North African Trad Food Risk Profiling

Traditional Fermented Foods of North African Countries: Technology and Food Safety Challenges With Regard to Microbiological Risks
Noreddine Benkerroum 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 ofcial 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 scientic basis due to the lack of consumption patterns, epidemiological data, and appropriate surveillance programs. The scarcity of scientic studies on the incidence of hazards in this specic category of foods adds to the difculties in conducting scientically sound risk assessment or proling 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 prole the health risks associated with their consumption, and consequently, take the necessary measures to reduce such risks. A tentative risk proling 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.
from the blend of nutritional habits brought by these civilizations and their interactions with those of the original inhabitants such as the Amazigh/Berber people in the Maghreb. For example, inuence from the Romans (146 BC) can be recognized throughout the region, as wheat is the basis for the main staple foods: bread and couscous. Islamic inuence can be recognized in the strict prohibition of wine and pork meat, while the other meat products must be obtained from game animals or those slaughtered according to the Islamic requirements to be considered as halal, permitted (lawful) for consumption from a religious standpoint (for a review see Regenstein and others 2003; Daoudi and others 2006). Yet, other foods consumed by religious or ethnic minorities in the region are also available and retailed throughout the existing marketing routes. This historical sociocultural situation has created a clear distinction between nutritional habits of the North Africa region and those of Northern Mediterranean countries. This review provides a brief description of technologies of the most popular North African traditional foods of animal and plant origin, and presents an overview of the available data on their microbiology and presence of microbial toxins as sources of risk to consumers. Risk factors as well as safety factors are MS 20121004 Submitted 7/23/2012, Accepted 10/8/2012. The Author is with discussed in the perspective to provide producers with technical Inst. Agronomique et Vtrinaire Hassan II, Dpt. des Sciences Alimentaires et Nu- means to enhance the safety of such foods. Proling selected traee e tritionnelles, BP 6202, Instituts, 10101-Rabat, Morocco. Direct inquiries to author ditional North African foods based on a risk categorization model Benkerroum (E-mail: n.benkerroum@gmail.com). (RCM) developed by Health Canada was conducted, and the North African countries have an ancient tradition in food technology, and many traditional foods have been passed down from one generation to another through the ages. In Egypt, for example, fermented dairy and meat products, as well as wine and beer, have been traced back at least to the pharaoh era of 4000 BC (Ross and others 2002). Some cheese varieties have also been suggested to have been brought to that region by the Greeks (Osman 1987). Although the diet in these countries is typically Mediterranean (Padilla and others 2005; Alexandratos 2006), the inuence of the different civilizations that have been established throughout history in the region is still evident in all aspects of life including culinary habits. Indeed, these countries are heavily inuenced by ancient civilizations, such as those of the Greeks, Phoenicians, Egyptians, Romans, and Vandals, and more recently by the Islamic civilization starting with the Arab conquest (late 7th century) and the presence of Ottomans (Turkish invaders), also Muslims, during the 15th and 16th centuries (Stearns and others 2010). Therefore, North African countries share many traditional foods resulting
54 Comprehensive Reviews in Food Science and Food Safety r Vol. 12, 2013
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Introduction
Safety of North African traditional foods . . .
Atlantic A Ocean O
Morocco Algeria
Tunisia
M Mediterranean Sea a a
Libya Egypt
Mauritania Sudan
Figure 1Countries of the North Africa subregion according to the most accepted denition (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 signicantly 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 diversied 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 denition 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 The overall consumption of meat products in North African changing political status of the countries throughout the history of 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 attral 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 justies 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 denition 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, retries. 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 denition 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 denition 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 posis part of the Asian continent. Nonetheless, regardless of the ge- sible without being spoiled or becoming hazardous to consumers ographical or geopolitical denition, Morocco, Algeria, Tunisia, health. This was achieved by treatments combining different natLibya, 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 techmain demographic, economic, social, and cultural data for these nology as recently advocated by Leistner (2000a). Although spices and herbs were added to traditional meat products, primarily as countries.
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Red Sea

Table 1 The main demographic, social, economic, and cultural data of the North African countries. Data were compiled from the World Bank (http://www.worldbank.org), The United Nation Development Program (UNDP) (http://hdrstats.undp.org/fr/indicators/87.html) and the Food and Agricultural Organization of the United Nations (FAO) (http://faostat.fao.org/) websites. Accessed on April 17, 2012. Statistic data and indices are for the year 2011, unless otherwise stated in the footnotes. The country Morocco Algeria Tunisia Libya Egypt Area Population Urban (km2 ) (millions) population (%) Main economic activity 710,850 32.27 58.8 Agriculture, phosphates mines, tourism, and sea foods 2,381,741 35.98 67.1 Oil and natural gas 163,610 10.60 67.7 Agriculture, mining, manufacturing, and tourism 1,759,541 6.42 78.1 Oil and natural gas 1,002,450 82.54 43.5 Agriculture, oil, and tourism GNI per capitaa 4,196 7,658 7,281 12,637 5,269 PINb HDIc 120.90 0.582 116.00 0.630 98.05 0.698 102.31 0.760 102.78 0.644 Ofcial Ofcial religiond language Islam Arabic + Tamazight Islam Islam Islam Islam Arabic + Tamazight Arabic + Tamazight Arabic + Tamazight Arabic
a Gross national income (GNI) per capita in PPP terms (constant 2005 international $, see the denition at http://www.who.int/choice/costs/ppp/en/): Aggregate income of an economy generated by its production and its ownership of factors of production, less the incomes paid for the use of factors of production owned by the rest of the world, converted to international dollars using purchasing power parity (PPP) rates, divided by midyear population. b Food production index (PIN) per capita for the year 2010 based on 2004 to 2006 = 1000. c Human development index (HDI). Countries with HDI 0.456 and 0.741 are considered to have a medium level of development for the year 2011 (FAOSTAT 2012). d Minorities of other religious and cultural backgrounds such as Christians and Jewish are also present. NA: Not available.
Table 2Production 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 (1000 metric tons) Milk Cheese Meat 2304.00 1.540 609.26 5742.40 940.15 1731.14 222.70 NA 186.68 2009.55 43.73 1036.13 1093.10 4.14 274.76 Consumption (kg/capita/year) Milk Cheese Meat 117.36 0.65 20.13 61.81 7.47 22.08 75.03 1.78 27.84 44.49 0.82 25.02 106.91 0.26 27.34
Country Algeria Egypt Libya Morocco Tunisia
NA: Not available.
may also be further processed into khlii (see below). Although the original purpose of transforming meat into gueddid was its preservation to last as long as possible, given the lack of adequate storage facilities; it is now regarded as prestigious and highly prized cultural heritage food in North African countries. Therefore, local meat industries are trying to standardize its technology for an adequate transfer to industrial scale, as has been done with jerky 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.
avoring and aromatizing agents, it is now well established that they also contribute to the improvement of food safety and keeping quality, as many of them have been shown to possess potent antimicrobial activities (Al-Delaimy and Barakat 1971; Kivanc 1988; Ghal and others 2007; Kong and others 2007; Ivanova and others 2009; Rattanachaikunsopon and Phumkhachorn 2009, 2010a, b). Among these, garlic, curcuma, cinnamon, cumin, ginger, cloves, paprika, and pepper (black, white, or red) coriander (leaves or grain) have been the most frequently used in traditional meat preparations. Also, pretreatments such as cooking or marinating into an acid, spicy preparation called sharmula for 1 or 2 d were applied to raw meat in order to improve its microbiological quality in addition to the enhancement of the nal gustatory quality of the meat products deriving thereof. Moreover, traditional meat products of North African origin are primarily obtained from bovine, lamb, goat, buffalo, or camel meat, which have the halal status according to the Islamic rules. Yet, traditional pork meat products are also available, but they are claimed by Christian local minorities such as the Copts in Egypt, or destined to temporary residents (foreign employees and diplomats or tourists) from other countries, and hence they are produced in very limited quantities. Similarly, the kosher traditional meat products are mainly produced at the household level in Jewish families.
Pastirma/ basterma/basturma/pastrami This traditional meat product is the most popular in Egypt and consists of cured and dried meat strips encased in a mixture of garlic, fenugreek, and various spices (Figure 2b). It is believed that pastirma has been brought to Egypt from Turkey, most likely during the Ottoman domination in Middle Eastern and North African areas in the 15th and 16th centuries. In fact, the term bastirma means strong pressing action in Turkish as pressure is a crucial step in the preparation of the product (Obuz and others 2012). Yet, it has been suggested that pastirma is originally a Roman (Byzantine) food product (Adamson 2002). Although pastirma is preferably made from beef, various other meat types are also used, including lamb, goat, buffalo, and camel. A typical method for pastirma preparation is summarized in Figure 4. The nished product has a pH of 4.5 to 5.8, a salt content of 6.0%, water activity of 0.85 to 0.90, and moisture of 35% to 52% (Leistner 2000b; Bechtel 2001; Obuz and others 2012). Pastirma is consumed with scrambled eggs, cut into slices and fried, grilled lightly over a charcoal re, or added as an ingredient to various culinary preparations such as bean stew. Khlii/khlia and related products Khlii is a candied meat product obtained from salted-dried meat, which is cooked and conditioned in fat (Figure 2c). It is a typical Moroccan cured meat product, probably brought to the country by Arab conquerors (early 8th century) on their way to Andalusia in the Iberian Peninsula (Daoudi and others 2006). Due to its extended shelf life even when stored under abusive temperature (more than 2 y when stored properly), it was the main food supply for Arab warriors to avoid food shortage while providing them with such tasty and nutritious food. Although genuine khlii is believed to be made from camel meat, beef is the most widely used in practice. Typical traditional technologies of khlii and some
c
Gueddid The oldest means to preserve meat is probably by salting and sun-drying (Nummer and others 2004). Gueddid (Figure 2a), a typical meat product of the Maghreb countries (Morocco, Algeria, and Tunisia), is obtained by such a basic technology yielding stable salty dry meat, which can be stored at room temperature for more than a year. It is primarily prepared from lamb meat or beef; in the subarid zones of the region, camel and goat meats are mostly used as depicted in Figure 3. At consumption, gueddid is softened and desalted by immersion in water to make it tender before use

Table 3Main 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). Vernacular name Leben or lben (maghreb), or Laban khad/laban kherbah (in Egypt) Zebda beldia/zebda baladi/zebda beldi Smen Description Fermented milk (buttermilk) obtained by churning spontaneously soured milk to remove butter. A common dairy product in all North African countries though with different names. Raw butter, with a strong diacetyl avor, separated from lben after churning spontaneously coagulated milk. Zebda beldi is a common dairy product to all North African countries. Rancid butter of Maghreb countries obtained from raw butter salted (8% to 10%) and matured in the dark under anaerobic cool (13 to 15 C) conditions for a period of 6 to 12 mo. An Algerian claried butter oil obtained by churning spontaneously acidied camel milk. The butter is then boiled and claried while still liquid after the addition of a clarifying agent (for example, crushed dates) and skimming it off after occulation of impurities. Main microorganisms involved in fermentation as part of safety factors References
Lactic acid bacteria: L. lactis subsp Tantaoui-Elaraki and El Marrakchi lactis, S. salivarius subsp. 1987; Benkerroum and Tamime thermophilus, Lb. delbrueckii subsp. 2004 bulgaricus, plantarum, yeasts: Saccharomyces cervisiae, Kluyveromyces marxianus Same as leben from which it derives but Tantaoui-Elaraki and El Marrakchi dominated by Lc. lactis subsp. lactis 1987; Samet-Bali and others and subsp. cremoris. 2009 Staph. aureus coagulase-negative, Bacillus spp. (not cereus) Yeasts, molds Benkerroum and Tamime 2004; Samet-Bali and others 2009 Kacem and Karam 2006b
Shmen
Raib
Laben zeer
Semna/Sman
Arish, kariesh, or karish cheese
Jben
Klila
Aoules
Lc. lactis ssp. cremoris Lc. lactis ssp. lactis biovar diacetylactis Lb. plantarum Lb. delbrueckii ssp. bulgaricus Lb. paracasei ssp. paracasei Leu. pseudomesenteroides Leu. gelidum Spontaneously curdled raw milk. It may be a Lc. lactis. nished product (consumed as such) or an Lc. lactis ssp. lactis biovar diacetylactis, intermediate for the production of traditional Leuconostoc mesenteroides. cheeses or other fermented milks. A common dairy Leuconostoc mesenteroides subsp. product in all North African countries though with mesenteroides. different names. An Egyptian thick fermented milk obtained by Lb. casei, plantarum, and brevis storage of leben (see above) in an amphorachapped porous earthenware container (zeer) at room temperature allowing it to further sour (nal pH 3.5 to 3.8) and concentrate as a result of whey permeation through the zeer wall. Raw butter that separates from leben preparation is NA heated and claried by sieving through a strainer. A common batter derivative in Egypt and Tunisia, and the same product is called Ghee in India. An Egyptian white soft cheese made from the LAB: Lc. lactis, Lb. casei. remaining curd after removal of the upper cream Yeast: Saccharomyces ker. layer from spontaneously coagulated milk (raib) in an earthenware pot (matared). Unlike the zeer, the matared used to prepare arish is treated to prevent whey permeation (soaking the inside of the pot by seed or olive oil, or a mixture of egg yolk and oil followed by heating in an oven). Arish may be salted before consumption to enhance the taste, or further processed into mish cheese (see below). Fresh cheese obtained by spontaneous fermentation Lc. lactis subsp. of milk followed by whey drainage. It is lactis and subsp. occasionally brined in a saturated saline solution lactis biovar diacetylactis (25 to 30 g salt per 100 mL water) at room Lb. casei susbp. casei, Leuconostoc lactis temperature for 2 to 15 d. Widely consumed in Maghreb countries (Morocco, Tunisia, and Algeria). Cheese curd obtained from a 3- to 4-d-old lben by Pediococcus acidilactis heating and sieving through a muslin cloth or straw basket to discard whey. Usually consumed in Lb. confusus Algeria and Morocco as whey to prevent wastage Ent. faecalis, Ent. faecium of too sour lben. A typical Algerian dry goat milk cheese (87% to NA 92% dry matter) obtained from spontaneously coagulated goat milk, which is churned to remove butter. The resulting goat lben is poured into a clay pot and heated moderately on an open re until proteins precipitate, in a similar manner as klila. The precipitate is strained in a straw basket and the curd is kneaded in small quantity at a time to be given the shape of a at small cylinder (2 cm thick, 6 to 8 cm diameter). The cheese is then sun-dried. Aoules is ground and mixed with date paste or beverage for consumption.
Benkerroum and Tamime 2004; Mechai and Kirane 2008; Bendimerad and others 2012
El-Gendy 1983
FAO 1990
Kurmann and others 1992; Steinkraus 1995
Benkerroum and Tamime 2004; Abd-El Salam and Benkerroum 2006
Abd-El Salam and Benkerroum 2006
FAO 1990
(Continued)

