 <2 3.0 3.5 4.0 0.1 <2

Enterobacteriaceae <1 <1 <1 3.0 0.1 4.0 3.0 <1

Pseudomonas spp 3.7 0.2 3.0 1.0 4.3 0.3 3.0 0.1 7.0 3.5 0.5 2.0

Yeasts and moulds 3.7 0.3 4.5 0.5 4.3 0.7 5.5 0.5 4.0 5.0 1.0 2.0

pH 4.6 0.1 4.4 0.1 4.4 0.1 4.2 0.1 6.0 0.5 5.1 0.4 4.3 0.1

a standard error Values with no standard error indicate enumeration of the respective microorganism in only one sample.

Trang 7

years) and they are normally consumed without cooking.

Consuming food products without cooking makes contamination

with pathogens a public health concern, even for fermented

products However, fermentation is an excellent preservation

technique as the activity of lactic acid bacteria results in the

production of a variety of metabolic compounds, in which lactate

and acetate predominate, lowering the pH of the brine and

decreasing thus the presence of pathogenic microorganisms

(Caplice & Fitzgerald, 1999;Ross, Morgan, & Hill, 2002) In addition,

antimicrobial compounds (e.g ethanol, bacteriocins) produced by

certain strains of lactic acid bacteria contribute to a better

preser-vation effect of the ﬁnal product (Lee, 2004; Rubia-Soria et al.,

2006) For this reason, fermented foods have been generally

considered less likely to cause foodborne infection or intoxication,

although several pathogens have been reported to survive the

fermentation process (Nout, 1994)

Transmission of pathogenic bacteria through fermented olives

has not been documented so far, but occurrence of L monocytogenes

during Spanish-style green olive fermentation has been reported

recently (Caggia, Randazzo, Salvo, Romeo, & Giudici, 2004)

Speciﬁcally, from a total of 69 samples of olives analyzed for the

presence of L monocytogenes in Italy, 36 were contaminated with

Listeria from which 26 were identiﬁed as L monocytogenes

Although L monocytogenes is considered pathogenic to humans,

the presence of any Listeria species in food can be an indicator of

poor hygiene Moreover, the microbiological and safety evaluation

of green table olives marketed in Italy has also been reported

(Franzetti, Scarpellini, Vecchio, & Planeta, 2011) Forty green table

olive samples from retail outlets (street markets and supermarkets)

were analyzed for microﬂora and food safety indices including

Salmonella spp., L monocytogenes, and S aureus Results showed

that there was a wide heterogeneity in the microﬂora, with yeasts

and lactic acid bacteria dominating the microbial population as

a result of the fermentation process Their numbers together with

their metabolic activity resulted in the development of unfavorable

conditions for the survival of pathogenic microﬂora on olives In

another survey of table olives undertaken in the Spanish market

(López-López, García-García, Duran-Quintana, &

Garrido-Fernán-dez, 2004), 67 samples of green, directly brined, and black ripe

olives were analyzed to determine their microbiological and

physicochemical proﬁle Results showed that lactic acid bacteria

and yeasts were the dominant microbial groups, the former being

more abundant than the latter Spore-forming mesophilic aerobes

(e.g Bacillus cereus), which can be considered contaminants from

ingredients or product handling, were present in only some

samples and were always at low levels Finally, a similar survey was

carried out in Greece involving 69 different commercially available

table olive preparations, including Spanish-style green olives,

naturally black olives and dry-salted olives (Panagou, Tassou, & Skandamis, 2006) The prevailing microbiota consisted of lactic acid bacteria and yeasts coming from the spontaneous fermenta-tion process, whereas no enterobacteriaceae, pseudomonads, B cereus, or Clostridium perfringens were detected in any of the samples analyzed given the physicochemical characteristics found (average pH, 3.9e4.3; salt content, 6.2e7.3)

