North African Trad Food Risk Profiling

Traditional Fermented Foods of North AfricanCountries: Technology and Food SafetyChallenges With Regard to Microbiological RisksNoreddine Benkerroum

Abstract: North African countries have a rich tradition in food technology, and many traditional foods of animal orplant origin are still widely consumed and highly appreciated. In fact, these foods play an important role in the economyand food security in these countries. Yet, they are still mainly prepared at the household level under poor sanitaryconditions and marketed through informal routes. They thus remain beyond any official control for their compliance tonational regulatory standards. Therefore, their consumption is anticipated to put the public health at risk, although suchrisk has never been estimated on a scientific basis due to the lack of consumption patterns, epidemiological data, andappropriate surveillance programs. The scarcity of scientific studies on the incidence of hazards in this specific category offoods adds to the difficulties in conducting scientifically sound risk assessment or profiling studies. This review providesa brief description of technologies of the most popular traditional foods of animal and plant origin in North Africa anddiscusses the potential microbiological risks associated with their consumption and the food safety challenges that theyraise. The review also aims to draw the attention of stakeholders including decision makers in North African countriesto the imperious need to assess or profile the health risks associated with their consumption, and consequently, take thenecessary measures to reduce such risks. A tentative risk profiling of selected traditional North African foods is presentedusing as a template the “risk categorization model for food retail/food service establishments” developed by HealthCanada.

IntroductionNorth African countries have an ancient tradition in food tech-

nology, and many traditional foods have been passed down fromone generation to another through the ages. In Egypt, for exam-ple, fermented dairy and meat products, as well as wine and beer,have been traced back at least to the pharaoh era of 4000 BC (Rossand others 2002). Some cheese varieties have also been suggestedto 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 influence ofthe different civilizations that have been established throughouthistory in the region is still evident in all aspects of life includ-ing culinary habits. Indeed, these countries are heavily influencedby ancient civilizations, such as those of the Greeks, Phoenicians,Egyptians, Romans, and Vandals, and more recently by the Islamiccivilization starting with the Arab conquest (late 7th century) andthe presence of Ottomans (Turkish invaders), also Muslims, duringthe 15th and 16th centuries (Stearns and others 2010). Therefore,North African countries share many traditional foods resulting

MS 20121004 Submitted 7/23/2012, Accepted 10/8/2012. The Author is withInst. Agronomique et Veterinaire Hassan II, Dept. des Sciences Alimentaires et Nu-tritionnelles, BP 6202, Instituts, 10101-Rabat, Morocco. Direct inquiries to authorBenkerroum (E-mail: [email protected]).

from the blend of nutritional habits brought by these civilizationsand their interactions with those of the original inhabitants such asthe Amazigh/Berber people in the Maghreb. For example, influ-ence from the Romans (146 BC) can be recognized throughoutthe region, as wheat is the basis for the main staple foods: breadand couscous. Islamic influence can be recognized in the strictprohibition of wine and pork meat, while the other meat prod-ucts must be obtained from game animals or those slaughteredaccording 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 others2006). Yet, other foods consumed by religious or ethnic minoritiesin the region are also available and retailed throughout the existingmarketing routes. This historical sociocultural situation has createda clear distinction between nutritional habits of the North Africaregion and those of Northern Mediterranean countries.

This review provides a brief description of technologies ofthe most popular North African traditional foods of animal andplant origin, and presents an overview of the available data ontheir microbiology and presence of microbial toxins as sourcesof risk to consumers. Risk factors as well as safety factors arediscussed in the perspective to provide producers with technicalmeans to enhance the safety of such foods. Profiling selected tra-ditional North African foods based on a risk categorization model(RCM) developed by Health Canada was conducted, and the

54 Comprehensive Reviews in Food Science and Food Safety � Vol. 12, 2013c© 2012 Institute of Food Technologists®

doi: 10.1111/j.1541-4337.2012.00215.x

Safety of North African traditional foods . . .

AOAtlantic Ocean

Mauritania

Algeria

M

Libya

Mediterraanean Sea

Sudan

a

Red

Sea

MoroccoTunisia

Egypt

Figure 1–Countries of the North Africa subregion according to the most accepted definition (underlined boldface). Either Mauritania or Sudan (normalfonts on a gray background) is occasionally considered as part of this region.

results showed that most North African traditional foods put con-sumers at high risk, a challenging situation that should be addressedurgently, and different actions involving all interested parties arediscussed.

The North African Region at a GlanceLocated along the southern coast of the Mediterranean basin,

North Africa is the northernmost region of the African continentspanning from the Atlantic Ocean in the West to the Red Seain the East. In the south, it is surrounded from west to east bya subarid Sahara (desert in Arabic) belt called Sahel (Figure 1).The North Africa region now consists essentially of 5 countries(Morocco, Algeria, Tunisia, Libya, and Egypt), and is classicallydivided into 2 subregions: the Maghreb/Maghrib, meaning “thesunset place” (West) in Arabic, typically including Morocco, Al-geria, and Tunisia, and the Mashrek (Libya and Egypt), meaning“the sunrise place” (East). Although this definition of the NorthAfrican region is the most widely accepted, it is not the onlyone due to the multiplicity of geopolitical considerations and thechanging political status of the countries throughout the history ofthe region. Mauritania is occasionally added as part of the “GreatArab Maghreb” that also includes Libya in addition to the 3 cen-tral countries of the Maghreb (Morocco, Algeria, and Tunisia). In1989, the latter 5 countries have established the Arab MaghrebUnion (UMA) on the basis of geographical considerations andthe common social, cultural, and historical heritage in additionto economic complementarities. On the other hand, the UnitedNations’ definition of North Africa region includes Sudan butexcludes Mauritania, which is considered among the Sahel coun-tries. Furthermore, the fact that Egypt is also part of the MiddleEastern region, which with North Africa forms the Arab world,adds some confusion to the definition of the exact geographi-cal boarders of the North African region. This definition is evenmore confusing in that the Sinai desert, in North-Eastern Egypt,is part of the Asian continent. Nonetheless, regardless of the ge-ographical or geopolitical definition, Morocco, Algeria, Tunisia,Libya, and Egypt form the core of the North Africa region andwill thus be considered in this review. Table 1 summarizes themain demographic, economic, social, and cultural data for thesecountries.

Popular Traditional Foods in North African CountriesDairy products

Although the North African diet is typically low in foods ofanimal origin compared to foods of plant origin, mainly cereals andolives (Grigg 1999; Padilla and others 2005; Alexandratos 2006), avariety of centuries-old dairy products are known and still highlyappreciated by consumers in these countries. The most popularof them are jben, lben, and smen, which have been reviewedpreviously (Benkerroum and Tamime 2004; Abd-El Salam andBenkerroum 2006). However, in Egypt where the production andconsumption of cheese are significantly higher than in the othercountries of North Africa (Table 2), there are more diversifiedand elaborated cheese types, among which brined cheeses are themost dominant (Abd-El Salam and Benkerroum 2006). Table 3presents selected traditional North African dairy products witha brief description of their technologies (for further details, seeAboudonia 1996; Benkerroum and Tamime 2004; Abd-El Salamand Benkerroum 2006).

Meat productsThe overall consumption of meat products in North African

countries (Table 2) is below the global average of 38 kg per capitaper year (Speedy 2003). Although this situation is primarily at-tributed to the low level of meat production (Table 2), the cost ofmeat products, not always afforded by the majority of consumers,justifies further this limitation. Nonetheless, various traditionalmeat products have long been known in the region and preparedfor family or religious feasts. They were also made as a meansto preserve meat when it was available at quantities exceedingimmediate needs, while appropriate storage means such as ice, re-frigerators, and freezers were lacking. For example, in the religiousfeast “Al Adha,” each Muslim family ought to slaughter a lamb,and there is usually more meat than can be consumed in few days(2 to 3 d). Surplus meat was then transformed into more stableproducts that could be kept at room temperature for as long as pos-sible without being spoiled or becoming hazardous to consumers’health. This was achieved by treatments combining different nat-ural hurdles to microbial growth such as curing, salting, drying,and fermentation, in an empirical application of the hurdle tech-nology as recently advocated by Leistner (2000a). Although spicesand herbs were added to traditional meat products, primarily as

c© 2012 Institute of Food Technologists® Vol. 12, 2013 � Comprehensive Reviews in Food Science and Food Safety 55


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 andAgricultural Organization of the United Nations (FAO) (http://faostat.fao.org/) websites. Accessed on April 17, 2012. Statistic data and indices arefor the year 2011, unless otherwise stated in the footnotes.

Area Population Urban GNI per Official OfficialThe country (km2) (millions) population (%) Main economic activity capitaa PINb HDIc religiond language

Morocco 710,850 32.27 58.8 Agriculture, phosphates mines,tourism, and sea foods

4,196 120.90 0.582 Islam Arabic + Tamazight

Algeria 2,381,741 35.98 67.1 Oil and natural gas 7,658 116.00 0.630 Islam Arabic + TamazightTunisia 163,610 10.60 67.7 Agriculture, mining,

manufacturing, and tourism7,281 98.05 0.698 Islam Arabic + Tamazight

Libya 1,759,541 6.42 78.1 Oil and natural gas 12,637 102.31 0.760 Islam Arabic + TamazightEgypt 1,002,450 82.54 43.5 Agriculture, oil, and tourism 5,269 102.78 0.644 Islam ArabicaGross national income (GNI) per capita in PPP terms (constant 2005 international $, see the definition at http://www.who.int/choice/costs/ppp/en/): Aggregate income of an economy generated by itsproduction 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.bFood production index (PIN) per capita for the year 2010 based on 2004 to 2006 = 1000.cHuman 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).dMinorities of other religious and cultural backgrounds such as Christians and Jewish are also present.NA: Not available.

Table 2–Production and apparent consumption for the years 2010 and2007, respectively, of milk, cheese, and meat in North African countries.

Production Consumption(1000 metric tons) (kg/capita/year)

Country Milk Cheese Meat Milk Cheese Meat

Algeria 2304.00 1.540 609.26 117.36 0.65 20.13Egypt 5742.40 940.15 1731.14 61.81 7.47 22.08Libya 222.70 NA 186.68 75.03 1.78 27.84Morocco 2009.55 43.73 1036.13 44.49 0.82 25.02Tunisia 1093.10 4.14 274.76 106.91 0.26 27.34

NA: Not available.

flavoring and aromatizing agents, it is now well established thatthey also contribute to the improvement of food safety and keep-ing quality, as many of them have been shown to possess potent an-timicrobial activities (Al-Delaimy and Barakat 1971; Kivanc 1988;Ghalfi and others 2007; Kong and others 2007; Ivanova and others2009; Rattanachaikunsopon and Phumkhachorn 2009, 2010a, b).Among these, garlic, curcuma, cinnamon, cumin, ginger, cloves,paprika, and pepper (black, white, or red) coriander (leaves orgrain) have been the most frequently used in traditional meatpreparations. Also, pretreatments such as cooking or marinatinginto an acid, spicy preparation called sharmula for 1 or 2 d wereapplied to raw meat in order to improve its microbiological qualityin addition to the enhancement of the final gustatory quality ofthe meat products deriving thereof. Moreover, traditional meatproducts of North African origin are primarily obtained frombovine, lamb, goat, buffalo, or camel meat, which have the “halal”status according to the Islamic rules. Yet, traditional pork meatproducts are also available, but they are claimed by Christian localminorities such as the Copts in Egypt, or destined to temporaryresidents (foreign employees and diplomats or tourists) from othercountries, and hence they are produced in very limited quanti-ties. Similarly, the “kosher” traditional meat products are mainlyproduced at the household level in Jewish families.

GueddidThe oldest means to preserve meat is probably by salting and

sun-drying (Nummer and others 2004). Gueddid (Figure 2a), atypical meat product of the Maghreb countries (Morocco, Algeria,and Tunisia), is obtained by such a basic technology yielding stablesalty dry meat, which can be stored at room temperature for morethan a year. It is primarily prepared from lamb meat or beef; inthe subarid zones of the region, camel and goat meats are mostlyused as depicted in Figure 3. At consumption, gueddid is softenedand desalted by immersion in water to make it tender before use

as an ingredient in various dishes, such as the well-known NorthAfrican couscous or legume stews. The cured variant of gueddidmay also be further processed into “khlii” (see below). Althoughthe original purpose of transforming meat into gueddid was itspreservation to last as long as possible, given the lack of adequatestorage facilities; it is now regarded as prestigious and highly prizedcultural heritage food in North African countries. Therefore, localmeat industries are trying to standardize its technology for anadequate transfer to industrial scale, as has been done with jerkymeat (Draganski 2012), in response to consumer demands andfor export to other countries with high concentration of NorthAfrican communities such as France, Italy, Spain, and Canada.