Table 3(Continued) Vernacular name Domiati cheese Description Main microorganisms involved in fermentation as part of safety factors References Aboudonia 1996; Abd-El Salam and Benkerroum 2006
Tallaga cheese Mish cheese
Kishk
Rigouta
Zabadi
A typical Egyptian brined cheese obtained from raw E. faecalis, E. faecium, Lc. lactis, subsp. milk salted (10 to 15 g/100 mL) and coagulated lactis, Lc. lactis subsp. cremoris, Lc. (mixed coagulation: acid and rennet), and the curd garvieae, Lb. casei subsp. casei, Lb. is drained under moderate pressure. Pieces (about plantarum, Lb. brevis, Lb. Delbrueckii, 500 g) are put into brine (15 to 20 g salt per 100 subsp. lactis, Lb. alimentarius, Lb. mL whey) and then conditioned into tightly closed versmoldensis, Pediococcus containers where it ripens for about 3 mo at room inopinatus, and Leu. mesenteroides temperature. subsp. cremoris, Brevibacterium linens and Propionibacterium jensenii Yeasts: Triechospora spp., Saccharomyces spp., Pichia spp., Debrayomyces, Hansenula spp., Torulopsis spp., Endomycopsis spp., Cryptococcus spp. Similar to domiati cheese, but it is not brined and is Lc. Lactis, subsp. cremoris, Lb. casei, and subsp. casei matured under refrigeration temperature (4 to 7 C) for a longer period (up to 9 mo). An Egyptian cheese obtained from a blend of Arish Lactic acid bacteria, Bacillus spp. cheese and lben in a porous earthenware pot (zeer); the mixture is avored with different types of pepper (for example, green, red, hot, and paprika) or black cumin, salted (about 10 g/100 g) and placed in a warm place to ripen. Brine permeation through the porous walls of zeer during the ripening period allows mish to concentrate and be eventually converted into paste. A mixture of dry fermented milk and crushed cereal, Lactococcus spp., Lactobacillus spp., Lb. usually wheat, (2 : 1 to 1 : 3; cereal to yogurt) brevis, Lb. casei, Lb. plantarum widely consumed in Egypt. It is traditionally made from dough containing spontaneously soured milk (leben), parboiled cracked wheat, and salt. This mixture is spread in a thin layer and sun-dried to reach 85% to 90% dry matter, and nally ground into pieces of 2 to 4 mm size. Kishk can be kept for 1 y at room temperature and may be consumed in a variety of ways, but one popular use is in the preparation of a hot porridge-like gruel. Similar to the Italian riccota, rigouta is obtained from Lc. lactis, Enterococcus foecalis cheese whey, which is heated (80 to 90 C) to coagulate the whey proteins (albumins and globulins); the coagulum is then allowed to drain in a traditional straw basket, clean clothes, or other porous plastic or metal containers. Similar to set yogurt, zabadi is prepared from milk Lb. bulgaricus; Streptococcus fortied with skim milk powder, dried whey or Thermophilus. soybean our, heat-treated and inoculated with the yogurt starter culture (Lactobacillus delbrueckii subsp. bulgaricus and Streptococcus salivarius subsp. thermophilus), then kept at 30 to 35 C until coagulation occurs (4 to 24 h)
Aboudonia 1996 Abd-El Salam and Benkerroum 2006
Morcos and others 1973; Steinkraus 1983; Tamime and OConnor 1995
Ghrairi and others 2004
El-Neshawy and El-Shae 1988; Mehanna 1991
NA Not available
of its variants are summarized in Figure 5. The so-called diet khlii (Figure 2d and 5), where meat strips are dipped into olive oil instead of animal fat, is being increasingly popular due to consumer awareness of the risks for cardiovascular diseases associated with cholesterol and other metabolism and nutrition disorders. Properly made and conditioned khlii can be preserved for more than 2 y at room temperature; it is consumed as such (ready-to-eat meat product) or fried with eggs for breakfast. It could also be used as an ingredient in different traditional dishes such as soups, pancakes, and couscous or, more recently, as a topping for pizza.
and drying conditions when applicable. Figure 6 presents a typical process to make sujuk as shown in the photograph of Figure 2e..
Naqaneq/sujuk/soudjouk/msrana Naqaneq is a generic Arabic term used to designate any sausage either raw or cooked obtained from ground meat (beef, lamb, buffalo, or poultry), seasoned and pushed into a natural casing (bovine or ovine intestine) previously soaked in boiling water. Therefore, these products are highly variable from one country to another and even among regions of the same country, depending on the seasoning, the specic casing used, as well as the maturation
Merguez Merguez is a typical Maghreb raw sausage with a small diameter (18 to 22 mm) and which does not undergo maturation or drying, contrary to msrana or sujuk (Figure 2e). Poultry merguez made from turkey or chicken is being increasingly made in a similar way as the beef variety, but without addition of paprika or other food color additives to keep the typical grayish color (Figure 2g). At present, merguez is mainly produced by modern butcher shops at a semi-industrial scale using modern machines to chop the meat and push the batter into the casing, in addition to the use of nitrites functioning as salt, coloring (development of red color if appropriate), and as a preservative agent to prevent the outgrowth of Clostridium botulinum spores and production of botulism-causing toxin. Furthermore, natural casing is being gradually replaced by synthetic collagen casing. Merguez is a highly perishable product and should therefore be consumed within 2 d after preparation
c
Figure 2Main traditional meat products in North African countries. (kourdass: http://www.comlive.net/L-harissa-Tout-Simplement,124674, 780.htm; gueddid: http://ririeur.centerblog.net/6585659-recettes-aid-el-kebir; sujuk: http://www.pockasabi.com): Visited on 23 July 2012.
even when stored under refrigeration conditions. It is usually fried or barbecued to prepare sandwiches. However, in some countries, such as Tunisia and Algeria, it is commonly added as an ingredient in couscous.
by gourmets. Bubanita, tehal, kourdass, and ban-shems are examples of such products, and their technologies with their main physicochemical characteristics that have an impact on microbial growth are summarized in Table 4.
Miscellaneous Vegetable products In addition to muscle tissues, offal is also used to prepare tradiProducts of plant origin (fruits and vegetables) represent an imtional meat products, some of which considered to be a delicacy portant component in the diet of North African countries despite
c
Meat: r Beef, lamb, goat or camel Keeping at room ys ure temperatu for 2 day Aged meat Aging Meat preparation
c
Trimming
Removed fat Lean meat Cutting
eat Strips of me (about 4 cm wide, 40 -60 ong, cm lo and 1-2 cm thick)
Salting 100 (5.0-7.0 g salt/1 g meat)
Seasoning: (Salt, garlic, cum and grou grains of ginger) , min, und f onal: Optio Application of curcuma oring or paprika as colo ts r agent (yellow or red) Cure meat ed Optional: tion of groun chili Addit nd er peppe to: giv a hot spic taste, ve cy an nd rep insects d pel during op pen-air sun-d drying Cur ed gueddid Curing
ing l Placi in a cool perature temp (3 to 4 days)
cal Typic gueddid/Keddid
Figure 3Traditional process to produce 2 gueddid variants. Meat strips being dried are collected daily before sunset and stored overnight in an aerated cool place, then re-exposed to the sun during the day.
their relatively modest per capita consumption (Table 5) as compared to China, for example, where the highest consumption of vegetables worldwide has been recorded over the last 2 decades. Nonetheless, the overall consumption of vegetable products in NA is higher than the minimum level of 146 kg per capita per year recommended by the joint commission of the World Health Organization (WHO) and the Food and Agriculture Organization (FAO) of the United Nations (FAO/WHO 2004). Moreover, an overall tendency to increased fruit and vegetable consumption has been recorded in North African countries in the period of 2000 to 2007 (Figure 7). Figure 7b shows also that the per capita consumption of fruits in most North African countries remained low compared to the global average recorded during the period of 2000 to 2007. Nonetheless, the high per capita consumption of vegetables in these countries during the same period (Figure 7a) would compensate for such a deciency to meet the WHO recommended level for the overall consumption of vegetable products. Although fruits and vegetables are generally consumed fresh, an important part of the harvest is processed for preservation, either at the household level by using traditional low-cost technologies
or in modern factories. Traditional preservation technologies of vegetables products have long been practiced in North African areas to make these wholesome foods available throughout the year. Fermentation, pickling, cooking, and/or drying have been the main traditional techniques used to preserve many ripe products available only at given periods of the year such as olives, lemons, onions, green peppers, carrots, gs, grapes, prickly pears, and so on. Among these, olives are probably the oldest and the most culturally and economically signicant products in the region, and hence their preservation by traditional technologies will be discussed in some details here.
Table olives Olive (Olea europaea L.) is typically a Mediterranean tree that has been grown in the region for millennia, and its fruit has been used in a variety of ways in the diet as a table olive or as raw material to produce olive oil. A number of traditional technologies have long been used in North African countries to produce palatable table olives that could be stored for a relatively long period at ambient
Drying
un-drying*: Su g Hanging meat strips on a ire laundry rope or a wi (5 to 7 days) t
Product t cle Musc lean meat (lion, rib, flank, and ro ound)
Step S
tting Cut Lean strips (50-60 cm long, 10-15 cm wide an d m 5 les than 5 cm thick) ss Sal lting each meat strip: 20 g salt/100 g meat Stacking salted strips in a box Pile of cured meat strips f t (up to 1-meter thic ckness) Rinsing meat st trips to remove excess salt Draining in a cool place Drained meat strips s sing : Press A wooden press (about n 1 ton per meter thickness): 12-24 h Pr ressed meat strips s enting: Ceme ing ip Coati each stri with a 5-8 mm ste layer of spicy pas (cemen c, e): paste Curry, smashed garlic fenugreek, paprika, flour, and ter) salt mixed in wat Spice-coated meat strips t nd Secon drying: Open air place (3 to 10 days) Pastirma
Figure 4Flow diagram of traditional pastirma production (Daoudi and others 2006; Obuz and others 2012).
y-curing Dry (3-4 days)
t First drying o (3 to 5 days)
temperature. However, despite the diversity of these methods, they are based on 2 main procedures: (i) pickling and (ii) drysalting. Both procedures rely, rst on salt to remove the glycoside euloropein that makes olives unpalatable even when they are fully ripened (black olives) and, second, on microbial fermentation to develop acidity and specic aroma while contributing to the microbiological safety of the nal product. Other processes such as the Spanish green olive style and the California style use sodium hydroxide (as a debittering agent to remove euloropein) and other chemical products (for example food-grade acids and potassium chloride) in addition to salt (Cardoso and others 2008; Panagou and others 2013). The latter techniques will not be considered further, as they are used for large-scale commercial production and unlike in European countries (Panagou and others 2013), the addition of chemicals, including sodium chloride, has not been practiced traditionally in North African countries. A typical North African traditional olive pickling procedure is presented in Figure 8. Pickled olives may be seasoned before
consumption by addition of different spices and avoring ingredients including rosemary, coriander leaves, grated garlic, oregano, chopped onion, hot red pepper, and/or lemon juice, lemon pieces, or harissa (Figure 9f). In addition to pickling, table olives may be obtained by drysalting techniques; the most commonly used of which involves packing olives in plain salt for at least 1 mo to produce the socalled Greek style olive. It is the simplest and probably the oldest technique used to preserve olives and make it palatable after removal of the euloropein. In North African countries, this traditional method is exclusively used for fully mature black olives, by placing them in a container as interposed layers with salt in a proportion of 40 g salt to 100 g olives. These salted olives are kept at room temperature until a pleasant avor is reached, generally after 30 to 60 d (Cardoso and others 2008). A related traditional procedure widely used in Maghreb countries consists of placing black olives in a burlap sack or a straw basket and evenly mixing them with salt (10 g per 100 g olives). A heavy weight (usually
eat Muscle me Beef, lamb, goat or camel ,
t Lean meat Cutting 5-10 cm) Strip of meat (5 ps Addi ition of mari inade/sharmula (salt, smash garlic, vi hed inegar, cumi ground in, cori iander grains and seed o and s, oil), Direct use of t keepin at a cool place with o ng occasional cured gueddid stirring for 24 to 36 h trips Cured meat st C Sun-drying: Hanging meat strips on a laundry H rope or a wire (5 to 7 days) trips Dry meat st aw about 6.6 6 Pot containing water, fat and olive c oil with frequ ent stirring u l, until complete evap oration of w water Bulk Khlii batch
h Agrish Small meat pieces m ered from khlii recove arate batch, as they sepa he ps from th meat strip while cooking. c
Diet Khlii Khlii strips dipped in s olive o and oil condition in a ned similar man nner as the typical khlii l
Figure 5Traditional process to produce khlii and 2 of its main variants.
stones of approximately half the weight of the olives) is placed on the top of the sack or basket to accelerate extrusion of olive juice, and euloropein with it. The whole package is left to ferment for 5 d in a warm place (20 to 25 C). Olives are taken out of the sack or basket and spread out under the sun on plastic mat for 1 d, and then put back in the sack or basket for another period of 5 d. This operation is repeated 3 times and then the olives are exposed to the sun for 2 successive days to be ready for consumption. The resulting olives from the application of the latter process have a more pleasant and less salty taste than the Greek-style olives, but they have a limited shelf life not exceeding few months at ambient temperature. Dry salted olives may be rolled in olive oil for a desired taste and shiny appearance and/or avored with various herbs, spices, lemon pieces, and crushed garlic.
Lemons Lemons are widely used as a avoring agent in North African cuisine including tajine, soups, stews, and sh-based dishes. However, they are available at affordable price only during winter and spring seasons when ripening. Therefore, many traditional preser-
vation techniques have been used to make lemon available during summer and autumn when scarce and expensive. The most common of such techniques involves dry-salting and fermentation, usually referred to as the Moroccan style pickled lemon (Figure 9c). According to this technique, ripe lemons (yellow in color) are soaked in fresh water for 3 d while changing the water daily to reduce the bitterness. Each lemon is then cut into quarters from the pointed end to about 2 cm of the stalk end, opened without breaking the quarters apart and lled with coarse salt (about 100 g each). The salted lemons are rmly packed in a clear glass container that is tightly sealed to prevent air access and left in a cool dry place for 4 to 6 wk. Meanwhile, the osmotic pressure exerted by the salt causes lemon juice exude and dissolve the salt, thereby creating a strongly salty and acidic brine that covers partly or totally the lemons in the container. These conditions select for the microorganisms (acid- and salt-tolerant) to govern the fermentation process; they are predominantly lactic acid bacteria and yeasts (Bousmaha and others 2006). However, a recent study on such a cured lemon called msayer or msir in Morocco showed that yeast, represented by Candida parapsislosis and unclassied
c
Conditioning
Cooking
Drying
Curing
Preparation
Pieces of fat
Trimming
Blend of spices (salt, black pepper, Lean ground beef + Fat (1:1)* e cinnamon, cumin, ginger, red hot pepper, paprik a, ground gr rains of coria ander, cardamom, cloves, and garlic) ) 90% 1 10% Bat tter S Stuffing into natural casi o ing ( bovine intes stine) Staffed ca asing: Raw sausages : Drying and fe ermentation: wire Hanging on a rope or a w in an aerated place (3-5 days) n
Sujuk
Figure 6A 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 LAB are only weakly represented during the early steps of curing, and were not detected in the nished product (Aayah and others 2010). Lemon when pickled may be stored for more than a year at room temperature and can be used in various ways as whole or chopped in small pieces. In some instances, only the peel is used. Another type of pickled lemon widely consumed in North Africa, mainly of the Mashreq countries (Libya and Egypt), is the lamoun makbouss. Thoroughly washed lemons are thinly sliced, copiously sprinkled with salt, and left to mature on a plate for 24 h. At this stage, the lemon slices become soft and their bitterness is reduced, they are then placed in layers in a clear jar while sprinkling paprika between the layers. Flavored seed oil (preferred to olive oil with too strong aroma) is added to cover the slices in the container that is then tightly closed and left at room temperature for at least 3 wk (Roden 1974).
ecological parameters during fermentation and storage should be set to promote the lactic acid fermentation, and hence, the growth of LAB (Niketi -Aleksi and others 1973; Peres and others 2012). c c Typically, this procedure involves the preparation of vegetables by sorting, washing, and occasionally slicing. After this preparation step, the vegetables are submerged with the appropriate brine solution in a glass container, which is then tightly sealed and left in a cool place to allow for fermentation. A recent modication of this technique consists in adding vinegar to the brine to ensure successful fermentation, especially when low-salt brine is used. Lowering the initial pH, along with the moderate salinity, helps the LAB predominate over the other microbial groups from the early crucial steps of fermentation when the microbial population is the most complex, thereby ensuring the safety while extending the shelf life of the nal product.
Horticulture vegetables Miscellaneous r Harissa: A typical Tunisian hot paste, but also available in Many garden vegetables such as carrots, turnips, green or red peppers, onions (especially the small variety of pearl onions), and the other North African countries, harissa is prepared from cauliower are commonly preserved, individually or as mixtures, a blend of spices, with dried chili as the key ingredient, in whole or in pieces, by traditional North African techniques. The water. Coarsely ground dried chili and other ingredients, inmost commonly used of such techniques is brining in weak or cluding crushed garlic, paprika, coriander seeds, cumin, nely strong brine depending on the desired gustatory quality and the chopped spearmint leaves, and salt, are mixed with water to expected shelf life of the nal product. Weak brine (about 2.5 g make a heavy red paste (Figure 9f). Traditionally, harissa is per 100 mL water) yields mildly salty and acidic products with a used with cooked meats such as kebabs and appears on the relatively short shelf life (3 to 6 mo), while strong brine (>10 of table in small plates as a multipurpose sauce or appetizer, essalt per 100 mL water) yields salty but moderately acidic products pecially in restaurants; it is also used as seasoning for brined that may be stored for more than a year. However, the latter green olives. r Tabil: A variant of harissa prepared in the same way except products should generally be soaked or rinsed in fresh water before consumption to dilute the saltiness. In both cases, the prevailing that cumin and paprika are omitted to make it hotter.
c

