North African Trad Food Risk Profiling
North African Trad Food Risk Profiling
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Abstract: North African countries have a rich tradition in food technology, and many traditional foods of animal or
plant origin are still widely consumed and highly appreciated. In fact, these foods play an important role in the economy
and food security in these countries. Yet, they are still mainly prepared at the household level under poor sanitary
conditions and marketed through informal routes. They thus remain beyond any official control for their compliance to
national regulatory standards. Therefore, their consumption is anticipated to put the public health at risk, although such
risk has never been estimated on a scientific basis due to the lack of consumption patterns, epidemiological data, and
appropriate surveillance programs. The scarcity of scientific studies on the incidence of hazards in this specific category of
foods adds to the difficulties in conducting scientifically sound risk assessment or profiling studies. This review provides
a brief description of technologies of the most popular traditional foods of animal and plant origin in North Africa and
discusses the potential microbiological risks associated with their consumption and the food safety challenges that they
raise. The review also aims to draw the attention of stakeholders including decision makers in North African countries
to the imperious need to assess or profile the health risks associated with their consumption, and consequently, take the
necessary measures to reduce such risks. A tentative risk profiling of selected traditional North African foods is presented
using as a template the “risk categorization model for food retail/food service establishments” developed by Health
Canada.
c 2012 Institute of Food Technologists®
54 Comprehensive Reviews in Food Science and Food Safety r Vol. 12, 2013 doi: 10.1111/j.1541-4337.2012.00215.x
Safety of North African traditional foods . . .
Atlantic
A Tunisia
O
Ocean Morocco M
Mediterraanean Seaa
Algeria
Libya
Egypt
Red Sea
Mauritania
Sudan
Figure 1–Countries of the North Africa subregion according to the most accepted definition (underlined boldface). Either Mauritania or Sudan (normal
fonts on a gray background) is occasionally considered as part of this region.
results showed that most North African traditional foods put con- Popular Traditional Foods in North African Countries
sumers at high risk, a challenging situation that should be addressed Dairy products
urgently, and different actions involving all interested parties are Although the North African diet is typically low in foods of
discussed. animal origin compared to foods of plant origin, mainly cereals and
olives (Grigg 1999; Padilla and others 2005; Alexandratos 2006), a
variety of centuries-old dairy products are known and still highly
appreciated by consumers in these countries. The most popular
The North African Region at a Glance of them are jben, lben, and smen, which have been reviewed
Located along the southern coast of the Mediterranean basin, previously (Benkerroum and Tamime 2004; Abd-El Salam and
North Africa is the northernmost region of the African continent Benkerroum 2006). However, in Egypt where the production and
spanning from the Atlantic Ocean in the West to the Red Sea consumption of cheese are significantly higher than in the other
in the East. In the south, it is surrounded from west to east by countries of North Africa (Table 2), there are more diversified
a subarid Sahara (desert in Arabic) belt called Sahel (Figure 1). and elaborated cheese types, among which brined cheeses are the
The North Africa region now consists essentially of 5 countries most dominant (Abd-El Salam and Benkerroum 2006). Table 3
(Morocco, Algeria, Tunisia, Libya, and Egypt), and is classically presents selected traditional North African dairy products with
divided into 2 subregions: the Maghreb/Maghrib, meaning “the a brief description of their technologies (for further details, see
sunset place” (West) in Arabic, typically including Morocco, Al- Aboudonia 1996; Benkerroum and Tamime 2004; Abd-El Salam
geria, and Tunisia, and the Mashrek (Libya and Egypt), meaning and Benkerroum 2006).
“the sunrise place” (East). Although this definition of the North
African region is the most widely accepted, it is not the only
one due to the multiplicity of geopolitical considerations and the Meat products
changing political status of the countries throughout the history of The overall consumption of meat products in North African
the region. Mauritania is occasionally added as part of the “Great countries (Table 2) is below the global average of 38 kg per capita
Arab Maghreb” that also includes Libya in addition to the 3 cen- per year (Speedy 2003). Although this situation is primarily at-
tral countries of the Maghreb (Morocco, Algeria, and Tunisia). In tributed to the low level of meat production (Table 2), the cost of
1989, the latter 5 countries have established the Arab Maghreb meat products, not always afforded by the majority of consumers,
Union (UMA) on the basis of geographical considerations and justifies further this limitation. Nonetheless, various traditional
the common social, cultural, and historical heritage in addition meat products have long been known in the region and prepared
to economic complementarities. On the other hand, the United for family or religious feasts. They were also made as a means
Nations’ definition of North Africa region includes Sudan but to preserve meat when it was available at quantities exceeding
excludes Mauritania, which is considered among the Sahel coun- immediate needs, while appropriate storage means such as ice, re-
tries. Furthermore, the fact that Egypt is also part of the Middle frigerators, and freezers were lacking. For example, in the religious
Eastern region, which with North Africa forms the Arab world, feast “Al Adha,” each Muslim family ought to slaughter a lamb,
adds some confusion to the definition of the exact geographi- and there is usually more meat than can be consumed in few days
cal boarders of the North African region. This definition is even (2 to 3 d). Surplus meat was then transformed into more stable
more confusing in that the Sinai desert, in North-Eastern Egypt, products that could be kept at room temperature for as long as pos-
is part of the Asian continent. Nonetheless, regardless of the ge- sible without being spoiled or becoming hazardous to consumers’
ographical or geopolitical definition, Morocco, Algeria, Tunisia, health. This was achieved by treatments combining different nat-
Libya, and Egypt form the core of the North Africa region and ural hurdles to microbial growth such as curing, salting, drying,
will thus be considered in this review. Table 1 summarizes the and fermentation, in an empirical application of the hurdle tech-
main demographic, economic, social, and cultural data for these nology as recently advocated by Leistner (2000a). Although spices
countries. and herbs were added to traditional meat products, primarily as
c 2012 Institute of Food Technologists® Vol. 12, 2013 r Comprehensive Reviews in Food Science and Food Safety 55
Safety of North African traditional foods . . .
Table 1– The main demographic, social, economic, and cultural data of the North African countries. Data were compiled from the World Bank
([Link] The United Nation Development Program (UNDP) ([Link] and the Food and
Agricultural Organization of the United Nations (FAO) ([Link] websites. Accessed on April 17, 2012. Statistic data and indices are
for the year 2011, unless otherwise stated in the footnotes.
Table 2–Production and apparent consumption for the years 2010 and as an ingredient in various dishes, such as the well-known North
2007, respectively, of milk, cheese, and meat in North African countries. African couscous or legume stews. The cured variant of gueddid
Production Consumption may also be further processed into “khlii” (see below). Although
(1000 metric tons) (kg/capita/year) the original purpose of transforming meat into gueddid was its
Country Milk Cheese Meat Milk Cheese Meat preservation to last as long as possible, given the lack of adequate
Algeria 2304.00 1.540 609.26 117.36 0.65 20.13 storage facilities; it is now regarded as prestigious and highly prized
Egypt 5742.40 940.15 1731.14 61.81 7.47 22.08 cultural heritage food in North African countries. Therefore, local
Libya 222.70 NA 186.68 75.03 1.78 27.84
Morocco 2009.55 43.73 1036.13 44.49 0.82 25.02 meat industries are trying to standardize its technology for an
Tunisia 1093.10 4.14 274.76 106.91 0.26 27.34 adequate transfer to industrial scale, as has been done with jerky
NA: Not available. meat (Draganski 2012), in response to consumer demands and
for export to other countries with high concentration of North
African communities such as France, Italy, Spain, and Canada.
flavoring and aromatizing agents, it is now well established that
they also contribute to the improvement of food safety and keep- Pastirma/ basterma/basturma/pastrami
ing quality, as many of them have been shown to possess potent an- This traditional meat product is the most popular in Egypt and
timicrobial activities (Al-Delaimy and Barakat 1971; Kivanc 1988; consists of cured and dried meat strips encased in a mixture of
Ghalfi and others 2007; Kong and others 2007; Ivanova and others garlic, fenugreek, and various spices (Figure 2b). It is believed
2009; Rattanachaikunsopon and Phumkhachorn 2009, 2010a, b). that pastirma has been brought to Egypt from Turkey, most likely
Among these, garlic, curcuma, cinnamon, cumin, ginger, cloves, during the Ottoman domination in Middle Eastern and North
paprika, and pepper (black, white, or red) coriander (leaves or African areas in the 15th and 16th centuries. In fact, the term
grain) have been the most frequently used in traditional meat “bastirma” means “strong pressing action” in Turkish as pressure
preparations. Also, pretreatments such as cooking or marinating is a crucial step in the preparation of the product (Obuz and oth-
into an acid, spicy preparation called sharmula for 1 or 2 d were ers 2012). Yet, it has been suggested that pastirma is originally
applied to raw meat in order to improve its microbiological quality a Roman (Byzantine) food product (Adamson 2002). Although
in addition to the enhancement of the final gustatory quality of pastirma is preferably made from beef, various other meat types
the meat products deriving thereof. Moreover, traditional meat are also used, including lamb, goat, buffalo, and camel. A typi-
products of North African origin are primarily obtained from cal method for pastirma preparation is summarized in Figure 4.
bovine, lamb, goat, buffalo, or camel meat, which have the “halal” The finished product has a pH of 4.5 to 5.8, a salt content of
status according to the Islamic rules. Yet, traditional pork meat 6.0%, water activity of 0.85 to 0.90, and moisture of 35% to 52%
products are also available, but they are claimed by Christian local (Leistner 2000b; Bechtel 2001; Obuz and others 2012). Pastirma
minorities such as the Copts in Egypt, or destined to temporary is consumed with scrambled eggs, cut into slices and fried, grilled
residents (foreign employees and diplomats or tourists) from other lightly over a charcoal fire, or added as an ingredient to various
countries, and hence they are produced in very limited quanti- culinary preparations such as bean stew.
ties. Similarly, the “kosher” traditional meat products are mainly
produced at the household level in Jewish families. Khlii/khlia and related products
Khlii is a candied meat product obtained from salted-dried meat,
Gueddid which is cooked and conditioned in fat (Figure 2c). It is a typical
The oldest means to preserve meat is probably by salting and Moroccan cured meat product, probably brought to the country
sun-drying (Nummer and others 2004). Gueddid (Figure 2a), a by Arab conquerors (early 8th century) on their way to Andalusia
typical meat product of the Maghreb countries (Morocco, Algeria, in the Iberian Peninsula (Daoudi and others 2006). Due to its
and Tunisia), is obtained by such a basic technology yielding stable extended shelf life even when stored under abusive temperature
salty dry meat, which can be stored at room temperature for more (more than 2 y when stored properly), it was the main food supply
than a year. It is primarily prepared from lamb meat or beef; in for Arab warriors to avoid food shortage while providing them
the subarid zones of the region, camel and goat meats are mostly with such tasty and nutritious food. Although genuine khlii is
used as depicted in Figure 3. At consumption, gueddid is softened believed to be made from camel meat, beef is the most widely
and desalted by immersion in water to make it tender before use used in practice. Typical traditional technologies of khlii and some
56 Comprehensive Reviews in Food Science and Food Safety r Vol. 12, 2013
c 2012 Institute of Food Technologists®
Safety of North African traditional foods . . .
Table 3–Main traditional North African dairy products; a brief description of their technologies (for further reading see Steinkraus 1995; Benkerroum
and Tamime 2004; Abd-El Salam and Benkerroum 2006).
c 2012 Institute of Food Technologists® Vol. 12, 2013 r Comprehensive Reviews in Food Science and Food Safety 57
Safety of North African traditional foods . . .
Table 3–(Continued)
of its variants are summarized in Figure 5. The so-called « diet » and drying conditions when applicable. Figure 6 presents a typical
khlii (Figure 2d and 5), where meat strips are dipped into olive oil process to make sujuk as shown in the photograph of Figure 2e..
instead of animal fat, is being increasingly popular due to consumer
awareness of the risks for cardiovascular diseases associated with Merguez
cholesterol and other metabolism and nutrition disorders. Properly Merguez is a typical Maghreb raw sausage with a small diameter
made and conditioned khlii can be preserved for more than 2 y (18 to 22 mm) and which does not undergo maturation or drying,
at room temperature; it is consumed as such (ready-to-eat meat contrary to msrana or sujuk (Figure 2e). Poultry merguez made
product) or fried with eggs for breakfast. It could also be used as an from turkey or chicken is being increasingly made in a similar way
ingredient in different traditional dishes such as soups, pancakes, as the beef variety, but without addition of paprika or other food
and couscous or, more recently, as a topping for pizza. color additives to keep the typical grayish color (Figure 2g). At
present, merguez is mainly produced by modern butcher shops at
Naqaneq/sujuk/soudjouk/msrana a semi-industrial scale using modern machines to chop the meat
“Naqaneq” is a generic Arabic term used to designate any and push the batter into the casing, in addition to the use of
sausage either raw or cooked obtained from ground meat (beef, nitrites functioning as salt, coloring (development of red color if
lamb, buffalo, or poultry), seasoned and pushed into a natural cas- appropriate), and as a preservative agent to prevent the outgrowth
ing (bovine or ovine intestine) previously soaked in boiling water. of Clostridium botulinum spores and production of botulism-causing
Therefore, these products are highly variable from one country to toxin. Furthermore, natural casing is being gradually replaced by
another and even among regions of the same country, depending synthetic collagen casing. Merguez is a highly perishable product
on the seasoning, the specific casing used, as well as the maturation and should therefore be consumed within 2 d after preparation
58 Comprehensive Reviews in Food Science and Food Safety r Vol. 12, 2013
c 2012 Institute of Food Technologists®
Safety of North African traditional foods . . .
Figure 2–Main traditional meat products in North African countries. (kourdass: [Link]
[Link]; gueddid: [Link] sujuk: [Link] Visited on 23 July 2012.
even when stored under refrigeration conditions. It is usually fried by gourmets. Bubanita, tehal, kourdass, and ban-shems are ex-
or barbecued to prepare sandwiches. However, in some countries, amples of such products, and their technologies with their main
such as Tunisia and Algeria, it is commonly added as an ingredient physicochemical characteristics that have an impact on microbial
in “couscous.” growth are summarized in Table 4.
c 2012 Institute of Food Technologists® Vol. 12, 2013 r Comprehensive Reviews in Food Science and Food Safety 59
Safety of North African traditional foods . . .