Pastirma/ basterma/basturma/pastramiThis traditional meat product is the most popular in Egypt and

consists of cured and dried meat strips encased in a mixture ofgarlic, fenugreek, and various spices (Figure 2b). It is believedthat pastirma has been brought to Egypt from Turkey, most likelyduring the Ottoman domination in Middle Eastern and NorthAfrican areas in the 15th and 16th centuries. In fact, the term“bastirma” means “strong pressing action” in Turkish as pressureis a crucial step in the preparation of the product (Obuz and oth-ers 2012). Yet, it has been suggested that pastirma is originallya Roman (Byzantine) food product (Adamson 2002). Althoughpastirma is preferably made from beef, various other meat typesare also used, including lamb, goat, buffalo, and camel. A typi-cal method for pastirma preparation is summarized in Figure 4.The finished product has a pH of 4.5 to 5.8, a salt content of6.0%, water activity of 0.85 to 0.90, and moisture of 35% to 52%(Leistner 2000b; Bechtel 2001; Obuz and others 2012). Pastirmais consumed with scrambled eggs, cut into slices and fried, grilledlightly over a charcoal fire, or added as an ingredient to variousculinary preparations such as bean stew.

Khlii/khlia and related productsKhlii is a candied meat product obtained from salted-dried meat,

which is cooked and conditioned in fat (Figure 2c). It is a typicalMoroccan cured meat product, probably brought to the countryby Arab conquerors (early 8th century) on their way to Andalusiain the Iberian Peninsula (Daoudi and others 2006). Due to itsextended shelf life even when stored under abusive temperature(more than 2 y when stored properly), it was the main food supplyfor Arab warriors to avoid food shortage while providing themwith such tasty and nutritious food. Although genuine khlii isbelieved to be made from camel meat, beef is the most widelyused in practice. Typical traditional technologies of khlii and some

56 Comprehensive Reviews in Food Science and Food Safety � Vol. 12, 2013 c© 2012 Institute of Food Technologists®


Table 3–Main traditional North African dairy products; a brief description of their technologies (for further reading see Steinkraus 1995; Benkerroumand Tamime 2004; Abd-El Salam and Benkerroum 2006).

Main microorganisms involved inVernacular name Description fermentation as part of safety factors References

Leben or lben(maghreb), orLaban khad/labankherbah (in Egypt)

Fermented milk (buttermilk) obtained by churningspontaneously soured milk to remove butter. Acommon dairy product in all North Africancountries though with different names.

Lactic acid bacteria: L. lactis subsplactis, S. salivarius subsp.thermophilus, Lb. delbrueckii subsp.bulgaricus, plantarum, yeasts:Saccharomyces cervisiae,Kluyveromyces marxianus

Tantaoui-Elaraki and El Marrakchi1987; Benkerroum and Tamime2004

Zebda beldia/zebdabaladi/zebda beldi

Raw butter, with a strong diacetyl flavor, separatedfrom lben after churning spontaneouslycoagulated milk. Zebda beldi is a common dairyproduct to all North African countries.

Same as leben from which it derives butdominated by Lc. lactis subsp. lactisand subsp. cremoris.

Tantaoui-Elaraki and El Marrakchi1987; Samet-Bali and others2009

Smen Rancid butter of Maghreb countries obtained fromraw butter salted (8% to 10%) and matured in the

Staph. aureus coagulase-negative,Bacillus spp. (not cereus)

Benkerroum and Tamime 2004;Samet-Bali and others 2009

dark under anaerobic cool (13 to 15 ◦C) conditionsfor a period of 6 to 12 mo.

Yeasts, molds

Shmen An Algerian clarified butter oil obtained by churning Lc. lactis ssp. cremoris Kacem and Karam 2006bspontaneously acidified camel milk. The butter is Lc. lactis ssp. lactis biovar diacetylactisthen boiled and clarified while still liquid after Lb. plantarumthe addition of a clarifying agent (for example, Lb. delbrueckii ssp. bulgaricuscrushed dates) and skimming it off after Lb. paracasei ssp. paracaseiflocculation of impurities. Leu. pseudomesenteroides

Leu. gelidumRaib Spontaneously curdled raw milk. It may be a Lc. lactis. Benkerroum and Tamime 2004;

finished product (consumed as such) or anintermediate for the production of traditional

Lc. lactis ssp. lactis biovar diacetylactis,Leuconostoc mesenteroides.

Mechai and Kirane 2008;Bendimerad and others 2012

cheeses or other fermented milks. A common dairyproduct in all North African countries though withdifferent names.

Leuconostoc mesenteroides subsp.mesenteroides.

Laben zeer An Egyptian thick fermented milk obtained bystorage of leben (see above) in an amphora-chapped porous earthenware container (zeer) atroom temperature allowing it to further sour (finalpH 3.5 to 3.8) and concentrate as a result of wheypermeation through the zeer wall.

Lb. casei, plantarum, and brevis El-Gendy 1983

Semna/Sman Raw butter that separates from leben preparation isheated and clarified by sieving through a strainer.A common batter derivative in Egypt and Tunisia,and the same product is called Ghee in India.

NA FAO 1990

Arish, kariesh, or An Egyptian white soft cheese made from the LAB: Lc. lactis, Lb. casei. Kurmann and others 1992;karish cheese remaining curd after removal of the upper cream

layer from spontaneously coagulated milk (raib) inan earthenware pot (matared). Unlike the zeer,the matared used to prepare arish is treated toprevent whey permeation (soaking the inside ofthe pot by seed or olive oil, or a mixture of egg yolkand oil followed by heating in an oven). Arish maybe salted before consumption to enhance thetaste, or further processed into mish cheese (seebelow).

Yeast: Saccharomyces kefir. Steinkraus 1995

Jben Fresh cheese obtained by spontaneous fermentation Lc. lactis subsp. Benkerroum and Tamime 2004;of milk followed by whey drainage. It is lactis and subsp. Abd-El Salam and Benkerroumoccasionally brined in a saturated saline solution lactis biovar diacetylactis 2006(25 to 30 g salt per 100 mL water) at roomtemperature for 2 to 15 d. Widely consumed inMaghreb countries (Morocco, Tunisia, andAlgeria).

Lb. casei susbp. casei, Leuconostoc lactis

Klila Cheese curd obtained from a 3- to 4-d-old lben by Pediococcus acidilactis Abd-El Salam and Benkerroumheating and sieving through a muslin cloth or 2006straw basket to discard whey. Usually consumed in Lb. confususAlgeria and Morocco as whey to prevent wastageof too sour lben.

Ent. faecalis, Ent. faecium

Aoules A typical Algerian dry goat milk cheese (87% to92% dry matter) obtained from spontaneouslycoagulated goat milk, which is churned to removebutter. The resulting goat lben is poured into aclay pot and heated moderately on an open fireuntil proteins precipitate, in a similar manner asklila. The precipitate is strained in a straw basketand the curd is kneaded in small quantity at a timeto be given the shape of a flat small cylinder (2 cmthick, 6 to 8 cm diameter). The cheese is thensun-dried. Aoules is ground and mixed with datepaste or beverage for consumption.

NA FAO 1990

(Continued)



Table 3–(Continued)

Main microorganisms involved inVernacular name Description fermentation as part of safety factors References

Domiati cheese A typical Egyptian brined cheese obtained from rawmilk salted (10 to 15 g/100 mL) and coagulated(mixed coagulation: acid and rennet), and the curdis drained under moderate pressure. Pieces (about500 g) are put into brine (15 to 20 g salt per 100mL whey) and then conditioned into tightly closedcontainers where it ripens for about 3 mo at roomtemperature.

E. faecalis, E. faecium, Lc. lactis, subsp.lactis, Lc. lactis subsp. cremoris, Lc.garvieae, Lb. casei subsp. casei, Lb.plantarum, Lb. brevis, Lb. Delbrueckii,subsp. lactis, Lb. alimentarius, Lb.versmoldensis, Pediococcusinopinatus, and Leu. mesenteroidessubsp. cremoris, Brevibacteriumlinens and Propionibacterium jensenii

Aboudonia 1996; Abd-El Salamand Benkerroum 2006

Yeasts: Triechospora spp.,Saccharomyces spp., Pichia spp.,Debrayomyces, Hansenula spp.,Torulopsis spp., Endomycopsis spp.,Cryptococcus spp.

Tallaga cheese Similar to domiati cheese, but it is not brined and ismatured under refrigeration temperature (4 to 7◦C) for a longer period (up to 9 mo).

Lc. Lactis, subsp. cremoris, Lb. casei, andsubsp. casei

Aboudonia 1996

Mish cheese An Egyptian cheese obtained from a blend of Arishcheese and lben in a porous earthenware pot(zeer); the mixture is flavored with different typesof pepper (for example, green, red, hot, andpaprika) or black cumin, salted (about 10 g/100g) and placed in a warm place to ripen. Brinepermeation through the porous walls of zeerduring the ripening period allows mish toconcentrate and be eventually converted intopaste.

Lactic acid bacteria, Bacillus spp. Abd-El Salam and Benkerroum2006

Kishk A mixture of dry fermented milk and crushed cereal,usually wheat, (2 : 1 to 1 : 3; cereal to yogurt)widely consumed in Egypt. It is traditionally madefrom dough containing spontaneously soured milk(leben), parboiled cracked wheat, and salt. Thismixture is spread in a thin layer and sun-dried toreach 85% to 90% dry matter, and finally groundinto pieces of 2 to 4 mm size. Kishk can be kept for1 y at room temperature and may be consumed ina variety of ways, but one popular use is in thepreparation of a hot porridge-like gruel.

Lactococcus spp., Lactobacillus spp., Lb.brevis, Lb. casei, Lb. plantarum

Morcos and others 1973;Steinkraus 1983; Tamime andO’Connor 1995

Rigouta Similar to the Italian riccota, rigouta is obtained fromcheese whey, which is heated (80 to 90 ◦C) tocoagulate the whey proteins (albumins andglobulins); the coagulum is then allowed to drainin a traditional straw basket, clean clothes, orother porous plastic or metal containers.

Lc. lactis, Enterococcus foecalis Ghrairi and others 2004

Zabadi Similar to set yogurt, zabadi is prepared from milkfortified with skim milk powder, dried whey orsoybean flour, heat-treated and inoculated withthe yogurt starter culture (Lactobacillusdelbrueckii subsp. bulgaricus and Streptococcussalivarius subsp. thermophilus), then kept at 30 to35 ◦C until coagulation occurs (4 to 24 h)

Lb. bulgaricus; StreptococcusThermophilus.

El-Neshawy and El-Shafie 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 oilinstead of animal fat, is being increasingly popular due to consumerawareness of the risks for cardiovascular diseases associated withcholesterol and other metabolism and nutrition disorders. Properlymade and conditioned khlii can be preserved for more than 2 yat room temperature; it is consumed as such (ready-to-eat meatproduct) or fried with eggs for breakfast. It could also be used as aningredient in different traditional dishes such as soups, pancakes,and couscous or, more recently, as a topping for pizza.

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 cas-ing (bovine or ovine intestine) previously soaked in boiling water.Therefore, these products are highly variable from one country toanother and even among regions of the same country, dependingon the seasoning, the specific casing used, as well as the maturation

and drying conditions when applicable. Figure 6 presents a typicalprocess to make sujuk as shown in the photograph of Figure 2e..

MerguezMerguez 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 madefrom turkey or chicken is being increasingly made in a similar wayas the beef variety, but without addition of paprika or other foodcolor additives to keep the typical grayish color (Figure 2g). Atpresent, merguez is mainly produced by modern butcher shops ata semi-industrial scale using modern machines to chop the meatand push the batter into the casing, in addition to the use ofnitrites functioning as salt, coloring (development of red color ifappropriate), and as a preservative agent to prevent the outgrowthof Clostridium botulinum spores and production of botulism-causingtoxin. Furthermore, natural casing is being gradually replaced bysynthetic collagen casing. Merguez is a highly perishable productand should therefore be consumed within 2 d after preparation



Figure 2–Main traditional meat products in North African countries. (kourdass: http://www.comlive.net/L-harissa-Tout-Simplement,124674,780.htm; gueddid: http://ririfleur.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 friedor barbecued to prepare sandwiches. However, in some countries,such as Tunisia and Algeria, it is commonly added as an ingredientin “couscous.”