Table 4Traditional meat food products of North African countries: technology and main physicochemical characteristics. Product Meat Products Gueddid Pastirma Khlii Mkila Technological process Main physicochemical characteristics pH See Figure 3 See Figure 4 See Figure 5 Fresh lamb or goat meat strips salted, marinated, and cooked in a fry pan (Makla in Arabic), and then conditioned in animal fat, the product is called Mkila after the utensil (Mkila, diminutive of Makla) where it is cooked Prepared by using fresh beef strips marinated into sharmula for 1 h, cooked and dipped in animal fat for conservation Prepared from ground meat (30% to 20% fat) mixed with different spices (salt, black pepper, cumin, hot red pepper, paprika, and ginger), and stuffed into natural casing (ovine or goat small intestine) See Figure 6 aw Moisture (%) Bennani and others 1995 Obuz and others 2012 Bennani 2003 Chafa 2012 Reference
5.2 to 5.3 0.50 to 0.65 7.54 to 14.26 4.5 to 5.8 0.85 to 0.90 39 to 52 5.2 0.65 11.78 NA NA NA
Express khlii Merguez
NA 5.0 to 5.5
NA NA
NA 77.5
Chafa 2012 Benkerroum and others 2003b; Yin and Cheng 2003 Kayaard and Gok 2003; Hwang and others 2009 Daoudi and others 2006
Sujuk
4.6 to 5.6 0.86 to 0.92 NA NA
36.49 NA
Bubanita/boubanita A typical Moroccan specialty prepared from lamb meat cut into small cubic pieces, seasoned with spices (cinnamon, cumin, ginger, red chili, paprika, coriander, olive oil, and salt) and stuffed into previously cleaned lamb rumen, which is then tied at its openings with a rope and hung to a roof where it is left to dry and ferment slowly in the shade. Tehal/tehane Bovine spleen stuffed with ground beef that is seasoned with various spices, including hot chili, and cooked in an oven (Figure 2f). Kourdass/kurdass A Moroccan meat product made with lamb stomach, intestines, liver, lung, and fat. All the constituents are cut into pieces, dry-salted and seasoned with black pepper and occasionally cumin. Stomach pieces of about 1510 cm are used to wrap the pieces of liver, lung, and fat into rolls (the rough side of the stomach toward the exterior). Each roll is diametrically rolled up in the intestine to be sealed and sun-dried for 7d (Figure 2g). Ban-shems A Libyan traditional meat product prepared from bovine stomach stuffed with pieces of kidney, liver, and lung. The stomach and the other offal pieces are sun-dried separately, and the pieces of kidney, liver, and lung are packed into the stomach, and then cooked and conditioned in animal fat in a similar manner as for khlii.
NA NA
NA NA
NA NA
Daoudi and others 2006 Daoudi and others 2006
NA
NA
NA
Daoudi and others 2006
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- oor/roof or any kind of surface, the fruits should be spaced about tries (FAOSTAT 2012). Data of China are given for comparison. Country Algeria Egypt Libya Morocco Tunisia China Production Fruits Vegetables 3,535.544 4,535.92 9,581.15 19,516.40 386.05 948.35 3,292.41 5,487.02 1,254.78 2,675.93 122,184.94 473,062.94 Consumption Fruits Vegetables 63.72 119.02 99.87 203.13 66.23 203.03 69.68 136.44 87.46 216.14 64.42 279.89
Fruits Traditional techniques, especially sun-dying, have long been used in North African countries to preserve some highly perishable fruits such as gs, grapes, and prickly pears. These fruits are produced for a few weeks during summer or autumn seasons and should be consumed as quickly as possible after harvest, as is the case for gs, which should be consumed the same day. In this period of the year, the weather conditions are optimal for the drying operation; the temperature averages 25 to 30 C and the air is generally dry. Such conditions have, indeed, been reported to give the best-quality sun-dried fruits (Tang and Yang 2004). Upon full maturation, fruits are evenly spread over the oor of open space (threshing) or a cottage roof coated with a plastic or straw mat, large foliage such as that of g, grape, or carob leaves may be used. Recently, a mesh wire has been preferred as a mat for g
2 cm from each other to allow good aeration and water evaporation. In some Moroccan regions, grapes are pretreated by dipping for a few minutes in a sieved solution consisting of a mixture of ash from incinerated fava bean stems, quicklime, and salt in water. Such treatment is believed to prevent alterations due to fermentation, rot, or mold growth during drying or storage (Mazhour 1983). Figs are usually dried as a whole fruit, but in some instances, they are cut open and sprinkled with nely ground herbs such as thyme, rosemary, or pennyroyal, before drying. This procedure is especially used when the dry gs are intended for home consumption or sale in neighboring rural markets, as they cannot be preserved for more than 3 mo (Figure 10b). This product is essentially known in the Jbala and Tizi-Ouzou regions of Morocco and Algeria, respectively, where it is called shreeha. While raisins (zabib) obtained from dried grapes are consumed directly or utilized in various culinary preparations (pastries, dishes, appetizers, and so on), dried gs are consumed as such, especially during Ramadan (the fasting month for Muslims) with soup. Drying of prickly pears is conducted in a similar manner after removing the peel; however, it is a rare practice and is restricted to only a small number of villages in remote areas in Morocco and Tunisia (Mazhour 1983). Likewise, the most available raisins in North African markets are those obtained in modern factories using industrial dryers and chemical additives such as sulfur dioxide.
Safety of North African traditional foods . . . Potential microbiological hazards associated with traditional foods of North Africa Irrespective of the origin of traditional foods (plant or animal), the raw material used for their manufacture is nutritionally rich and provides an adequate environment for the growth of various microorganisms including those of health and spoilage signicance. In addition, the raw material generally hosts an abundant and complex microbial ora whose microbial groups would potentially grow and compete for nutrients. Therefore, the main purpose of traditional technologies is the alteration of ecological parameters of the raw material in a way to select for specic benecial groups of microorganisms that will govern the processing steps and eventually predominate (Steinkraus 2002). The product may then be considered safe while having the desired and unique nutritional and gustatory qualities. On the other hand, some traditional technologies aim to inhibit or inactivate as many of the microorganisms as possible initially present in the food to allow the least microbiological changes during storage, thereby extending the shelf life of the food as long as possible. This is usually achieved by heat treatment (scalding or boiling), dehydration, and/or use of high salt or sugar concentration. Some traditional meat products, such as gueddid and khlii, dairy products including kishk, domiati, tallaga, and aoules, and vegetable products such as pickled lemon, dried gs, prickly pears, and raisins, are examples of such foods. Nonetheless, survival or adaptation of microbial strains/groups to extreme conditions is well documented (for a review, see Beales 2004; Allen and others 2007), and these products may still be at risk to consumers.
Figure 7Consumption trend of (a) vegetables and (b) fruits in North African countries and in the world (global average consumption of 200 FAO member countries) during the period of 2000 to 2007. Compiled from FAOSTAT (2012).
Microbiology of Traditional North African Foods and Associated Hazards

In North Africa, traditional technologies for food preservation rely almost exclusively on natural hurdles (fermentation, dehydration, high osmotic pressure and/or, heating) to inhibit the growth of undesirable bacteria and provide safe and stable foods. The contribution of the resulting products to food security in North African countries is undeniably due to their availability at affordable prices, high nutritive value, and health-promoting properties (Anukam and Reid 2009; Peres and others 2012). However, their hygienic quality is highly variable depending on many factors including the microbiological quality of raw materials and ingredients, as well as the sanitary conditions during harvest, manufacture, packaging, and storage. They may thus compromise the consumers health. Indeed, contamination of such foods with pathogens and/or microbial toxins is well documented. Table 6 provides examples of bacterial pathogens associated with the main traditional dairy, mat, and plant products. Moreover, traditional foods have been reported to be associated with infectious diseases and intoxications (Cosivi and others 1998, Belomaria and others 2007, Bendahou and others 2008) or with other pathogens of concern to food safety (Paramithiotis and others 2012). Yet, only few traditional food-related outbreaks have been recorded in North African countries due to the poor public awareness and the lack of media reports, especially when the issues of intoxication episodes are not severe or do not require emergency hospitalizations.
c
Dairy products Traditional dairy products of North African countries are generally obtained from raw milk, with few exceptions where the milk is heated or boiled, which undergoes spontaneous acidication with LAB (Table 3) before proceeding to other technological steps depending on the desired nal product. Therefore, these dairy technologies rely essentially on the fermentation with LAB as a barrier to prevent the growth of pathogenic and spoilage microorganisms. LAB bacteria have the generally recognized as safe status (GRAS) due to their long history of safe consumption by humans, and to the fact that they have rarely been associated with food intoxications or infectious diseases (Hammes and Tichaczek 1994). In addition, virtually, all species of LAB have been shown to produce a variety of biologically active substances, including organic acids, hydrogen peroxide, carbon dioxide, diacetyl, reuterins, and bacteriocins, all with antagonistic activities against microorganisms of health and spoilage signicance (Piard 1992; Ouwehand 1998). Moreover, proteolytic LAB have been shown to generate endogenous bioactive peptides with potent antimicrobial activities upon hydrolysis of milk proteins during fermentation (Hayes and others 2006; Benkerroum 2010; Ghal and others 2010). Nonetheless, studies on traditional North African dairy products have revealed that those among them which rely only on the lactic acid fermentation and the consequent lowering of the pH (3.8 to 4.5), such as fermented milk products including zabadi, raib, lben, and fresh cheeses are generally of poor microbiological quality, as suggested by the high counts of indicator bacteria, fecal coliforms, and enterococci, which exceed 104 colony forming unit (CFU)/mL or g (Hamama 1992), and the occurrence of serious foodborne pathogens (Table 6). In addition, these products have a short shelf life (3 to 10 d) even when stored at refrigeration temperature (Samet-Bali and others 2009), suggesting that they are prone to support the growth of various undesirable
-color olives only) Ha arvested olives (Green and changing Cleaning (re emoval of dust, leaves and other plant debris) Washing Sorting ves ed Sorte clean oliv Slightly crushing olives with a stone Pr rickling each olive sever times ral r with a fork, or Cu utting each o olive with 1 to 3 deep ansverse slit ts tra njured olives In Placing in an earthenware pot or a e ucket bu Covering wit h a saline so olution (5 g salt/100 mL water) Daily replace ement of the brine y with a freshly prepared one during 12 days
ced es Olive with reduc bitterness Replacing the brine with a s stronger e: one 10 to 12 g salt per 100 mL water Promoting anae erobiosis: -Addition of a n olive oil layer (about 1 cm thick) o n the top of the brine f ing -Tightly seali the container -Placing the c ontainer at a cool temperature (about 15-20C)
Conditions that favor the growth of mesophilic lacitic acid bacteria
ves: Pickled oliv Ready for consumption (20-30 days of ferme d entation) Optim taste after 3 months of fermentation mal
Figure 8Flow diagram of traditional pickling of olives as practiced in North African countries.
microorganisms. To circumvent such a limitation and enhance the safety and keeping quality of North African traditional dairy products, other hurdles to microbial growth including salting and/or drying (low aw ) or heating have often been combined with lactic acid fermentation. Examples of such products are the Moroccanbrined cheese jben malah (matured and stored in saturated brine), Egyptian domiati and tallaga cheeses (5% to 10% salt content and stored in brine), dried kishk, and Algerian aoules obtained from spontaneous acidication of milk followed by heat treatment and sun-drying. The pH of these products is as low as 3.5 and their dry matter increases to levels as high as 90% to 92%, corresponding to water activity (aw ) values of 0.34 to 0.43 where microorganisms can no longer survive (Steinkraus 1983; FAO 1990; Tamime and McNulty 1999; Mennane and others 2007). Addition of aromatic plants (thyme, oregano, and rosemary) along with high
salt concentration to some traditional dairy products, such as the Moroccan smen, has also been practiced empirically to add a safety factor and to avoid surface spoilage with molds, as these plants are well known for their potent antifungal activities (Cowan 1999; Hammer and others 1999; Chebli and others 2003; Rota and others 2004; Amarti and others 2008). In spite of these treatments, pathogenic bacteria and molds have been detected in virtually all North African traditional dairy products, and some of these bacteria would grow and produce highly toxic metabolites under certain conditions. Survival of raw milk pathogens to the processing steps or contaminations due to the lack of good manufacture practices (GMPs) and personal hygiene, or improper storage conditions, are the most frequent causes for the presence of undesirable microorganisms in nished products. Moreover, the poor sanitary conditions during milking and the lack of veterinary care for
Brining/Fermentation
Debettering g
Oli preparation ti Olive
Figure 9Selected 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 husbandry in North Africa), in addition to the low hygienic quality of water, contribute to produce raw milk of poor microbiological quality. Regardless of the type of domestic milk animal (cow, sheep, goat, buffalo, and camel), the total viable counts usually exceed 106 CFU/mL and the counts of fecal indicators (coliform and enterococci) are higher than 104 CFU/mL (Hamama 1992; Benkerroum and others 2003a; El-Diasty and El-Kaseh 2007). Moreover, foodborne pathogens of major concern in food safety such as Listeria monocytogenes, Mycobacterium bovis, Mycobacterium tuberculosis, enterohemorrhagic Escherichia coli, Staphylococcus aureus, and Campylobacter jejuni have frequently been
isolated from raw milk in North African countries (Hamama 1992; El Marrakchi and others 1993; WHO 1994; Cosivi and others 1998; Benkerroum and others 2004b; Bendahou and others 2008). Therefore, the frequent presence of pathogens in fermented milks or cheeses obtained from such raw milk is not surprising. When raw milk is heavily contaminated and the technological processes are carried out under poor sanitary conditions, as is usually the case in North African dairy farms, natural hurdles to microbial growth are a limited safety factor (Benkerroum and Tamime 2004). Another issue of concern related to North African traditional dairy products is the presence of enterococci at high levels, usually
Figure 10Figs being dried on a roof covered with a mesh wire (a) and 3 types of dried gs: (b) cut open dried g, (c) gs dried as whole, pricked from the center and put together in the form of beads with a string, and (d) whole dried gs packaged in bulk.
exceeding 104 CFU/mL, with Enterococcus faecalis and foecium as the predominating species (Benkerroum and others 1984; TantaouiElaraki and El Marrakchi 1987; Benkerroum and Tamime 2004). The presence of this group of microorganisms in fermented foods is, in fact, controversial. Although members of Enterococcus genus have been shown to possess highly desirable technological and health promoting properties (Bertolami and Farnworth 2003; Belamri and Benkerroum 2005; Pollmann and others 2005; Moreno and others 2006; Zeyner and Boldt 2006), their association with food spoilage (Franz and others 1999), food intoxication (Giraffa and others 1997; Gardini and others 2001), nosocomial infections (Kayser 2003), and spreading of antibiotic resistance through the food chain (Valenzuela and others 2008) has also been well documented. In a survey on risk factors in enterococcal strains isolated from Moroccan dairy products, Valenzuela and others (2008) revealed the widespread multiantibiotic resistance and/or occurrence of virulence factors (sex pheromones, collagen adhesins, enterococcal endocarditis antigen, and enterococcal surface proteins) among the isolates of Ent. faecalis and Ent. faecium (Valenzuela and others 2008). According to these authors, high counts of enterococci represent a risk factor in Moroccan foods, and appropriate measures should be taken to reduce their incidence. In addition to food safety concerns related to bacteria and fungi, the presence of viruses, parasites, and protozoa in North African traditional dairy products may also represent serious hazards to consumers, which has so far been disregarded or overlooked. The occurrence of the latter microorganisms in North African raw milk has been repeatedly demonstrated (Carter 2005; Dawson 2005; Pollmann and others 2005) and is of paramount importance to the safety of dairy products, especially when no heat treatment is applied during processing or at point of consumption. In view of the high incidence of zoonotic diseases in North African herds (Araba and Essalhi 2007; Berrag and others 2009; Bouzid and others 2010) especially with the lack of veterinary care in small farms and the poor hygienic quality of water (the probable vehicle
for various viruses, protozoa, and parasites), this issue warrants due attention from all stakeholders and scientists. The presence of mycotoxins in traditional North African dairy products also raises an increasingly alarming concern regarding public health safety. It is well established that mycotoxins may contaminate dairy products by molds growing on them under certain conditions, or by the carryover of mycotoxins occurring in animal feedstuffs ingested by dairy animals and later transferred from blood into milk (van Egmond 1983; Veldman and others 1992; Galvano and others 1996; Zinedine and others 2006; Masoero and others 2007). The most important of such mycotoxins to dairy products is aatoxin M1 (AM1) derived from the conversion of ingested aatoxin G1 in the animal liver (TantaouiElaraki and Khabbazi 1984). AM1 was detected at concentrations ranging between 4.0 and 6.0 g/L in 12.5% of Libyan raw milk (El-Diasty and El-Kaseh 2007). In a study on the occurrence of AM1 in raw milk marketed in different cities of Libya, Elgerbi and others (2004) showed that 35 samples of raw bovine milk out of a total of 49 (71.7%) tested positive for AM1, with average concentrations varying between 0.12 and 0.72 g/L depending on the city from which the samples were taken; 34 among the 35 positive samples (about 97%) were contaminated with levels exceeding the maximum tolerable level (MLT) of 0.05 g/L (Elgerbi and others 2004). Higher concentrations (average of 6.3 g/L) were reported in Egyptian raw bovine milk (El-Sayed and others 2000). Such levels of contamination with AM1 are alarming in view of the MLT which should be less than 0.05 g/kg or L, depending on the country and commodity (Dohlman 2003). In Moroccan pasteurized milk, AM1 was detected at high frequencies (88.8%), but at relatively low concentrations compared to those found in Libyan and Egyptian milks; the concentrations reported ranged between 0.001 and 0.117, with an average of 0.018 g/L, and 7.4% of the samples contained higher levels than the MTL (Zinedine and others 2007a; Zinedine and Ma es 2009). Accordn ing to Tantaoui-Elaraki and Khabbazi (1984), AM1 concentration