Meat:
Beef, lamb, goat orr camel
Keeping at room Aging
temperatu ys
ure for 2 day
Meat preparation
Aged meat Trimming
Removed fat
Seasoning:
Salting
(Salt,, garlic, cum
min, and grouund grains off ginger)
100 g meat)
(5.0-7.0 g salt/1
Optioonal:
Curing
Placiing in a cooll Application of curcuma
tempperature or paprika as colooring
(3 to 4 days) agentts (yellow orr red)
Cureed meat
Optional:
Addittion of grounnd chili
Suun-drying*: peppeer to:
Hangingg meat strips on a • givve a hot spiccy taste,
Drying
laundry rope or a wiire (5 annd
to
t 7 days) • reppel insects dduring
oppen-air sun-ddrying
Typiccal
gueddid/Keddid Cur ed gueddid
their relatively modest per capita consumption (Table 5) as com- or in modern factories. Traditional preservation technologies of
pared to China, for example, where the highest consumption of vegetables products have long been practiced in North African
vegetables worldwide has been recorded over the last 2 decades. areas to make these wholesome foods available throughout the
Nonetheless, the overall consumption of vegetable products in NA year. Fermentation, pickling, cooking, and/or drying have been
is higher than the minimum level of 146 kg per capita per year the main traditional techniques used to preserve many ripe prod-
recommended by the joint commission of the World Health Or- ucts available only at given periods of the year such as olives,
ganization (WHO) and the Food and Agriculture Organization lemons, onions, green peppers, carrots, figs, grapes, prickly pears,
(FAO) of the United Nations (FAO/WHO 2004). Moreover, an and so on. Among these, olives are probably the oldest and the
overall tendency to increased fruit and vegetable consumption has most culturally and economically significant products in the re-
been recorded in North African countries in the period of 2000 to gion, and hence their preservation by traditional technologies will
2007 (Figure 7). Figure 7b shows also that the per capita consump- be discussed in some details here.
tion of fruits in most North African countries remained low com-
pared to the global average recorded during the period of 2000 to Table olives
2007. Nonetheless, the high per capita consumption of vegetables Olive (Olea europaea L.) is typically a Mediterranean tree that has
in these countries during the same period (Figure 7a) would com- been grown in the region for millennia, and its fruit has been used
pensate for such a deficiency to meet the WHO recommended in a variety of ways in the diet as a table olive or as raw material
level for the overall consumption of vegetable products. to produce olive oil.
Although fruits and vegetables are generally consumed fresh, an A number of traditional technologies have long been used
important part of the harvest is processed for preservation, either in North African countries to produce palatable table olives
at the household level by using traditional low-cost technologies that could be stored for a relatively long period at ambient
60 Comprehensive Reviews in Food Science and Food Safety r Vol. 12, 2013
c 2012 Institute of Food Technologists®
Safety of North African traditional foods . . .
Product Step
S
Cuttting
Lean strips
(50-60 cm
m long, 10-15 5 cm wide an d
lesss than 5 cm thick)
Pastirma
Figure 4–Flow diagram of traditional pastirma production (Daoudi and others 2006; Obuz and others 2012).
temperature. However, despite the diversity of these methods, consumption by addition of different spices and flavoring ingredi-
they are based on 2 main procedures: (i) pickling and (ii) dry- ents including rosemary, coriander leaves, grated garlic, oregano,
salting. Both procedures rely, first on salt to remove the glycoside chopped onion, hot red pepper, and/or lemon juice, lemon pieces,
euloropein that makes olives unpalatable even when they are fully or harissa (Figure 9f).
ripened (black olives) and, second, on microbial fermentation to In addition to pickling, table olives may be obtained by dry-
develop acidity and specific aroma while contributing to the mi- salting techniques; the most commonly used of which involves
crobiological safety of the final product. Other processes such as the packing olives in plain salt for at least 1 mo to produce the so-
“Spanish green olive style” and the “California style” use sodium called “Greek style” olive. It is the simplest and probably the
hydroxide (as a debittering agent to remove euloropein) and other oldest technique used to preserve olives and make it palatable
chemical products (for example food-grade acids and potassium after removal of the euloropein. In North African countries, this
chloride) in addition to salt (Cardoso and others 2008; Panagou traditional method is exclusively used for fully mature black olives,
and others 2013). The latter techniques will not be considered by placing them in a container as interposed layers with salt in a
further, as they are used for large-scale commercial production proportion of 40 g salt to 100 g olives. These salted olives are kept
and unlike in European countries (Panagou and others 2013), the at room temperature until a pleasant flavor is reached, generally
addition of chemicals, including sodium chloride, has not been after 30 to 60 d (Cardoso and others 2008). A related traditional
practiced traditionally in North African countries. procedure widely used in Maghreb countries consists of placing
A typical North African traditional olive pickling procedure black olives in a burlap sack or a straw basket and evenly mixing
is presented in Figure 8. Pickled olives may be seasoned before them with salt (10 g per 100 g olives). A heavy weight (usually
c 2012 Institute of Food Technologists® Vol. 12, 2013 r Comprehensive Reviews in Food Science and Food Safety 61
Safety of North African traditional foods . . .
Muscle meeat
Beef,, lamb, goat or camel
Trimming
Pieces of fat
Preparation
Lean meatt
Cutting
Curing
Directt use of
cured gueddid keepinng at a cool place with ooccasional
stirring for 24 to 36 h
Cured
C meat sttrips
Sun-drying:
Drying
Hanging
H meat strips on a laundry
rope or a wire (5 to 7 days)
Cooking
Pot containing
c water, fat and olive
oill, with frequ ent stirring uuntil
complete evap oration of w water
Conditioning
Agrishh “Diet”” Khlii
Small meat
m pieces Khlii stripss dipped in
recoveered from khlii olive ooil and
batch, as they sepaarate conditionned in a
from thhe meat strip
ps similar mannner as the
while cooking.
c typicall khlii
stones of approximately half the weight of the olives) is placed on vation techniques have been used to make lemon available dur-
the top of the sack or basket to accelerate extrusion of olive juice, ing summer and autumn when scarce and expensive. The most
and euloropein with it. The whole package is left to ferment for common of such techniques involves dry-salting and fermenta-
5 d in a warm place (20 to 25 ◦ C). Olives are taken out of the tion, usually referred to as the “Moroccan style” pickled lemon
sack or basket and spread out under the sun on plastic mat for 1 d, (Figure 9c). According to this technique, ripe lemons (yellow in
and then put back in the sack or basket for another period of 5 d. color) are soaked in fresh water for 3 d while changing the water
This operation is repeated 3 times and then the olives are exposed daily to reduce the bitterness. Each lemon is then cut into quarters
to the sun for 2 successive days to be ready for consumption. The from the pointed end to about 2 cm of the stalk end, opened with-
resulting olives from the application of the latter process have a out breaking the quarters apart and filled with coarse salt (about
more pleasant and less salty taste than the Greek-style olives, but 100 g each). The salted lemons are firmly packed in a clear glass
they have a limited shelf life not exceeding few months at ambient container that is tightly sealed to prevent air access and left in a
temperature. Dry salted olives may be rolled in olive oil for a cool dry place for 4 to 6 wk. Meanwhile, the osmotic pressure
desired taste and shiny appearance and/or flavored with various exerted by the salt causes lemon juice exude and dissolve the salt,
herbs, spices, lemon pieces, and crushed garlic. thereby creating a strongly salty and acidic brine that covers partly
or totally the lemons in the container. These conditions select
Lemons for the microorganisms (acid- and salt-tolerant) to govern the fer-
Lemons are widely used as a flavoring agent in North African mentation process; they are predominantly lactic acid bacteria and
cuisine including tajine, soups, stews, and fish-based dishes. How- yeasts (Bousmaha and others 2006). However, a recent study on
ever, they are available at affordable price only during winter and such a cured lemon called “msayer or msir” in Morocco showed
spring seasons when ripening. Therefore, many traditional preser- that yeast, represented by Candida parapsislosis and unclassified
62 Comprehensive Reviews in Food Science and Food Safety r Vol. 12, 2013
c 2012 Institute of Food Technologists®
Safety of North African traditional foods . . .
90%
110%
Battter
S
Stuffing intoo natural casiing
( bovine intesstine)
Staffed caasing:
Raw sausages
Sujuk
Figure 6–A schematic presentation for sujuk making as described by FAO (1982).
∗ The fat is preferably taken from lamb tail to give sujuk a typical pleasant taste.
saccharomycetales, is the predominating microbial group, while ecological parameters during fermentation and storage should be
LAB are only weakly represented during the early steps of curing, set to promote the lactic acid fermentation, and hence, the growth
and were not detected in the finished product (Aayah and others of LAB (Niketić-Aleksić and others 1973; Peres and others 2012).
2010). Lemon when pickled may be stored for more than a year Typically, this procedure involves the preparation of vegetables by
at room temperature and can be used in various ways as whole sorting, washing, and occasionally slicing. After this preparation
or chopped in small pieces. In some instances, only the peel is step, the vegetables are submerged with the appropriate brine
used. Another type of pickled lemon widely consumed in North solution in a glass container, which is then tightly sealed and left
Africa, mainly of the Mashreq countries (Libya and Egypt), is the in a cool place to allow for fermentation. A recent modification
“lamoun makbouss.” Thoroughly washed lemons are thinly sliced, of this technique consists in adding vinegar to the brine to ensure
copiously sprinkled with salt, and left to mature on a plate for 24 successful fermentation, especially when low-salt brine is used.
h. At this stage, the lemon slices become soft and their bitterness Lowering the initial pH, along with the moderate salinity, helps
is reduced, they are then placed in layers in a clear jar while sprin- the LAB predominate over the other microbial groups from the
kling paprika between the layers. Flavored seed oil (preferred to early crucial steps of fermentation when the microbial population
olive oil with too strong aroma) is added to cover the slices in the is the most complex, thereby ensuring the safety while extending
container that is then tightly closed and left at room temperature the shelf life of the final product.
for at least 3 wk (Roden 1974).
c 2012 Institute of Food Technologists® Vol. 12, 2013 r Comprehensive Reviews in Food Science and Food Safety 63
Safety of North African traditional foods . . .
Table 4–Traditional meat food products of North African countries: technology and main physicochemical characteristics.
Table 5– Production (1000 tons) and apparent per capita consumption drying due to its convenience (Figure 10a). When spread on the
(kg/capita/year) of fruits and vegetables in 2005 in North African coun- floor/roof or any kind of surface, the fruits should be spaced about
tries (FAOSTAT 2012). Data of China are given for comparison.
2 cm from each other to allow good aeration and water evapora-
Country Production Consumption tion. In some Moroccan regions, grapes are pretreated by dipping
Fruits Vegetables Fruits Vegetables for a few minutes in a sieved solution consisting of a mixture of
Algeria 3,535.544 4,535.92 63.72 119.02 ash from incinerated fava bean stems, quicklime, and salt in water.
Egypt 9,581.15 19,516.40 99.87 203.13 Such treatment is believed to prevent alterations due to fermen-
Libya 386.05 948.35 66.23 203.03 tation, rot, or mold growth during drying or storage (Mazhour
Morocco 3,292.41 5,487.02 69.68 136.44
Tunisia 1,254.78 2,675.93 87.46 216.14 1983). Figs are usually dried as a whole fruit, but in some instances,
China 122,184.94 473,062.94 64.42 279.89 they are cut open and sprinkled with finely ground herbs such as
thyme, rosemary, or pennyroyal, before drying. This procedure
is especially used when the dry figs are intended for home con-
Fruits sumption or sale in neighboring rural markets, as they cannot be
Traditional techniques, especially sun-dying, have long been preserved for more than 3 mo (Figure 10b). This product is essen-
used in North African countries to preserve some highly perish- tially known in the Jbala and Tizi-Ouzou regions of Morocco and
able fruits such as figs, grapes, and prickly pears. These fruits are Algeria, respectively, where it is called shreeha. While raisins
produced for a few weeks during summer or autumn seasons and (zabib) obtained from dried grapes are consumed directly or
should be consumed as quickly as possible after harvest, as is the utilized in various culinary preparations (pastries, dishes, appe-
case for figs, which should be consumed the same day. In this pe- tizers, and so on), dried figs are consumed as such, especially
riod of the year, the weather conditions are optimal for the drying during Ramadan (the fasting month for Muslims) with soup.
operation; the temperature averages 25 to 30 ◦ C and the air is Drying of prickly pears is conducted in a similar manner after
generally dry. Such conditions have, indeed, been reported to give removing the peel; however, it is a rare practice and is restricted
the best-quality sun-dried fruits (Tang and Yang 2004). Upon full to only a small number of villages in remote areas in Morocco
maturation, fruits are evenly spread over the floor of open space and Tunisia (Mazhour 1983). Likewise, the most available raisins
(threshing) or a cottage roof coated with a plastic or straw mat, in North African markets are those obtained in modern facto-
large foliage such as that of fig, grape, or carob leaves may be ries using industrial dryers and chemical additives such as sulfur
used. Recently, a mesh wire has been preferred as a mat for fig dioxide.
64 Comprehensive Reviews in Food Science and Food Safety r Vol. 12, 2013
c 2012 Institute of Food Technologists®
Safety of North African traditional foods . . .
c 2012 Institute of Food Technologists® Vol. 12, 2013 r Comprehensive Reviews in Food Science and Food Safety 65
Safety of North African traditional foods . . .