MiscellaneousIn addition to muscle tissues, offal is also used to prepare tradi-

tional meat products, some of which considered to be a delicacy

by gourmets. Bubanita, tehal, kourdass, and ban-shems are ex-amples of such products, and their technologies with their mainphysicochemical characteristics that have an impact on microbialgrowth are summarized in Table 4.

Vegetable productsProducts of plant origin (fruits and vegetables) represent an im-

portant component in the diet of North African countries despite



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their relatively modest per capita consumption (Table 5) as com-pared to China, for example, where the highest consumption ofvegetables worldwide has been recorded over the last 2 decades.Nonetheless, the overall consumption of vegetable products in NAis higher than the minimum level of 146 kg per capita per yearrecommended by the joint commission of the World Health Or-ganization (WHO) and the Food and Agriculture Organization(FAO) of the United Nations (FAO/WHO 2004). Moreover, anoverall tendency to increased fruit and vegetable consumption hasbeen recorded in North African countries in the period of 2000 to2007 (Figure 7). Figure 7b shows also that the per capita consump-tion of fruits in most North African countries remained low com-pared to the global average recorded during the period of 2000 to2007. Nonetheless, the high per capita consumption of vegetablesin these countries during the same period (Figure 7a) would com-pensate for such a deficiency to meet the WHO recommendedlevel for the overall consumption of vegetable products.

Although fruits and vegetables are generally consumed fresh, animportant part of the harvest is processed for preservation, eitherat the household level by using traditional low-cost technologies

or in modern factories. Traditional preservation technologies ofvegetables products have long been practiced in North Africanareas to make these wholesome foods available throughout theyear. Fermentation, pickling, cooking, and/or drying have beenthe main traditional techniques used to preserve many ripe prod-ucts available only at given periods of the year such as olives,lemons, onions, green peppers, carrots, figs, grapes, prickly pears,and so on. Among these, olives are probably the oldest and themost culturally and economically significant products in the re-gion, and hence their preservation by traditional technologies willbe discussed in some details here.

Table olivesOlive (Olea europaea L.) is typically a Mediterranean tree that has

been grown in the region for millennia, and its fruit has been usedin a variety of ways in the diet as a table olive or as raw materialto produce olive oil.

A number of traditional technologies have long been usedin North African countries to produce palatable table olivesthat could be stored for a relatively long period at ambient



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temperature. However, despite the diversity of these methods,they are based on 2 main procedures: (i) pickling and (ii) dry-salting. Both procedures rely, first on salt to remove the glycosideeuloropein that makes olives unpalatable even when they are fullyripened (black olives) and, second, on microbial fermentation todevelop acidity and specific aroma while contributing to the mi-crobiological safety of the final product. Other processes such as the“Spanish green olive style” and the “California style” use sodiumhydroxide (as a debittering agent to remove euloropein) and otherchemical products (for example food-grade acids and potassiumchloride) in addition to salt (Cardoso and others 2008; Panagouand others 2013). The latter techniques will not be consideredfurther, as they are used for large-scale commercial productionand unlike in European countries (Panagou and others 2013), theaddition of chemicals, including sodium chloride, has not beenpracticed traditionally in North African countries.

A typical North African traditional olive pickling procedureis presented in Figure 8. Pickled olives may be seasoned before

consumption by addition of different spices and flavoring ingredi-ents 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 dry-salting techniques; the most commonly used of which involvespacking olives in plain salt for at least 1 mo to produce the so-called “Greek style” olive. It is the simplest and probably theoldest technique used to preserve olives and make it palatableafter removal of the euloropein. In North African countries, thistraditional method is exclusively used for fully mature black olives,by placing them in a container as interposed layers with salt in aproportion of 40 g salt to 100 g olives. These salted olives are keptat room temperature until a pleasant flavor is reached, generallyafter 30 to 60 d (Cardoso and others 2008). A related traditionalprocedure widely used in Maghreb countries consists of placingblack olives in a burlap sack or a straw basket and evenly mixingthem with salt (10 g per 100 g olives). A heavy weight (usually



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stones of approximately half the weight of the olives) is placed onthe top of the sack or basket to accelerate extrusion of olive juice,and euloropein with it. The whole package is left to ferment for5 d in a warm place (20 to 25 ◦C). Olives are taken out of thesack 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 exposedto the sun for 2 successive days to be ready for consumption. Theresulting olives from the application of the latter process have amore pleasant and less salty taste than the Greek-style olives, butthey have a limited shelf life not exceeding few months at ambienttemperature. Dry salted olives may be rolled in olive oil for adesired taste and shiny appearance and/or flavored with variousherbs, spices, lemon pieces, and crushed garlic.

LemonsLemons are widely used as a flavoring agent in North African

cuisine including tajine, soups, stews, and fish-based dishes. How-ever, they are available at affordable price only during winter andspring seasons when ripening. Therefore, many traditional preser-

vation techniques have been used to make lemon available dur-ing summer and autumn when scarce and expensive. The mostcommon of such techniques involves dry-salting and fermenta-tion, usually referred to as the “Moroccan style” pickled lemon(Figure 9c). According to this technique, ripe lemons (yellow incolor) are soaked in fresh water for 3 d while changing the waterdaily to reduce the bitterness. Each lemon is then cut into quartersfrom the pointed end to about 2 cm of the stalk end, opened with-out breaking the quarters apart and filled with coarse salt (about100 g each). The salted lemons are firmly packed in a clear glasscontainer that is tightly sealed to prevent air access and left in acool dry place for 4 to 6 wk. Meanwhile, the osmotic pressureexerted by the salt causes lemon juice exude and dissolve the salt,thereby creating a strongly salty and acidic brine that covers partlyor totally the lemons in the container. These conditions selectfor the microorganisms (acid- and salt-tolerant) to govern the fer-mentation process; they are predominantly lactic acid bacteria andyeasts (Bousmaha and others 2006). However, a recent study onsuch a cured lemon called “msayer or msir” in Morocco showedthat yeast, represented by Candida parapsislosis and unclassified



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saccharomycetales, is the predominating microbial group, whileLAB are only weakly represented during the early steps of curing,and were not detected in the finished product (Aayah and others2010). Lemon when pickled may be stored for more than a yearat room temperature and can be used in various ways as wholeor chopped in small pieces. In some instances, only the peel isused. Another type of pickled lemon widely consumed in NorthAfrica, 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 24h. At this stage, the lemon slices become soft and their bitternessis reduced, they are then placed in layers in a clear jar while sprin-kling paprika between the layers. Flavored seed oil (preferred toolive oil with too strong aroma) is added to cover the slices in thecontainer that is then tightly closed and left at room temperaturefor at least 3 wk (Roden 1974).

Horticulture vegetablesMany garden vegetables such as carrots, turnips, green or red

peppers, onions (especially the small variety of pearl onions), andcauliflower are commonly preserved, individually or as mixtures,whole or in pieces, by traditional North African techniques. Themost commonly used of such techniques is brining in weak orstrong brine depending on the desired gustatory quality and theexpected shelf life of the final product. Weak brine (about 2.5 gper 100 mL water) yields mildly salty and acidic products with arelatively short shelf life (3 to 6 mo), while strong brine (>10 ofsalt per 100 mL water) yields salty but moderately acidic productsthat may be stored for more than a year. However, the latterproducts should generally be soaked or rinsed in fresh water beforeconsumption to dilute the saltiness. In both cases, the prevailing

ecological parameters during fermentation and storage should beset to promote the lactic acid fermentation, and hence, the growthof LAB (Niketic-Aleksic and others 1973; Peres and others 2012).Typically, this procedure involves the preparation of vegetables bysorting, washing, and occasionally slicing. After this preparationstep, the vegetables are submerged with the appropriate brinesolution in a glass container, which is then tightly sealed and leftin a cool place to allow for fermentation. A recent modificationof this technique consists in adding vinegar to the brine to ensuresuccessful fermentation, especially when low-salt brine is used.Lowering the initial pH, along with the moderate salinity, helpsthe LAB predominate over the other microbial groups from theearly crucial steps of fermentation when the microbial populationis the most complex, thereby ensuring the safety while extendingthe shelf life of the final product.

Miscellaneous� Harissa: A typical Tunisian hot paste, but also available in

the other North African countries, harissa is prepared froma blend of spices, with dried chili as the key ingredient, inwater. Coarsely ground dried chili and other ingredients, in-cluding crushed garlic, paprika, coriander seeds, cumin, finelychopped spearmint leaves, and salt, are mixed with water tomake a heavy red paste (Figure 9f). Traditionally, harissa isused with cooked meats such as kebabs and appears on thetable in small plates as a multipurpose sauce or appetizer, es-pecially in restaurants; it is also used as seasoning for brinedgreen olives.

� Tabil: A variant of harissa prepared in the same way exceptthat cumin and paprika are omitted to make it hotter.



Table 4–Traditional meat food products of North African countries: technology and main physicochemical characteristics.

Main physicochemical characteristicsProduct Technological process ReferencepH aw Moisture (%)

Meat ProductsGueddid See Figure 3 5.2 to 5.3 0.50 to 0.65 7.54 to 14.26 Bennani and others 1995Pastirma See Figure 4 4.5 to 5.8 0.85 to 0.90 39 to 52 Obuz and others 2012Khlii See Figure 5 5.2 0.65 11.78 Bennani 2003Mkila Fresh lamb or goat meat strips salted, marinated, and

cooked in a fry pan (“Makla” in Arabic), and thenconditioned in animal fat, the product is called Mkila afterthe utensil (Mkila, diminutive of Makla) where it is cooked

NA NA NA Chafaı 2012

Express khlii Prepared by using fresh beef strips marinated into sharmula∗for 1 h, cooked and dipped in animal fat for conservation

NA NA NA Chafaı 2012

Merguez Prepared from ground meat (30% to 20% fat) mixed withdifferent spices (salt, black pepper, cumin, hot red pepper,paprika, and ginger), and stuffed into natural casing(ovine or goat small intestine)

5.0 to 5.5 NA 77.5∗ Benkerroum and others2003b; Yin and Cheng2003

Sujuk See Figure 6 4.6 to 5.6 0.86 to 0.92 36.49 Kayaardı and Gok 2003;Hwang and others 2009

Bubanita/boubanita A typical Moroccan specialty prepared from lamb meat cutinto small cubic pieces, seasoned with spices (cinnamon,cumin, ginger, red chili, paprika, coriander, olive oil, andsalt) and stuffed into previously cleaned lamb rumen,which is then tied at its openings with a rope and hung toa roof where it is left to dry and ferment slowly in theshade.

NA NA NA Daoudi and others 2006

Tehal/tehane Bovine spleen stuffed with ground beef that is seasonedwith various spices, including hot chili, and cooked in anoven (Figure 2f).


Kourdass/kurdass A Moroccan meat product made with lamb stomach,intestines, liver, lung, and fat. All the constituents are cutinto pieces, dry-salted and seasoned with black pepperand occasionally cumin. Stomach pieces of about 15×10cm are used to wrap the pieces of liver, lung, and fat intorolls (the rough side of the stomach toward the exterior).Each roll is diametrically rolled up in the intestine to besealed and sun-dried for 7d (Figure 2g).


Ban-shems A Libyan traditional meat product prepared from bovinestomach stuffed with pieces of kidney, liver, and lung. Thestomach and the other offal pieces are sun-driedseparately, and the pieces of kidney, liver, and lung arepacked into the stomach, and then cooked andconditioned in animal fat in a similar manner as for khlii.


Table 5–Production (1000 tons) and apparent per capita consumption(kg/capita/year) of fruits and vegetables in 2005 in North African coun-tries (FAOSTAT 2012). Data of China are given for comparison.