Recently, survival studies of E coli O157:H7 in Spanish-style fermentation of Conservolea green olives, in brines supplemented with different concentrations (0, 0.1, 0.3, 0.5, and 1%, w/v) of carbon sources (glucose or sucrose), showed that reduction of the path-ogen was evident in all processes However, the pathpath-ogen survived even at low numbers probably due to acid adaptation during the gradual reduction of pH in the brines (Spyropoulou, Chorianopoulos, Skandamis, & Nychas, 2001) The ﬁnal pop-ulation of E coli O157:H7 was related to the initial concentration of carbon source, and hence theﬁnal pH value of the fermentation process, as the highest concentration caused the highest decline (ca 6.0 logs) in the pathogen’s numbers Similar observations were obtained for the survival of B cereus in green olive fermentation, the population of which declined steadily during the process, but

a tailing effect was observed when the pathogen reached 2 log CFU/

ml (Fig 1), at which point it does not pose a risk to human health (Panagou, Tassou, Vamvakoula, Saravanos, & Nychas, 2008) However, this was not the case with Salmonella Enteritidis PT4 in the spontaneous fermentation of naturally black olives, where the numbers of the pathogen declined rapidly within theﬁrst 3 days of the process, beyond which no cells were detected (Fig 2) A survival period (shoulder) of 1.3 days was evident followed by a sharp decline thereafter (Panagou, Tassou, Chorianopoulos, & Nychas,

2007) Overall, the existing data suggest that as the brine envi-ronment seems to be hostile for the survival of foodborne patho-gens further research is needed to determine their behavior during post-processing contamination Moreover, the application of appropriate thermal treatment to ensure the safety of such

a popular product could be considered, if needed

4.4 Emulsion-type appetizers or salads Preservation of these products is based mainly on their high acidity and on chemical preservatives employed to inhibit the growth of spoilage and pathogenic microorganisms, although their use is considered undesirable by consumers who demand reduced levels of additives in foods Although the safety of these items is supposed to be ensured primarily by their low pH, several patho-gens, namely E coli O157:H7, L monocytogenes, and Salmonella spp., have been reported to survive or even grow in these foods (Smittle,

2000) Usually, the vehicle of the pathogen is the raw ingredients as

Table 3

Population a (log CFU/g) of different microbial groups and pH values of cheese samples sold in bulk.

Feta cheese Goat cheese Cow cheese Mizithra Anthotyros Manouri Katiki Total mesophilic bacteria 7.4 0.2 7.4 0.3 7.8 0.2 8.0 8.0 0.1 8.3 0.3 7.0 1.0 Lactic acid bacteria 7.6 0.1 7.8 0.2 7.9 0.3 5.0 7.6 0.2 8.1 0.5 7.3 0.3 Lactococcus spp 7.5 0.1 7.5 0.3 7.5 0.5 5.0 7.9 0.3 8.3 0.3 7.0 1.0 Enterococcus spp 4.3 0.3 4.7 1.4 5.0 4.5 5.3 0.3 4.5 6.0

Staphylococcus spp 3.7 0.3 3.0 5.0 1.0 2 5.7 0.4 2.7 0.7 <2

Enterobacteriaceae 3.0 0.6 2.0 5.0 5.0 5.8 0.6 3.0 0.6 2.0 0.1 Escherichia coli <2 <2 4.0 <2 5.3 0.3 <2 <2

Pseudomonas spp 4.1 0.3 3.7 0.5 6.0 2.0 8.0 7.2 0.6 4.5 0.5 2.8 0.8

Yeasts and Moulds 4.3 0.3 4.5 0.3 6.3 1.3 3.0 3.8 0.6 4.5 0.5 4.3 1.3

pH 4.7 0.1 4.5 0.1 5.0 0.1 6.5 5.9 0.1 4.8 0.1 4.3 0.1

a Mean values standard error Values with no standard error indicate enumeration of the respective microorganism in only one sample.