Table 6Hazards of microbiological (pathogens and/or their toxins) associated with North African traditional food products. Commodity Dairy products Lben Smen Associated pathogens Staph. aureus, Salmonella spp. Pathotypes of E. coli Staph. aureus, Cl. perfringens, Cl. Botulinum Bacillus cereus E. coli O157, L. monocytogenes, Staph. aureus, Y. enterocolitica E. coli O157, L. monocytogenes, Coagulase positive Staph. aureus, Salmonella spp. E. coli O157 H7 Campylobacter spp., L. monocytogenes, Cl. perfringens, Staph. aureus, Vibrio spp. B. cereus Clostridium spp. B. cereus, Cl. botulinum, Cl. perfringens Staph. aureus, Cl. botulinum Cl. botulinum, Cl. perfringens, Staph. aureus, E. coli O157:H7 Cl. botulinum, Bacillus spp. NA NA Cl. botulinum, perfringens, Staph. aureus, Campylobacter spp., L. monocytogenes, various pathotypes of E. coli, Salmonella Manhattan, Salmonella spp., Staph. aureus Cl. botulinum, E. coli O157:H7, S. Typhimurium, L. monocytogenes Staph. aureus, Cl. botulinum Cl. botulinum, Cl. perfringens, coagulase-positive Staph. aureus, E. coli O157:H7 Bacillus spp. NA NA Cl. Botulinum, perfringens, Campylobacter spp., L. monocytogenes, various pathotypes of E. coli, Salmonella Manhattan, Salmonella spp., Staph. aureus Cl. botulinum, E. coli O157:H7, S. Typhimurium, L. monocytogenes Cl. botulinum, Cl. perfringens, L. monocytogenes, Bacillus cereus Cl. botulinum Pseudomonas enteridis, L. monocytogenes Reference Hamama 1992; El Marrakchi and others 1993; Benkerroum and others 2004b Tantaoui-Elaraki and El Marrakchi 1987; EL Marrakchi and others 1988; Benkerroum and Tamime 2004 Hamama 1992; Hamama and others 1992; El Marrakchi and Hamama 1995; Hamama and others 2002; Benkerroum and others 2004a; Achemchem and others 2006 Hamama and others 1992; Elotmani and others 2002 Quinto and others 2000 Nour and others 1987; Abd-El Salam and Benkerroum 2006; Sadek and others 2006; El-Baradei and others 2007 Abd-El Salam and Benkerroum 2006; Sadek and others 2006 Taha and Abdel-Samie 1961 Tamime and McNulty 1999 Bennani and others 1995 El-Khateib 1997; El-Safey and Abdu El-Raouf 2003; Obuz and others 2012 Bennani 2003 NA NA Ettriqui and others 1995; El-Khateib 1997; Bendeddouch and Lebres 2003; Benkerroum and others 2003b; El-Safey and Abdu El-Raouf 2003; Yin and Cheng 2003; Benkerroum and others 2004b; Al-Gallas and others 2006; Nol and others 2007; Cohen and others 2008; Badri and others 2009 e Kayaard and Gok 2003; Hwang and others 2009 (Bennani and others 1995) El-Khateib 1997; El-Safey and Abdu El-Raouf 2003; Obuz and others 2012 Bennani 2003 NA NA Ettriqui and others 1995; El-Khateib 1997; Bendeddouch and Lebres 2003; Benkerroum and others 2003b; El-Safey and Abdu El-Raouf 2003; Yin and Cheng 2003; Benkerroum and others 2004b; Al-Gallas and others 2006; Nol and others 2007; Cohen and others 2008; Badri and others 2009 e Kayaard and Gok 2003; Hwang and others 2009
Jben Raib Zabadi Domiati cheese Tallaga cheese Mish cheese Kishk Meat products Gueddid Pastirma Khlii Mkila Express khlii Merguez (fresh sausages) Sujuk Gueddid Pastirma Khlii Mkila Express khlii Merguez (fresh sausages) Sujuk Plant products Pickled green olives Black olives Pickled vegetables
Caggia and others 2004; Panagou and others 2008; Pereira and others 2008 Anon 2012 Okudaira and others 1962; Fleming and others 1992; Lee 2004
Not detected but suggested to have a potential to contaminate and survive in these products, especially when their acidity is mild (Fleming and others 1992; Lee 2004).
in raw milk increased by 3.2- to 3.7-fold in cheeses made from contaminated milk, as neither heat treatment nor the subsequent steps in cheese making (curd drainage, handling, and maturation) removed much of the toxin initially present in the milk. It could be anticipated, on this basis, that levels of AM1 in cheeses obtained from contaminated milk would exceed the MTL even when the initial level of AM1 in raw milk is below this value. However, a survey on the occurrence of AM1, aatoxin B1 (AB1), and aatoxin G1 (AG1) in Egyptian dairy products revealed that AM1 was detected in raw milk more frequently and in more elevated amounts than in different cheese varieties or in dried milk; AM1 concentrations of 6.3, 5.0, 6.0, and 0.5 g/L or kg were detected in raw milk, dried milk, hard cheese, and soft cheese, respectively, whereas AB1 and AG1 were detected in hard cheese at concentrations of 3 and 6 g/kg, respectively (El-Sayed and others 2000). Similarly, the average concentrations of AM1 in Libyan white soft cheeses (from 0.21 to 0.34 g/kg) were lower than those determined in raw milk; yet, 15 cheese samples out of 20 (75%) tested positive for AM1 and contained concentrations exceeding the MTL (Elgerbi and others 2004). It could be argued, however,
that there is no correlation between the levels of mycotoxins in the cheeses samples analyzed in the latter studies and those determined in the raw milk, as all the samples were taken at random from local markets. In a more relevant study, Hassanin (2006) has monitored the level of AM1 in yogurt, yogurt-cheese, and acidied milk produced from a naturally contaminated milk with AM1. The results revealed that the concentration of AM1 signicantly decreases as a function of time during storage at refrigeration temperature, which was explained by the interference of LAB with mycotoxin activity. Many studies have shown that LAB are able to sequester, or inhibit, the in situ production or toxicity of mycotoxins, thereby reducing their potential risk in fermented milks and cheeses (Gourama and Bullerman 1995; Kim 2007; Bianchini and Bullerman 2009). Dairy lactic acid bacteria belonging to different genera have been reported to be effective in removing AB1 and AM1 (El-Nezami and others 1998; Oatley and others 2000; Pierides and others 2000). Nonetheless, further studies are needed to accurately estimate the concentrations of mycotoxins and monitor their fate during processing and/or storage in different traditional North African dairy products obtained from the milk of

Table 7Average microbial counts (log CFU/g) in different meat and offal the water activity to levels below 0.86 where no pathogenic bacsamples in 2 major Moroccan cities. teria would grow (Jay 1986; Barbosa-C novas and others 2003), a Microorganisms TAC Coliforms E. coli Staph. aureus Cl. perfringens SRC Beef 7.3 3.7 3.2 2.3 1.3 NA Casablanca Lamb Heart 6.7 6.4 3.7 3.3 3.2 1.8 2.8 3.1 1.2 1.2 NA NA Liver 7.5 3.8 3.4 2.0 1.8 NA Fez Ground beef 6.1 4.8 3.9 2.3 NA 1.5
(Cohen and others 2006). (Oumokhtar and others 2008).
TAC: Total aerobic counts. NA: Not available. SRC: Sulte-reducing clostridia.
different animal species. Such studies are crucial to characterize the risk and estimate the dose/response in a risk-assessment process, the cornerstone in any future regulatory or control measure related to food safety worldwide.
Meat products The overall safety of meat products is contingent on many factors including the initial quality of meat and ingredients, the sanitary conditions during handling, processing, and storage, as well as the preservation hurdles used. Raw and offal meat used to produce North African traditional meat products is generally heavily contaminated with microorganisms of hygienic signicance. In this regard, a study conducted by Cohen and others (2006) on beef, lamb, and beef-offal marketed in the city of Casablanca (Morocco) has shown that these products were highly contaminated; and pathogenic staphylococci and Cl. perfringens were detected at relatively high counts (Table 7). A similar study on ground beef marketed in the city of Fez (Morocco), carried out by Oumokhtar and others (2008) also demonstrated the poor sanitary quality of the product (Tables 7), with more than 80% of the analyzed samples not meeting the Moroccan regulatory standards for meat products (http://www.onssa.gov.ma/onssa/fr/vv_dec15.php). In the latter study, Salmonella sp. and Shigella were detected in a 25 g sample at the respective frequencies of 17.5% and 2.5%. Furthermore, pathogens such as enterohemorrhagic E. coli, Yersinia enterocolitica, L. monocytogenes, and Salmonella spp. have been repeatedly isolated from meat samples in Morocco and other North African countries (Karib and others 1994; Ettriqui and others 1995; AbdulRaouf and others 1996; Al-Gallas and others 2002; Khosrof Ben Jaafar and others 2002; Benkerroum and others 2004b). Occurrence of parasites (protozoa and helminthes) of the genera Toxoplasma, Sarcocystis, Cryptosporidium, Fasciola, Flatworms, Tapeworm, and roudwarms in meat and offal is also well documented (Sawadogo and others 2005; Valinezhad and others 2008; AbdelGhaffar and others 2009; Berrag and others 2009). Given the poor hygienic quality of raw meat, traditional technologies in developing countries use more than one hurdle, acting in synergy, to ensure a relatively satisfactory degree of hygienic quality. Indeed, almost all the traditional technologies for meat transformation in North African countries combine salting, herb and spice addition, drying, and, occasionally, cooking, especially when long shelf life and a high degree of safety are sought. Less stringent conditions are used when a product is not intended for an extended preservation period and is cooked before consumption, as is the case for merguez and tehal. In cured and fermented meat products, such as sujuk, gueddid, kourdass, and pastirma, salting, drying, and herb and spice adjunction are the main parameters used to ensure their safety and stability. While salting and/or drying reduce
spices inhibit specic microorganisms including bacteria, molds, protozoa, and viruses (Farag and others 1989; El-Khateib 1997; Cowan 1999; Daferera and others 2000). In addition, a decrease in the pH to about 5.5 at the rst phase of maturation, while not efcient by itself to inhibit many pathogens, stimulates the growth of LAB, which, in turn, will further inhibit undesirable microorganisms through antibiosis interactions. In this regard, the wide occurrence of bacteriocin-producing enterococci has been reported in Tunisian gueddid (Ben Belgacem and others 2008), 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, such as the Moroccan khlii and Libyan ban-shems, the cooking during processing inactivates microbial pathogens or toxins that may be present on the meat or offal used for their preparation. Although there is a lack of scientic data regarding the hygienic quality of North African traditional meat products and epidemiological studies on their involvement in food outbreaks, it could be anticipated that they may compromise food safety as suggested by the widespread occurrence of pathogens in North African traditional meat products (Table 6), and also for the main reasons below: r Lack or inappropriate veterinary care in the farms where meat-production animals are raised; a weak prophylactic program and inadequate treatment of diagnosed bacterial infections or parasitic infestations (Berrag and others 2009). r Slaughtering, carcass dressing, evisceration, and meat cutting are generally done in poor sanitary conditions which, combined with the nonrigorous or absent (farm-slaughtering) veterinary inspection at slaughter, strongly suggest that meat or offal deriving from animals infected with virulent bacteria, viruses, or parasites would be used to manufacture traditional meat products. r Production of traditional meat products in small farms, butcheries, or food shops where the sanitary conditions are usually not appropriate, and none of the GMP, good hygiene practice (GHP), or hazard analysis and critical control point (HACCP) program is implemented. r Inadequate conditioning, packaging, and storage conditions. Yet, efforts in packaging are being increasingly made as part of a marketing approach. In fact, it is well established that these are the main factors that impact the safety and keeping quality of the nished meat products, and failure to address any of them properly will invariably result in a meat product of high risk to consumers. Nonetheless, on the basis of moisture content, North African traditional meat products may be divided into 3 groups as dened by Marshall and Bala (1998) and Leistner (2000b), each of which present a different pattern of health risks to consumers from the microbiological standpoint: (i) dry meat products (less than 15% moisture) such as gueddid, kurdass, khlii, and ban-shems, (ii) intermediatemoisture meat products (15% to 20% moisture or an aw of 0.65 to 0.90) typically represented by pastirma and certain types of sujuk (Table 4), and (iii) fresh meat products (>20% moisture) including merguez, mkila, tehal, and some types of sujuk where no or partial drying is applied during processing. Due to their low moisture and/or high salt contents, the rst 2 groups are generally regarded as microbiologically safe, and they may be consumed as such or after being lightly cooked; these include khlii, some sujuk types, and pastirma. Such an assumption has been substantiated by some
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studies, showing that the overall microbiological counts are either low or dominated by benecial LAB and that some foodborne pathogens do not grow or survive in these products (El-Khateib 1997; Bennani and others 2000; Huang and Nip 2001; Kalalou and others 2003). El-Khateib (1997) showed that the numbers of Enterobacteriaceae, and yeasts and molds were less than 100 CFU/g in 50 samples of Egyptian pastirma, which were also free from Salmonella. The absence of Salmonella was explained by the inhibitory effect of the spice paste used to cover pastirma, as has been demonstrated in vitro (El-Khateib 1997). The same study showed that the total aerobic count (TAC) and the Lactobacillaceae ranged between 1104 and 9106 CFU/g, suggesting that LAB are the main responsible for the evolution of the product during ripening, which represents a good indication regarding the safety of the product. In addition to the antimicrobial effect of the cover paste, inhibition of pathogenic bacteria in pastirma was suggested to be due to the combined effect of water loss and salt content (4.5% to 6%) with the consequent decrease in water activity (Leistner 2000a; Bechtel 2001). In effect, challenge studies between an E. coli O157 : H7 strain and protective cultures of Lb. sakei and Staph. xylosus in pastirma have demonstrated that the most signicant reduction in the counts of the pathogen was recorded after the drying step regardless of whether or not the protective cultures were present (Aksu and others 2008). Similar results were reported for Moroccan gueddid where numbers of TAC, coliforms, and staphylococci showed a dramatic decrease after the maturation step to reach an undetectable level in a 1 g sample for coliforms and staphylococci, and about 40 CFU/g for TAC (Kalalou and others 2003). According to their study, the sharp decrease in the microbial counts paralleled the decrease in water activity (aw ) to a nal value of 0.66. Furthermore, neither Salmonella nor clostridia were detected in laboratory-made or commercial gueddid samples (Bennani and others 1995; Bennani and others 2000). However, despite such reassuring data, though partial and fragmentary, there is no absolute guarantee for the safety of these products. Indeed, the related salted-dried jerky meat prepared in a similar manner and having a water activity value as low as 0.3 has repeatedly been associated with a number of Salmonella and Staph. aureus outbreaks in the U.S.A. (CDC 1995; Eidson and others 2000; Smelser 2004; Allen and others 2007). Nonetheless, it could be assumed that the marinated variant of gueddid would be microbiologically safer than the classical type. The application of acid marinade to meat before drying has been shown to enhance signicantly the microbiological quality of the nal product (Nummer and others 2004). On the other hand, North African traditional fresh meat products are usually heavily contaminated with microorganisms of health and spoilage signicance; they thus present a higher risk to consumers than their dry or intermediate-moisture counterparts. However, such risk may be reduced at consumption, as these products are cooked or grilled before consumption. In this regard, a study on the microbiology of different Egyptian fresh sausages showed that the aerobic plate count (APC) and Enterobacteriaceae counts ranged from 1.1104 to 1108 and from 1102 to 1107 CFU/g, respectively, and Cl. perfringens and coagulase-positive Staph. aureus were detected at the respective frequencies of 26% and 29% (El-Khateib 1997). Moreover, in a study on the incidence of shiga toxin-producing E. coli O157 in Moroccan meat products, the pathogen was detected in 20% of the spiced ground meat normally used in merguez preparation, but not in merguez sausages; such a discrepancy could be explained by the sampling procedure and the limited number of samples studied (Benkerroum and others 2004b).
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Mycotoxins are contaminants of microbial origin, which also raise concern about the safety of meat products. The presence of molds in meat and meat products is well documented, and under certain conditions, they may grow and produce mycotoxins (Sweeney and Dobson 1998). Molds usually grow on dry or intermediate-moisture meat products during the rst days of drying, especially if the drying process is slow or the relative humidity in the atmosphere is high. They may also grow in the nished product if the storage conditions are not adequate. However, this growth is usually considered by the producers only as a harmless surface discoloration and is then removed by brushing the sausages or cleaning them with a wet cloth to avoid wasting meat. Yet, such growth may represent a serious risk factor if the contaminating molds are toxinogenic. A study on the mycology of pastirma has revealed the predominance of species belonging to Penicillium and Aspergillus genera (Abdel-Rahman and others 1984). These genera are well known for their ability to produce mycotoxins (Sweeney and Dobson 1998). A study on Egyptian pastirma showed that the numbers of molds varied from 103 to 106 CFU/g in summer and from 102 to 105 CFU/g in winter, and that Aspergillus, Penicillium, Mucor, Rhizopus, Fusarium, and Cladosporium were the predominating genera in the product (Refai and others 2004). In addition, the spices used in the preparation of North African traditional meat products are usually contaminated with variable levels of mycotoxins and are thus potential sources for the contamination of these products. Aatoxins were determined in the pastirma spice paste and its constitutive spices individually; the contamination level of the spice paste varied from 9.6 to 120 g/kg, and in pepper (285.6 g/kg), garlic (224.4 g/kg), fenugreek (194.2 g/kg), coriander (166.4 g/kg), and capsicum (42.4 g/kg) (Refai and others 2004). These concentrations largely exceed the maximum tolerable limit of aatoxin B1 in spices (5.0 g/kg) according to the European regulations (Zinedine and Ma es 2009). Therefore, n it might be anticipated that pastirma and related North African traditional meat products represent a serious health risk factor associated with the consumption of these products. Pastirma was, indeed, reported to contain aatoxins at levels varying from 2.8 to 47 g/kg (Refai and others 2004).
Vegetable products Fruits and vegetables are contaminated by a wide variety of microorganisms including bacteria, fungi, viruses, and protozoa of different origins. These contaminations may occur in the eld (soil, manure, compost, wastewater sludge, irrigation water, equipment, workers, animals, and so on), during postharvest operations (conditioning, packaging, and distribution), or at the household prior to consumption (Burnett and Beuchat 2001; Matthews 2006). Therefore, microorganisms initially present in fruits and vegetables are highly variable in numbers and in nature, and are generally predominated by saprophytic bacteria and molds, considered as the resident microora, that do not raise serious health concerns (Jay 1986; Badosa and others 2000). Nonetheless, fruits and vegetables have extensively been shown to be contaminated with a variety of pathogenic bacteria, protozoa, and viruses (Beuchat 1998; Badosa and others 2000; Robertson and Gjerde 2000; Buck and others 2003; Bhagwat 2006; Matthews 2006), which is regarded as a risk factor for public health. Indeed, the increase in consumption of fruit and vegetable that has been recorded worldwide in the last 2 decades has been paralleled by an increase in foodborne disease outbreaks attributed to fresh produce (Beuchat 1996; Tauxe and others 1997; Buck and others 2003). This was corroborated by the association