Olive preparation
• Sorting
ti
Sorteed clean olivves
• Slightly crushing olives with a stone
• Prrickling each olive severral times
Oli
with a fork, orr
• Cu utting each oolive with 1 to 3 deep
traansverse slitts
njured olives
In
Debettering
g
• Daily replaceement of the brine
with a freshlyy prepared one during
12 days
Brining/Fermentation
• Promoting anaeerobiosis:
-Addition of a n olive oil layer (about
Conditions that favor the 1 cm thick) o n the top off the brine
growth of mesophilic -Tightly sealiing the container
lacitic acid bacteria -Placing the c ontainer at a cool
temperature (about 15-20°C)
ves:
Pickled oliv
• Ready for consumption (20-30 days
d of fermeentation)
• Optim
mal taste after 3 months of fermentation
Figure 8–Flow diagram of traditional pickling of olives as practiced in North African countries.
microorganisms. To circumvent such a limitation and enhance the salt concentration to some traditional dairy products, such as the
safety and keeping quality of North African traditional dairy prod- Moroccan smen, has also been practiced empirically to add a safety
ucts, other hurdles to microbial growth including salting and/or factor and to avoid surface spoilage with molds, as these plants are
drying (low aw ) or heating have often been combined with lactic well known for their potent antifungal activities (Cowan 1999;
acid fermentation. Examples of such products are the Moroccan- Hammer and others 1999; Chebli and others 2003; Rota and oth-
brined cheese jben malah (matured and stored in saturated brine), ers 2004; Amarti and others 2008). In spite of these treatments,
Egyptian domiati and tallaga cheeses (5% to 10% salt content pathogenic bacteria and molds have been detected in virtually all
and stored in brine), dried kishk, and Algerian aoules obtained North African traditional dairy products, and some of these bacte-
from spontaneous acidification of milk followed by heat treatment ria would grow and produce highly toxic metabolites under certain
and sun-drying. The pH of these products is as low as 3.5 and conditions. Survival of raw milk pathogens to the processing steps
their dry matter increases to levels as high as 90% to 92%, corre- or contaminations due to the lack of good manufacture practices
sponding to water activity (aw ) values of 0.34 to 0.43 where mi- (GMPs) and personal hygiene, or improper storage conditions,
croorganisms can no longer survive (Steinkraus 1983; FAO 1990; are the most frequent causes for the presence of undesirable mi-
Tamime and McNulty 1999; Mennane and others 2007). Addition croorganisms in finished products. Moreover, the poor sanitary
of aromatic plants (thyme, oregano, and rosemary) along with high conditions during milking and the lack of veterinary care for
66 Comprehensive Reviews in Food Science and Food Safety r Vol. 12, 2013
c 2012 Institute of Food Technologists®
Safety of North African traditional foods . . .
Figure 9–Selected fermented vegetables of North African countries; (a) pickled green olives; (b) dry-salted fermented black olives; (c) dry-salted
“Moroccan style” lemon; (d) North African “lamoun makbouss”; (e)-various pickled garden vegetables in glass containers; (f) Harissa (solid arrow) and
olives seasoned with harissa (dashed arrow).
traditional small herders (the prevailing management system of isolated from raw milk in North African countries (Hamama 1992;
husbandry in North Africa), in addition to the low hygienic El Marrakchi and others 1993; WHO 1994; Cosivi and oth-
quality of water, contribute to produce raw milk of poor mi- ers 1998; Benkerroum and others 2004b; Bendahou and others
crobiological quality. Regardless of the type of domestic milk 2008). Therefore, the frequent presence of pathogens in fermented
animal (cow, sheep, goat, buffalo, and camel), the total viable milks or cheeses obtained from such raw milk is not surprising.
counts usually exceed 106 CFU/mL and the counts of fecal indi- When raw milk is heavily contaminated and the technological pro-
cators (coliform and enterococci) are higher than 104 CFU/mL cesses are carried out under poor sanitary conditions, as is usually
(Hamama 1992; Benkerroum and others 2003a; El-Diasty and the case in North African dairy farms, natural hurdles to micro-
El-Kaseh 2007). Moreover, foodborne pathogens of major con- bial growth are a limited safety factor (Benkerroum and Tamime
cern in food safety such as Listeria monocytogenes, Mycobacterium 2004).
bovis, Mycobacterium tuberculosis, enterohemorrhagic Escherichia coli, Another issue of concern related to North African traditional
Staphylococcus aureus, and Campylobacter jejuni have frequently been dairy products is the presence of enterococci at high levels, usually
c 2012 Institute of Food Technologists® Vol. 12, 2013 r Comprehensive Reviews in Food Science and Food Safety 67
Safety of North African traditional foods . . .
Figure 10–Figs being dried on a roof covered with a mesh wire (a) and 3 types of dried figs: (b) cut open dried fig, (c) figs dried as whole, pricked from
the center and put together in the form of beads with a string, and (d) whole dried figs packaged in bulk.
exceeding 104 CFU/mL, with Enterococcus faecalis and foecium as the for various viruses, protozoa, and parasites), this issue warrants due
predominating species (Benkerroum and others 1984; Tantaoui- attention from all stakeholders and scientists.
Elaraki and El Marrakchi 1987; Benkerroum and Tamime 2004). The presence of mycotoxins in traditional North African dairy
The presence of this group of microorganisms in fermented foods products also raises an increasingly alarming concern regarding
is, in fact, controversial. Although members of Enterococcus genus public health safety. It is well established that mycotoxins may
have been shown to possess highly desirable technological and contaminate dairy products by molds growing on them under cer-
health promoting properties (Bertolami and Farnworth 2003; Be- tain conditions, or by the carryover of mycotoxins occurring in
lamri and Benkerroum 2005; Pollmann and others 2005; Moreno animal feedstuffs ingested by dairy animals and later transferred
and others 2006; Zeyner and Boldt 2006), their association with from blood into milk (van Egmond 1983; Veldman and oth-
food spoilage (Franz and others 1999), food intoxication (Giraffa ers 1992; Galvano and others 1996; Zinedine and others 2006;
and others 1997; Gardini and others 2001), nosocomial infections Masoero and others 2007). The most important of such myco-
(Kayser 2003), and spreading of antibiotic resistance through the toxins to dairy products is aflatoxin M1 (AM1) derived from the
food chain (Valenzuela and others 2008) has also been well doc- conversion of ingested aflatoxin G1 in the animal liver (Tantaoui-
umented. In a survey on risk factors in enterococcal strains iso- Elaraki and Khabbazi 1984). AM1 was detected at concentrations
lated from Moroccan dairy products, Valenzuela and others (2008) ranging between 4.0 and 6.0 µg/L in 12.5% of Libyan raw milk
revealed the widespread multiantibiotic resistance and/or occur- (El-Diasty and El-Kaseh 2007). In a study on the occurrence of
rence of virulence factors (sex pheromones, collagen adhesins, en- AM1 in raw milk marketed in different cities of Libya, Elgerbi
terococcal endocarditis antigen, and enterococcal surface proteins) and others (2004) showed that 35 samples of raw bovine milk out
among the isolates of Ent. faecalis and Ent. faecium (Valenzuela and of a total of 49 (71.7%) tested positive for AM1, with average
others 2008). According to these authors, high counts of entero- concentrations varying between 0.12 and 0.72 µg/L depending
cocci represent a risk factor in Moroccan foods, and appropriate on the city from which the samples were taken; 34 among the
measures should be taken to reduce their incidence. 35 positive samples (about 97%) were contaminated with levels
In addition to food safety concerns related to bacteria and fungi, exceeding the maximum tolerable level (MLT) of 0.05 µg/L (El-
the presence of viruses, parasites, and protozoa in North African gerbi and others 2004). Higher concentrations (average of 6.3
traditional dairy products may also represent serious hazards to µg/L) were reported in Egyptian raw bovine milk (El-Sayed and
consumers, which has so far been disregarded or overlooked. The others 2000). Such levels of contamination with AM1 are alarm-
occurrence of the latter microorganisms in North African raw ing in view of the MLT which should be less than 0.05 µg/kg or
milk has been repeatedly demonstrated (Carter 2005; Dawson L, depending on the country and commodity (Dohlman 2003). In
2005; Pollmann and others 2005) and is of paramount importance Moroccan pasteurized milk, AM1 was detected at high frequencies
to the safety of dairy products, especially when no heat treatment (88.8%), but at relatively low concentrations compared to those
is applied during processing or at point of consumption. In view found in Libyan and Egyptian milks; the concentrations reported
of the high incidence of zoonotic diseases in North African herds ranged between 0.001 and 0.117, with an average of 0.018 µg/L,
(Araba and Essalhi 2007; Berrag and others 2009; Bouzid and and 7.4% of the samples contained higher levels than the MTL
others 2010) especially with the lack of veterinary care in small (Zinedine and others 2007a; Zinedine and Mañes 2009). Accord-
farms and the poor hygienic quality of water (the probable vehicle ing to Tantaoui-Elaraki and Khabbazi (1984), AM1 concentration
68 Comprehensive Reviews in Food Science and Food Safety r Vol. 12, 2013
c 2012 Institute of Food Technologists®
Safety of North African traditional foods . . .
Table 6–Hazards of microbiological (pathogens and/or their toxins) associated with North African traditional food products.
in raw milk increased by 3.2- to 3.7-fold in cheeses made from that there is no correlation between the levels of mycotoxins in
contaminated milk, as neither heat treatment nor the subsequent the cheeses samples analyzed in the latter studies and those deter-
steps in cheese making (curd drainage, handling, and maturation) mined in the raw milk, as all the samples were taken at random
removed much of the toxin initially present in the milk. It could from local markets. In a more relevant study, Hassanin (2006) has
be anticipated, on this basis, that levels of AM1 in cheeses obtained monitored the level of AM1 in yogurt, yogurt-cheese, and acidi-
from contaminated milk would exceed the MTL even when the fied milk produced from a naturally contaminated milk with AM1.
initial level of AM1 in raw milk is below this value. However, a The results revealed that the concentration of AM1 significantly
survey on the occurrence of AM1, aflatoxin B1 (AB1), and afla- decreases as a function of time during storage at refrigeration tem-
toxin G1 (AG1) in Egyptian dairy products revealed that AM1 perature, which was explained by the interference of LAB with
was detected in raw milk more frequently and in more elevated mycotoxin activity. Many studies have shown that LAB are able to
amounts than in different cheese varieties or in dried milk; AM1 sequester, or inhibit, the in situ production or toxicity of mycotox-
concentrations of 6.3, 5.0, 6.0, and 0.5 µg/L or kg were detected ins, thereby reducing their potential risk in fermented milks and
in raw milk, dried milk, hard cheese, and soft cheese, respectively, cheeses (Gourama and Bullerman 1995; Kim 2007; Bianchini and
whereas AB1 and AG1 were detected in hard cheese at concentra- Bullerman 2009). Dairy lactic acid bacteria belonging to differ-
tions of 3 and 6 µg/kg, respectively (El-Sayed and others 2000). ent genera have been reported to be effective in removing AB1
Similarly, the average concentrations of AM1 in Libyan white soft and AM1 (El-Nezami and others 1998; Oatley and others 2000;
cheeses (from 0.21 to 0.34 µg/kg) were lower than those de- Pierides and others 2000). Nonetheless, further studies are needed
termined in raw milk; yet, 15 cheese samples out of 20 (75%) to accurately estimate the concentrations of mycotoxins and mon-
tested positive for AM1 and contained concentrations exceeding itor their fate during processing and/or storage in different tra-
the MTL (Elgerbi and others 2004). It could be argued, however, ditional North African dairy products obtained from the milk of
c 2012 Institute of Food Technologists® Vol. 12, 2013 r Comprehensive Reviews in Food Science and Food Safety 69
Safety of North African traditional foods . . .
Table 7–Average microbial counts (log CFU/g) in different meat and offal the water activity to levels below 0.86 where no pathogenic bac-
samples in 2 major Moroccan cities. teria would grow (Jay 1986; Barbosa-Cánovas and others 2003),
Casablanca∗ spices inhibit specific microorganisms including bacteria, molds,
Fez∗∗
Microorganisms Beef Lamb Heart Liver Ground beef protozoa, and viruses (Farag and others 1989; El-Khateib 1997;
TAC 7.3 6.7 6.4 7.5 6.1 Cowan 1999; Daferera and others 2000). In addition, a decrease
Coliforms 3.7 3.7 3.3 3.8 4.8 in the pH to about 5.5 at the first phase of maturation, while not
E. coli 3.2 3.2 1.8 3.4 3.9 efficient by itself to inhibit many pathogens, stimulates the gro-
Staph. aureus 2.3 2.8 3.1 2.0 2.3
Cl. perfringens 1.3 1.2 1.2 1.8 NA wth of LAB, which, in turn, will further inhibit undesirable mi-
SRC NA NA NA NA 1.5 croorganisms through antibiosis interactions. In this regard, the
∗ (Cohen and others 2006). wide occurrence of bacteriocin-producing enterococci has been
∗∗ (Oumokhtar and others 2008).
TAC: Total aerobic counts.
reported in Tunisian gueddid (Ben Belgacem and others 2008),
NA: Not available.
SRC: Sulfite-reducing clostridia.
and the protective effect of bacteriocins in meat systems has been
demonstrated (Benkerroum and others 2003b, 2005). In addition
to these conditions, some traditional North African meat products,
different animal species. Such studies are crucial to characterize such as the Moroccan khlii and Libyan ban-shems, the cooking
the risk and estimate the dose/response in a risk-assessment pro- during processing inactivates microbial pathogens or toxins that
cess, the cornerstone in any future regulatory or control measure may be present on the meat or offal used for their preparation.
related to food safety worldwide. Although there is a lack of scientific data regarding the hygienic
quality of North African traditional meat products and epidemi-
Meat products ological studies on their involvement in food outbreaks, it could
The overall safety of meat products is contingent on many factors be anticipated that they may compromise food safety as suggested
including the initial quality of meat and ingredients, the sanitary by the widespread occurrence of pathogens in North African tra-
conditions during handling, processing, and storage, as well as the ditional meat products (Table 6), and also for the main reasons
preservation hurdles used. Raw and offal meat used to produce below:
North African traditional meat products is generally heavily con- r Lack or inappropriate veterinary care in the farms where
taminated with microorganisms of hygienic significance. In this meat-production animals are raised; a weak prophylactic pro-
regard, a study conducted by Cohen and others (2006) on beef, gram and inadequate treatment of diagnosed bacterial infec-
lamb, and beef-offal marketed in the city of Casablanca (Mo- tions or parasitic infestations (Berrag and others 2009).
rocco) has shown that these products were highly contaminated; r Slaughtering, carcass dressing, evisceration, and meat cutting
and pathogenic staphylococci and Cl. perfringens were detected at are generally done in poor sanitary conditions which, com-
relatively high counts (Table 7). A similar study on ground beef bined with the nonrigorous or absent (farm-slaughtering)
marketed in the city of Fez (Morocco), carried out by Oumokhtar veterinary inspection at slaughter, strongly suggest that meat
and others (2008) also demonstrated the poor sanitary quality of or offal deriving from animals infected with virulent bacteria,
the product (Tables 7), with more than 80% of the analyzed samples viruses, or parasites would be used to manufacture traditional
not meeting the Moroccan regulatory standards for meat products meat products.