Country Production ConsumptionFruits Vegetables Fruits Vegetables

Algeria 3,535.544 4,535.92 63.72 119.02Egypt 9,581.15 19,516.40 99.87 203.13Libya 386.05 948.35 66.23 203.03Morocco 3,292.41 5,487.02 69.68 136.44Tunisia 1,254.78 2,675.93 87.46 216.14China 122,184.94 473,062.94 64.42 279.89

FruitsTraditional techniques, especially sun-dying, have long been

used in North African countries to preserve some highly perish-able fruits such as figs, grapes, and prickly pears. These fruits areproduced for a few weeks during summer or autumn seasons andshould be consumed as quickly as possible after harvest, as is thecase for figs, which should be consumed the same day. In this pe-riod of the year, the weather conditions are optimal for the dryingoperation; the temperature averages 25 to 30 ◦C and the air isgenerally dry. Such conditions have, indeed, been reported to givethe best-quality sun-dried fruits (Tang and Yang 2004). Upon fullmaturation, fruits are evenly spread over the floor of open space(threshing) or a cottage roof coated with a plastic or straw mat,large foliage such as that of fig, grape, or carob leaves may beused. Recently, a mesh wire has been preferred as a mat for fig

drying due to its convenience (Figure 10a). When spread on thefloor/roof or any kind of surface, the fruits should be spaced about2 cm from each other to allow good aeration and water evapora-tion. In some Moroccan regions, grapes are pretreated by dippingfor a few minutes in a sieved solution consisting of a mixture ofash from incinerated fava bean stems, quicklime, and salt in water.Such treatment is believed to prevent alterations due to fermen-tation, rot, or mold growth during drying or storage (Mazhour1983). Figs are usually dried as a whole fruit, but in some instances,they are cut open and sprinkled with finely ground herbs such asthyme, rosemary, or pennyroyal, before drying. This procedureis especially used when the dry figs are intended for home con-sumption or sale in neighboring rural markets, as they cannot bepreserved for more than 3 mo (Figure 10b). This product is essen-tially known in the Jbala and Tizi-Ouzou regions of Morocco andAlgeria, respectively, where it is called shreeha. While raisins(zabib) obtained from dried grapes are consumed directly orutilized in various culinary preparations (pastries, dishes, appe-tizers, and so on), dried figs are consumed as such, especiallyduring Ramadan (the fasting month for Muslims) with soup.Drying of prickly pears is conducted in a similar manner afterremoving the peel; however, it is a rare practice and is restrictedto only a small number of villages in remote areas in Moroccoand Tunisia (Mazhour 1983). Likewise, the most available raisinsin North African markets are those obtained in modern facto-ries using industrial dryers and chemical additives such as sulfurdioxide.



Figure 7–Consumption trend of (a) vegetables and (b) fruits in NorthAfrican countries and in the world (global average consumption of 200FAO member countries) during the period of 2000 to 2007. Compiledfrom FAOSTAT (2012).

Microbiology of Traditional North African Foodsand Associated Hazards

In North Africa, traditional technologies for food preservationrely almost exclusively on natural hurdles (fermentation, dehydra-tion, high osmotic pressure and/or, heating) to inhibit the growthof undesirable bacteria and provide safe and stable foods. Thecontribution of the resulting products to food security in NorthAfrican countries is undeniably due to their availability at afford-able prices, high nutritive value, and health-promoting proper-ties (Anukam and Reid 2009; Peres and others 2012). However,their hygienic quality is highly variable depending on many fac-tors including the microbiological quality of raw materials andingredients, as well as the sanitary conditions during harvest,manufacture, packaging, and storage. They may thus compromisethe consumer’s health. Indeed, contamination of such foods withpathogens and/or microbial toxins is well documented. Table 6provides examples of bacterial pathogens associated with the maintraditional dairy, mat, and plant products. Moreover, traditionalfoods have been reported to be associated with infectious diseasesand intoxications (Cosivi and others 1998, Belomaria and others2007, Bendahou and others 2008) or with other pathogens of con-cern to food safety (Paramithiotis and others 2012). Yet, only fewtraditional food-related outbreaks have been recorded in NorthAfrican countries due to the poor public awareness and the lack ofmedia reports, especially when the issues of intoxication episodesare not severe or do not require emergency hospitalizations.

Potential microbiological hazards associated with tradi-tional foods of North Africa

Irrespective of the origin of traditional foods (plant or animal),the raw material used for their manufacture is nutritionally richand provides an adequate environment for the growth of variousmicroorganisms including those of health and spoilage signifi-cance. In addition, the raw material generally hosts an abundantand complex microbial flora whose microbial groups would po-tentially grow and compete for nutrients. Therefore, the mainpurpose of traditional technologies is the alteration of ecologicalparameters of the raw material in a way to select for specific benefi-cial groups of microorganisms that will govern the processing stepsand eventually predominate (Steinkraus 2002). The product maythen be considered safe while having the desired and unique nutri-tional and gustatory qualities. On the other hand, some traditionaltechnologies aim to inhibit or inactivate as many of the microor-ganisms as possible initially present in the food to allow the leastmicrobiological changes during storage, thereby extending theshelf life of the food as long as possible. This is usually achieved byheat treatment (scalding or boiling), dehydration, and/or use ofhigh 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 figs, prickly pears, and raisins, are examples of such foods.Nonetheless, survival or adaptation of microbial strains/groups toextreme conditions is well documented (for a review, see Beales2004; Allen and others 2007), and these products may still be atrisk to consumers.

Dairy productsTraditional dairy products of North African countries are gen-

erally obtained from raw milk, with few exceptions where themilk is heated or boiled, which undergoes spontaneous acidifica-tion with LAB (Table 3) before proceeding to other technologicalsteps depending on the desired final product. Therefore, thesedairy technologies rely essentially on the fermentation with LABas a barrier to prevent the growth of pathogenic and spoilagemicroorganisms. LAB bacteria have the generally recognized assafe status (GRAS) due to their long history of safe consumptionby humans, and to the fact that they have rarely been associ-ated with food intoxications or infectious diseases (Hammes andTichaczek 1994). In addition, virtually, all species of LAB havebeen shown to produce a variety of biologically active substances,including organic acids, hydrogen peroxide, carbon dioxide, di-acetyl, reuterins, and bacteriocins, all with antagonistic activitiesagainst microorganisms of health and spoilage significance (Piard1992; Ouwehand 1998). Moreover, proteolytic LAB have beenshown to generate endogenous bioactive peptides with potent an-timicrobial activities upon hydrolysis of milk proteins during fer-mentation (Hayes and others 2006; Benkerroum 2010; Ghalfi andothers 2010). Nonetheless, studies on traditional North Africandairy products have revealed that those among them which relyonly on the lactic acid fermentation and the consequent loweringof the pH (3.8 to 4.5), such as fermented milk products includingzabadi, raib, lben, and fresh cheeses are generally of poor microbi-ological quality, as suggested by the high counts of indicator bac-teria, fecal coliforms, and enterococci, which exceed 104 colonyforming unit (CFU)/mL or g (Hamama 1992), and the occur-rence of serious foodborne pathogens (Table 6). In addition, theseproducts have a short shelf life (3 to 10 d) even when stored at re-frigeration temperature (Samet-Bali and others 2009), suggestingthat they are prone to support the growth of various undesirable



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microorganisms. To circumvent such a limitation and enhance thesafety and keeping quality of North African traditional dairy prod-ucts, other hurdles to microbial growth including salting and/ordrying (low aw) or heating have often been combined with lacticacid fermentation. Examples of such products are the Moroccan-brined cheese jben malah (matured and stored in saturated brine),Egyptian domiati and tallaga cheeses (5% to 10% salt contentand stored in brine), dried kishk, and Algerian aoules obtainedfrom spontaneous acidification of milk followed by heat treatmentand sun-drying. The pH of these products is as low as 3.5 andtheir dry matter increases to levels as high as 90% to 92%, corre-sponding to water activity (aw) values of 0.34 to 0.43 where mi-croorganisms can no longer survive (Steinkraus 1983; FAO 1990;Tamime and McNulty 1999; Mennane and others 2007). Additionof aromatic plants (thyme, oregano, and rosemary) along with high

salt concentration to some traditional dairy products, such as theMoroccan smen, has also been practiced empirically to add a safetyfactor and to avoid surface spoilage with molds, as these plants arewell known for their potent antifungal activities (Cowan 1999;Hammer and others 1999; Chebli and others 2003; Rota and oth-ers 2004; Amarti and others 2008). In spite of these treatments,pathogenic bacteria and molds have been detected in virtually allNorth African traditional dairy products, and some of these bacte-ria would grow and produce highly toxic metabolites under certainconditions. Survival of raw milk pathogens to the processing stepsor 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 mi-croorganisms in finished products. Moreover, the poor sanitaryconditions during milking and the lack of veterinary care for



Figure 9–Selected fermented vegetables of North African countries; (a) pickled green olives; (b) dry-salted fermented black olives; (c) dry-salted“Moroccan style” lemon; (d) North African “lamoun makbouss”; (e)-various pickled garden vegetables in glass containers; (f) Harissa (solid arrow) andolives seasoned with harissa (dashed arrow).

traditional small herders (the prevailing management system ofhusbandry in North Africa), in addition to the low hygienicquality of water, contribute to produce raw milk of poor mi-crobiological quality. Regardless of the type of domestic milkanimal (cow, sheep, goat, buffalo, and camel), the total viablecounts usually exceed 106 CFU/mL and the counts of fecal indi-cators (coliform and enterococci) are higher than 104 CFU/mL(Hamama 1992; Benkerroum and others 2003a; El-Diasty andEl-Kaseh 2007). Moreover, foodborne pathogens of major con-cern in food safety such as Listeria monocytogenes, Mycobacteriumbovis, 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 oth-ers 1998; Benkerroum and others 2004b; Bendahou and others2008). Therefore, the frequent presence of pathogens in fermentedmilks or cheeses obtained from such raw milk is not surprising.When raw milk is heavily contaminated and the technological pro-cesses are carried out under poor sanitary conditions, as is usuallythe case in North African dairy farms, natural hurdles to micro-bial growth are a limited safety factor (Benkerroum and Tamime2004).

Another issue of concern related to North African traditionaldairy products is the presence of enterococci at high levels, usually



Figure 10–Figs being dried on a roof covered with a mesh wire (a) and 3 types of dried figs: (b) cut open dried fig, (c) figs dried as whole, pricked fromthe center and put together in the form of beads with a string, and (d) whole dried figs packaged in bulk.

exceeding 104 CFU/mL, with Enterococcus faecalis and foecium as thepredominating species (Benkerroum and others 1984; Tantaoui-Elaraki and El Marrakchi 1987; Benkerroum and Tamime 2004).The presence of this group of microorganisms in fermented foodsis, in fact, controversial. Although members of Enterococcus genushave been shown to possess highly desirable technological andhealth promoting properties (Bertolami and Farnworth 2003; Be-lamri and Benkerroum 2005; Pollmann and others 2005; Morenoand others 2006; Zeyner and Boldt 2006), their association withfood spoilage (Franz and others 1999), food intoxication (Giraffaand others 1997; Gardini and others 2001), nosocomial infections(Kayser 2003), and spreading of antibiotic resistance through thefood chain (Valenzuela and others 2008) has also been well doc-umented. In a survey on risk factors in enterococcal strains iso-lated from Moroccan dairy products, Valenzuela and others (2008)revealed the widespread multiantibiotic resistance and/or occur-rence of virulence factors (sex pheromones, collagen adhesins, en-terococcal endocarditis antigen, and enterococcal surface proteins)among the isolates of Ent. faecalis and Ent. faecium (Valenzuela andothers 2008). According to these authors, high counts of entero-cocci represent a risk factor in Moroccan foods, and appropriatemeasures 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 Africantraditional dairy products may also represent serious hazards toconsumers, which has so far been disregarded or overlooked. Theoccurrence of the latter microorganisms in North African rawmilk has been repeatedly demonstrated (Carter 2005; Dawson2005; Pollmann and others 2005) and is of paramount importanceto the safety of dairy products, especially when no heat treatmentis applied during processing or at point of consumption. In viewof the high incidence of zoonotic diseases in North African herds(Araba and Essalhi 2007; Berrag and others 2009; Bouzid andothers 2010) especially with the lack of veterinary care in smallfarms and the poor hygienic quality of water (the probable vehicle

for various viruses, protozoa, and parasites), this issue warrants dueattention from all stakeholders and scientists.