of a number of fruits and vegetables from around the world with gastroenteritis outbreaks (Buck and others 2003; Matthews 2006), most of which were of bacterial origin, with Salmonella and E. coli O157 : H7 as the primary etiological agents (Heaton and Jones 2008). On the other hand, some microbial groups among the resident microora play a key role in the transformation of vegetables into more stable, safe, and palatable products when fresh produce is preserved for consumption out of season. Among the benecial of these epiphytic microorganisms in fruits and vegetables, LAB, and to a lesser extent yeasts, are responsible for spontaneous fermentation of a number of vegetable products such as olives and various vegetables. Natural fermentation has long been used on an empirical basis in the preservation of vegetable products, and in particular, in the case of olives, it is even necessary to make the fruit edible. In fact, natural olive fermentation fullls 2 main objectives: (i) inhibition of microorganisms of health and spoilage signicance, thereby reducing health risks and product losses, and (ii) making olives palatable, essentially by removal of the bitter glycoside euloropein, production of various aroma compounds, and softening, to some degree, the esh of the fruit during fermentation. As mentioned earlier, vegetable products are traditionally preserved in the North African region by lactic acid fermentation combined with salting (dry salt or brine), direct acidication (addition of vinegar) or, in few instances, by sun-drying. Conversely, fruits such as grapes, gs, and prickly pears are essentially dried, as the loss of moisture combined with the consequent increase in sugar concentration in the fruit results in a sharp decrease in water activity, thereby restricting the growth of spoilage and pathogenic microorganisms. The high diversity of North African traditional vegetable products and the raw material from which they derive, in addition to the variability in the technological processes and the sanitary conditions used for their manufacture, make the microbiological characteristics of the nished products and related risk factors also variable. Nonetheless, the fruits and vegetables eaten raw or after being transformed by traditional technologies are regarded as safe and wholesome for most North African consumers. Yet, this presumed safety has not been substantiated by microbiological and epidemiological studies, a situation that reects the lack of awareness of the health risks associated with the consumption of vegetable products in these countries. Furthermore, because of the lack of foodborne disease investigations and surveillance, most disease outbreaks related to the consumption of vegetable products remain undetected and insufciently reported in the scientic literature. Also, the level of contamination and the incidence of pathogenic microorganisms of/in fruits and vegetables are anticipated to be higher in North African countries than in developed countries. The lack of implementation of quality assurance programs including GAP, GMP, and HACCP throughout the entire production and distribution chain (pre- and postharvest, transportation, handling, and so on) increases the health risk associated with the consumption of such products. The risk is even greater as untreated urban wastewater and sewage sludge or manure continue to be used for irrigation or fertilization (Bazza 2003; Ghazy and others 2009). This practice, though recognized to be illegal, is tolerated by regulatory authorities in North African countries, and is widely used. In Morocco, about 70 million m3 of untreated urban wastewater are used annually to irrigate some 7000 ha of fruit orchards and vegetables as an alternative fresh water source, and as an easy and economical way for disposing wastewater (Bazza 2003; Choukr-Allah 2004). Similarly, the capacity of wastewatertreatment facilities in Egypt is either short or produces insufciently treated wastewater (Ghazy and others 2009); therefore, large amounts of wastewater and sewage sludge are used to irrigate and fertilize fruit orchards and vegetables in the country. The use of raw wastewater in agricultural activities has been demonstrated to increase the potential of the resulting crops to spread bacterial or parasitic diseases (Ait Melloul and Hassani 1999; Ait Melloul and others 2002). A bacteriological analysis of various vegetables obtained from several wastewater-irrigated agricultural regions in Morocco showed high counts of TAC (>9 log10 CFU/g) and fecal indicators (total-coliforms, fecal-coliforms, and enterococci)(>5 log10 CFU/g), suggesting that the consumption of these vegetables put consumers at high risk (Ibenyassine and others 2007). The same study showed that opportunistic Gram-negative pathogens of the Enterobacteriaceae family (Citrobacter freundii, Enterobacter cloacae, E. coli, Klebsiella pneumoniae, and Serratia liquefaciens) were detected in the studied vegetables at frequencies varying from 11% to 28%, with Enterobacter sakazakii (12%) and Salmonella arizona (0.7%) being the pathogens of the most concern to the safety of these crops. Moreover, in a Moroccan region (Al Haouzia, Marrakech) where untreated wastewater spreading is widely practiced for the production of vegetables such as lettuce, tomatoes, parsley, and potatoes, as well as cereals, the prevalence of Salmonella infection (32.56%) in the community living in the region and consuming locally produced crops has been shown to be signicantly higher than that recorded in a control region where no wastewater spreading is practiced (1.14%). Another study carried out in the same region revealed that the prevalence of protozoan infections (giardiasis and amebiasis) among children of the wastewater-irrigated region was signicantly higher (72%) than that recorded in the control area (45%) (Ait Melloul and others 2002). Traditional food products of plant origin in North African countries are generally obtained from locally produced crops with inconsistent sanitary quality. Therefore, the safety of nished products is largely dependent on the efcacy of natural hurdles to inhibit or inactivate undesirable microorganisms initially present in the raw material. Olives are the most important vegetable products that are transformed by traditional technologies in North African countries; they are either brined (green olives) or drysalted (black ripe olives). In both cases, they undergo spontaneous lactic acid fermentation, although in the latter case, the fermentation is greatly retarded by the high salt concentrations used for their preservation (8 to 14 g salt per 100 g olives). Other vegetables such as peppers, onions, carrots, string beans, chili, and cauliower are either brined in a similar manner as for green olives (Steinkraus 1983) or salted and packed into an acid solution (usually vinegar) of a pH value below 3.0 as unfermented (fresh-pack) pickles. In the fresh-pack pickles, the raw material is usually heated or soaked in hot water for few minutes to reduce the overall microbial load of the product before pickling. Therefore, it would be reasonable to expect that these unfermented pickles do not raise serious health concerns essentially due to the low pH of the brine in addition to the heat treatment where microbial growth is very unlikely to occur (G mez and others 2006). They would o therefore be categorized as low-risk vegetable foods. Conversely, in fermented vegetable products, faulty fermentation is not uncommon and pathogenic microorganisms may grow or survive in the nished products (Fleming and others 1985; Caggia and others 2004). In fermented pickled vegetable products, microbial competition, acidity, and reduced water activity (high salt content) are the main parameters that inhibit undesirable microorganisms to safeguard the health of consumers. However, the usual salt concentration used in the brine (5 to 7 g salt/100 mL) is not high
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Table 8Monitoring 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 period (days) 60 7.76 2.33 2.52 6.55 5.55 3.84 3.88
Microbial group Total aerobic count Coliforms Staphylococci Lactic acid bacteria Lactobacilli Yeasts Psychrotrophs
15 4.52 2.12 2.03 3.8 3.6 1.88 4.22
90 6.88 1.96 1.35 6.96 5.66 5.98 1.53
enough to reduce the water activity to levels that would strongly inhibit the growth of undesirable microorganisms. In addition, when more than 8% (w/v) of salt is used in the brine, the growth of LAB is also retarded signicantly and the pH remains relatively high at the end of fermentation (about 4.5) (Fern ndez and others a 1997), conditions that provide an opportunity for salt-tolerant or halophilic pathogens and spoilage microorganisms to grow during the early stages of fermentation. Staphylococci grow well at salt concentrations between 7% and 10% and a low pH of 4.2, and other pathogens such as E. coli O157 : H7, L. monocytogenes, and Salmonella spp. have been shown to develop resistance under stressful conditions, including low pH (Gahan and others 1996; Lou and Yousef 1997; Beales 2004; Lee 2004). Therefore, in the fermentation of green olives, the usual salt concentration used does not exceed 7 g salt/100 mL brine to allow good growth of fermentative LAB. These bacteria, which represent only a small proportion of the initial epiphytic microora of the product, should rapidly outgrow the competing microbial groups and produce sufcient acidity to reach a pH of about 3.5 to 3.8, and then the resulting product may be considered reasonably safe. LAB have been shown to predominate throughout the entire fermentation period (90 d) in naturally fermented Algerian green olives, although yeasts were consistently present at relatively high counts (3 to 6 log10 CFU/g of olives) as a secondary microora (Kacem and Karam 2006b). These authors have shown that the counts of LAB increased steadily since early phases of fermentation to reach about 7 log10 CFU/mL after 90 d of fermentation. A signicant increase in yeast counts has also been noted, starting from day 60 of fermentation, in a typical behavior of a secondary fermentation ora (Fleming and others 1985). Meanwhile, the counts of coliforms, staphylococci, and psychroptrophs were reduced to different extents (Table 8). Such a decline may be attributed not only to the effect of pH and salt content of the Algerian fermented green olives (Kacem and Karam 2006a), but also to inhibitory substances inherently present in olives or to specic metabolites produced by the predominating species of LAB and yeasts during
Enteritidis, Vibrio parahaemolyticus, Staph. aureus, and Vibrio cholerae (Tassou and Nychas 1994; Tassou and Nychas 1995; Bisignano and others 1999). Among LAB isolated from fermented green olives in North African countries (Table 9) and elsewhere (Fleming and others 1985), Lb. plantarum has been consistently reported to be the predominating species throughout the fermentation period (Kacem and others 2004; Chamkha and others 2008); and strains of this species have extensively been shown to produce bacteriocins active against Gram-positive and Gram-negative bacteria (Kacem and others 2004, 2005; Dobson and others 2012). Likewise, yeasts have been reported to be consistently present at elevated counts (> 6 log10 CFU/g) in North African fermented olives (Asehraou and others 2000; Asehraou and others 2002; Kacem and Karam 2006a; Hern ndez and others 2007), and to contribute to their a safety. It is indeed well established that yeasts produce aroma compounds including organic acids, diacetyl, ethanol, and other metabolites resulting from lipolytic activities that also possess antimicrobial activities, thereby contributing to avor development as well as to the safety improvement of foods (Hern ndez and otha ers 2007; Arroyo-Lopez and others 2008). Furthermore, among the major yeast species isolated from fermented olives (Table 9), the so-called killer yeasts tend to predominate owing to their ability to produce a killer toxin essentially active against other competing yeasts (Llorente and others 1997; Asehraou and others 2000; Hern ndez and others 2007; Maqueda and others 2012), a but could also inhibit various pathogenic Gram-positive bacteria (Izg and Altinbay 1997). Therefore, killer yeasts would not only u reduce the incidence of bloater defect (Asehraou and others 2002), but also contribute to the enhancement of the safety of nished products. Nonetheless, the safety of naturally fermented olives may not rely only on the above-mentioned safety factors, as the degree of protection they offer vary widely depending on the fermentation parameters and from a batch to batch (Asehraou and others 2000; Kacem and Karam 2006b). In effect, foodborne pathogens of concern to food safety have been isolated or shown to survive from/on Spanish-style green olives or Greek-style black olives (Table 6), and cases of botulism and other food poisoning disease due to consumption of fermented green or black olives have been reported (Okudaira and others 1962; Pereira and others 2008; Pingeon and others 2011; Anon 2012). The competitiveness of the predominating LAB and yeasts as determined by their ability to produce inhibitory metabolites or competition for nutrients, and the initial bacteriological quality of olives and brine, in addition to the sanitary conditions during manufacture, are the main parameters that determine the safety status of traditional fermented olives. Presently, olives are heat-treated before or after preservation and
Table 9Predominating 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 identied isolates. Microbial group Country of origin Algeria LAB Lb. casei Lb. paracasei Lb. plantarum Ent. faecium Lc. lactis Lb. plantarum NA Lb. plantarum Lb. collinoides Yeasts Sac. cerevisiae Candida parapsilosis NA Sac. cerevisiae, Pichia anomala Pichia membranaefaciens Reference Kacem and Karam 2006a
Kacem and others 2004 Asehraou and others 2000 Chamkha and others 2008
Morocco Tunisia
NA = Not available.