([Link] In the latter r Production of traditional meat products in small farms,
study, Salmonella sp. and Shigella were detected in a 25 g sample butcheries, or food shops where the sanitary conditions are
at the respective frequencies of 17.5% and 2.5%. Furthermore, usually not appropriate, and none of the GMP, good hygiene
pathogens such as enterohemorrhagic E. coli, Yersinia enterocolitica, practice (GHP), or hazard analysis and critical control point
L. monocytogenes, and Salmonella spp. have been repeatedly isolated (HACCP) program is implemented.
from meat samples in Morocco and other North African coun- r Inadequate conditioning, packaging, and storage conditions.
tries (Karib and others 1994; Ettriqui and others 1995; Abdul- Yet, efforts in packaging are being increasingly made as part
Raouf and others 1996; Al-Gallas and others 2002; Khosrof Ben of a marketing approach.
Jaafar and others 2002; Benkerroum and others 2004b). Oc- In fact, it is well established that these are the main factors that
currence of parasites (protozoa and helminthes) of the genera impact the safety and keeping quality of the finished meat prod-
Toxoplasma, Sarcocystis, Cryptosporidium, Fasciola, Flatworms, Tape- ucts, and failure to address any of them properly will invariably
worm, and roudwarms in meat and offal is also well documented result in a meat product of high risk to consumers. Nonetheless,
(Sawadogo and others 2005; Valinezhad and others 2008; Abdel- on the basis of moisture content, North African traditional meat
Ghaffar and others 2009; Berrag and others 2009). Given the poor products may be divided into 3 groups as defined by Marshall
hygienic quality of raw meat, traditional technologies in develop- and Bal’a (1998) and Leistner (2000b), each of which present a
ing countries use more than one hurdle, acting in synergy, to different pattern of health risks to consumers from the microbio-
ensure a relatively satisfactory degree of hygienic quality. Indeed, logical standpoint: (i) dry meat products (less than 15% moisture)
almost all the traditional technologies for meat transformation in such as gueddid, kurdass, khlii, and ban-shems, (ii) intermediate-
North African countries combine salting, herb and spice addition, moisture meat products (15% to 20% moisture or an aw of 0.65 to
drying, and, occasionally, cooking, especially when long shelf life 0.90) typically represented by pastirma and certain types of sujuk
and a high degree of safety are sought. Less stringent conditions (Table 4), and (iii) fresh meat products (>20% moisture) including
are used when a product is not intended for an extended preser- merguez, mkila, tehal, and some types of sujuk where no or par-
vation period and is cooked before consumption, as is the case for tial drying is applied during processing. Due to their low moisture
merguez and tehal. In cured and fermented meat products, such and/or high salt contents, the first 2 groups are generally regarded
as sujuk, gueddid, kourdass, and pastirma, salting, drying, and as microbiologically safe, and they may be consumed as such or
herb and spice adjunction are the main parameters used to en- after being lightly cooked; these include khlii, some sujuk types,
sure their safety and stability. While salting and/or drying reduce and pastirma. Such an assumption has been substantiated by some
70 Comprehensive Reviews in Food Science and Food Safety r Vol. 12, 2013
c 2012 Institute of Food Technologists®
Safety of North African traditional foods . . .
studies, showing that the overall microbiological counts are either Mycotoxins are contaminants of microbial origin, which also
low or dominated by beneficial LAB and that some foodborne raise concern about the safety of meat products. The presence
pathogens do not grow or survive in these products (El-Khateib of molds in meat and meat products is well documented, and
1997; Bennani and others 2000; Huang and Nip 2001; Kalalou under certain conditions, they may grow and produce mycotox-
and others 2003). El-Khateib (1997) showed that the numbers of ins (Sweeney and Dobson 1998). Molds usually grow on dry or
Enterobacteriaceae, and yeasts and molds were less than 100 CFU/g intermediate-moisture meat products during the first days of dry-
in 50 samples of Egyptian pastirma, which were also free from ing, especially if the drying process is slow or the relative humidity
Salmonella. The absence of Salmonella was explained by the in- in the atmosphere is high. They may also grow in the finished
hibitory effect of the spice paste used to cover pastirma, as has product if the storage conditions are not adequate. However, this
been demonstrated in vitro (El-Khateib 1997). The same study growth is usually considered by the producers only as a harmless
showed that the total aerobic count (TAC) and the Lactobacillaceae surface discoloration and is then removed by brushing the sausages
ranged between 1×104 and 9×106 CFU/g, suggesting that LAB or cleaning them with a wet cloth to avoid wasting meat. Yet, such
are the main responsible for the evolution of the product during growth may represent a serious risk factor if the contaminating
ripening, which represents a good indication regarding the safety molds are toxinogenic. A study on the mycology of pastirma has
of the product. In addition to the antimicrobial effect of the cover revealed the predominance of species belonging to Penicillium and
paste, inhibition of pathogenic bacteria in pastirma was suggested Aspergillus genera (Abdel-Rahman and others 1984). These genera
to be due to the combined effect of water loss and salt con- are well known for their ability to produce mycotoxins (Sweeney
tent (4.5% to 6%) with the consequent decrease in water activity and Dobson 1998). A study on Egyptian pastirma showed that the
(Leistner 2000a; Bechtel 2001). In effect, challenge studies be- numbers of molds varied from 103 to 106 CFU/g in summer and
tween an E. coli O157 : H7 strain and protective cultures of Lb. from 102 to 105 CFU/g in winter, and that Aspergillus, Penicillium,
sakei and Staph. xylosus in pastirma have demonstrated that the Mucor, Rhizopus, Fusarium, and Cladosporium were the predominat-
most significant reduction in the counts of the pathogen was ing genera in the product (Refai and others 2004). In addition, the
recorded after the drying step regardless of whether or not the spices used in the preparation of North African traditional meat
protective cultures were present (Aksu and others 2008). Similar products are usually contaminated with variable levels of mycotox-
results were reported for Moroccan gueddid where numbers of ins and are thus potential sources for the contamination of these
TAC, coliforms, and staphylococci showed a dramatic decrease products. Aflatoxins were determined in the pastirma spice paste
after the maturation step to reach an undetectable level in a 1 and its constitutive spices individually; the contamination level
g sample for coliforms and staphylococci, and about 40 CFU/g of the spice paste varied from 9.6 to 120 µg/kg, and in pepper
for TAC (Kalalou and others 2003). According to their study, (285.6 µg/kg), garlic (224.4 µg/kg), fenugreek (194.2 µg/kg),
the sharp decrease in the microbial counts paralleled the decrease coriander (166.4 µg/kg), and capsicum (42.4 µg/kg) (Refai and
in water activity (aw ) to a final value of 0.66. Furthermore, nei- others 2004). These concentrations largely exceed the maximum
ther Salmonella nor clostridia were detected in laboratory-made tolerable limit of aflatoxin B1 in spices (5.0 µg/kg) according to
or commercial gueddid samples (Bennani and others 1995; Ben- the European regulations (Zinedine and Mañes 2009). Therefore,
nani and others 2000). However, despite such reassuring data, it might be anticipated that pastirma and related North African
though partial and fragmentary, there is no absolute guarantee for traditional meat products represent a serious health risk factor as-
the safety of these products. Indeed, the related salted-dried jerky sociated with the consumption of these products. Pastirma was,
meat prepared in a similar manner and having a water activity indeed, reported to contain aflatoxins at levels varying from 2.8 to
value as low as 0.3 has repeatedly been associated with a num- 47 µg/kg (Refai and others 2004).
ber of Salmonella and Staph. aureus outbreaks in the U.S.A. (CDC
1995; Eidson and others 2000; Smelser 2004; Allen and others Vegetable products
2007). Nonetheless, it could be assumed that the marinated vari- Fruits and vegetables are contaminated by a wide variety of
ant of gueddid would be microbiologically safer than the classical microorganisms including bacteria, fungi, viruses, and protozoa
type. The application of acid marinade to meat before drying has of different origins. These contaminations may occur in the
been shown to enhance significantly the microbiological quality of field (soil, manure, compost, wastewater sludge, irrigation wa-
the final product (Nummer and others 2004). On the other hand, ter, equipment, workers, animals, and so on), during posthar-
North African traditional fresh meat products are usually heavily vest operations (conditioning, packaging, and distribution), or
contaminated with microorganisms of health and spoilage signifi- at the household prior to consumption (Burnett and Beuchat
cance; they thus present a higher risk to consumers than their dry 2001; Matthews 2006). Therefore, microorganisms initially present
or intermediate-moisture counterparts. However, such risk may in fruits and vegetables are highly variable in numbers and in
be reduced at consumption, as these products are cooked or grilled nature, and are generally predominated by saprophytic bacte-
before consumption. In this regard, a study on the microbiology ria and molds, considered as the resident microflora, that do
of different Egyptian fresh sausages showed that the aerobic plate not raise serious health concerns (Jay 1986; Badosa and others
count (APC) and Enterobacteriaceae counts ranged from 1.1×104 to 2000). Nonetheless, fruits and vegetables have extensively been
1×108 and from 1×102 to 1×107 CFU/g, respectively, and Cl. shown to be contaminated with a variety of pathogenic bacteria,
perfringens and coagulase-positive Staph. aureus were detected at the protozoa, and viruses (Beuchat 1998; Badosa and others 2000;
respective frequencies of 26% and 29% (El-Khateib 1997). More- Robertson and Gjerde 2000; Buck and others 2003; Bhagwat
over, in a study on the incidence of shiga toxin-producing E. coli 2006; Matthews 2006), which is regarded as a risk factor for
O157 in Moroccan meat products, the pathogen was detected in public health. Indeed, the increase in consumption of fruit and
20% of the spiced ground meat normally used in merguez prepa- vegetable that has been recorded worldwide in the last 2 decades
ration, but not in merguez sausages; such a discrepancy could be has been paralleled by an increase in foodborne disease outbreaks
explained by the sampling procedure and the limited number of attributed to fresh produce (Beuchat 1996; Tauxe and others 1997;
samples studied (Benkerroum and others 2004b). Buck and others 2003). This was corroborated by the association
c 2012 Institute of Food Technologists® Vol. 12, 2013 r Comprehensive Reviews in Food Science and Food Safety 71
Safety of North African traditional foods . . .
of a number of fruits and vegetables from around the world with ciently treated wastewater (Ghazy and others 2009); therefore,
gastroenteritis outbreaks (Buck and others 2003; Matthews 2006), large amounts of wastewater and sewage sludge are used to irrigate
most of which were of bacterial origin, with Salmonella and E. and fertilize fruit orchards and vegetables in the country. The use
coli O157 : H7 as the primary etiological agents (Heaton and Jones of raw wastewater in agricultural activities has been demonstrated
2008). On the other hand, some microbial groups among the resi- to increase the potential of the resulting crops to spread bacterial
dent microflora play a key role in the transformation of vegetables or parasitic diseases (Ait Melloul and Hassani 1999; Ait Melloul
into more stable, safe, and palatable products when fresh produce and others 2002). A bacteriological analysis of various vegetables
is preserved for consumption out of season. Among the bene- obtained from several wastewater-irrigated agricultural regions in
ficial of these epiphytic microorganisms in fruits and vegetables, Morocco showed high counts of TAC (>9 log10 CFU/g) and fecal
LAB, and to a lesser extent yeasts, are responsible for sponta- indicators (total-coliforms, fecal-coliforms, and enterococci)(>5
neous fermentation of a number of vegetable products such as log10 CFU/g), suggesting that the consumption of these vegeta-
olives and various vegetables. Natural fermentation has long been bles put consumers at high risk (Ibenyassine and others 2007). The
used on an empirical basis in the preservation of vegetable prod- same study showed that opportunistic Gram-negative pathogens of
ucts, and in particular, in the case of olives, it is even necessary the Enterobacteriaceae family (Citrobacter freundii, Enterobacter cloacae,
to make the fruit edible. In fact, natural olive fermentation ful- E. coli, Klebsiella pneumoniae, and Serratia liquefaciens) were detected
fills 2 main objectives: (i) inhibition of microorganisms of health in the studied vegetables at frequencies varying from 11% to 28%,
and spoilage significance, thereby reducing health risks and prod- with Enterobacter sakazakii (12%) and Salmonella arizona (0.7%) be-
uct losses, and (ii) making olives palatable, essentially by removal of ing the pathogens of the most concern to the safety of these crops.
the bitter glycoside euloropein, production of various aroma com- Moreover, in a Moroccan region (Al Haouzia, Marrakech) where
pounds, and softening, to some degree, the flesh of the fruit during untreated wastewater spreading is widely practiced for the produc-
fermentation. tion of vegetables such as lettuce, tomatoes, parsley, and potatoes,
As mentioned earlier, vegetable products are traditionally pre- as well as cereals, the prevalence of Salmonella infection (32.56%)
served in the North African region by lactic acid fermentation in the community living in the region and consuming locally pro-
combined with salting (dry salt or brine), direct acidification (ad- duced crops has been shown to be significantly higher than that
dition of vinegar) or, in few instances, by sun-drying. Conversely, recorded in a control region where no wastewater spreading is
fruits such as grapes, figs, and prickly pears are essentially dried, practiced (1.14%). Another study carried out in the same region
as the loss of moisture combined with the consequent increase in revealed that the prevalence of protozoan infections (giardiasis and
sugar concentration in the fruit results in a sharp decrease in water amebiasis) among children of the wastewater-irrigated region was
activity, thereby restricting the growth of spoilage and pathogenic significantly higher (72%) than that recorded in the control area
microorganisms. The high diversity of North African traditional (45%) (Ait Melloul and others 2002).