The presence of mycotoxins in traditional North African dairyproducts also raises an increasingly alarming concern regardingpublic health safety. It is well established that mycotoxins maycontaminate dairy products by molds growing on them under cer-tain conditions, or by the carryover of mycotoxins occurring inanimal feedstuffs ingested by dairy animals and later transferredfrom blood into milk (van Egmond 1983; Veldman and oth-ers 1992; Galvano and others 1996; Zinedine and others 2006;Masoero and others 2007). The most important of such myco-toxins to dairy products is aflatoxin M1 (AM1) derived from theconversion of ingested aflatoxin G1 in the animal liver (Tantaoui-Elaraki and Khabbazi 1984). AM1 was detected at concentrationsranging between 4.0 and 6.0 µg/L in 12.5% of Libyan raw milk(El-Diasty and El-Kaseh 2007). In a study on the occurrence ofAM1 in raw milk marketed in different cities of Libya, Elgerbiand others (2004) showed that 35 samples of raw bovine milk outof a total of 49 (71.7%) tested positive for AM1, with averageconcentrations varying between 0.12 and 0.72 µg/L dependingon the city from which the samples were taken; 34 among the35 positive samples (about 97%) were contaminated with levelsexceeding the maximum tolerable level (MLT) of 0.05 µg/L (El-gerbi and others 2004). Higher concentrations (average of 6.3µg/L) were reported in Egyptian raw bovine milk (El-Sayed andothers 2000). Such levels of contamination with AM1 are alarm-ing in view of the MLT which should be less than 0.05 µg/kg orL, depending on the country and commodity (Dohlman 2003). InMoroccan pasteurized milk, AM1 was detected at high frequencies(88.8%), but at relatively low concentrations compared to thosefound in Libyan and Egyptian milks; the concentrations reportedranged between 0.001 and 0.117, with an average of 0.018 µg/L,and 7.4% of the samples contained higher levels than the MTL(Zinedine and others 2007a; Zinedine and Manes 2009). Accord-ing to Tantaoui-Elaraki and Khabbazi (1984), AM1 concentration



Table 6–Hazards of microbiological (pathogens and/or their toxins) associated with North African traditional food products.

Commodity Associated pathogens Reference

Dairy productsLben Staph. aureus, Salmonella spp. Hamama 1992; El Marrakchi and others 1993; Benkerroum and others 2004b

Pathotypes of E. coliSmen Staph. aureus, Cl. perfringens, Cl. Tantaoui-Elaraki and El Marrakchi 1987; EL Marrakchi and others 1988;

Benkerroum and Tamime 2004BotulinumBacillus cereus

Jben E. coli O157, L. monocytogenes, Staph. aureus, Y.enterocolitica

Hamama 1992; Hamama and others 1992; El Marrakchi and Hamama 1995;Hamama and others 2002; Benkerroum and others 2004a; Achemchem andothers 2006

Raib E. coli O157, L. monocytogenes, Coagulase positiveStaph. aureus, Salmonella spp.

Hamama and others 1992; Elotmani and others 2002

Zabadi E. coli O157 H7 Quinto and others 2000Domiati cheese Campylobacter spp., L. monocytogenes, Cl.

perfringens, Staph. aureus, Vibrio spp.Nour and others 1987; Abd-El Salam and Benkerroum 2006; Sadek and others

2006; El-Baradei and others 2007Tallaga cheese B. cereus Abd-El Salam and Benkerroum 2006; Sadek and others 2006Mish cheese Clostridium spp. Taha and Abdel-Samie 1961Kishk B. cereus, Cl. botulinum, Cl. perfringens Tamime and McNulty 1999Meat productsGueddid Staph. aureus, Cl. botulinum Bennani and others 1995Pastirma Cl. botulinum, Cl. perfringens, Staph. aureus, E. coli

O157:H7El-Khateib 1997; El-Safey and Abdu El-Raouf 2003; Obuz and others 2012

Khlii Cl. botulinum, Bacillus spp. Bennani 2003Mkila NA NAExpress khlii NA NAMerguez (fresh

sausages)Cl. botulinum, perfringens, Staph. aureus,

Campylobacter spp., L. monocytogenes, variouspathotypes of E. coli, Salmonella

Ettriqui and others 1995; El-Khateib 1997; Bendeddouch and Lebres 2003;Benkerroum and others 2003b; El-Safey and Abdu El-Raouf 2003; Yin andCheng 2003; Benkerroum and others 2004b; Al-Gallas and others 2006;

Manhattan, Salmonella spp., Staph. aureus Noel and others 2007; Cohen and others 2008; Badri and others 2009Sujuk Cl. botulinum, E. coli O157:H7, S. Typhimurium, L.

monocytogenesKayaardı and Gok 2003; Hwang and others 2009

Gueddid Staph. aureus, Cl. botulinum (Bennani and others 1995)Pastirma Cl. botulinum, Cl. perfringens, coagulase-positive

Staph. aureus, E. coli O157:H7El-Khateib 1997; El-Safey and Abdu El-Raouf 2003; Obuz and others 2012

Khlii Bacillus spp. Bennani 2003Mkila NA NAExpress khlii NA NAMerguez (fresh

sausages)Cl. Botulinum, perfringens, Campylobacter spp., L.

monocytogenes, various pathotypes of E. coli,Salmonella

Ettriqui and others 1995; El-Khateib 1997; Bendeddouch and Lebres 2003;Benkerroum and others 2003b; El-Safey and Abdu El-Raouf 2003; Yin andCheng 2003; Benkerroum and others 2004b; Al-Gallas and others 2006;

Manhattan, Salmonella spp., Staph. aureus Noel and others 2007; Cohen and others 2008; Badri and others 2009Sujuk Cl. botulinum, E. coli O157:H7, S. Typhimurium, L.

monocytogenesKayaardı and Gok 2003; Hwang and others 2009

Plant productsPickled green olives Cl. botulinum, Cl. perfringens, L. monocytogenes,

Bacillus cereusCaggia and others 2004; Panagou and others 2008; Pereira and others 2008

Black olives Cl. botulinum Anon 2012Pickled vegetables Pseudomonas enteridis, L. monocytogenes∗ 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 fromcontaminated milk, as neither heat treatment nor the subsequentsteps in cheese making (curd drainage, handling, and maturation)removed much of the toxin initially present in the milk. It couldbe anticipated, on this basis, that levels of AM1 in cheeses obtainedfrom contaminated milk would exceed the MTL even when theinitial level of AM1 in raw milk is below this value. However, asurvey on the occurrence of AM1, aflatoxin B1 (AB1), and afla-toxin G1 (AG1) in Egyptian dairy products revealed that AM1was detected in raw milk more frequently and in more elevatedamounts than in different cheese varieties or in dried milk; AM1concentrations of 6.3, 5.0, 6.0, and 0.5 µg/L or kg were detectedin raw milk, dried milk, hard cheese, and soft cheese, respectively,whereas AB1 and AG1 were detected in hard cheese at concentra-tions of 3 and 6 µg/kg, respectively (El-Sayed and others 2000).Similarly, the average concentrations of AM1 in Libyan white softcheeses (from 0.21 to 0.34 µg/kg) were lower than those de-termined in raw milk; yet, 15 cheese samples out of 20 (75%)tested positive for AM1 and contained concentrations exceedingthe MTL (Elgerbi and others 2004). It could be argued, however,

that there is no correlation between the levels of mycotoxins inthe cheeses samples analyzed in the latter studies and those deter-mined in the raw milk, as all the samples were taken at randomfrom local markets. In a more relevant study, Hassanin (2006) hasmonitored the level of AM1 in yogurt, yogurt-cheese, and acidi-fied milk produced from a naturally contaminated milk with AM1.The results revealed that the concentration of AM1 significantlydecreases as a function of time during storage at refrigeration tem-perature, which was explained by the interference of LAB withmycotoxin activity. Many studies have shown that LAB are able tosequester, or inhibit, the in situ production or toxicity of mycotox-ins, thereby reducing their potential risk in fermented milks andcheeses (Gourama and Bullerman 1995; Kim 2007; Bianchini andBullerman 2009). Dairy lactic acid bacteria belonging to differ-ent genera have been reported to be effective in removing AB1and AM1 (El-Nezami and others 1998; Oatley and others 2000;Pierides and others 2000). Nonetheless, further studies are neededto accurately estimate the concentrations of mycotoxins and mon-itor their fate during processing and/or storage in different tra-ditional North African dairy products obtained from the milk of



Table 7–Average microbial counts (log CFU/g) in different meat and offalsamples in 2 major Moroccan cities.

Casablanca∗Fez∗∗

Microorganisms Beef Lamb Heart Liver Ground beefTAC 7.3 6.7 6.4 7.5 6.1Coliforms 3.7 3.7 3.3 3.8 4.8E. coli 3.2 3.2 1.8 3.4 3.9Staph. aureus 2.3 2.8 3.1 2.0 2.3Cl. perfringens 1.3 1.2 1.2 1.8 NASRC NA NA NA NA 1.5∗(Cohen and others 2006).∗∗(Oumokhtar and others 2008).TAC: Total aerobic counts.NA: Not available.SRC: Sulfite-reducing clostridia.

different animal species. Such studies are crucial to characterizethe risk and estimate the dose/response in a risk-assessment pro-cess, the cornerstone in any future regulatory or control measurerelated to food safety worldwide.

Meat productsThe overall safety of meat products is contingent on many factors

including the initial quality of meat and ingredients, the sanitaryconditions during handling, processing, and storage, as well as thepreservation hurdles used. Raw and offal meat used to produceNorth African traditional meat products is generally heavily con-taminated with microorganisms of hygienic significance. In thisregard, a study conducted by Cohen and others (2006) on beef,lamb, and beef-offal marketed in the city of Casablanca (Mo-rocco) has shown that these products were highly contaminated;and pathogenic staphylococci and Cl. perfringens were detected atrelatively high counts (Table 7). A similar study on ground beefmarketed in the city of Fez (Morocco), carried out by Oumokhtarand others (2008) also demonstrated the poor sanitary quality ofthe product (Tables 7), with more than 80% of the analyzed samplesnot meeting the Moroccan regulatory standards for meat products(http://www.onssa.gov.ma/onssa/fr/vv_dec15.php). In the latterstudy, Salmonella sp. and Shigella were detected in a 25 g sampleat 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 isolatedfrom meat samples in Morocco and other North African coun-tries (Karib and others 1994; Ettriqui and others 1995; Abdul-Raouf and others 1996; Al-Gallas and others 2002; Khosrof BenJaafar and others 2002; Benkerroum and others 2004b). Oc-currence of parasites (protozoa and helminthes) of the generaToxoplasma, Sarcocystis, Cryptosporidium, Fasciola, Flatworms, Tape-worm, and roudwarms in meat and offal is also well documented(Sawadogo and others 2005; Valinezhad and others 2008; Abdel-Ghaffar and others 2009; Berrag and others 2009). Given the poorhygienic quality of raw meat, traditional technologies in develop-ing countries use more than one hurdle, acting in synergy, toensure a relatively satisfactory degree of hygienic quality. Indeed,almost all the traditional technologies for meat transformation inNorth African countries combine salting, herb and spice addition,drying, and, occasionally, cooking, especially when long shelf lifeand a high degree of safety are sought. Less stringent conditionsare used when a product is not intended for an extended preser-vation period and is cooked before consumption, as is the case formerguez and tehal. In cured and fermented meat products, suchas sujuk, gueddid, kourdass, and pastirma, salting, drying, andherb and spice adjunction are the main parameters used to en-sure their safety and stability. While salting and/or drying reduce

the water activity to levels below 0.86 where no pathogenic bac-teria would grow (Jay 1986; Barbosa-Canovas and others 2003),spices inhibit specific microorganisms including bacteria, molds,protozoa, and viruses (Farag and others 1989; El-Khateib 1997;Cowan 1999; Daferera and others 2000). In addition, a decreasein the pH to about 5.5 at the first phase of maturation, while notefficient by itself to inhibit many pathogens, stimulates the gro-wth of LAB, which, in turn, will further inhibit undesirable mi-croorganisms through antibiosis interactions. In this regard, thewide occurrence of bacteriocin-producing enterococci has beenreported in Tunisian gueddid (Ben Belgacem and others 2008),and the protective effect of bacteriocins in meat systems has beendemonstrated (Benkerroum and others 2003b, 2005). In additionto these conditions, some traditional North African meat products,such as the Moroccan khlii and Libyan ban-shems, the cookingduring processing inactivates microbial pathogens or toxins thatmay be present on the meat or offal used for their preparation.