Table 10Incidence of mycotoxins (g/kg) in selected vegetable products in some North African countries. Commodity Table olives Mycotoxin OTA OTA AFB CIT OTA AFB1 AFG1 OTA OTA AFB1 OTA OTA AFB1 AFT, CIT, OT, PAT, STG, DAX, T-2 toxin, ZEA Frequency (%) 36 100 100 80 5 30 65 100 20 1 35 2 0
Range (Average) 0.62 to 4.8 (1.43) up to 1.02 up to > 0.5 0.45 to 0.52 (0.5) 46830 0.28 0.28 to 32.9 (8.70) 0.03 to 1.42 (0.33) 60 to 120 3.2 to 13.9 (10.7) 250 0.05 to 4.95 (0.96) 300 ND
Origin Morocco Morocco Morocco Morocco Tunisia Morocco Morocco Morocco Egypt Morocco Egypt Morocco Egypt Egypt
Reference Zinedine and others 2004 El Adlouni and others 2006 Maarou and others 1995a Juan and others 2008 Zinedine and others 2007b Zohri and Khayria 2007 Juan and others 2008 Youssef and others 2000 Zinedine and others 2007b Youssef and others 2000 Zohri and Khayria 2007
Figs
Raisins
One sample analyzed; LOD: Limit of detection; ND: Not detected; AFT: Total aatoxins; AFB: Aatoxin B; OT: Total ochratoxins; OTA: Ochratoxin A; CIT: Citrinin; PAT: Patulin; STG: Sterigmatocystine; DAX: Diacetoxyscirpenol; ZEA: Zearalenone.
various chemical food-grade additives such as acids, sorbates, and benzoates and parabens are added to pickled or dry-salted olives in North African countries in order to enhance their safety and keeping quality. In the market place, the latter products are known as romy, litrally meaning coming from Rome but commonly used to refer to modern and sophisticated products, as opposed to baladi/beldi products (products of the country, in Arabic). It is worth mentioning, in this regard, that the baladi products are the most preferred by consumers though less attractive in appearance and their hygienic quality is questionable as compared to the romy ones. Further studies should be carried out on the hygienic quality of different commercial and home-made fermented green olives samples, and from different geographical locations of North African countries, in order to provide a sound conclusion regarding sanitary quality of naturally fermented olives and to allow an accurate assessment of the health risk associated with their consumption. Particular attention should be given to the occurrence of Cl. botuminum and its toxin, since this is considered as one of the most important safety issues in fermented olives worldwide, although the occurrence of Cl. botulinum in fermented olives appears to be rare, and only very few outbreak intoxications due to botulism of type B have been recorded (Pereira and others 2008; Anon 2012). In addition, the botulism toxin formation is unlikely at pH and aw < 4.8 and 0.94, respectively (Odlaug and Pug 1979; Briozzo and others 1986); values of these parameters are generally lower in naturally fermented olives. In addition to the bacteriological hazards discussed above, mycotoxins represent a major issue regarding the safety of traditional vegetable products in North Africa. Among these products, table olives and dry fruits such as gs and raisins have repeatedly been reported to be contaminated with various mycotoxins (Table 10). The high salt contents (5 to 12 g salt/100 g product) in table olives select for the halophilic or salt-tolerant molds especially, those of the genera Penicillium and Aspergillus. Similarly, raisins and dried gs have been shown to be frequently contaminated with mycotoxin-producing strains of A. avus and A. niger due to the osmophilic character of these species (Rao and Kalyanasundaram 1983; Pitt and others 2009; Selouane and others 2009). Contamination of table olives with various mycotoxins is well documented, and Greek-style black olives are the most incriminated (Maarou and others 1995a; El Adlouni and others 2006). The high salt content (about 7% to 12% g salt/g olive) inhibits the growth of almost all competing bacteria (Asehraou and others 1992; Efstathios 2006), thereby providing an opportunity for the salt-tolerant molds to grow and possibly produce mycotoxins.
Among these, the most frequently encountered in North African table olives are species of the genera Aspergillus and Penicillium (Tantaoui-Elaraki and Le Tutour 1985; Gourama and Bullerman 1988; Maouni and others 2002), and the most frequently detected mycotoxins are OTA, citrinin (CIT), and AFB (El Adlouni and others 2006; Zinedine and Ma es 2009). Nonetheless, studies n have shown that black olives are not good substrates for mycotoxin production (Gourama and Bullerman 1988; Eltem 1996). In this regard, Tantaoui-Elaraki and Le Tutour (1985) have demonstrated the inability of A. avus and A. ochraceus to produce detectable amounts of mycotoxins in Moroccan table olives, while the same strains had been shown to produce high concentrations of mycotoxins in laboratory media. Similar observation has been made by Leontopoulos and others (2003) who have demonstrated that a toxinogenic strain of A. parasiticus was unable to produce AFB1 in damaged black olives originating from Greece. Similarly, Gourama and Bullerman (1988) showed that A. avus did not produce AFB1 in pastes made from Moroccan Greekstyle black olives. Furthermore, Eltem (1996) showed that fresh whole black olives, fresh damaged black olives, and whole black olive paste inhibited or greatly reduced the production of aatoxins by toxinogenic strains of A. avus and A. parasiticus isolated from naturally fermented black olives. Although these studies concurred to suggest that olives, especially the black, are not suitable substrates for the production of mycotoxins at hazardous levels, the occurrence of various mycotoxins in table olives in North African countries and elsewhere has extensively been documented (Table 10). A study carried out by Tantaoui-Elaraki and Le Tutour (1985) revealed the presence of the AFB1 and OTA at appreciable amounts in commercial samples of Moroccan table black olives in spite of the fact that these mycotoxins were shown not to be produced when black olives were articially contaminated with selected strains of toxinogenic molds. Also, a survey carried out by Zinedine and others (2004) revealed that 36% of Moroccan table black olives were contaminated with OTA at levels ranging between 0.62 and 4.8 g/kg with an average concentration of 1.43 g/kg. Furthermore, OTA and AFB have been detected in 100% of sampled Moroccan dry-salted olives at levels exceeding 0.65 and 0.5 g/kg, respectively (El Adlouni and others 2006). Therefore, the occurrence of toxigenic molds and the frequent detection of mycotoxins in traditionally processed black olives rank these products among the commodities of high risk to public health in North African countries. Such a risk is even greater when more than one mycotoxin is present in table olives, as was demonstrated by El Adlouni and others (2006) who showed the concomitant
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presence of OTA, CIT, and AFB in dry-salted commercial Moroccan Greek-style black olives. Furthermore, the prevalence of chronic nephropathy diseases in Tunisia has been correlated to the consumption of various foods contaminated with OTA, among which black table olives were incriminated, as abnormally high levels of this mycotoxin (up to 46.83 mg/kg) were found in this product (Maarou and others 1995a, b). The decrease in moisture content to about 14% (Canellas and others 1993; Karathanos 1999) and the subsequent increase in sugar concentration in fruits during drying resulted in an almost selective medium for xerotolerant molds, among which members of the Aspergillus section Nigri have been shown to predominate. These black aspergilli are particularly severe and widespread in grapes of the warmer areas of the Mediterranean basin including North African countries (Battilani and others 2008). Strains of A. niger aggregate and A. carbonarius have been shown to be the main contaminants of Moroccan grapes and to produce high amounts of OTA (0.24 and 0.22 g/g, respectively) at optimal environmental conditions (Selouane and others 2009). A similar situation is expected in the other grape-producing North African countries including Algeria, Tunisia, and Egypt, despite the lack of reports, as these countries share the same climatic conditions as well as sociocultural conditions. In addition to A. niger aggregate and A. carbonarius, A. aculeatus has also been found to predominate during the entire drying process of grapes; from the fresh fruits to the fully dried raisins (Leong and others 2008). However, this study showed that among the 3 fungal species, only A. carbonarius was able to produce OTA in vitro as detected by the emission of uorescence under UV light upon cultivation on coconut cream agar plates. The incidence of occurrence of AFs and OTA in Moroccan commercial raisins and dried gs has been reported to be 30% and 65%, respectively, and the levels ranged between 0.03 and 1.42 g/kg, with an average of 0.33 g/kg in dried gs, and between 0.05 and 4.95 g/kg with an average of 0.96 g/kg in dried raisins (Zinedine and others 2007b). In Egypt, OTA was detected in gs at levels varying from 60 to 120 g/kg, while raisin samples have proven to be free from AFs (B1 , B2 , G1, and G2), CIT, ochratoxins (OT), patulin (PAT), sterigmatocystin (STG), diacetoxyscirpenol (DAX), T-2 toxin, and zearalenone (ZEA). In another survey on 100 samples for the occurrence of mycotoxins, Egyptian raisins were found to be contaminated at very high levels of AFB1 (300 g/kg) and OTA (250 g/kg), though at the low frequencies of 2% and 1%, respectively (Youssef and others 2000). From the above data, it is clear that the occurrence of mycotoxins in fruits and vegetables presents a real threat to consumers health in these countries, as well as a serious limitation for the export of local produce toward developed countries, especially the traditional economic partners of the European Union (EU) and North America. The latter countries are in the process of harmonizing their regulations on mycotoxins in foods and feeds with a clear tendency to be more restrictive. On the other hand, there are presently no specic regulations on mycotoxins in North African countries, which is expected to hamper, on a medium or long run, the export of vegetable products from these countries to Europe and other partners from developed countries. It is worth mentioning that Morocco, Algeria, Tunisia, and Egypt are among the main suppliers of fruits and vegetables to Europe, which represents a major income to those North African countries where agriculture is the essential economic activity, especially in Morocco and Tunisia. However, despite the lack of specic regulatory limits for mycotoxins in these countries, the problem of mycotoxins is well recognized from both public health and economic views. Projects
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for the tolerable limits of aatoxins and ochratoxins in foods have been proposed in some North African countries, but they have not come into force yet (Zinedine and Ma es 2009). This is essenn tially due to the belief of stakeholders in these countries that the strict implementation of mycotoxin regulations will have limited effects in terms of health protection. The prevalence of subsistence farming and the continued practice of traditional technologies for the transformation of food products in poor sanitary conditions will certainly hinder any effort to enforce such regulations. Indeed, the mycotoxin issue in North Africa or other developing countries needs to be viewed in the overall context of local food safety, health, and agricultural practice issues.
Prospects for Safety Improvement of Traditional North African Foods: Opportunities and Constraints
General context Like most developing countries around the world, those of North Africa are at the crossroads between many strategic choices regarding food policies aiming at the improvement of food safety while adapting to the advent of globalization. Nonetheless, regardless of the strategy to be adopted, North African countries should necessarily upgrade the safety of their local foods to take advantage of the opportunities of globalization and to promote the trading of such foods either internationally or in domestic markets in face of the increasingly competitive global trade. To this end, North African countries should take into account, in addition to the national constraints, the regional and global economic environment characterized by a multiplicity of bilateral, multilateral, subregional, regional, and international agreements. The most signicant of these agreements are undoubtedly the Sanitary and Phytosanitary (SPS) and Technical Barriers to Trade (TBT) agreements of the World Trade Organization (WTO), which raised the food safety to the forefront of the international trade requirements. Moreover, the SPS agreements have recognized the Codex Alimentarius Commission (CAC) as a key organ for the harmonization of food standards among member countries to reach the WTO objective of market globalization of safe foods. Although controversial, it is believed that the application of SPS measures and the consequent strengthening of food safety regulations would progressively lead developing countries, including North African ones, to improve safety and quality control practices in agriculture and food technology. Such improvements would ultimately result in new forms of competitive benets for developing countries and contribute to more sustainable and protable trade in the long run (FAO 2004). Indeed, the application of GMP and HACCP in the sh industry in Tunisia and Morocco, for example, as mandatory measures or on a voluntary basis, respectively, has drastically improved the safety and quality of sh products, and consequently, their access to importing markets, especially the EU. Also, the need for compliance of Moroccan, Tunisian, and Egyptian fruit and vegetable exports with the food safety regulations of importing developed countries, such as those of the EU, to enter these markets has resulted in a signicant advance of these 3 North African countries in the implementation of modern food control systems. Therefore, efforts to produce traditional foods that meet the standards of the Codex Alimentarius (CA) would increase their safety, and consequently, their local and international market share, as has been reported for traditional Greek foods (Panagou and others 2013). It is worth mentioning, however, that North African countries do not have the same status as regards international, regional, and subregional organizations (Table 11), nor do they have the same economic resources and priorities in regards to

Table 11Membership status of North African countries in different international organizations and agreements with impact on trade, food safety, and food security. International agreements CA OIE X X X X X X X X X X Regional IPPC X X X X X NEPAD X X X S X MEDA X X X X X Subregional UMA X X X X Bilateral OECD X
Country Algeria Egypt Libya Morocco Tunisia
WTO A X R X X
FTA X
X: Full membership. A: Application submitted and the negotiation process is ongoing. R: Request submitted and the negotiation process has not started yet. -: Not relevant. CA: Codex alimentarius. WTO: World Trade Organization. OIE: World Organization for Animal Health (Ofce International des Epizooties). IPPC: International Plant Protection Convention. NEPAD: New Partnership for Africas Development. MEDA: Mediterranean Economic Development Area; Morocco was granted the advanced partnership status with EU in Mai 2008. S: Membership suspended since 1984, and is in the process to be restored. UMA: Maghreb Arab Union (Union du Maghreb Arab). AENP: Advanced European Neighborhood partnership. FTA: Free trade Agreement between Morocco and the U.S.A. signed in June 2004 and entered into force in January 2006. OECD: Organization of Economic and Cooperation Development (Trade preferences status for Egypt).
food safety. This situation, which deters these countries from having a common food safety policy, should be addressed for mutual benet and to obtain the best advantage for the opportunities of globalization; each of these countries should endeavor to promote the safety of its own traditional foods while encouraging the exchange of these foods with the other North Africa countries that share many common dietary habits.
Safety of North African traditional foods There is a clear trend in North Africa to increase the availability and diversity of industrial foods either produced locally or imported from other countries. Nonetheless, the consumption of traditional food products in these countries, though difcult to accurately estimate, is signicant especially in the rural areas where an average of about 40% of the entire North African population lives (Table 1). Many dairy products (brined and soft cheeses, zabadi, raib, lben, zebda, and smen), meat products (khlii, pastirma and sujuk), and vegetable products essentially represented by various table olive types and pickled vegetables are examples of such foods highly appreciated and widely consumed in North African countries. Consumer preference for traditional foods is essentially driven by the fact that these foods are considered as a valuable heritage, and hence, part of the cultural identity to preserve, in addition to their believed health virtues and highly appreciated gustatory properties. This particular issue has been extensively discussed over the last 2 decades as a means to preserve the cultural diversity, including nutritional habits, within the inevitable globalization of the world food supply. Nevertheless, this situation creates a dilemma to the government ofcials who should encourage and support the production and consumption of local traditional foods which, on the other hand, may present increased health risks to consumers due to their usual nonconformity with regulatory standards. Such risks, especially those related to microbiological hazards, are anticipated to be especially high for traditional foods, as they are generally produced under poor hygienic conditions without any systematic control measures. The widespread presence of pathogenic bacteria and molds in North African traditional foods, and reported cases of food intoxications linked to the consumption of a number of these foods, strongly supports the assumption that they put the public health at a high risk. Therefore, there is an urgent need to improve the hygienic quality of these products, not only to safeguard consumer health, but also to improve competitiveness and market share so that they can efciently contribute to
the availability of safe traditional food in North African countries. Marketing of traditional food commodities would also help the rural populations to generate greater income and meet other needs not available locally. In this regard, the world food security (WFS) framework developed by the FAO under the Special Program for Food Security (SPFS) aims to improve food security within poor households through national and regional programs for food security. Morocco, Tunisia, and Egypt are among the participating countries of the WFS. The main challenge resides therefore in the development of practical technologies and/or the adoption of adequate strategies to improve the safety and stability of traditional foods in conformity with international regulations and standards (especially Codex Alimentarius standards) while preserving their authenticity and palatability. To meet such a challenge, it is necessary to develop national strategies for food safety based on a holistic or food chain approach that extends from harvest to consumption and involves all the relevant actors (government ofcials, food industry, local producers, researchers, academia, analysis laboratories, the media, consumers and their organizations, and so on), within the framework of a predened action plan such as that proposed to the Middle East and North Africa (MENA) region by the FAO (2004). However, the implementation of such an action plan appears to need greater nancial and technical assistance from the governments and a longer transitional period to upgrade the quality of traditional food production while keeping their authenticity. A number of authors have suggested the transfer of traditional technologies to small or medium industrial scales where the hygienic conditions and microbiological contamination could be better controlled than household production through the application of appropriate quality assurance programs such as GMP and HACCP (Fellows and others 1995; Motarjemi 2002; Benkerroum and Tamime 2004). In the case of traditional fermented foods, it has been suggested to adopt controlled fermentation using selected industrial starter cultures and/or heat treatment of the raw materials, such as milk, as appropriate (Benkerroum and Tamime 2004). According to Panagou and others (2013), the transition from artisan practices in traditional food manufacturing to well-equipped industrial units under strict processing and hygienic conditions has resulted in drastic improvement in the microbiological quality of Greek foods similar to those reviewed herein (fermented meats, dairy products, and fermented vegetables), and hence their safety records. The addition of chemical preservatives including sorbates/benzoates or sultes has also been suggested in the fermentation of table olives or drying of raisins, respectively,

to increase their safety and stability (Canellas and others 1993; Asehraou and others 2002; Panagou and others 2013). However, it could be argued that the resulting foods from such technology transfer may lose their authenticity and uniqueness as the selected strains of the starter cultures cannot be representative of the complex and changing microora involved in the different steps of the natural fermentation. Alternatively, it has been suggested that safe and authentic traditional foods could be obtained by improving the sanitary conditions of the traditional technologies along the whole production chain by the application of Good Agriculture Practices (GAP), Good Harvest practices (GHaP), GHP, HACCP, and the use of adequate conditioning, packaging, and transportation facilities (Fellows and others 1995; Flamant 1996; Valyasevi and Rolle 2002). However, the production of typical traditional foods may also include the acceptance of a residual risk. For example, the use of raw milk to produce traditional cheese by application of good practices reduces risk of listeriosis, but it does not remove it, while initial sterilization of milk followed by controlled fermentation with pure starter cultures can meet the zero tolerance status; however, the resulting cheese will loose its uniqueness and typical gustatory quality. Therefore, though the residual risk could be accepted, it has been recommended to prohibit the consumption of such traditional foods by the high-risk groups: elderly, pregnant women, young children, and immunocompromised individuals. ganizations is necessary for the execution of such an action plan in North African countries. In addition, a transition period is needed before all measures are operational. This period appears to be particularly long for traditional foods, which have received little attention so far, partly due to the lack of political commitment from the interested countries to act as partners having common weaknesses and complementary assets.
Ofcial food control measures The success of any strategy to promote food safety and quality should involve all the relevant actors, with the government playing a central role in the coordination and supervision of the implementation of the strategy. In this regard, the 27th FAO regional conference for the Near East recommended a number of specic measures that the governments of Middle Eastern and North African (MENA) countries should take to improve food safety and quality, and be prepared for the upcoming challenges related to the inspection and certication of food imports and exports and the provisions of scientic risk assessment as needed (FAO 2004). According to these recommendations, government ofcials are responsible for the establishment and management to enable institutional, policy, and regulatory frameworks for food safety, and carry out food control activities that protect consumers from risks arising from unsafe food and fraudulent or deceptive practices. To this end, government ofcials should work with interested parties at the national and regional levels to build capacity and to strengthen national food control programs and activities. Among the main recommendations, the conference stressed the need to strengthen and modernize food control facilities and procedures through a risk-based approach. The conference also recommended creating or reinforcing capacities for national foodborne disease surveillances accompanied by a rapid alert system and mechanism for communication with food control authorities along with an efcient means to implement corrective measures. The development of cooperation between the countries of the region to facilitate communication and exchange of information in foodborne disease surveillance, as well as information about foodborne hazards, was also among the main FAO recommendations. In this regard, MENA countries were particularly urged to create a risk assessment body(ies) that provides scientic advice to risk managers on issues of particular interest and to form interregional networks of laboratories (FAO 2004). However, efcient implementation of these measures is costly and requires highly skilled personnel; therefore, nancial and/or technical support from developed countries or international orc
Adequacy of current food control regulations and possible alternatives The nature and degree of sophistication of food control systems vary widely among North African countries, which otherwise suffer from common difculties that limit the performance and efciency of their food control and inspection systems. These include: r Multiplicity of the food control systemswhereby modern safety and quality assurance systems using GMP, GHP, and HACCP programs are used by certain enterprises to produce foods for export or urban retail sales, and to exist alongside an informal food sector subject to minimal or no food safety or quality control. The latter situation applies to North African traditional foods generally sold in informal ways in rural markets, shops, butcher shops (meat products), creameries (dairy products), and grocery stores or by street vendors. r The multiplicity of bodies involved in food safety and quality control, which are usually afliated with different ministerial departments (agriculture, public health, interior, trade, industry, environment, energy, and possibly others) (http://www.reading.ac.uk/foodlaw/ip2000/tunisia.htm). Although these departments play, in principle, different and complementary roles and act to ensure the highest possible level of consumer health protection, they have often been a source of problems and distortions due to the lack of clear boundaries between the specic tasks of each institution, and also due to intrinsic competition to be the leading authority in food safety and quality in the country. r Management of food safety issues is considered as an exclusive government mandate, and there is no or marginal inclusion of other stakeholders (industry, research institutions, consumers, nongovernment organizations (NGOs), and so on) in the decision-making process regarding the policy of food safety. r In most North African countries, the current laws on food control are generally not specic to foods but cover all kinds of goods. Furthermore, many regulatory standards and threshold values are obsolete and do not match with the recent advances in food technology and the techniques used for the detection of conventional or emerging microbial or chemical contaminants, such as Creutzfeldt-Jakob prion, avian inuenza virus, Ent. sakazakii, dioxin, and acrylamide. Furthermore, they do not meet the international trade requirements for accreditation, certication, traceability, and required high food safety standards. In fact, ofcials of North African countries are aware of the inadequacy and vulnerability of their food safety policies in view of global trends. Therefore, they have been modifying, at different rates, their food safety systems to meet WTO requirements and harmonize their standards with those of the CAC. However, the transition from the conventional control and inspection systems to a modern food safety framework requires profound institutional and legal changes in addition to substantial investment and technical needs. Morocco, for example, has been working on this issue with the support of FAO since 2000, and has only recently