vegetable products and the raw material from which they derive, Traditional food products of plant origin in North African
in addition to the variability in the technological processes and the countries are generally obtained from locally produced crops with
sanitary conditions used for their manufacture, make the micro- inconsistent sanitary quality. Therefore, the safety of finished prod-
biological characteristics of the finished products and related risk ucts is largely dependent on the efficacy of natural hurdles to in-
factors also variable. Nonetheless, the fruits and vegetables eaten hibit or inactivate undesirable microorganisms initially present in
raw or after being transformed by traditional technologies are re- the raw material. Olives are the most important vegetable prod-
garded as safe and wholesome for most North African consumers. ucts that are transformed by traditional technologies in North
Yet, this presumed safety has not been substantiated by microbio- African countries; they are either brined (green olives) or dry-
logical and epidemiological studies, a situation that reflects the lack salted (black ripe olives). In both cases, they undergo spontaneous
of awareness of the health risks associated with the consumption lactic acid fermentation, although in the latter case, the fermen-
of vegetable products in these countries. Furthermore, because of tation is greatly retarded by the high salt concentrations used for
the lack of foodborne disease investigations and surveillance, most their preservation (8 to 14 g salt per 100 g olives). Other vegetables
disease outbreaks related to the consumption of vegetable prod- such as peppers, onions, carrots, string beans, chili, and cauliflower
ucts remain undetected and insufficiently reported in the scientific are either brined in a similar manner as for green olives (Steinkraus
literature. Also, the level of contamination and the incidence of 1983) or salted and “packed” into an acid solution (usually vine-
pathogenic microorganisms of/in fruits and vegetables are antici- gar) of a pH value below 3.0 as unfermented (fresh-pack) pickles.
pated to be higher in North African countries than in developed In the fresh-pack pickles, the raw material is usually heated or
countries. The lack of implementation of quality assurance pro- soaked in hot water for few minutes to reduce the overall mi-
grams including GAP, GMP, and HACCP throughout the entire crobial load of the product before pickling. Therefore, it would
production and distribution chain (pre- and postharvest, trans- be reasonable to expect that these unfermented pickles do not
portation, handling, and so on) increases the health risk associated raise serious health concerns essentially due to the low pH of the
with the consumption of such products. The risk is even greater brine in addition to the heat treatment where microbial growth
as untreated urban wastewater and sewage sludge or manure con- is very unlikely to occur (Gómez and others 2006). They would
tinue to be used for irrigation or fertilization (Bazza 2003; Ghazy therefore be categorized as low-risk vegetable foods. Conversely,
and others 2009). This practice, though recognized to be illegal, in fermented vegetable products, faulty fermentation is not un-
is tolerated by regulatory authorities in North African countries, common and pathogenic microorganisms may grow or survive
and is widely used. In Morocco, about 70 million m3 of untreated in the finished products (Fleming and others 1985; Caggia and
urban wastewater are used annually to irrigate some 7000 ha of others 2004). In fermented pickled vegetable products, microbial
fruit orchards and vegetables as an alternative fresh water source, competition, acidity, and reduced water activity (high salt content)
and as an easy and economical way for disposing wastewater (Bazza are the main parameters that inhibit undesirable microorganisms
2003; Choukr-Allah 2004). Similarly, the capacity of wastewater- to safeguard the health of consumers. However, the usual salt con-
treatment facilities in Egypt is either short or produces insuffi- centration used in the brine (5 to 7 g salt/100 mL) is not high
72 Comprehensive Reviews in Food Science and Food Safety r Vol. 12, 2013
c 2012 Institute of Food Technologists®
Safety of North African traditional foods . . .
Table 8–Monitoring the counts (logCFU/g) of microbial groups in Algerian fermentation. Euloropein has been shown to inhibit, to different
green olives during fermentation. After Kacem and Karam (2006a). extents, various pathogens including Salmonella typhi, Salmonella
Fermentation Enteritidis, Vibrio parahaemolyticus, Staph. aureus, and Vibrio cholerae
period (days) (Tassou and Nychas 1994; Tassou and Nychas 1995; Bisignano and
Microbial group 15 60 90 others 1999). Among LAB isolated from fermented green olives
Total aerobic count 4.52 7.76 6.88 in North African countries (Table 9) and elsewhere (Fleming and
Coliforms 2.12 2.33 1.96 others 1985), Lb. plantarum has been consistently reported to be
Staphylococci 2.03 2.52 1.35
Lactic acid bacteria 3.8 6.55 6.96 the predominating species throughout the fermentation period
Lactobacilli 3.6 5.55 5.66 (Kacem and others 2004; Chamkha and others 2008); and strains
Yeasts 1.88 3.84 5.98 of this species have extensively been shown to produce bacteriocins
Psychrotrophs 4.22 3.88 1.53
active against Gram-positive and Gram-negative bacteria (Kacem
and others 2004, 2005; Dobson and others 2012). Likewise, yeasts
enough to reduce the water activity to levels that would strongly have been reported to be consistently present at elevated counts
inhibit the growth of undesirable microorganisms. In addition, (> 6 log10 CFU/g) in North African fermented olives (Asehraou
when more than 8% (w/v) of salt is used in the brine, the growth and others 2000; Asehraou and others 2002; Kacem and Karam
of LAB is also retarded significantly and the pH remains relatively 2006a; Hernández and others 2007), and to contribute to their
high at the end of fermentation (about 4.5) (Fernández and others safety. It is indeed well established that yeasts produce aroma
1997), conditions that provide an opportunity for salt-tolerant or compounds including organic acids, diacetyl, ethanol, and other
halophilic pathogens and spoilage microorganisms to grow during metabolites resulting from lipolytic activities that also possess an-
the early stages of fermentation. Staphylococci grow well at salt timicrobial activities, thereby contributing to flavor development
concentrations between 7% and 10% and a low pH of 4.2, and as well as to the safety improvement of foods (Hernández and oth-
other pathogens such as E. coli O157 : H7, L. monocytogenes, and ers 2007; Arroyo-Lopez and others 2008). Furthermore, among
Salmonella spp. have been shown to develop resistance under stress- the major yeast species isolated from fermented olives (Table 9),
ful conditions, including low pH (Gahan and others 1996; Lou and the so-called killer yeasts tend to predominate owing to their
Yousef 1997; Beales 2004; Lee 2004). Therefore, in the fermen- ability to produce a “killer toxin” essentially active against other
tation of green olives, the usual salt concentration used does not competing yeasts (Llorente and others 1997; Asehraou and others
exceed 7 g salt/100 mL brine to allow good growth of fermenta- 2000; Hernández and others 2007; Maqueda and others 2012),
tive LAB. These bacteria, which represent only a small proportion but could also inhibit various pathogenic Gram-positive bacteria
of the initial epiphytic microflora of the product, should rapidly (Izgü and Altinbay 1997). Therefore, killer yeasts would not only
outgrow the competing microbial groups and produce sufficient reduce the incidence of bloater defect (Asehraou and others 2002),
acidity to reach a pH of about 3.5 to 3.8, and then the resulting but also contribute to the enhancement of the safety of finished
product may be considered reasonably safe. products. Nonetheless, the safety of naturally fermented olives may
LAB have been shown to predominate throughout the entire not rely only on the above-mentioned safety factors, as the degree
fermentation period (90 d) in naturally fermented Algerian green of protection they offer vary widely depending on the fermenta-
olives, although yeasts were consistently present at relatively high tion parameters and from a batch to batch (Asehraou and others
counts (3 to 6 log10 CFU/g of olives) as a secondary microflora 2000; Kacem and Karam 2006b). In effect, foodborne pathogens
(Kacem and Karam 2006b). These authors have shown that the of concern to food safety have been isolated or shown to survive
counts of LAB increased steadily since early phases of fermentation from/on Spanish-style green olives or Greek-style black olives
to reach about 7 log10 CFU/mL after 90 d of fermentation. A sig- (Table 6), and cases of botulism and other food poisoning disease
nificant increase in yeast counts has also been noted, starting from due to consumption of fermented green or black olives have been
day 60 of fermentation, in a typical behavior of a secondary fer- reported (Okudaira and others 1962; Pereira and others 2008; Pin-
mentation flora (Fleming and others 1985). Meanwhile, the counts geon and others 2011; Anon 2012). The competitiveness of the
of coliforms, staphylococci, and psychroptrophs were reduced to predominating LAB and yeasts as determined by their ability to
different extents (Table 8). Such a decline may be attributed not produce inhibitory metabolites or competition for nutrients, and
only to the effect of pH and salt content of the Algerian fermented the initial bacteriological quality of olives and brine, in addition to
green olives (Kacem and Karam 2006a), but also to inhibitory the sanitary conditions during manufacture, are the main parame-
substances inherently present in olives or to specific metabolites ters that determine the safety status of traditional fermented olives.
produced by the predominating species of LAB and yeasts during Presently, olives are heat-treated before or after preservation and
Table 9–Predominating species of LAB and yeasts in North African naturally fermented green olives. Data are adapted from the references to present
microbial species representing more than 70% of the total identified isolates.
Microbial group
Country of origin LAB Yeasts Reference
Algeria Lb. casei Sac. cerevisiae Kacem and Karam 2006a
Lb. paracasei Candida parapsilosis
Lb. plantarum
Ent. faecium
Lc. lactis NA Kacem and others 2004
Lb. plantarum
Morocco NA Sac. cerevisiae, Pichia anomala Asehraou and others 2000
Tunisia Lb. plantarum Pichia membranaefaciens Chamkha and others 2008
Lb. collinoides
NA = Not available.
c 2012 Institute of Food Technologists® Vol. 12, 2013 r Comprehensive Reviews in Food Science and Food Safety 73
Safety of North African traditional foods . . .
Table 10–Incidence of mycotoxins (µg/kg) in selected vegetable products in some North African countries.
various chemical food-grade additives such as acids, sorbates, and Among these, the most frequently encountered in North African
benzoates and parabens are added to pickled or dry-salted olives table olives are species of the genera Aspergillus and Penicillium
in North African countries in order to enhance their safety and (Tantaoui-Elaraki and Le Tutour 1985; Gourama and Bullerman
keeping quality. In the market place, the latter products are known 1988; Maouni and others 2002), and the most frequently de-
as “romy,” litrally meaning “coming from Rome” but commonly tected mycotoxins are OTA, citrinin (CIT), and AFB (El Adlouni
used to refer to modern and sophisticated products, as opposed and others 2006; Zinedine and Mañes 2009). Nonetheless, studies
to “baladi/beldi” products (products of the country, in Arabic). have shown that black olives are not good substrates for myco-
It is worth mentioning, in this regard, that the “baladi” prod- toxin production (Gourama and Bullerman 1988; Eltem 1996). In
ucts are the most preferred by consumers though less attractive this regard, Tantaoui-Elaraki and Le Tutour (1985) have demon-
in appearance and their hygienic quality is questionable as com- strated the inability of A. flavus and A. ochraceus to produce de-
pared to the “romy” ones. Further studies should be carried out tectable amounts of mycotoxins in Moroccan table olives, while
on the hygienic quality of different commercial and home-made the same strains had been shown to produce high concentra-
fermented green olives samples, and from different geographical tions of mycotoxins in laboratory media. Similar observation has
locations of North African countries, in order to provide a sound been made by Leontopoulos and others (2003) who have demon-
conclusion regarding sanitary quality of naturally fermented olives strated that a toxinogenic strain of A. parasiticus was unable to
and to allow an accurate assessment of the health risk associated produce AFB1 in damaged black olives originating from Greece.
with their consumption. Particular attention should be given to Similarly, Gourama and Bullerman (1988) showed that A. flavus
the occurrence of Cl. botuminum and its toxin, since this is consid- did not produce AFB1 in pastes made from Moroccan Greek-
ered as one of the most important safety issues in fermented olives style black olives. Furthermore, Eltem (1996) showed that fresh
worldwide, although the occurrence of Cl. botulinum in fermented whole black olives, fresh damaged black olives, and whole black
olives appears to be rare, and only very few outbreak intoxications olive paste inhibited or greatly reduced the production of afla-
due to botulism of type B have been recorded (Pereira and others toxins by toxinogenic strains of A. flavus and A. parasiticus isolated
2008; Anon 2012). In addition, the botulism toxin formation is from naturally fermented black olives. Although these studies con-
unlikely at pH and aw < 4.8 and 0.94, respectively (Odlaug and curred to suggest that olives, especially the black, are not suitable
Pflug 1979; Briozzo and others 1986); values of these parameters substrates for the production of mycotoxins at hazardous levels,
are generally lower in naturally fermented olives. the occurrence of various mycotoxins in table olives in North
In addition to the bacteriological hazards discussed above, my- African countries and elsewhere has extensively been documented
cotoxins represent a major issue regarding the safety of traditional (Table 10). A study carried out by Tantaoui-Elaraki and Le Tutour
vegetable products in North Africa. Among these products, table (1985) revealed the presence of the AFB1 and OTA at appreciable
olives and dry fruits such as figs and raisins have repeatedly been amounts in commercial samples of Moroccan table black olives
reported to be contaminated with various mycotoxins (Table 10). in spite of the fact that these mycotoxins were shown not to be
The high salt contents (5 to 12 g salt/100 g product) in table produced when black olives were artificially contaminated with
olives select for the halophilic or salt-tolerant molds especially, selected strains of toxinogenic molds. Also, a survey carried out by
those of the genera Penicillium and Aspergillus. Similarly, raisins and Zinedine and others (2004) revealed that 36% of Moroccan table
dried figs have been shown to be frequently contaminated with black olives were contaminated with OTA at levels ranging be-
mycotoxin-producing strains of A. flavus and A. niger due to the tween 0.62 and 4.8 µg/kg with an average concentration of 1.43
osmophilic character of these species (Rao and Kalyanasundaram µg/kg. Furthermore, OTA and AFB have been detected in 100%
1983; Pitt and others 2009; Selouane and others 2009). of sampled Moroccan dry-salted olives at levels exceeding 0.65 and
Contamination of table olives with various mycotoxins is well 0.5 µg/kg, respectively (El Adlouni and others 2006). Therefore,
documented, and Greek-style black olives are the most incrimi- the occurrence of toxigenic molds and the frequent detection
nated (Maaroufi and others 1995a; El Adlouni and others 2006). of mycotoxins in traditionally processed black olives rank these
The high salt content (about 7% to 12% g salt/g olive) inhibits products among the commodities of high risk to public health in
the growth of almost all competing bacteria (Asehraou and oth- North African countries. Such a risk is even greater when more
ers 1992; Efstathios 2006), thereby providing an opportunity for than one mycotoxin is present in table olives, as was demonstrated
the salt-tolerant molds to grow and possibly produce mycotoxins. by El Adlouni and others (2006) who showed the concomitant
74 Comprehensive Reviews in Food Science and Food Safety r Vol. 12, 2013
c 2012 Institute of Food Technologists®
Safety of North African traditional foods . . .
presence of OTA, CIT, and AFB in dry-salted commercial Mo- for the tolerable limits of aflatoxins and ochratoxins in foods have
roccan Greek-style black olives. Furthermore, the prevalence of been proposed in some North African countries, but they have
chronic nephropathy diseases in Tunisia has been correlated to the not come into force yet (Zinedine and Mañes 2009). This is essen-
consumption of various foods contaminated with OTA, among tially due to the belief of stakeholders in these countries that the
which black table olives were incriminated, as abnormally high strict implementation of mycotoxin regulations will have limited
levels of this mycotoxin (up to 46.83 mg/kg) were found in this effects in terms of health protection. The prevalence of subsistence
product (Maaroufi and others 1995a, b). farming and the continued practice of traditional technologies for
The decrease in moisture content to about 14% (Canellas and the transformation of food products in poor sanitary conditions
others 1993; Karathanos 1999) and the subsequent increase in will certainly hinder any effort to enforce such regulations. In-
sugar concentration in fruits during drying resulted in an almost deed, the mycotoxin issue in North Africa or other developing
selective medium for xerotolerant molds, among which members countries needs to be viewed in the overall context of local food
of the Aspergillus section Nigri have been shown to predominate. safety, health, and agricultural practice issues.