Although there is a lack of scientific data regarding the hygienicquality of North African traditional meat products and epidemi-ological studies on their involvement in food outbreaks, it couldbe anticipated that they may compromise food safety as suggestedby the widespread occurrence of pathogens in North African tra-ditional meat products (Table 6), and also for the main reasonsbelow:

� Lack or inappropriate veterinary care in the farms wheremeat-production animals are raised; a weak prophylactic pro-gram and inadequate treatment of diagnosed bacterial infec-tions or parasitic infestations (Berrag and others 2009).

� Slaughtering, carcass dressing, evisceration, and meat cuttingare generally done in poor sanitary conditions which, com-bined with the nonrigorous or absent (farm-slaughtering)veterinary inspection at slaughter, strongly suggest that meator offal deriving from animals infected with virulent bacteria,viruses, or parasites would be used to manufacture traditionalmeat products.

� Production of traditional meat products in small farms,butcheries, or food shops where the sanitary conditions areusually not appropriate, and none of the GMP, good hygienepractice (GHP), or hazard analysis and critical control point(HACCP) program is implemented.

� Inadequate conditioning, packaging, and storage conditions.Yet, efforts in packaging are being increasingly made as partof a marketing approach.

In fact, it is well established that these are the main factors thatimpact the safety and keeping quality of the finished meat prod-ucts, and failure to address any of them properly will invariablyresult in a meat product of high risk to consumers. Nonetheless,on the basis of moisture content, North African traditional meatproducts may be divided into 3 groups as defined by Marshalland Bal’a (1998) and Leistner (2000b), each of which present adifferent pattern of health risks to consumers from the microbio-logical standpoint: (i) dry meat products (less than 15% moisture)such as gueddid, kurdass, khlii, and ban-shems, (ii) intermediate-moisture meat products (15% to 20% moisture or an aw of 0.65 to0.90) typically represented by pastirma and certain types of sujuk(Table 4), and (iii) fresh meat products (>20% moisture) includingmerguez, mkila, tehal, and some types of sujuk where no or par-tial drying is applied during processing. Due to their low moistureand/or high salt contents, the first 2 groups are generally regardedas microbiologically safe, and they may be consumed as such orafter being lightly cooked; these include khlii, some sujuk types,and pastirma. Such an assumption has been substantiated by some



studies, showing that the overall microbiological counts are eitherlow or dominated by beneficial LAB and that some foodbornepathogens do not grow or survive in these products (El-Khateib1997; Bennani and others 2000; Huang and Nip 2001; Kalalouand others 2003). El-Khateib (1997) showed that the numbers ofEnterobacteriaceae, and yeasts and molds were less than 100 CFU/gin 50 samples of Egyptian pastirma, which were also free fromSalmonella. The absence of Salmonella was explained by the in-hibitory effect of the spice paste used to cover pastirma, as hasbeen demonstrated in vitro (El-Khateib 1997). The same studyshowed that the total aerobic count (TAC) and the Lactobacillaceaeranged between 1×104 and 9×106 CFU/g, suggesting that LABare the main responsible for the evolution of the product duringripening, which represents a good indication regarding the safetyof the product. In addition to the antimicrobial effect of the coverpaste, inhibition of pathogenic bacteria in pastirma was suggestedto be due to the combined effect of water loss and salt con-tent (4.5% to 6%) with the consequent decrease in water activity(Leistner 2000a; Bechtel 2001). In effect, challenge studies be-tween an E. coli O157 : H7 strain and protective cultures of Lb.sakei and Staph. xylosus in pastirma have demonstrated that themost significant reduction in the counts of the pathogen wasrecorded after the drying step regardless of whether or not theprotective cultures were present (Aksu and others 2008). Similarresults were reported for Moroccan gueddid where numbers ofTAC, coliforms, and staphylococci showed a dramatic decreaseafter the maturation step to reach an undetectable level in a 1g sample for coliforms and staphylococci, and about 40 CFU/gfor TAC (Kalalou and others 2003). According to their study,the sharp decrease in the microbial counts paralleled the decreasein water activity (aw) to a final value of 0.66. Furthermore, nei-ther Salmonella nor clostridia were detected in laboratory-madeor commercial gueddid samples (Bennani and others 1995; Ben-nani and others 2000). However, despite such reassuring data,though partial and fragmentary, there is no absolute guarantee forthe safety of these products. Indeed, the related salted-dried jerkymeat prepared in a similar manner and having a water activityvalue as low as 0.3 has repeatedly been associated with a num-ber of Salmonella and Staph. aureus outbreaks in the U.S.A. (CDC1995; Eidson and others 2000; Smelser 2004; Allen and others2007). Nonetheless, it could be assumed that the marinated vari-ant of gueddid would be microbiologically safer than the classicaltype. The application of acid marinade to meat before drying hasbeen shown to enhance significantly the microbiological quality ofthe final product (Nummer and others 2004). On the other hand,North African traditional fresh meat products are usually heavilycontaminated with microorganisms of health and spoilage signifi-cance; they thus present a higher risk to consumers than their dryor intermediate-moisture counterparts. However, such risk maybe reduced at consumption, as these products are cooked or grilledbefore consumption. In this regard, a study on the microbiologyof different Egyptian fresh sausages showed that the aerobic platecount (APC) and Enterobacteriaceae counts ranged from 1.1×104 to1×108 and from 1×102 to 1×107 CFU/g, respectively, and Cl.perfringens and coagulase-positive Staph. aureus were detected at therespective frequencies of 26% and 29% (El-Khateib 1997). More-over, in a study on the incidence of shiga toxin-producing E. coliO157 in Moroccan meat products, the pathogen was detected in20% of the spiced ground meat normally used in merguez prepa-ration, but not in merguez sausages; such a discrepancy could beexplained by the sampling procedure and the limited number ofsamples studied (Benkerroum and others 2004b).

Mycotoxins are contaminants of microbial origin, which alsoraise concern about the safety of meat products. The presenceof molds in meat and meat products is well documented, andunder certain conditions, they may grow and produce mycotox-ins (Sweeney and Dobson 1998). Molds usually grow on dry orintermediate-moisture meat products during the first days of dry-ing, especially if the drying process is slow or the relative humidityin the atmosphere is high. They may also grow in the finishedproduct if the storage conditions are not adequate. However, thisgrowth is usually considered by the producers only as a harmlesssurface discoloration and is then removed by brushing the sausagesor cleaning them with a wet cloth to avoid wasting meat. Yet, suchgrowth may represent a serious risk factor if the contaminatingmolds are toxinogenic. A study on the mycology of pastirma hasrevealed the predominance of species belonging to Penicillium andAspergillus genera (Abdel-Rahman and others 1984). These generaare well known for their ability to produce mycotoxins (Sweeneyand Dobson 1998). A study on Egyptian pastirma showed that thenumbers of molds varied from 103 to 106 CFU/g in summer andfrom 102 to 105 CFU/g in winter, and that Aspergillus, Penicillium,Mucor, Rhizopus, Fusarium, and Cladosporium were the predominat-ing genera in the product (Refai and others 2004). In addition, thespices used in the preparation of North African traditional meatproducts are usually contaminated with variable levels of mycotox-ins and are thus potential sources for the contamination of theseproducts. Aflatoxins were determined in the pastirma spice pasteand its constitutive spices individually; the contamination levelof the spice paste varied from 9.6 to 120 µg/kg, and in pepper(285.6 µg/kg), garlic (224.4 µg/kg), fenugreek (194.2 µg/kg),coriander (166.4 µg/kg), and capsicum (42.4 µg/kg) (Refai andothers 2004). These concentrations largely exceed the maximumtolerable limit of aflatoxin B1 in spices (5.0 µg/kg) according tothe European regulations (Zinedine and Manes 2009). Therefore,it might be anticipated that pastirma and related North Africantraditional meat products represent a serious health risk factor as-sociated with the consumption of these products. Pastirma was,indeed, reported to contain aflatoxins at levels varying from 2.8 to47 µg/kg (Refai and others 2004).

Vegetable productsFruits and vegetables are contaminated by a wide variety of

microorganisms including bacteria, fungi, viruses, and protozoaof different origins. These contaminations may occur in thefield (soil, manure, compost, wastewater sludge, irrigation wa-ter, equipment, workers, animals, and so on), during posthar-vest operations (conditioning, packaging, and distribution), orat the household prior to consumption (Burnett and Beuchat2001; Matthews 2006). Therefore, microorganisms initially presentin fruits and vegetables are highly variable in numbers and innature, and are generally predominated by saprophytic bacte-ria and molds, considered as the resident microflora, that donot raise serious health concerns (Jay 1986; Badosa and others2000). Nonetheless, fruits and vegetables have extensively beenshown 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; Bhagwat2006; Matthews 2006), which is regarded as a risk factor forpublic health. Indeed, the increase in consumption of fruit andvegetable that has been recorded worldwide in the last 2 decadeshas been paralleled by an increase in foodborne disease outbreaksattributed 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 withgastroenteritis 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 Jones2008). On the other hand, some microbial groups among the resi-dent microflora play a key role in the transformation of vegetablesinto more stable, safe, and palatable products when fresh produceis preserved for consumption out of season. Among the bene-ficial of these epiphytic microorganisms in fruits and vegetables,LAB, and to a lesser extent yeasts, are responsible for sponta-neous fermentation of a number of vegetable products such asolives and various vegetables. Natural fermentation has long beenused on an empirical basis in the preservation of vegetable prod-ucts, and in particular, in the case of olives, it is even necessaryto make the fruit edible. In fact, natural olive fermentation ful-fills 2 main objectives: (i) inhibition of microorganisms of healthand spoilage significance, thereby reducing health risks and prod-uct losses, and (ii) making olives palatable, essentially by removal ofthe bitter glycoside euloropein, production of various aroma com-pounds, and softening, to some degree, the flesh of the fruit duringfermentation.

As mentioned earlier, vegetable products are traditionally pre-served in the North African region by lactic acid fermentationcombined with salting (dry salt or brine), direct acidification (ad-dition of vinegar) or, in few instances, by sun-drying. Conversely,fruits such as grapes, figs, and prickly pears are essentially dried,as the loss of moisture combined with the consequent increase insugar concentration in the fruit results in a sharp decrease in wateractivity, thereby restricting the growth of spoilage and pathogenicmicroorganisms. The high diversity of North African traditionalvegetable products and the raw material from which they derive,in addition to the variability in the technological processes and thesanitary conditions used for their manufacture, make the micro-biological characteristics of the finished products and related riskfactors also variable. Nonetheless, the fruits and vegetables eatenraw or after being transformed by traditional technologies are re-garded as safe and wholesome for most North African consumers.Yet, this presumed safety has not been substantiated by microbio-logical and epidemiological studies, a situation that reflects the lackof awareness of the health risks associated with the consumptionof vegetable products in these countries. Furthermore, because ofthe lack of foodborne disease investigations and surveillance, mostdisease outbreaks related to the consumption of vegetable prod-ucts remain undetected and insufficiently reported in the scientificliterature. Also, the level of contamination and the incidence ofpathogenic microorganisms of/in fruits and vegetables are antici-pated to be higher in North African countries than in developedcountries. The lack of implementation of quality assurance pro-grams including GAP, GMP, and HACCP throughout the entireproduction and distribution chain (pre- and postharvest, trans-portation, handling, and so on) increases the health risk associatedwith the consumption of such products. The risk is even greateras untreated urban wastewater and sewage sludge or manure con-tinue to be used for irrigation or fertilization (Bazza 2003; Ghazyand 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 untreatedurban wastewater are used annually to irrigate some 7000 ha offruit orchards and vegetables as an alternative fresh water source,and as an easy and economical way for disposing wastewater (Bazza2003; Choukr-Allah 2004). Similarly, the capacity of wastewater-treatment facilities in Egypt is either short or produces insuffi-

ciently treated wastewater (Ghazy and others 2009); therefore,large amounts of wastewater and sewage sludge are used to irrigateand fertilize fruit orchards and vegetables in the country. The useof raw wastewater in agricultural activities has been demonstratedto increase the potential of the resulting crops to spread bacterialor parasitic diseases (Ait Melloul and Hassani 1999; Ait Mellouland others 2002). A bacteriological analysis of various vegetablesobtained from several wastewater-irrigated agricultural regions inMorocco showed high counts of TAC (>9 log10 CFU/g) and fecalindicators (total-coliforms, fecal-coliforms, and enterococci)(>5log10 CFU/g), suggesting that the consumption of these vegeta-bles put consumers at high risk (Ibenyassine and others 2007). Thesame study showed that opportunistic Gram-negative pathogens ofthe Enterobacteriaceae family (Citrobacter freundii, Enterobacter cloacae,E. coli, Klebsiella pneumoniae, and Serratia liquefaciens) were detectedin the studied vegetables at frequencies varying from 11% to 28%,with Enterobacter sakazakii (12%) and Salmonella arizona (0.7%) be-ing the pathogens of the most concern to the safety of these crops.Moreover, in a Moroccan region (Al Haouzia, Marrakech) whereuntreated wastewater spreading is widely practiced for the produc-tion 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 pro-duced crops has been shown to be significantly higher than thatrecorded in a control region where no wastewater spreading ispracticed (1.14%). Another study carried out in the same regionrevealed that the prevalence of protozoan infections (giardiasis andamebiasis) among children of the wastewater-irrigated region wassignificantly higher (72%) than that recorded in the control area(45%) (Ait Melloul and others 2002).