adopted a new law (Law 025-08) stipulating the creation of a National Food Safety Ofce (ONSSA) (ofcial bulletin N 5714 of 5 March 2009). This act has been designed to induce deep changes in the Moroccan food safety policy and control practices so as to meet the recommendations of regional and international organizations including WTO (SPS, TBT), WHO and FAO (CA, IPPC), EU, OIE. In view of these changes, traditional products should also be considered under the law 25-06 on the distinguishing marks of origin and quality of agricultural products and foodstuffs to improve their safety and competitiveness. Under this law, traditional foods are subject to ofcial food control and inspection. Indeed, standardization of traditional foods and protection of their origin and quality through such legislations has been reported to motivate the small-scale production of traditional foods and to expand their export potential (Panagou and others 2013). Adoption of an adequate surveillance system is another crucial factor to accurately assess the health risk associated with the consumption of traditional foods, and consequently, design appropriate preventive measures to reduce risks to as low levels as possible. This aspect was also emphasized in the new Moroccan food safety act. in the long run. To this end, the government could simplify the administrative routine, reduce taxes, and provide technical assistance to design a business plan and later implement it. r Facilitating loans at reduced rates for the acquisition of small equipment and machinery. Rural food producers usually lack the basic capital to start producing foods for trade, and small or medium loans with reduced rates would help them start a business either individually or within associations or cooperatives. Many successful creameries in Moroccan cities have started in this way, which could be extended to traditional meat products (gueddid, khlia, mkila, and so on) or vegetable products. r Subsidizing traditional food products, especially those produced in cooperatives or professional associations as an encouragement during a limited period. r Encouraging women associations to produce traditional foods. It is of paramount importance for women in North African countries to know that the foods they produce at the household level have nancial value and constitute a signicant source of income for their own autonomy and nancial 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 usually better achieved by a group of women within associations. r Organizing training sessions for all the personnel involved in the production process including technicians and food handlers on a regular basis under the supervision of ofcial agencies or NGOs, and at no fees for targeted participants. r Organizing yearly prizes for individuals or associations producing the most competitive traditional food products that also meet the safety standards. It is worth mentioning, however, that these measures can only be effective if the other basic requirements for such technology transfer (infrastructure, transportation vehicles, electricity, potable water, and so on) are met (for a review see Rolle and Satin 2002), and this is a matter of sustainable development of the country as a whole.
Incentives to food producers and infrastructure improvements To improve the safety of traditional North African food products, it is necessary to adopt certain measures that would encourage food producers, usually rural, including the provision of nancial and technical incentives to help them upgrade the hygienic quality of their products and be aware of the benets of such an approach in the medium and long term. Some of these incentives may be: r Preferential rates of water and electricity fees. The prices of water and electricity are relatively high in most North African countries due to the water shortage and limited capacity in the production of electricity; a situation that deters rural food producers from using water and electric urban facilities to prepare traditional food products. Instead, they use wells or open surface water as available; they thus expose the nal product to various chemical and microbiological contaminants originating from a polluted water supply. Also, the provision of electricity at a reduced rate would encourage rural food producers to use electric machines (dryers, churning machines, heated vats, meat cutters, refrigerators, and so on) for better control of the technological processes or for storage of the nished product before sale. r Provision of technical assistance at the farm level: Rural food producers are usually not aware of the critical steps in traditional processes that may lead to defective nal products or inconsistent gustatory quality if not adequately controlled. Therefore, technical assistance by trained persons would draw the attention of rural food producers to the critical steps of the traditional processes, and help them ensure the production of foods with consistent quality. For example, the relevance of cleaning/sanitation, as well as personal hygiene, to the quality and safety of the nal products is overlooked or even ignored by rural food producers. The organization of adequate training sessions would contribute to the sensitization of food producers to the impact of these practices on the quality of the nished food products. r Facilitating technology transfer from the household level to small or medium industrial scale for traditional food products when such transfer is deemed viable and economically feasible
The role of NGOs The role of NGOs in the promotion of the safety and quality of foods is no longer questionable and should be further encouraged by the governments. Depending on the objectives of these organizations, they may play critical roles at many levels for the promotion of the safety of foods in general and specically of traditional foods. According to the approach of risk analysis, NGOs should work closely with other stakeholders, by virtue of the risk communication component of the approach, to defend the consumers right to safe foods as was recommended by the CAC in the 1990s. They should therefore be involved in the denition of national food safety policies to request appropriate standards of food safety, and also at the production level to ensure that foods are handled, stored, and prepared in accordance with good hygienic practices (GHPs). Furthermore, NGOs that focus particularly on rural development would provide valuable technical assistance to rural individuals or associations to develop economic activities adapted to their environment including the production of traditional foods, so they can be formally marketed through the country or the region. Such organizations are being increasingly active in all aspects of development in North African countries and may be an asset for the modernization of the traditional food production sector. Indeed, subsequent to the CAC recommendation to
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promote consumers participation in food-related decisionmaking at national and international levels, North African countries have encouraged the organization of independent consumer associations and their representation in all food safety-related issues including those debated within the National Codex Committees (NCC) and subsidiary bodies. In Tunisia, the Consumers Protection Defense Organization (CPDO), for example, plays an active role alongside with technical committees in preparing standards as a member of the Tunisian NCC and in all the afliated technical committees. In Morocco, there are more than 20 associations organized under 2 federations (F d ration Nationale des Associe e ations de Consommateurs, FNAC; and Conf d ration des Assoe e ciations des Consommateurs; CAC-Maroc), which participate in the work of the NCC and working groups. Among other activities, they include consumer protection from deceptive practices in commerce and the provision of technical and legal advice to individuals or groups of consumers. In Egypt, there are more than 60 consumer protection associations, which are represented in the NCC and in the various technical committees established by the Egyptian Organization for Standardization (ESO). In Algeria and Libya, the contribution of independent consumers associations to food safety has started only recently and is still in its infancy; however, it is expected to grow and play an increasing role in consumers protection from illicit or fraudulent practice in foods. In fact, an Algerian Federation of Consumers (FACs) encompassing many local associations has been created recently, but its actions are rather diffuse including many goods, which may limit its efcacy as regards food safety, especially in a developing country context. In addition, other stakeholder such as NGOs including producers associations of farmers and processors may play a signicant role in the promotion of food safety awareness or in technology transfer implementation. Although the primary role of such organizations is to defend the producers interest, they also endeavor to promote the quality of their produce and ensure that they meet government requirements and consumer expectations to be competitive. Such a trend has been ofcially encouraged in all North African countries since the 1980s in response to the foreseen food market and trade liberalization (Desrues 2005). Therefore, many professional organizations and associations have been created in different food production elds including citrus, olives, red meat, poultry, viticulture, sheries, dairy, fruits and vegetables, and so on, as well as in food processing industries. However, in spite of the fact that the role of such organizations and their impact on the promotion of food safety and quality has been evident in recent years, a critical analysis of their actual input in Moroccan agriculture, for example, suggested that they are of benet to inuential and the biggest farmers/producers more so than to consumers or small-producer members (Desrues 2005); a situation that all North African countries may share. Yet, further development of professional organizations and associations in North African countries to fulll adequately their role in economic development and continual upgrading of food safety is necessary (Ayad and others 2011) despite the present limitations that may be regarded as stimulatory factors for future developments. The role of these organizations/associations, as professional representatives and also as mediators between professionals and ofcials, has been recognized as an essential tool for the implementation of any balanced strategy for sustainable development. Their involvement in risk analysis and interaction with risk assessors and risk managers, for the purpose of risk communication, has been specically mentioned among the interested Parties in the CA (WHO/FAO 2007).
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Promotion of food safety awareness The increased dissemination of information worldwide regarding foodborne illnesses through mass media (written and audiovisual) has greatly contributed to raising food safety awareness among North African citizens of the relevance of food safety to the welfare of consumers and to sustainable development. Also, government ofcials are increasingly aware of the cost of foodborne diseases in terms of medical care, labor days-off, and foods losses. However, greater efforts are yet to be made to raise such awareness to a level where consumers, food producers, as well as government leaders and heads of concerned agencies are convinced of the economic, social, and health benets resulting from upgrading the safety and quality of foods among which traditional foods constitute a substantial part. Consumer organizations have an important role to play in the promotion of food safety awareness and the need to strengthen food control among North African countries. For example, Tunisian CPDO plays an active role in consumer awareness and guidance through audiovisual and written mass media. The Moroccan consumer associations afliated with each of the 2 consumer protection federations are also involved in the enhancement of consumer awareness through various mass media and the organization and participation in/of seminars and meetings at universities, high schools, or in local communities to disseminate information related to food safety. Similarly, in Egypt, a Consumer Protection Unit (CPU) has been created within ESO to undertake consumer-related activities in addition to issuing a newsletter on a regular basis, among other means, to disseminate information on food safety. However, despite the ofcial trend to encourage these associations in North African countries and their contribution to raise food safety awareness among consumers, all efforts may be hampered by limited data on the incidence and prevalence of foodborne diseases among North African traditional foods. In addition, the weak food control capacity of these countries makes it difcult to demonstrate the risk associated with the consumption of such foods on human health and the impact on economic development. Indeed, in the absence of risk assessment or proling studies, and with the lack of epidemiological data and reports on intoxication/infection cases, it is difcult to convince consumers who do not question the wholesomeness of traditional foods and rmly consider that these foods have been part of their diets through generations without representing a threat to health. It is even more difcult to convince most consumers about the risk for chronic diseases such as those caused by mycotoxins. Incidentally, traditional and homemade foods have recently been identied as important nonconventional exposure sources for OTA, due to the widespread of this toxin among such foods (Duarte and others 2009). Nonetheless, traditional foods, especially the fermented types, have been recognized to have good safety records worldwide, including developing countries where they are usually manufactured by people without training in microbiology or chemistry. According to Steinkraus (2002), the safety of such foods is related to different intrinsic protecting principles that discourage the growth of undesirable microorganisms and may also contribute to reduce the levels of mycotoxins. However, the same author emphasized that these principles would not indenitely guarantee a high degree of foods safety, as they would not compensate for unsanitary conditions such as improper storage and handling, use of contaminated water supply, preparation in environments heavily contaminated with human waste, improper personal hygiene by food handlers, infestation with insects spreading disease organisms, and raw materials carrying food poisoning or human pathogens.
Safety of North African traditional foods . . . Effective contribution to the implementation of food safety regulations and control of traditional foods Over the last 2 decades, risk analysis has emerged as a powerful tool that can be used by national food safety authorities to make proportionate and scientically based decisions on food safety issues. Also, as an integral part of Codex Alimentarius, risk analysis can support and improve the development of standards and regulations on a scientic basis and address food safety issues that result from emerging hazards or breakdowns in food control systems. The relevance of risk analysis to all the food safety issues has become increasingly important since its adoption within the SPS agreement. While risk analysis and its scientic component risk assessment are now widely applied in developed countries in Europe, America, and Australia, its extension to developing countries is hindered by many limitations, the most important of which are: r General lack of awareness among ofcials, manufacturers, scientists, and consumers of the real gain that the implementation of risk analysis approaches would represent to national food safety status compared with the conventional food safety and food control measures. r Lack of infrastructure, technical and nancial resources, adequate institutional framework, and necessary expertise to effectively respond to existing and emerging food safety and quality problems. r Insufcient information about the hazards and risks associated with traditional foods due to the lack or poorly documented epidemiological, intoxication records, and scientic investigations. r Lack of data on consumption patterns and insufcient knowledge about levels and occurrence of hazards (chemical and biological) in foods. In view of these limitations, FAO and WHO have been working together to increase the awareness and adoption of risk analysis principles in developing countries, both as a tool for national food safety authorities and the provision of scientic advice and evaluations. These United Nation organizations have also been providing technical and nancial support to developing countries to help them build capacities and strengthen national food control and inspection systems, and activities in order to adopt new food safety frameworks based on risk analysis. Among North African countries, Morocco has beneted from this assistance to reform its food safety policy, as conrmed by the promulgation of the new Law 25-08 on February 18th, 2009. Under this law, the ONSSA has been established as the only institution responsible for protecting the consumer health as well as that of animals and plants (http://www.onssa.gov.ma/onssa/fr/loi_creation.php). Nonetheless, risk assessment of North African traditional foods, at the present, remains incomplete and inaccurate due to the lack of necessary data to produce credible and reliable risk assessment. In fact, this situation has been reported to be the main constraint facing risk assessment worldwide regardless of the type of foods. Yet, the extent of shortage of relevant data and records to conduct risk assessment is variable depending on the country, with developing countries being the most affected. In particular, the lack of the necessary data to estimate exposure to hazards has been identied as one of the critical missing parts in a risk assessment process, as an inaccurate risk estimate would provide risk managers with a false global picture of the situation, which may eventually lead them to make inappropriate decisions (Luetzow 2003). The same author has recommended improving the collection and dissemination of such data worldwide to progressively ll in the gaps for more
reliable estimates of exposure and specically mentioned that a consideration should be given to developing countries by providing them with assistance and resources for generating meaningful food consumption data and subsequent exposure assessments. Alternatively, it has been suggested to perform risk proling with the available data, which should then be revised periodically and amended as new data are generated from scientic studies and surveillance programs to ultimately allow quantitative risk assessment (FAO 2006; Bidlack and others 2009). Meanwhile, risk proling that categorizes food products into groups with high, moderate/medium, or low risk may be a useful tool to assist the decision-making process and to set priority for action. In fact, under certain circumstances, including cases where risk assessment is either unnecessary or not feasible to carry out, risk proling may serve as a basis to identify and select food control measures and risk management decisions. Notable examples of such cases are: (i) the Canadian approach to regulating L. monocytogenes in ready-toeat foods, (ii) the Swedish approach to regulating acrylamides in baked and fried starchy foods, and (iii) the prohibition of certain antibiotics from veterinary care in many countries on the basis of risk proling that suggests microbial resistance to some antibiotics used in both human medicine and animal health care (FAO 2006). A systematic risk proling approach would be appropriate and amply justied for North African traditional foods at the present time. It is generally admitted that the main risks associated with North African traditional food products are of microbial origin (pathogenic bacteria and their toxins, mold toxins, parasites, and viruses), although hazards of another nature, such as pesticide residues and heavy metals (Zaida and others 2007), not discussed in this review, should not be overlooked. Depending on the natural hurdles to microbial growth (salt, sugar, moisture evaporation, fermentation, and so on) used in the manufacturing processes, traditional products may harbor different hazards and the same hazard may present different health risk patterns depending on the product (Larsen 2006; Bidlack and others 2009). Table 6 presents documented hazards of microbial origin associated with North African traditional dairy, meat, and vegetable food products. Table 12 shows various risk factors associated with North African traditional foods and the protective hurdles on which the traditional technology relies to ensure their safety and stability. Corrective actions are proposed on the basis of harvest-to-consumption approach (Table 12). Taking into account the global situation of North African traditional foods and the uncertainties regarding their wholesomeness, it appears urgent to start preliminary risk proling with the presently available knowledge on these products. Simultaneously, scientic studies and chemical and microbiological analyses involving universities and research institutions along with surveillance programs should be initiated to provide new information to progressively rene and update risk proling. However, since traditional food products differ among North African countries and even among localities of the same country, it is vital to facilitate communication and information exchange in foodborne disease surveillance as well as information about foodborne hazards between these countries according to the recommendations of the 27th FAO regional conference (FAO 2004).
Ranking risk of North African traditional foods In order to compare microbiological risks associated with traditional foods from North Africa, the RCM developed by the Federal/Provincial/Territorial Committee on Food Safety Policy (FPTCFSP 2007) was modied and used to prole selected North African traditional foods. This model, originally designed to
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Table 12A 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 scientic basis are also proposed. Risk factors Type of commodities Dairy products Microbial contaminants Mycotoxins Safety factors Corrective actions
r Contaminated raw milk, r Poor sanitary conditions during r Opportunity for pathogens to grow r Contaminated water supply r Usually ready-to-eat r High exposure r No application of any quality
assurance program and produce toxins during processing or storage processing and handling
r Contaminated milk (carryover of r Contamination and growth of

toxinogenic molds on nished product or during storage mycotoxins from feeds)
r Lactic fermentation r Veterinary care of dairy r Predominance of safe or herd (control of mastitis r Reduced aw (dry-salted,
brined cheeses, dried cheese) r Addition of herbs and spices health promoting microorganisms
r GHaP, GHP, GMPs, r Use of selected starter or