These black aspergilli are particularly severe and widespread in
grapes of the warmer areas of the Mediterranean basin includ- Prospects for Safety Improvement of Traditional North
ing North African countries (Battilani and others 2008). Strains African Foods: Opportunities and Constraints
of A. niger aggregate and A. carbonarius have been shown to be General context
the main contaminants of Moroccan grapes and to produce high Like most developing countries around the world, those of
amounts of OTA (0.24 and 0.22 µg/g, respectively) at optimal North Africa are at the crossroads between many strategic choices
environmental conditions (Selouane and others 2009). A similar regarding food policies aiming at the improvement of food safety
situation is expected in the other grape-producing North African while adapting to the advent of globalization. Nonetheless, re-
countries including Algeria, Tunisia, and Egypt, despite the lack gardless of the strategy to be adopted, North African countries
of reports, as these countries share the same climatic conditions as should necessarily upgrade the safety of their local foods to take
well as sociocultural conditions. In addition to A. niger aggregate advantage of the opportunities of globalization and to promote the
and A. carbonarius, A. aculeatus has also been found to predominate trading of such foods either internationally or in domestic markets
during the entire drying process of grapes; from the fresh fruits in face of the increasingly competitive global trade. To this end,
to the fully dried raisins (Leong and others 2008). However, this North African countries should take into account, in addition to
study showed that among the 3 fungal species, only A. carbonarius the national constraints, the regional and global economic envi-
was able to produce OTA in vitro as detected by the emission of ronment characterized by a multiplicity of bilateral, multilateral,
fluorescence under UV light upon cultivation on coconut cream subregional, regional, and international agreements. The most sig-
agar plates. The incidence of occurrence of AFs and OTA in Mo- nificant of these agreements are undoubtedly the Sanitary and
roccan commercial raisins and dried figs has been reported to be Phytosanitary (SPS) and Technical Barriers to Trade (TBT) agree-
30% and 65%, respectively, and the levels ranged between 0.03 ments of the World Trade Organization (WTO), which raised
and 1.42 µg/kg, with an average of 0.33 µg/kg in dried figs, and the food safety to the forefront of the international trade require-
between 0.05 and 4.95 µg/kg with an average of 0.96 µg/kg in ments. Moreover, the SPS agreements have recognized the Codex
dried raisins (Zinedine and others 2007b). In Egypt, OTA was de- Alimentarius Commission (CAC) as a key organ for the harmo-
tected in figs at levels varying from 60 to 120 µg/kg, while raisin nization of food standards among member countries to reach the
samples have proven to be free from AFs (B1 , B2 , G1, and G2), WTO objective of market globalization of safe foods. Although
CIT, ochratoxins (OT), patulin (PAT), sterigmatocystin (STG), controversial, it is believed that the application of SPS measures
diacetoxyscirpenol (DAX), T-2 toxin, and zearalenone (ZEA). In and the consequent strengthening of food safety regulations would
another survey on 100 samples for the occurrence of mycotoxins, progressively lead developing countries, including North African
Egyptian raisins were found to be contaminated at very high levels ones, to improve safety and quality control practices in agriculture
of AFB1 (300 µg/kg) and OTA (250 µg/kg), though at the low and food technology. Such improvements would ultimately result
frequencies of 2% and 1%, respectively (Youssef and others 2000). in new forms of competitive benefits for developing countries and
From the above data, it is clear that the occurrence of mycotoxins contribute to more sustainable and profitable trade in the long run
in fruits and vegetables presents a real threat to consumers’ health (FAO 2004). Indeed, the application of GMP and HACCP in the
in these countries, as well as a serious limitation for the export fish industry in Tunisia and Morocco, for example, as mandatory
of local produce toward developed countries, especially the tradi- measures or on a voluntary basis, respectively, has drastically im-
tional economic partners of the European Union (EU) and North proved the safety and quality of fish products, and consequently,
America. The latter countries are in the process of harmonizing their access to importing markets, especially the EU. Also, the
their regulations on mycotoxins in foods and feeds with a clear need for compliance of Moroccan, Tunisian, and Egyptian fruit
tendency to be more restrictive. On the other hand, there are and vegetable exports with the food safety regulations of import-
presently no specific regulations on mycotoxins in North African ing developed countries, such as those of the EU, to enter these
countries, which is expected to hamper, on a medium or long run, markets has resulted in a significant advance of these 3 North
the export of vegetable products from these countries to Europe African countries in the implementation of modern food control
and other partners from developed countries. It is worth men- systems. Therefore, efforts to produce traditional foods that meet
tioning that Morocco, Algeria, Tunisia, and Egypt are among the the standards of the Codex Alimentarius (CA) would increase
main suppliers of fruits and vegetables to Europe, which represents their safety, and consequently, their local and international market
a major income to those North African countries where agricul- share, as has been reported for traditional Greek foods (Panagou
ture is the essential economic activity, especially in Morocco and and others 2013). It is worth mentioning, however, that North
Tunisia. However, despite the lack of specific regulatory limits for African countries do not have the same status as regards interna-
mycotoxins in these countries, the problem of mycotoxins is well tional, regional, and subregional organizations (Table 11), nor do
recognized from both public health and economic views. Projects they have the same economic resources and priorities in regards to
c 2012 Institute of Food Technologists® Vol. 12, 2013 r Comprehensive Reviews in Food Science and Food Safety 75
Safety of North African traditional foods . . .
Table 11–Membership status of North African countries in different international organizations and agreements with impact on trade, food safety, and
food security.
food safety. This situation, which deters these countries from hav- the availability of safe traditional food in North African countries.
ing a common food safety policy, should be addressed for mutual Marketing of traditional food commodities would also help the ru-
benefit and to obtain the best advantage for the opportunities of ral populations to generate greater income and meet other needs
globalization; each of these countries should endeavor to promote not available locally. In this regard, the world food security (WFS)
the safety of its own traditional foods while encouraging the ex- framework developed by the FAO under the Special Program for
change of these foods with the other North Africa countries that Food Security (SPFS) aims to improve food security within poor
share many common dietary habits. households through national and regional programs for food se-
curity. Morocco, Tunisia, and Egypt are among the participating
Safety of North African traditional foods countries of the WFS. The main challenge resides therefore in
There is a clear trend in North Africa to increase the avail- the development of practical technologies and/or the adoption of
ability and diversity of industrial foods either produced locally or adequate strategies to improve the safety and stability of traditional
imported from other countries. Nonetheless, the consumption of foods in conformity with international regulations and standards
traditional food products in these countries, though difficult to ac- (especially Codex Alimentarius standards) while preserving their
curately estimate, is significant especially in the rural areas where authenticity and palatability. To meet such a challenge, it is nec-
an average of about 40% of the entire North African popula- essary to develop national strategies for food safety based on a
tion lives (Table 1). Many dairy products (brined and soft cheeses, “holistic” or “food chain” approach that extends “from harvest to
zabadi, raib, lben, zebda, and smen), meat products (khlii, pastirma consumption” and involves all the relevant actors (government of-
and sujuk), and vegetable products essentially represented by var- ficials, food industry, local producers, researchers, academia, anal-
ious table olive types and pickled vegetables are examples of such ysis laboratories, the media, consumers and their organizations,
foods highly appreciated and widely consumed in North African and so on), within the framework of a predefined action plan such
countries. Consumer preference for traditional foods is essentially as that proposed to the Middle East and North Africa (MENA)
driven by the fact that these foods are considered as a valuable region by the FAO (2004). However, the implementation of such
heritage, and hence, part of the cultural identity to preserve, in an action plan appears to need greater financial and technical as-
addition to their believed health virtues and highly appreciated sistance from the governments and a longer transitional period to
gustatory properties. This particular issue has been extensively upgrade the quality of traditional food production while keeping
discussed over the last 2 decades as a means to preserve the cul- their authenticity. A number of authors have suggested the trans-
tural diversity, including nutritional habits, within the inevitable fer of traditional technologies to small or medium industrial scales
globalization of the world food supply. Nevertheless, this situa- where the hygienic conditions and microbiological contamination
tion creates a dilemma to the government officials who should could be better controlled than household production through the
encourage and support the production and consumption of local application of appropriate quality assurance programs such as GMP
traditional foods which, on the other hand, may present increased and HACCP (Fellows and others 1995; Motarjemi 2002; Benker-
health risks to consumers due to their usual nonconformity with roum and Tamime 2004). In the case of traditional fermented
regulatory standards. foods, it has been suggested to adopt controlled fermentation us-
Such risks, especially those related to microbiological hazards, ing selected industrial starter cultures and/or heat treatment of
are anticipated to be especially high for traditional foods, as they the raw materials, such as milk, as appropriate (Benkerroum and
are generally produced under poor hygienic conditions with- Tamime 2004). According to Panagou and others (2013), the tran-
out any systematic control measures. The widespread presence of sition from artisan practices in traditional food manufacturing to
pathogenic bacteria and molds in North African traditional foods, well-equipped industrial units under strict processing and hygienic
and reported cases of food intoxications linked to the consumption conditions has resulted in drastic improvement in the microbio-
of a number of these foods, strongly supports the assumption that logical quality of Greek foods similar to those reviewed herein
they put the public health at a high risk. Therefore, there is an (fermented meats, dairy products, and fermented vegetables), and
urgent need to improve the hygienic quality of these products, not hence their safety records. The addition of chemical preservatives
only to safeguard consumer health, but also to improve competi- including sorbates/benzoates or sulfites has also been suggested in
tiveness and market share so that they can efficiently contribute to the fermentation of table olives or drying of raisins, respectively,
76 Comprehensive Reviews in Food Science and Food Safety r Vol. 12, 2013
c 2012 Institute of Food Technologists®
Safety of North African traditional foods . . .
to increase their safety and stability (Canellas and others 1993; ganizations is necessary for the execution of such an action plan
Asehraou and others 2002; Panagou and others 2013). However, in North African countries. In addition, a transition period is
it could be argued that the resulting foods from such technology needed before all measures are operational. This period appears to
transfer may lose their authenticity and uniqueness as the selected be particularly long for traditional foods, which have received lit-
strains of the starter cultures cannot be representative of the com- tle attention so far, partly due to the lack of political commitment
plex and changing microflora involved in the different steps of the from the interested countries to act as partners having common
natural fermentation. Alternatively, it has been suggested that safe weaknesses and complementary assets.
and authentic traditional foods could be obtained by improving the
sanitary conditions of the traditional technologies along the whole Adequacy of current food control regulations and possible
production chain by the application of Good Agriculture Practices alternatives
(GAP), Good Harvest practices (GHaP), GHP, HACCP, and the The nature and degree of sophistication of food control systems
use of adequate conditioning, packaging, and transportation facil- vary widely among North African countries, which otherwise
ities (Fellows and others 1995; Flamant 1996; Valyasevi and Rolle suffer from common difficulties that limit the performance and
2002). However, the production of typical traditional foods may efficiency of their food control and inspection systems. These
also include the acceptance of a “residual” risk. For example, the include:
use of raw milk to produce traditional cheese by application of r Multiplicity of the food control systems—whereby modern
good practices reduces risk of listeriosis, but it does not remove it, safety and quality assurance systems using GMP, GHP, and
while initial sterilization of milk followed by controlled fermenta- HACCP programs are used by certain enterprises to produce
tion with pure starter cultures can meet the “zero tolerance” status; foods for export or urban retail sales, and to exist alongside an
however, the resulting cheese will loose its uniqueness and typi- informal food sector subject to minimal or no food safety or
cal gustatory quality. Therefore, though the residual risk could be quality control. The latter situation applies to North African
accepted, it has been recommended to prohibit the consumption traditional foods generally sold in informal ways in rural mar-
of such traditional foods by the high-risk groups: elderly, pregnant kets, shops, butcher shops (meat products), creameries (dairy
women, young children, and immunocompromised individuals. products), and grocery stores or by street vendors.
r The multiplicity of bodies involved in food safety and
Official food control measures quality control, which are usually affiliated with different
The success of any strategy to promote food safety and quality ministerial departments (agriculture, public health, interior,
should involve all the relevant actors, with the government playing trade, industry, environment, energy, and possibly others)
a central role in the coordination and supervision of the imple- ([Link]
mentation of the strategy. In this regard, the 27th FAO regional Although these departments play, in principle, different and
conference for the Near East recommended a number of spe- complementary roles and act to ensure the highest possible
cific measures that the governments of Middle Eastern and North level of consumer health protection, they have often been a
African (MENA) countries should take to improve food safety source of problems and distortions due to the lack of clear
and quality, and be prepared for the upcoming challenges related boundaries between the specific tasks of each institution, and
to the inspection and certification of food imports and exports and also due to intrinsic competition to be the leading authority
the provisions of scientific risk assessment as needed (FAO 2004). in food safety and quality in the country.