Traditional food products of plant origin in North Africancountries are generally obtained from locally produced crops withinconsistent sanitary quality. Therefore, the safety of finished prod-ucts is largely dependent on the efficacy of natural hurdles to in-hibit or inactivate undesirable microorganisms initially present inthe raw material. Olives are the most important vegetable prod-ucts that are transformed by traditional technologies in NorthAfrican countries; they are either brined (green olives) or dry-salted (black ripe olives). In both cases, they undergo spontaneouslactic acid fermentation, although in the latter case, the fermen-tation is greatly retarded by the high salt concentrations used fortheir preservation (8 to 14 g salt per 100 g olives). Other vegetablessuch as peppers, onions, carrots, string beans, chili, and cauliflowerare either brined in a similar manner as for green olives (Steinkraus1983) or salted and “packed” into an acid solution (usually vine-gar) of a pH value below 3.0 as unfermented (fresh-pack) pickles.In the fresh-pack pickles, the raw material is usually heated orsoaked in hot water for few minutes to reduce the overall mi-crobial load of the product before pickling. Therefore, it wouldbe reasonable to expect that these unfermented pickles do notraise serious health concerns essentially due to the low pH of thebrine in addition to the heat treatment where microbial growthis very unlikely to occur (Gomez and others 2006). They wouldtherefore be categorized as low-risk vegetable foods. Conversely,in fermented vegetable products, faulty fermentation is not un-common and pathogenic microorganisms may grow or survivein the finished products (Fleming and others 1985; Caggia andothers 2004). In fermented pickled vegetable products, microbialcompetition, acidity, and reduced water activity (high salt content)are the main parameters that inhibit undesirable microorganismsto safeguard the health of consumers. However, the usual salt con-centration used in the brine (5 to 7 g salt/100 mL) is not high



Table 8–Monitoring the counts (logCFU/g) of microbial groups in Algeriangreen olives during fermentation. After Kacem and Karam (2006a).

Fermentationperiod (days)

Microbial group 15 60 90

Total aerobic count 4.52 7.76 6.88Coliforms 2.12 2.33 1.96Staphylococci 2.03 2.52 1.35Lactic acid bacteria 3.8 6.55 6.96Lactobacilli 3.6 5.55 5.66Yeasts 1.88 3.84 5.98Psychrotrophs 4.22 3.88 1.53

enough to reduce the water activity to levels that would stronglyinhibit the growth of undesirable microorganisms. In addition,when more than 8% (w/v) of salt is used in the brine, the growthof LAB is also retarded significantly and the pH remains relativelyhigh at the end of fermentation (about 4.5) (Fernandez and others1997), conditions that provide an opportunity for salt-tolerant orhalophilic pathogens and spoilage microorganisms to grow duringthe early stages of fermentation. Staphylococci grow well at saltconcentrations between 7% and 10% and a low pH of 4.2, andother pathogens such as E. coli O157 : H7, L. monocytogenes, andSalmonella spp. have been shown to develop resistance under stress-ful conditions, including low pH (Gahan and others 1996; Lou andYousef 1997; Beales 2004; Lee 2004). Therefore, in the fermen-tation of green olives, the usual salt concentration used does notexceed 7 g salt/100 mL brine to allow good growth of fermenta-tive LAB. These bacteria, which represent only a small proportionof the initial epiphytic microflora of the product, should rapidlyoutgrow the competing microbial groups and produce sufficientacidity to reach a pH of about 3.5 to 3.8, and then the resultingproduct may be considered reasonably safe.

LAB have been shown to predominate throughout the entirefermentation period (90 d) in naturally fermented Algerian greenolives, although yeasts were consistently present at relatively highcounts (3 to 6 log10 CFU/g of olives) as a secondary microflora(Kacem and Karam 2006b). These authors have shown that thecounts of LAB increased steadily since early phases of fermentationto reach about 7 log10 CFU/mL after 90 d of fermentation. A sig-nificant increase in yeast counts has also been noted, starting fromday 60 of fermentation, in a typical behavior of a secondary fer-mentation flora (Fleming and others 1985). Meanwhile, the countsof coliforms, staphylococci, and psychroptrophs were reduced todifferent extents (Table 8). Such a decline may be attributed notonly to the effect of pH and salt content of the Algerian fermentedgreen olives (Kacem and Karam 2006a), but also to inhibitorysubstances inherently present in olives or to specific metabolitesproduced by the predominating species of LAB and yeasts during

fermentation. Euloropein has been shown to inhibit, to differentextents, various pathogens including Salmonella typhi, SalmonellaEnteritidis, Vibrio parahaemolyticus, Staph. aureus, and Vibrio cholerae(Tassou and Nychas 1994; Tassou and Nychas 1995; Bisignano andothers 1999). Among LAB isolated from fermented green olivesin North African countries (Table 9) and elsewhere (Fleming andothers 1985), Lb. plantarum has been consistently reported to bethe predominating species throughout the fermentation period(Kacem and others 2004; Chamkha and others 2008); and strainsof this species have extensively been shown to produce bacteriocinsactive against Gram-positive and Gram-negative bacteria (Kacemand others 2004, 2005; Dobson and others 2012). Likewise, yeastshave been reported to be consistently present at elevated counts(> 6 log10 CFU/g) in North African fermented olives (Asehraouand others 2000; Asehraou and others 2002; Kacem and Karam2006a; Hernandez and others 2007), and to contribute to theirsafety. It is indeed well established that yeasts produce aromacompounds including organic acids, diacetyl, ethanol, and othermetabolites resulting from lipolytic activities that also possess an-timicrobial activities, thereby contributing to flavor developmentas well as to the safety improvement of foods (Hernandez and oth-ers 2007; Arroyo-Lopez and others 2008). Furthermore, amongthe major yeast species isolated from fermented olives (Table 9),the so-called killer yeasts tend to predominate owing to theirability to produce a “killer toxin” essentially active against othercompeting yeasts (Llorente and others 1997; Asehraou and others2000; Hernandez and others 2007; Maqueda and others 2012),but could also inhibit various pathogenic Gram-positive bacteria(Izgu and Altinbay 1997). Therefore, killer yeasts would not onlyreduce the incidence of bloater defect (Asehraou and others 2002),but also contribute to the enhancement of the safety of finishedproducts. Nonetheless, the safety of naturally fermented olives maynot rely only on the above-mentioned safety factors, as the degreeof protection they offer vary widely depending on the fermenta-tion parameters and from a batch to batch (Asehraou and others2000; Kacem and Karam 2006b). In effect, foodborne pathogensof concern to food safety have been isolated or shown to survivefrom/on Spanish-style green olives or Greek-style black olives(Table 6), and cases of botulism and other food poisoning diseasedue to consumption of fermented green or black olives have beenreported (Okudaira and others 1962; Pereira and others 2008; Pin-geon and others 2011; Anon 2012). The competitiveness of thepredominating LAB and yeasts as determined by their ability toproduce inhibitory metabolites or competition for nutrients, andthe initial bacteriological quality of olives and brine, in addition tothe sanitary conditions during manufacture, are the main parame-ters that determine the safety status of traditional fermented olives.Presently, olives are heat-treated before or after preservation and

Table 9–Predominating species of LAB and yeasts in North African naturally fermented green olives. Data are adapted from the references to presentmicrobial species representing more than 70% of the total identified isolates.

Microbial groupCountry of origin LAB Yeasts Reference

Algeria Lb. casei Sac. cerevisiae Kacem and Karam 2006aLb. paracasei Candida parapsilosisLb. plantarumEnt. faeciumLc. lactis NA Kacem and others 2004Lb. plantarum

Morocco NA Sac. cerevisiae, Pichia anomala Asehraou and others 2000Tunisia Lb. plantarum Pichia membranaefaciens Chamkha and others 2008

Lb. collinoides

NA = Not available.



Table 10–Incidence of mycotoxins (µg/kg) in selected vegetable products in some North African countries.

Commodity Mycotoxin Frequency (%) Range (Average) Origin Reference

Table olives OTA 36 0.62 to 4.8 (1.43) Morocco Zinedine and others 2004OTA 100 up to 1.02 Morocco El Adlouni and others 2006AFB 100 up to > 0.5 MoroccoCIT 80 0.45 to 0.52 (0.5) MoroccoOTA – 46830∗ Tunisia Maaroufi and others 1995a

Figs AFB1 5∗ 0.28 Morocco Juan and others 2008AFG1 30 0.28 to 32.9 (8.70) MoroccoOTA 65 0.03 to 1.42 (0.33) Morocco Zinedine and others 2007bOTA 100 60 to 120 Egypt Zohri and Khayria 2007

Raisins AFB1 20 3.2 to 13.9 (10.7) Morocco Juan and others 2008OTA 1 250∗ Egypt Youssef and others 2000OTA 35 0.05 to 4.95 (0.96) Morocco Zinedine and others 2007bAFB1 2 300 Egypt Youssef and others 2000AFT, CIT, OT, PAT, STG,

DAX, T-2 toxin, ZEA0 ND Egypt Zohri and Khayria 2007

∗One sample analyzed; LOD: Limit of detection; ND: Not detected; AFT: Total aflatoxins; AFB: Aflatoxin 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, andbenzoates and parabens are added to pickled or dry-salted olivesin North African countries in order to enhance their safety andkeeping quality. In the market place, the latter products are knownas “romy,” litrally meaning “coming from Rome” but commonlyused to refer to modern and sophisticated products, as opposedto “baladi/beldi” products (products of the country, in Arabic).It is worth mentioning, in this regard, that the “baladi” prod-ucts are the most preferred by consumers though less attractivein appearance and their hygienic quality is questionable as com-pared to the “romy” ones. Further studies should be carried outon the hygienic quality of different commercial and home-madefermented green olives samples, and from different geographicallocations of North African countries, in order to provide a soundconclusion regarding sanitary quality of naturally fermented olivesand to allow an accurate assessment of the health risk associatedwith their consumption. Particular attention should be given tothe occurrence of Cl. botuminum and its toxin, since this is consid-ered as one of the most important safety issues in fermented olivesworldwide, although the occurrence of Cl. botulinum in fermentedolives appears to be rare, and only very few outbreak intoxicationsdue to botulism of type B have been recorded (Pereira and others2008; Anon 2012). In addition, the botulism toxin formation isunlikely at pH and aw < 4.8 and 0.94, respectively (Odlaug andPflug 1979; Briozzo and others 1986); values of these parametersare generally lower in naturally fermented olives.

In addition to the bacteriological hazards discussed above, my-cotoxins represent a major issue regarding the safety of traditionalvegetable products in North Africa. Among these products, tableolives and dry fruits such as figs and raisins have repeatedly beenreported to be contaminated with various mycotoxins (Table 10).The high salt contents (5 to 12 g salt/100 g product) in tableolives select for the halophilic or salt-tolerant molds especially,those of the genera Penicillium and Aspergillus. Similarly, raisins anddried figs have been shown to be frequently contaminated withmycotoxin-producing strains of A. flavus and A. niger due to theosmophilic character of these species (Rao and Kalyanasundaram1983; Pitt and others 2009; Selouane and others 2009).