Trang 8

well as any contamination from the processing environment and

packaging operation Another issue of major concern is the

so-called stress adaptation response of the microorganisms,

accord-ing to which microorganisms exposed to moderately acidic

envi-ronment may develop cells with enhanced resistance and longer

survival times when transferred to a more acidic condition (Lou &

Yousef, 1997;Samelis & Sofos, 2003) In a recent study on

tradi-tional Greek salads (Tassou et al., 2009), the survival of S

Enter-itidis, L monocytogenes, and E coli O157:H7 was investigated inﬁsh

roe (tarama) salad and eggplant salad with/without the addition of preservatives (0.1% benzoic and sorbic acid) at 10 C storage temperature Inoculation of both salads was carried out with acid and non-acid adapted cultures of the pathogens Results showed that in the absence of preservatives all pathogens managed to survive throughout storage, presenting a 1 log reduction for Listeria and 2 logs reduction for Salmonella and E coli in both salads In most cases, acid adaptation prolonged the survival of all pathogens even when preservatives were added In the presence of sorbic and benzoic acids pathogens were inhibited at 7e10, 8e12, and 5 days for Salmonella, Listeria, and E coli, respectively The authors concluded that the presence of preservatives in these kinds of products is essential to ensure the microbiological stability and that

a well-studied combination of hurdles would be appropriate for the safety of homemade traditional salads free of preservatives

It needs to be noted though, that from a marketing point of view, these products appear to be more attractive to consumers when less or no additives are used, as they have the image of “home-made” products Essential oils could make an important contribu-tion and become an alternative for synthetic preservatives (Nychas

& Tassou, 2000) For this reason, the responses of E coli O157:H7 and Salmonella Enteritidis were investigated in homemade auber-gine salad, mayonnaise and cod roe paste as a function of envi-ronmental factors (pH, temperature, oregano essential oil, and type

of oil used) In these foods, a reduction in viable counts was observed for both pathogens, and the rate of decline was depen-dent on the pH, storage temperature, and essential oil concentra-tion (Koutsoumanis, Lambropoulou, & Nychas, 1999; Radford, Tassou, Nychas, & Board, 1991;Skandamis & Nychas, 2000)

5 Conclusions Greece is justiﬁably proud of the high quality and palatability of

a wide range of traditional foods (fermented meats, dairy products, fermented vegetables) that have long made the traditional Greek diet distinct In the past, the manufacturing of these products was craft and empirical and presented differences from area to area, resulting inﬁnal products with variable microbiological, physico-chemical and sensory characteristics Artisan practices employed in traditional food manufacturing in combination with unsuitable hygienic conditions, especially in small-scale processing units, may have resulted in the survival of pathogenic bacteria that may be present throughout the distribution chain However, in the last decades, this situation has drastically changed and traditional Greek products are now produced in well-equipped industrial units under strict processing and hygienic conditions In addition, the need for safe traditional products with standard and desirable technological properties has resulted, for example, in the use of starter cultures for the production of the dry fermented sausages, to control the fermentation and ripening process, inhibiting the growth of other undesirable microorganisms This has been ach-ieved for other fermented products, such as table olives and cheese, enhancing thus their safety record

Recently, in the context of a EU funded project (www.truefood

eu), an extended retail survey was carried out in a variety of traditional Greek food commodities (fermented meats, dairy products, plant derived products) to quantify the presence of pathogenic and other spoilage microorganisms and establish the extent of contamination and the risk that is posed to the consumer The main focus on pathogens was given on E coli O157:H7, L monocytogenes and Salmonella spp Moreover, depending on the speciﬁc characteristics of the product under investigation, other pathogens were also taken into consideration, such as B cereus and

S aureus Results showed that the intrinsic properties of foods attained at the end of the process (e.g pH, a , salt content,

Fig 2 Changes in lactic acid bacteria (A), yeasts ( - ), enterobacteria (C), and

Salmonella Enteritidis PT4 (:) during the spontaneous fermentation of Conservolea

naturally black olives Data points represent mean values standard deviation of

duplicate fermentations.

Fig 1 Population dynamics of lactic acid bacteria (A), yeasts ( - ), and Bacillus cereus

(:) during the spontaneous Spanish-style fermentation of Conservolea green olives.

Data points represent mean values standard deviation of duplicate fermentations.

Trang 9

moisture), together with other technological characteristics (e.g.

use of preservatives, chill temperatures, modiﬁed atmosphere

packaging, etc.) resulted in absence of pathogenic microorganisms,

and consequently, Greek traditional foods could be considered to

have a good safety record

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