According to these recommendations, government officials are re- r Management of food safety issues is considered as an exclusive
sponsible for the establishment and management to enable institu- government mandate, and there is no or marginal inclusion of
tional, policy, and regulatory frameworks for food safety, and carry other stakeholders (industry, research institutions, consumers,
out food control activities that protect consumers from risks aris- nongovernment organizations (NGOs), and so on) in the
ing from unsafe food and fraudulent or deceptive practices. To this decision-making process regarding the policy of food safety.
end, government officials should work with interested parties at r In most North African countries, the current laws on food
the national and regional levels to build capacity and to strengthen control are generally not specific to foods but cover all kinds of
national food control programs and activities. Among the main goods. Furthermore, many regulatory standards and threshold
recommendations, the conference stressed the need to strengthen values are obsolete and do not match with the recent advances
and modernize food control facilities and procedures through a in food technology and the techniques used for the detection
risk-based approach. The conference also recommended creating of conventional or emerging microbial or chemical contami-
or reinforcing capacities for national foodborne disease surveil- nants, such as Creutzfeldt-Jakob prion, avian influenza virus,
lances accompanied by a rapid alert system and mechanism for Ent. sakazakii, dioxin, and acrylamide. Furthermore, they do
communication with food control authorities along with an effi- not meet the international trade requirements for accredita-
cient means to implement corrective measures. The development tion, certification, traceability, and required high food safety
of cooperation between the countries of the region to facilitate standards.
communication and exchange of information in foodborne dis- In fact, officials of North African countries are aware of the
ease surveillance, as well as information about foodborne hazards, inadequacy and vulnerability of their food safety policies in view
was also among the main FAO recommendations. In this regard, of global trends. Therefore, they have been modifying, at different
MENA countries were particularly urged to create a risk assess- rates, their food safety systems to meet WTO requirements and
ment body(ies) that provides scientific advice to risk managers on harmonize their standards with those of the CAC. However, the
issues of particular interest and to form interregional networks of transition from the conventional control and inspection systems
laboratories (FAO 2004). to a modern food safety framework requires profound institu-
However, efficient implementation of these measures is costly tional and legal changes in addition to substantial investment and
and requires highly skilled personnel; therefore, financial and/or technical needs. Morocco, for example, has been working on this
technical support from developed countries or international or- issue with the support of FAO since 2000, and has only recently
c 2012 Institute of Food Technologists® Vol. 12, 2013 r Comprehensive Reviews in Food Science and Food Safety 77
Safety of North African traditional foods . . .
adopted a new law (Law 025-08) stipulating the creation of a in the long run. To this end, the government could simplify
National Food Safety Office (ONSSA) (official bulletin N◦ 5714 the administrative routine, reduce taxes, and provide technical
of 5 March 2009). This act has been designed to induce deep assistance to design a business plan and later implement it.
changes in the Moroccan food safety policy and control practices r Facilitating loans at reduced rates for the acquisition of small
so as to meet the recommendations of regional and international equipment and machinery. Rural food producers usually lack
organizations including WTO (SPS, TBT), WHO and FAO (CA, the basic capital to start producing foods for trade, and small
IPPC), EU, OIE. or medium loans with reduced rates would help them start
In view of these changes, traditional products should also be a business either individually or within associations or coop-
considered under the law 25-06 on “the distinguishing marks of eratives. Many successful creameries in Moroccan cities have
origin and quality of agricultural products and foodstuffs” to im- started in this way, which could be extended to traditional
prove their safety and competitiveness. Under this law, traditional meat products (gueddid, khlia, mkila, and so on) or vegetable
foods are subject to official food control and inspection. Indeed, products.
standardization of traditional foods and protection of their origin r Subsidizing traditional food products, especially those pro-
and quality through such legislations has been reported to moti- duced in cooperatives or professional associations as an en-
vate the small-scale production of traditional foods and to expand couragement during a limited period.
their export potential (Panagou and others 2013). Adoption of an r Encouraging women associations to produce traditional
adequate surveillance system is another crucial factor to accurately foods. It is of paramount importance for women in North
assess the health risk associated with the consumption of traditional African countries to know that the foods they produce at the
foods, and consequently, design appropriate preventive measures household level have financial value and constitute a signifi-
to reduce risks to as low levels as possible. This aspect was also cant source of income for their own autonomy and financial
emphasized in the new Moroccan food safety act. independence. This also represents a means to support the
gender policies now being recognized as a limiting factor to
balanced economic growth in developing countries; this is
Incentives to food producers and infrastructure improve- usually better achieved by a group of women within associa-
ments tions.
To improve the safety of traditional North African food prod- r Organizing training sessions for all the personnel involved in
ucts, it is necessary to adopt certain measures that would encourage the production process including technicians and food han-
food producers, usually rural, including the provision of financial dlers on a regular basis under the supervision of official agen-
and technical incentives to help them upgrade the hygienic quality cies or NGOs, and at no fees for targeted participants.
of their products and be aware of the benefits of such an approach r Organizing yearly prizes for individuals or associations pro-
in the medium and long term. Some of these incentives may be: ducing the most competitive traditional food products that
r Preferential rates of water and electricity fees. The prices of also meet the safety standards.
water and electricity are relatively high in most North African It is worth mentioning, however, that these measures can only
countries due to the water shortage and limited capacity in be effective if the other basic requirements for such technology
the production of electricity; a situation that deters rural food transfer (infrastructure, transportation vehicles, electricity, potable
producers from using water and electric urban facilities to pre- water, and so on) are met (for a review see Rolle and Satin 2002),
pare traditional food products. Instead, they use wells or open and this is a matter of sustainable development of the country as a
surface water as available; they thus expose the final product whole.
to various chemical and microbiological contaminants orig-
inating from a polluted water supply. Also, the provision of The role of NGOs
electricity at a reduced rate would encourage rural food pro- The role of NGOs in the promotion of the safety and quality
ducers to use electric machines (dryers, churning machines, of foods is no longer questionable and should be further encour-
heated vats, meat cutters, refrigerators, and so on) for better aged by the governments. Depending on the objectives of these
control of the technological processes or for storage of the organizations, they may play critical roles at many levels for the
finished product before sale. promotion of the safety of foods in general and specifically of tra-
r Provision of technical assistance at the farm level: Rural food ditional foods. According to the approach of risk analysis, NGOs
producers are usually not aware of the critical steps in tra- should work closely with other stakeholders, by virtue of the risk
ditional processes that may lead to defective final products communication component of the approach, to defend the con-
or inconsistent gustatory quality if not adequately controlled. sumers’ right to safe foods as was recommended by the CAC in
Therefore, technical assistance by trained persons would draw the 1990s. They should therefore be involved in the definition
the attention of rural food producers to the critical steps of the of national food safety policies to request appropriate standards of
traditional processes, and help them ensure the production of food safety, and also at the production level to ensure that foods are
foods with consistent quality. For example, the relevance of handled, stored, and prepared in accordance with good hygienic
cleaning/sanitation, as well as personal hygiene, to the quality practices (GHPs). Furthermore, NGOs that focus particularly on
and safety of the final products is overlooked or even ignored rural development would provide valuable technical assistance to
by rural food producers. The organization of adequate train- rural individuals or associations to develop economic activities
ing sessions would contribute to the sensitization of food adapted to their environment including the production of tradi-
producers to the impact of these practices on the quality of tional foods, so they can be formally marketed through the country
the finished food products. or the region. Such organizations are being increasingly active in
r Facilitating technology transfer from the household level to all aspects of development in North African countries and may
small or medium industrial scale for traditional food products be an asset for the modernization of the traditional food produc-
when such transfer is deemed viable and economically feasible tion sector. Indeed, subsequent to the CAC recommendation to
78 Comprehensive Reviews in Food Science and Food Safety r Vol. 12, 2013
c 2012 Institute of Food Technologists®
Safety of North African traditional foods . . .
c 2012 Institute of Food Technologists® Vol. 12, 2013 r Comprehensive Reviews in Food Science and Food Safety 79
Safety of North African traditional foods . . .
Effective contribution to the implementation of food safety reliable estimates of exposure and specifically mentioned that a
regulations and control of traditional foods consideration should be given to developing countries by provid-
Over the last 2 decades, risk analysis has emerged as a powerful ing them with assistance and resources for generating meaningful
tool that can be used by national food safety authorities to make food consumption data and subsequent exposure assessments. Al-
proportionate and scientifically based decisions on food safety is- ternatively, it has been suggested to perform risk profiling with
sues. Also, as an integral part of Codex Alimentarius, risk analysis the available data, which should then be revised periodically and
can support and improve the development of standards and reg- amended as new data are generated from scientific studies and
ulations on a scientific basis and address food safety issues that surveillance programs to ultimately allow quantitative risk assess-
result from emerging hazards or breakdowns in food control sys- ment (FAO 2006; Bidlack and others 2009). Meanwhile, risk
tems. The relevance of risk analysis to all the food safety issues profiling that categorizes food products into groups with high,
has become increasingly important since its adoption within the moderate/medium, or low risk may be a useful tool to assist the
SPS agreement. While risk analysis and its scientific component decision-making process and to set priority for action. In fact, un-
risk assessment are now widely applied in developed countries in der certain circumstances, including cases where risk assessment is
Europe, America, and Australia, its extension to developing coun- either unnecessary or not feasible to carry out, risk profiling may
tries is hindered by many limitations, the most important of which serve as a basis to identify and select food control measures and
are: risk management decisions. Notable examples of such cases are: (i)
r General lack of awareness among officials, manufacturers, sci- the Canadian approach to regulating L. monocytogenes in ready-to-
entists, and consumers of the real gain that the implementa- eat foods, (ii) the Swedish approach to regulating acrylamides in
tion of risk analysis approaches would represent to national baked and fried starchy foods, and (iii) the prohibition of certain
food safety status compared with the conventional food safety antibiotics from veterinary care in many countries on the basis of
and food control measures. risk profiling that suggests microbial resistance to some antibiotics
r Lack of infrastructure, technical and financial resources, ad- used in both human medicine and animal health care (FAO 2006).
equate institutional framework, and necessary expertise to A systematic risk profiling approach would be appropriate and
effectively respond to existing and emerging food safety and amply justified for North African traditional foods at the present
quality problems. time. It is generally admitted that the main risks associated with
r Insufficient information about the hazards and risks associated North African traditional food products are of microbial origin
with traditional foods due to the lack or poorly documented (pathogenic bacteria and their toxins, mold toxins, parasites, and
epidemiological, intoxication records, and scientific investi- viruses), although hazards of another nature, such as pesticide
gations. residues and heavy metals (Zaida and others 2007), not discussed
r Lack of data on consumption patterns and insufficient knowl- in this review, should not be overlooked. Depending on the natu-
edge about levels and occurrence of hazards (chemical and ral hurdles to microbial growth (salt, sugar, moisture evaporation,
biological) in foods. fermentation, and so on) used in the manufacturing processes,
In view of these limitations, FAO and WHO have been work- traditional products may harbor different hazards and the same
ing together to increase the awareness and adoption of risk anal- hazard may present different health risk patterns depending on the
ysis principles in developing countries, both as a tool for national product (Larsen 2006; Bidlack and others 2009). Table 6 presents
food safety authorities and the provision of scientific advice and documented hazards of microbial origin associated with North
evaluations. These United Nation organizations have also been African traditional dairy, meat, and vegetable food products. Ta-
providing technical and financial support to developing coun- ble 12 shows various risk factors associated with North African
tries to help them build capacities and strengthen national food traditional foods and the protective hurdles on which the tradi-
control and inspection systems, and activities in order to adopt tional technology relies to ensure their safety and stability. Correc-
new food safety frameworks based on risk analysis. Among North tive actions are proposed on the basis of harvest-to-consumption
African countries, Morocco has benefited from this assistance to approach (Table 12). Taking into account the global situation of
reform its food safety policy, as confirmed by the promulgation North African traditional foods and the uncertainties regarding
of the new Law 25-08 on February 18th, 2009. Under this law, their wholesomeness, it appears urgent to start preliminary risk
the ONSSA has been established as the only institution responsi- profiling with the presently available knowledge on these products.
ble for protecting the consumer health as well as that of animals Simultaneously, scientific studies and chemical and microbiological
and plants ([Link] analyses involving universities and research institutions along with
Nonetheless, risk assessment of North African traditional foods, at surveillance programs should be initiated to provide new infor-
the present, remains incomplete and inaccurate due to the lack of mation to progressively refine and update risk profiling. However,
necessary data to produce credible and reliable risk assessment. In since traditional food products differ among North African coun-
fact, this situation has been reported to be the main constraint fac- tries and even among localities of the same country, it is vital to
ing risk assessment worldwide regardless of the type of foods. Yet, facilitate communication and information exchange in foodborne
the extent of shortage of relevant data and records to conduct risk disease surveillance as well as information about foodborne haz-
assessment is variable depending on the country, with developing ards between these countries according to the recommendations
countries being the most affected. In particular, the lack of the of the 27th FAO regional conference (FAO 2004).
necessary data to estimate exposure to hazards has been identified
as one of the critical missing parts in a risk assessment process, as an Ranking risk of North African traditional foods
inaccurate risk estimate would provide risk managers with a false In order to compare microbiological risks associated with tra-
global picture of the situation, which may eventually lead them to ditional foods from North Africa, the RCM developed by the
make inappropriate decisions (Luetzow 2003). The same author Federal/Provincial/Territorial Committee on Food Safety Pol-
has recommended improving the collection and dissemination of icy (FPTCFSP 2007) was modified and used to profile selected
such data worldwide to progressively fill in the gaps for more North African traditional foods. This model, originally designed to
80 Comprehensive Reviews in Food Science and Food Safety r Vol. 12, 2013
c 2012 Institute of Food Technologists®
Safety of North African traditional foods . . .
Table 12–A general presentation of the risk factors related to hazards of microbial origin and the natural hurdles empirically used in traditional
technologies to reduce the health risk associated with the consumption of such foods. Corrective actions to upgrade the safety and quality of North
African traditional foods on a scientific basis are also proposed.