HACCP (from the farm to storage)
diseases)
Meat products
r Contaminated raw material r Poor sanitary conditions at r Postprocessing contaminations r Opportunity for pathogens to grow r Poor veterinary care of livestock r No application of a quality
assurance program during processing and/or storage (prevalence of zoonotic diseases) slaughter and processing
r Mycotoxin-containing spices r Contamination and growth of r Presence in the liver and kidney of
animals fed with contaminated feeds (meat products using offal meat) toxinogenic molds on nished product during storage
adjunct starter cultures (controlled fermentation) with antimicrobial activities (for example, use of bacteriocin-producing lactic starter cultures) r Sourcing and potential testing of feed from GAP producers r Addition of herbs and GHP, GMP, on-farm spices HACCP, improve r Reduced aw (dry-salting, animal welfare GHP in brining, drying) food sale and r Heat treatment during preparation to reduce processing microbial r Usually cooked before contamination r Low exposure consumption GAP, GHP, on-farm HACCP, adequate conditioning and storage conditions, controlled fermentation
Vegetable products
r Contaminated raw material r Postprocessing r Contaminations r Opportunity to grow during r Poor hygiene during harvest, r Cross-contamination r Human reservoirs r Contaminated raw material (use of r Sanitary conditions during
wastewater sewage or sludge for irrigations and fertilization manufacture and storage processing, and storage processing or storage
r Presence in fresh vegetable products r Fermentation and persistence during processing r Chemical acidication r Growth of toxinogenic mold and r Reduction of water r Use of spices and condiments
contaminated with various mycotoxins opportunity to produce mycotoxins during processing or storage
r Addition of herbs and

spices with antimicrobial activities (occasionally) r Inherent antimicrobial substances such as euloropein and derivative substances in olives
activity (dry-salting, brining, drying)
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 proling for food retail and food service establishments, takes into account 8 major risk factors each of which is scored according to the extent of risk it poses to consumers. The total score of the 8 factors indicates the risk categorization of a product as per the following cutoff points: high risk (165 points or more); moderate risk (between 110 and 160 points); low risk (105 points or less). The RCM guide also provides an explanation for each risk factor, along with directions on how to determine the corresponding score. These risk factors were determined on the basis of a previous study reviewing factors that contributed to foodborne illness in Canada in the period of 1973 to 1977 (Todd 1983) in addition to other factors used by some jurisdictions to determine inspection frequency. The 8 factors used in this study were: 1. Types of food and intended uses: Scoring of this risk factor is based on 2 main considerations: (i) the likelihood of a food to contain pathogenic microorganisms above safety level and opportunities it provides for the microorganisms to grow and/or produce toxins, and (ii) whether the food is readyto-eat or undergoes further heat treatment or cooking before consumption. For this risk factor, the RCM considers only
biological hazards based on the epidemiological evidence, showing that the most frequent foodborne diseases are of microbial origin. In this study, we also omit microbial toxins, such as mycotoxins, or heat-stable E. coli or Staphylococcal toxins, which may be produced during processing or storage and would not be removed by treatments such as cooking or fermentation. Omission to consider microbial toxins in risk scoring was based on the same reason as stated in the RCM, in addition to the lack of reliable data on these contaminants (occurrence and concentrations) in North African traditional foods. Therefore, high- or medium-risk ready-to-eat foods are scored higher than those which undergo additional treatments (cooking, marinating, addition of herbs, and spices) to reduce or control microbial load before consumption. Similarly, high- or medium-risk foods, which receive further heat treatment or undergo other methods to reduce microbial pathogens, are at reduced risk. Low-risk foods are those that represent a hostile environment (reduced water activity, low pH, contain known antimicrobial substances, and so on) for microbial contamination and growth.

Table 13Risk categorization of traditional foods of North African countries based on the model developed by Health Canadaa using 8 risk factors (I to VIII).b Score of each risk factor Commodity Dairy products Lben Jben Smen Semna Arish cheese Klila Aoules Domiati cheese Mish cheese Kishk Rigouta Zabadi Meat products Gueddid Pastirma Khlii Naqaneq Merguez Vegetable products Pickled green olive Pickled lemon Dry gsf Black ripe olives I 40 40 25 40 40 25 25 30 40 30 25 40 40 40 10 40 40 40 10 10 25 II 40 40 25 25 40 10 25 25 40 25 25 40 40 40 10 40 25 40 10 10 40 III 15 15 15 20d 15 15 15 30 30 30 30 15 15 30 15 15 5 15 0 15 15 IV 30 30 30 30 30 30 30 30 30 30 30 30 30 30 30 30 30 30 30 30 30 V 30 30 30 30 30 30 30 30 30 30 30 30 30 30 0 30 30 30 0 0 30 VI 70d 40 20d 40 40 30 30 40 40 40 40 40 30 40 15 40 40 40 15 15 30 VII 10 10 10 10 20 5e 5e 20 10 10 10 20 10 10 10 10 20 10 10 10 10 VIII 15 15 5e 10e 10e 5e 5e 15 15 15 10 15 10 10 15 5 15 15 0 15 15 Total score (risk category)c 250 (High) 220 (High) 160 (Medium) 225 (High) 225 (High) 150 (Medium) 165 (High) 220 (High) 235 (High) 210 (High) 200 (High) 230 (High) 205 (High) 230 (High) 105 (Medium) 210 (High) 205 (High) 220 (High) 65 (Low) 105 (Low) 195 (High)
a Federal/Provincial/Territorial Committee on Food Safety Policy (FPTCFSP) of health Canada; available from
http://www.hc-sc.gc.ca/ahc-asc/pubs/hpfb-dgpsa/fd-da/risk_categorization-categorisation_risques01-eng.php. b Risk factors as dened by the FPTCFSP are: I = Types of Food and Intended Uses; II = Food Preparation and Processing; III = Equipment and Facility; IV = Management and Employee Food Safety knowledge; V = Food Safety Management Program; VI = Regulatory Compliance; VII = Volume of Food (exposure: rough estimation based on the place of a given food in the local dietary habits); VIII = Typical Patronage (exposure of vulnerable population). The scoring mode of each risk factor is explained in the guide at the website indicated above. c Cutoff points: High risk (165 points or more); moderate risk (between 110 and 160 points); low risk (105 points or less). d Thirty points were added to the original score because this product has been repeatedly associated with intoxications in Morocco during summer seasons. e Risk factors were assigned different scores from those proposed in the CRM taking into account the specic situation of North African traditional foods. f Would shift to the medium risk category if mycotoxins were considered as potential hazards associated with this product.
2. Food preparation and processing: This factor generally refers to whether the food was minimally processed or has undergone a process designed to minimize the likelihood of food safety hazards (pasteurization, boiling, cooking, marinating, fermentation, and so on). In addition, the amount of handling that a food undergoes during preparation is a determinant of the risk posed by a food. Indeed, extensively handled foods, especially if they are uncooked and unpackaged, are considered more likely to be subjected to microbial contaminations, and hence they score highest. 3. Equipment and facilities: To determine the risk linked to a factor, RCM considers the layout and design of food establishments, the way the ow of food goes from reception to service or sale, whether or not raw materials and foods of different risk categories are adequately separated in the establishment, waste storage, and disposal as well as the separation between nonfood activities from food preparation and processing areas. The water supply as food ingredient or for other needs (handwashing, warewashing, and sanitizing), equipment for food preparation or processing (suitability, age, made from nontoxic materials, easily cleanable). As most traditional North African traditional foods are either homemade or produced in small shops, scoring was based mainly on the conditions where a given food is generally prepared including the space, sanitary conditions of processing area, personal hygiene, access to drinkable water, and cleanliness of the utensils used. 4. Management and employee food safety knowledge: According to RCM, scores of this risk factor are attributed depending on the extent of food safety knowledge of employees, managers, and supervisors, which should be ade-
quate enough to ensure that safe food handling practices are being followed with the possibility to undertake corrective actions when necessary. In addition to certication that the managers and employees should have from recognized institutions, they must demonstrate to the regulatory agency that they are following safe practices. Food establishments that do not have adequately trained employees or practice safe food handling principles are at greater risk of being implicated in a foodborne illness. North African traditional foods are generally not produced in modern establishments, by qualied personnel, and after effective training sessions on regular basis, but rather at the household level or in shops, and generally by members of the same family, usually with a low level of education. Therefore, this risk factor would score high for all North African traditional foods. 5. Food safety management program: Development and implementation of food safety management programs such as Hazard Analysis Critical Control Point (HACCP) and its prerequisite support programs, including facility maintenance and sanitation and personal hygiene of foodservice workers, contribute signicantly to a better control of food processing and preparation stages. RCM considers that establishments that have such a program in place would be at less risk than those that have no controls. As was discussed for the former risk factor, North African traditional foods are generally produced with untrained personnel and in an environment where no food safety management program could be appropriately applied. Therefore, this risk factor also scores high for all these foods.

6. Regulatory compliance: Determination of the risk associated with the specic establishment as regards this factor is based on historical information about regulatory compliance with critical items. The occurrence of an outbreak at a foodservice establishment is also taken into consideration when an indication exists that food safety principles were not followed prior to the outbreak. Consumer complaints and responsiveness of the management of the establishment to act on previous advice are also considered to score this risk factor. As the term compliance refers to past and current compliance to inspections, and North African traditional foods are not ofcially inspected, we relied on scientic publications and reports to assess the microbiological compliance to known standards, either by the presence of pathogens or the counts of groups of microorganisms of hygienic significance (coliforms, fecal streptococci). Documented claims about implications of some North African traditional foods in intoxications were also considered. 7. Volume of food: In the RCM, this risk factor relates to the volume of foods sold or prepared, as estimated by the number of people served or provided food, or the number of employees at an establishment at a given time (shifts). Higher volumes of foods increase risk of foodborne illness. To adapt this scoring to North African traditional foods, the frequency and quantity a given traditional food is consumed at each meal, based on personal knowledge of the culinary habits of North African communities, were used to estimate the volume of the food. 8. Typical patronage: Serving foods to subgroups of a population (the young, elderly, and immunocompromised) who are the most vulnerable to foodborne disease will increase the likelihood of occurrence of a foodborne illness outbreak. Some North African traditional foods, especially dairy products such as zabadi and jben are served to young children or sick persons due to the believed health virtues; such products were attributed high scores regarding this risk factor. Table 13 presents a tentative risk proling of selected North African traditional foods using the FPTCFSP RCM after the adjustments/interpretations mentioned above. The outcome of this proling showed that the vast majority of North African traditional foods pose a high risk to consumers, few fall into the medium risk category, and only 2 of the proled products (pickled lemon and dry gs) would be of low risk owing to their extreme intrinsic physicochemical parameters and relatively low consumption pattern, and hence, low exposure. Pickled lemon is highly acidic and salty, while dried gs have low water activity due to their low moisture and high sugar contents. As for the consumption pattern, lemon is used in the North African cuisine as an ingredient in some cooked meals, and dry gs are mainly consumed during the fasting month of Ramadan in Muslim communities as an appetizer. However, the risk associated with the latter product may increase if contamination with mycotoxins are also considered as a potential hazard. Table 13 shows that the risk factors IV (management and employee food safety knowledge) and V (food safety management program) scored highest for almost all the proled foods. This demonstrates the prominent impact, either directly or indirectly, of employee education and the management system on the risk ranking of foods, and it implies that any improvement to reduce risks linked to these foods should rst address these aspects, which will, in turn, mitigate other risk factors. Indeed, there is general agreement that the standardization of technologies for these foods by transfer to small or medium scale is a necesc
sary means to improve the safety of traditional foods (Fellows and others 1995; Rolle and Satin 2002; Steinkraus 2002; Valyasevi and Rolle 2002; Benkerroum and Tamime 2004; Panagou and others 2013). According to this preliminary proling, North African traditional foods that constitute an important part of the North African diet warrant due attention to improve their safety. Risk proling should be ofcially conducted on a large scale through eld surveys in order to prioritize government actions and dene specic regulations and control measures, which should be strictly implemented. Meanwhile, accompanying measures should be taken by the government to provide the necessary assistance, encouragements, and other incentives as was suggested in this review and elsewhere (Rolle and Satin 2002; Valyasevi and Rolle 2002; Benkerroum and Tamime 2004) to gear all producers toward a voluntary adoption of quality assurance management systems to improve the quality and competitiveness of the foods they produce. Practical measures to improve the safety of North African traditional foods at the production level are suggested in Table 13.
Conclusions
With the advent of globalization and involvement of North African countries in many international, regional, subregional, or bilateral agreements (SPS, OIE, CA, European neighborhood partnership, FTA, and so on) and increasing demand in terms of quality and safety of foods for trade, it becomes urgent to reshape the food safety policies in North African countries, not only to upgrade the safety and quality of the foods they produce, but also to protect consumers from fraudulent or unsafe imported foods. The latter foods make up a very high percentage, up to 75%, of the food supply in some of these countries (Mboungou 2011). Any future food safety strategy should be based on a risk analysis approach, and national food regulatory standards should be aligned according to the CA. The standards, guidelines, and recommendations adopted by the CAC are, indeed, referred to in the WTO agreement on the application of SPS agreement as benchmarks for international harmonization of food regulations. Reliable risk assessment or proling studies need to be conducted on different foods of North Africa (including traditional foods) in order to set food control priorities. Despite their different economic, demographic, and political priorities, North African countries share much sociocultural specicity that would be an asset for their common sustainable development and the differences could, in fact, be regarded as complementarities that stimulate synergistic actions. Therefore, it is crucial to facilitate the exchange of information on all food safety-related issues and perform common risk proling and assessments when possible. Nonetheless, to make such profound changes in food safety policy, North African countries are facing various nancial, technical, cultural, and political challenges that they may not overcome if they rely only on their own potentialities and resources; they require greater and concrete synergistic actions between each other in addition to external assistance from international organizations (FAO, EU, OIE, OECD, WHO, and so on) and developed countries.
Acknowledgment
Deep appreciation is expressed to Dr. Dennis Bittisnich of the Australian Government Dept. of Agriculture, Fisheries and Forestry, and Dr. Manfred Luetzow, international food safety consultant, for reviewing the prepublication manuscript and for their expert comments and suggestions. The author is also grateful

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North African Trad Food Risk Profiling

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Traditional Fermented Foods of North African Countries: Technology and Food Safety Challenges With Regard to Microbiological Risks

Safety of North African traditional foods . . .

2012 Institute of Food Technologists

Safety of North African traditional foods . . .

Country Algeria Egypt Libya Morocco Tunisia

NA: Not available.

2012 Institute of Food Technologists

Safety of North African traditional foods . . .

Arish, kariesh, or karish cheese

Kurmann and others 1992; Steinkraus 1995

Benkerroum and Tamime 2004; Abd-El Salam and Benkerroum 2006

Abd-El Salam and Benkerroum 2006

2012 Institute of Food Technologists

Safety of North African traditional foods . . .

Tallaga cheese Mish cheese

Aboudonia 1996 Abd-El Salam and Benkerroum 2006

Ghrairi and others 2004

El-Neshawy and El-Shae 1988; Mehanna 1991

2012 Institute of Food Technologists

Safety of North African traditional foods . . .

2012 Institute of Food Technologists

Safety of North African traditional foods . . .

Removed fat Lean meat Cutting

eat Strips of me (about 4 cm wide, 40 -60 ong, cm lo and 1-2 cm thick)

Salting 100 (5.0-7.0 g salt/1 g meat)

ing l Placi in a cool perature temp (3 to 4 days)

cal Typic gueddid/Keddid

un-drying*: Su g Hanging meat strips on a ire laundry rope or a wi (5 to 7 days) t

Safety of North African traditional foods . . .

y-curing Dry (3-4 days)

t First drying o (3 to 5 days)

Safety of North African traditional foods . . .

eat Muscle me Beef, lamb, goat or camel ,

Figure 5Traditional process to produce khlii and 2 of its main variants.

2012 Institute of Food Technologists

Safety of North African traditional foods . . .

2012 Institute of Food Technologists

Safety of North African traditional foods . . .

Express khlii Merguez

4.6 to 5.6 0.86 to 0.92 NA NA

Daoudi and others 2006 Daoudi and others 2006

Daoudi and others 2006

Microbiology of Traditional North African Foods and Associated Hazards

2012 Institute of Food Technologists

Safety of North African traditional foods . . .

Conditions that favor the growth of mesophilic lacitic acid bacteria

Oli preparation ti Olive

Safety of North African traditional foods . . .

2012 Institute of Food Technologists

Safety of North African traditional foods . . .

2012 Institute of Food Technologists

Safety of North African traditional foods . . .

2012 Institute of Food Technologists

Safety of North African traditional foods . . .

(Cohen and others 2006). (Oumokhtar and others 2008).

2012 Institute of Food Technologists

Safety of North African traditional foods . . .

2012 Institute of Food Technologists

Safety of North African traditional foods . . .

2012 Institute of Food Technologists

Safety of North African traditional foods . . .

15 4.52 2.12 2.03 3.8 3.6 1.88 4.22

90 6.88 1.96 1.35 6.96 5.66 5.98 1.53