Risk factors
Type of commodities Microbial contaminants Mycotoxins Safety factors Corrective actions
Dairy products r Contaminated raw milk, r Contaminated milk (carryover of r Lactic fermentation r Veterinary care of dairy
r Poor sanitary conditions during mycotoxins from feeds) r Predominance of safe or herd (control of mastitis
processing and handling r Contamination and growth of health promoting diseases)
r Opportunity for pathogens to grow toxinogenic molds on finished microorganisms r GHaP, GHP, GMPs,
and produce toxins during product or during storage r Reduced aw (dry-salted, HACCP (from the farm
processing or storage brined cheeses, dried to storage)
r Contaminated water supply cheese) r Use of selected starter or
r Usually ready-to-eat r Addition of herbs and adjunct starter cultures
r High exposure spices (controlled
r No application of any quality fermentation) with
assurance program antimicrobial activities
(for example, use of
bacteriocin-producing
lactic starter cultures)
r Sourcing and potential
testing of feed from
GAP producers
Meat products r Contaminated raw material r Mycotoxin-containing spices r Addition of herbs and GHP, GMP, on-farm
r Poor sanitary conditions at r Contamination and growth of spices HACCP, improve
slaughter and processing toxinogenic molds on finished r Reduced aw (dry-salting, animal welfare GHP in
r Postprocessing contaminations product during storage brining, drying) food sale and
r Opportunity for pathogens to grow r Presence in the liver and kidney of r Heat treatment during preparation to reduce
during processing and/or storage animals fed with contaminated processing microbial
r Poor veterinary care of livestock feeds (meat products using offal r Usually cooked before contamination
(prevalence of zoonotic diseases) meat) consumption r Low exposure
r No application of a quality
assurance program
Vegetable products r Contaminated raw material r Presence in fresh vegetable products r Fermentation GAP, GHP, on-farm
r Postprocessing and persistence during processing r Chemical acidification HACCP, adequate
r Contaminations r Growth of toxinogenic mold and r Reduction of water conditioning and
r Opportunity to grow during opportunity to produce mycotoxins activity (dry-salting, storage conditions,
processing or storage during processing or storage brining, drying) controlled fermentation
r Poor hygiene during harvest, r Use of spices and condiments r Addition of herbs and
processing, and storage contaminated with various spices with
r Cross-contamination mycotoxins antimicrobial activities
r Human reservoirs (occasionally)
r Contaminated raw material (use of r Inherent antimicrobial
wastewater sewage or sludge for substances such as
irrigations and fertilization euloropein and
r Sanitary conditions during derivative substances
manufacture and storage in olives
r Post- and cross-contaminations,
r High exposure
GHaP: Good harvest practices.
GHP: Good hygiene practices.
GMP: Good manufacture practices.
HACCP: Hazard analysis critical control point.
NA: Not available.
conduct risk profiling for food retail and food service establish- biological hazards based on the epidemiological evidence,
ments, takes into account 8 major risk factors each of which is showing that the most frequent foodborne diseases are of
scored according to the extent of risk it poses to consumers. The microbial origin. In this study, we also omit microbial toxins,
total score of the 8 factors indicates the risk categorization of a such as mycotoxins, or heat-stable E. coli or Staphylococcal
product as per the following cutoff points: high risk (165 points or toxins, which may be produced during processing or storage
more); moderate risk (between 110 and 160 points); low risk (105 and would not be removed by treatments such as cooking or
points or less). The RCM guide also provides an explanation for fermentation. Omission to consider microbial toxins in risk
each risk factor, along with directions on how to determine the scoring was based on the same reason as stated in the RCM,
corresponding score. These risk factors were determined on the in addition to the lack of reliable data on these contaminants
basis of a previous study reviewing factors that contributed to food- (occurrence and concentrations) in North African traditional
borne illness in Canada in the period of 1973 to 1977 (Todd 1983) foods. Therefore, high- or medium-risk ready-to-eat foods
in addition to other factors used by some jurisdictions to deter- are scored higher than those which undergo additional treat-
mine inspection frequency. The 8 factors used in this study were: ments (cooking, marinating, addition of herbs, and spices) to
1. Types of food and intended uses: Scoring of this risk factor is reduce or control microbial load before consumption. Sim-
based on 2 main considerations: (i) the likelihood of a food ilarly, high- or medium-risk foods, which receive further
to contain pathogenic microorganisms above safety level and heat treatment or undergo other methods to reduce micro-
opportunities it provides for the microorganisms to grow bial pathogens, are at reduced risk. Low-risk foods are those
and/or produce toxins, and (ii) whether the food is ready- that represent a hostile environment (reduced water activity,
to-eat or undergoes further heat treatment or cooking before low pH, contain known antimicrobial substances, and so on)
consumption. For this risk factor, the RCM considers only for microbial contamination and growth.
c 2012 Institute of Food Technologists® Vol. 12, 2013 r Comprehensive Reviews in Food Science and Food Safety 81
Safety of North African traditional foods . . .
Table 13–Risk categorization of traditional foods of North African countries based on the model developed by Health Canadaa using 8 risk factors
(I to VIII).b
2. Food preparation and processing: This factor generally refers quate enough to ensure that safe food handling practices
to whether the food was minimally processed or has un- are being followed with the possibility to undertake cor-
dergone a process designed to minimize the likelihood of rective actions when necessary. In addition to certification
food safety hazards (pasteurization, boiling, cooking, mari- that the managers and employees should have from rec-
nating, fermentation, and so on). In addition, the amount ognized institutions, they must demonstrate to the regu-
of handling that a food undergoes during preparation is a latory agency that they are following safe practices. Food
determinant of the risk posed by a food. Indeed, extensively establishments that do not have adequately trained em-
handled foods, especially if they are uncooked and unpack- ployees or practice safe food handling principles are at
aged, are considered more likely to be subjected to microbial greater risk of being implicated in a foodborne illness.
contaminations, and hence they score highest. North African traditional foods are generally not produced
3. Equipment and facilities: To determine the risk linked to in modern establishments, by qualified personnel, and after
a factor, RCM considers the layout and design of food es- effective training sessions on regular basis, but rather at the
tablishments, the way the flow of food goes from reception household level or in shops, and generally by members of the
to service or sale, whether or not raw materials and foods same family, usually with a low level of education. There-
of different risk categories are adequately separated in the fore, this risk factor would score high for all North African
establishment, waste storage, and disposal as well as the sep- traditional foods.
aration between nonfood activities from food preparation 5. Food safety management program: Development and im-
and processing areas. The water supply as food ingredient plementation of food safety management programs such
or for other needs (handwashing, warewashing, and sani- as Hazard Analysis Critical Control Point (HACCP) and
tizing), equipment for food preparation or processing (suit- its prerequisite support programs, including facility main-
ability, age, made from nontoxic materials, easily cleanable). tenance and sanitation and personal hygiene of foodser-
As most traditional North African traditional foods are either vice workers, contribute significantly to a better control
homemade or produced in small shops, scoring was based of food processing and preparation stages. RCM consid-
mainly on the conditions where a given food is generally ers that establishments that have such a program in place
prepared including the space, sanitary conditions of process- would be at less risk than those that have no controls.
ing area, personal hygiene, access to drinkable water, and As was discussed for the former risk factor, North African
cleanliness of the utensils used. traditional foods are generally produced with untrained
4. Management and employee food safety knowledge: Accord- personnel and in an environment where no food safety
ing to RCM, scores of this risk factor are attributed de- management program could be appropriately applied.
pending on the extent of food safety knowledge of em- Therefore, this risk factor also scores high for all these
ployees, managers, and supervisors, which should be ade- foods.
82 Comprehensive Reviews in Food Science and Food Safety r Vol. 12, 2013
c 2012 Institute of Food Technologists®
Safety of North African traditional foods . . .
6. Regulatory compliance: Determination of the risk associ- sary means to improve the safety of traditional foods (Fellows and
ated with the specific establishment as regards this factor is others 1995; Rolle and Satin 2002; Steinkraus 2002; Valyasevi and
based on historical information about regulatory compli- Rolle 2002; Benkerroum and Tamime 2004; Panagou and oth-
ance with critical items. The occurrence of an outbreak at ers 2013). According to this preliminary profiling, North African
a foodservice establishment is also taken into consideration traditional foods that constitute an important part of the North
when an indication exists that food safety principles were African diet warrant due attention to improve their safety. Risk
not followed prior to the outbreak. Consumer complaints profiling should be officially conducted on a large scale through
and responsiveness of the management of the establishment field surveys in order to prioritize government actions and de-
to act on previous advice are also considered to score this risk fine specific regulations and control measures, which should be
factor. As the term “compliance” refers to past and current strictly implemented. Meanwhile, accompanying measures should
compliance to inspections, and North African traditional be taken by the government to provide the necessary assistance,
foods are not officially inspected, we relied on scientific pub- encouragements, and other incentives as was suggested in this re-
lications and reports to assess the microbiological compliance view and elsewhere (Rolle and Satin 2002; Valyasevi and Rolle
to known standards, either by the presence of pathogens or 2002; Benkerroum and Tamime 2004) to gear all producers toward
the counts of groups of microorganisms of hygienic signif- a voluntary adoption of quality assurance management systems to
icance (coliforms, fecal streptococci). Documented claims improve the quality and competitiveness of the foods they pro-
about implications of some North African traditional foods duce. Practical measures to improve the safety of North African
in intoxications were also considered. traditional foods at the production level are suggested in Table 13.
7. Volume of food: In the RCM, this risk factor relates to
the volume of foods sold or prepared, as estimated by the
Conclusions
number of people served or provided food, or the number
With the advent of globalization and involvement of North
of employees at an establishment at a given time (shifts).
African countries in many international, regional, subregional,
Higher volumes of foods increase risk of foodborne illness.
or bilateral agreements (SPS, OIE, CA, European neighborhood
To adapt this scoring to North African traditional foods, the
partnership, FTA, and so on) and increasing demand in terms of
frequency and quantity a given traditional food is consumed
quality and safety of foods for trade, it becomes urgent to reshape
at each meal, based on personal knowledge of the culinary
the food safety policies in North African countries, not only to
habits of North African communities, were used to estimate
upgrade the safety and quality of the foods they produce, but
the volume of the food.
also to protect consumers from fraudulent or unsafe imported
8. Typical patronage: Serving foods to subgroups of a popu-
foods. The latter foods make up a very high percentage, up to
lation (the young, elderly, and immunocompromised) who
75%, of the food supply in some of these countries (Mboungou
are the most vulnerable to foodborne disease will increase
2011). Any future food safety strategy should be based on a risk
the likelihood of occurrence of a foodborne illness outbreak.
analysis approach, and national food regulatory standards should
Some North African traditional foods, especially dairy prod-
be aligned according to the CA. The standards, guidelines, and
ucts such as zabadi and jben are served to young children or
recommendations adopted by the CAC are, indeed, referred to
sick persons due to the believed health virtues; such products
in the WTO agreement on the application of SPS agreement as
were attributed high scores regarding this risk factor.
benchmarks for international harmonization of food regulations.
Table 13 presents a tentative risk profiling of selected North
Reliable risk assessment or profiling studies need to be conducted
African traditional foods using the FPTCFSP RCM after the ad-
on different foods of North Africa (including traditional foods) in
justments/interpretations mentioned above. The outcome of this
order to set food control priorities.
profiling showed that the vast majority of North African traditional
Despite their different economic, demographic, and political
foods pose a high risk to consumers, few fall into the medium risk
priorities, North African countries share much sociocultural speci-
category, and only 2 of the profiled products (pickled lemon and
ficity that would be an asset for their common sustainable develop-
dry figs) would be of low risk owing to their extreme intrinsic
ment and the differences could, in fact, be regarded as complemen-
physicochemical parameters and relatively low consumption pat-
tarities that stimulate synergistic actions. Therefore, it is crucial to
tern, and hence, low exposure. Pickled lemon is highly acidic and
facilitate the exchange of information on all food safety-related
salty, while dried figs have low water activity due to their low
issues and perform common risk profiling and assessments when
moisture and high sugar contents. As for the consumption pat-
possible. Nonetheless, to make such profound changes in food
tern, lemon is used in the North African cuisine as an ingredient
safety policy, North African countries are facing various financial,
in some cooked meals, and dry figs are mainly consumed during technical, cultural, and political challenges that they may not over-
the fasting month of Ramadan in Muslim communities as an ap-
come if they rely only on their own potentialities and resources;
petizer. However, the risk associated with the latter product may
they require greater and concrete synergistic actions between each
increase if contamination with mycotoxins are also considered as other in addition to external assistance from international organi-
a potential hazard. Table 13 shows that the risk factors IV (man-
zations (FAO, EU, OIE, OECD, WHO, and so on) and developed
agement and employee food safety knowledge) and V (food safety
countries.
management program) scored highest for almost all the profiled
foods. This demonstrates the prominent impact, either directly or
indirectly, of employee education and the management system on Acknowledgment
the risk ranking of foods, and it implies that any improvement Deep appreciation is expressed to Dr. Dennis Bittisnich of
to reduce risks linked to these foods should first address these the Australian Government Dept. of Agriculture, Fisheries and
aspects, which will, in turn, mitigate other risk factors. Indeed, Forestry, and Dr. Manfred Luetzow, international food safety con-
there is general agreement that the standardization of technologies sultant, for reviewing the prepublication manuscript and for their
for these foods by transfer to small or medium scale is a neces- expert comments and suggestions. The author is also grateful
c 2012 Institute of Food Technologists® Vol. 12, 2013 r Comprehensive Reviews in Food Science and Food Safety 83
Safety of North African traditional foods . . .
to Prof. Mohamed Dehhaoui for his helpful discussions on sta- Asehraou A, Peres C, Faid M, Brito D. 2002. Reducing the bloater spoilage
tistical issues and for providing valuable documentation to this incidence in fermented green olives during storage. Grasas Aceites 53:330–4.
work. Ayad A, Habichou H, Lakhdari H. 2011. Le rôle des organisations
professionnelles dans l’accompagnement des PME en Algérie. [Internet
document]. 2011. [22 Jul 2012]. Available from: [Link]
[Link]/larevue09/Atmane AYAD_Hanane [Link]. Accessed
Sept 22, 2012.
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