Contamination of table olives with various mycotoxins is welldocumented, and Greek-style black olives are the most incrimi-nated (Maaroufi and others 1995a; El Adlouni and others 2006).The high salt content (about 7% to 12% g salt/g olive) inhibitsthe growth of almost all competing bacteria (Asehraou and oth-ers 1992; Efstathios 2006), thereby providing an opportunity forthe salt-tolerant molds to grow and possibly produce mycotoxins.

Among these, the most frequently encountered in North Africantable olives are species of the genera Aspergillus and Penicillium(Tantaoui-Elaraki and Le Tutour 1985; Gourama and Bullerman1988; Maouni and others 2002), and the most frequently de-tected mycotoxins are OTA, citrinin (CIT), and AFB (El Adlouniand others 2006; Zinedine and Manes 2009). Nonetheless, studieshave shown that black olives are not good substrates for myco-toxin production (Gourama and Bullerman 1988; Eltem 1996). Inthis regard, Tantaoui-Elaraki and Le Tutour (1985) have demon-strated the inability of A. flavus and A. ochraceus to produce de-tectable amounts of mycotoxins in Moroccan table olives, whilethe same strains had been shown to produce high concentra-tions of mycotoxins in laboratory media. Similar observation hasbeen made by Leontopoulos and others (2003) who have demon-strated that a toxinogenic strain of A. parasiticus was unable toproduce AFB1 in damaged black olives originating from Greece.Similarly, Gourama and Bullerman (1988) showed that A. flavusdid not produce AFB1 in pastes made from Moroccan Greek-style black olives. Furthermore, Eltem (1996) showed that freshwhole black olives, fresh damaged black olives, and whole blackolive paste inhibited or greatly reduced the production of afla-toxins by toxinogenic strains of A. flavus and A. parasiticus isolatedfrom naturally fermented black olives. Although these studies con-curred to suggest that olives, especially the black, are not suitablesubstrates for the production of mycotoxins at hazardous levels,the occurrence of various mycotoxins in table olives in NorthAfrican 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 appreciableamounts in commercial samples of Moroccan table black olivesin spite of the fact that these mycotoxins were shown not to beproduced when black olives were artificially contaminated withselected strains of toxinogenic molds. Also, a survey carried out byZinedine and others (2004) revealed that 36% of Moroccan tableblack olives were contaminated with OTA at levels ranging be-tween 0.62 and 4.8 µg/kg with an average concentration of 1.43µg/kg. Furthermore, OTA and AFB have been detected in 100%of sampled Moroccan dry-salted olives at levels exceeding 0.65 and0.5 µg/kg, respectively (El Adlouni and others 2006). Therefore,the occurrence of toxigenic molds and the frequent detectionof mycotoxins in traditionally processed black olives rank theseproducts among the commodities of high risk to public health inNorth African countries. Such a risk is even greater when morethan one mycotoxin is present in table olives, as was demonstratedby El Adlouni and others (2006) who showed the concomitant



presence of OTA, CIT, and AFB in dry-salted commercial Mo-roccan Greek-style black olives. Furthermore, the prevalence ofchronic nephropathy diseases in Tunisia has been correlated to theconsumption of various foods contaminated with OTA, amongwhich black table olives were incriminated, as abnormally highlevels of this mycotoxin (up to 46.83 mg/kg) were found in thisproduct (Maaroufi and others 1995a, b).

The decrease in moisture content to about 14% (Canellas andothers 1993; Karathanos 1999) and the subsequent increase insugar concentration in fruits during drying resulted in an almostselective medium for xerotolerant molds, among which membersof the Aspergillus section Nigri have been shown to predominate.These black aspergilli are particularly severe and widespread ingrapes of the warmer areas of the Mediterranean basin includ-ing North African countries (Battilani and others 2008). Strainsof A. niger aggregate and A. carbonarius have been shown to bethe main contaminants of Moroccan grapes and to produce highamounts of OTA (0.24 and 0.22 µg/g, respectively) at optimalenvironmental conditions (Selouane and others 2009). A similarsituation is expected in the other grape-producing North Africancountries including Algeria, Tunisia, and Egypt, despite the lackof reports, as these countries share the same climatic conditions aswell as sociocultural conditions. In addition to A. niger aggregateand A. carbonarius, A. aculeatus has also been found to predominateduring the entire drying process of grapes; from the fresh fruitsto the fully dried raisins (Leong and others 2008). However, thisstudy showed that among the 3 fungal species, only A. carbonariuswas able to produce OTA in vitro as detected by the emission offluorescence under UV light upon cultivation on coconut creamagar plates. The incidence of occurrence of AFs and OTA in Mo-roccan commercial raisins and dried figs has been reported to be30% and 65%, respectively, and the levels ranged between 0.03and 1.42 µg/kg, with an average of 0.33 µg/kg in dried figs, andbetween 0.05 and 4.95 µg/kg with an average of 0.96 µg/kg indried raisins (Zinedine and others 2007b). In Egypt, OTA was de-tected in figs at levels varying from 60 to 120 µg/kg, while raisinsamples 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). Inanother survey on 100 samples for the occurrence of mycotoxins,Egyptian raisins were found to be contaminated at very high levelsof AFB1 (300 µg/kg) and OTA (250 µg/kg), though at the lowfrequencies of 2% and 1%, respectively (Youssef and others 2000).From the above data, it is clear that the occurrence of mycotoxinsin fruits and vegetables presents a real threat to consumers’ healthin these countries, as well as a serious limitation for the exportof local produce toward developed countries, especially the tradi-tional economic partners of the European Union (EU) and NorthAmerica. The latter countries are in the process of harmonizingtheir regulations on mycotoxins in foods and feeds with a cleartendency to be more restrictive. On the other hand, there arepresently no specific regulations on mycotoxins in North Africancountries, which is expected to hamper, on a medium or long run,the export of vegetable products from these countries to Europeand other partners from developed countries. It is worth men-tioning that Morocco, Algeria, Tunisia, and Egypt are among themain suppliers of fruits and vegetables to Europe, which representsa major income to those North African countries where agricul-ture is the essential economic activity, especially in Morocco andTunisia. However, despite the lack of specific regulatory limits formycotoxins in these countries, the problem of mycotoxins is wellrecognized from both public health and economic views. Projects

for the tolerable limits of aflatoxins and ochratoxins in foods havebeen proposed in some North African countries, but they havenot come into force yet (Zinedine and Manes 2009). This is essen-tially due to the belief of stakeholders in these countries that thestrict implementation of mycotoxin regulations will have limitedeffects in terms of health protection. The prevalence of subsistencefarming and the continued practice of traditional technologies forthe transformation of food products in poor sanitary conditionswill certainly hinder any effort to enforce such regulations. In-deed, the mycotoxin issue in North Africa or other developingcountries needs to be viewed in the overall context of local foodsafety, health, and agricultural practice issues.

Prospects for Safety Improvement of Traditional NorthAfrican Foods: Opportunities and ConstraintsGeneral context

Like most developing countries around the world, those ofNorth Africa are at the crossroads between many strategic choicesregarding food policies aiming at the improvement of food safetywhile adapting to the advent of globalization. Nonetheless, re-gardless of the strategy to be adopted, North African countriesshould necessarily upgrade the safety of their local foods to takeadvantage of the opportunities of globalization and to promote thetrading of such foods either internationally or in domestic marketsin face of the increasingly competitive global trade. To this end,North African countries should take into account, in addition tothe national constraints, the regional and global economic envi-ronment characterized by a multiplicity of bilateral, multilateral,subregional, regional, and international agreements. The most sig-nificant of these agreements are undoubtedly the Sanitary andPhytosanitary (SPS) and Technical Barriers to Trade (TBT) agree-ments of the World Trade Organization (WTO), which raisedthe food safety to the forefront of the international trade require-ments. Moreover, the SPS agreements have recognized the CodexAlimentarius Commission (CAC) as a key organ for the harmo-nization of food standards among member countries to reach theWTO objective of market globalization of safe foods. Althoughcontroversial, it is believed that the application of SPS measuresand the consequent strengthening of food safety regulations wouldprogressively lead developing countries, including North Africanones, to improve safety and quality control practices in agricultureand food technology. Such improvements would ultimately resultin new forms of competitive benefits for developing countries andcontribute to more sustainable and profitable trade in the long run(FAO 2004). Indeed, the application of GMP and HACCP in thefish industry in Tunisia and Morocco, for example, as mandatorymeasures or on a voluntary basis, respectively, has drastically im-proved the safety and quality of fish products, and consequently,their access to importing markets, especially the EU. Also, theneed for compliance of Moroccan, Tunisian, and Egyptian fruitand vegetable exports with the food safety regulations of import-ing developed countries, such as those of the EU, to enter thesemarkets has resulted in a significant advance of these 3 NorthAfrican countries in the implementation of modern food controlsystems. Therefore, efforts to produce traditional foods that meetthe standards of the Codex Alimentarius (CA) would increasetheir safety, and consequently, their local and international marketshare, as has been reported for traditional Greek foods (Panagouand others 2013). It is worth mentioning, however, that NorthAfrican countries do not have the same status as regards interna-tional, regional, and subregional organizations (Table 11), nor dothey have the same economic resources and priorities in regards to



Table 11–Membership status of North African countries in different international organizations and agreements with impact on trade, food safety, andfood security.

International agreements Regional BilateralSubregionalCountry WTO CA OIE IPPC NEPAD MEDA UMA FTA OECD∗

Algeria A X X X X X X – –Egypt X X X X X X – – XLibya R X X X X X X – –Morocco X X X X S X X X –Tunisia X X X X X X 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 (Office International des Epizooties).IPPC: International Plant Protection Convention.NEPAD: New Partnership for Africa’s 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 hav-ing a common food safety policy, should be addressed for mutualbenefit and to obtain the best advantage for the opportunities ofglobalization; each of these countries should endeavor to promotethe safety of its own traditional foods while encouraging the ex-change of these foods with the other North Africa countries thatshare many common dietary habits.

Safety of North African traditional foodsThere is a clear trend in North Africa to increase the avail-

ability and diversity of industrial foods either produced locally orimported from other countries. Nonetheless, the consumption oftraditional food products in these countries, though difficult to ac-curately estimate, is significant especially in the rural areas wherean average of about 40% of the entire North African popula-tion lives (Table 1). Many dairy products (brined and soft cheeses,zabadi, raib, lben, zebda, and smen), meat products (khlii, pastirmaand sujuk), and vegetable products essentially represented by var-ious table olive types and pickled vegetables are examples of suchfoods highly appreciated and widely consumed in North Africancountries. Consumer preference for traditional foods is essentiallydriven by the fact that these foods are considered as a valuableheritage, and hence, part of the cultural identity to preserve, inaddition to their believed health virtues and highly appreciatedgustatory properties. This particular issue has been extensivelydiscussed over the last 2 decades as a means to preserve the cul-tural diversity, including nutritional habits, within the inevitableglobalization of the world food supply. Nevertheless, this situa-tion creates a dilemma to the government officials who shouldencourage and support the production and consumption of localtraditional foods which, on the other hand, may present increasedhealth risks to consumers due to their usual nonconformity withregulatory standards.

Such risks, especially those related to microbiological hazards,are anticipated to be especially high for traditional foods, as theyare generally produced under poor hygienic conditions with-out any systematic control measures. The widespread presence ofpathogenic bacteria and molds in North African traditional foods,and reported cases of food intoxications linked to the consumptionof a number of these foods, strongly supports the assumption thatthey put the public health at a high risk. Therefore, there is anurgent need to improve the hygienic quality of these products, notonly to safeguard consumer health, but also to improve competi-tiveness and market share so that they can efficiently contribute to

the availability of safe traditional food in North African countries.Marketing of traditional food commodities would also help the ru-ral populations to generate greater income and meet other needsnot available locally. In this regard, the world food security (WFS)framework developed by the FAO under the Special Program forFood Security (SPFS) aims to improve food security within poorhouseholds through national and regional programs for food se-curity. Morocco, Tunisia, and Egypt are among the participatingcountries of the WFS. The main challenge resides therefore inthe development of practical technologies and/or the adoption ofadequate strategies to improve the safety and stability of traditionalfoods in conformity with international regulations and standards(especially Codex Alimentarius standards) while preserving theirauthenticity and palatability. To meet such a challenge, it is nec-essary to develop national strategies for food safety based on a“holistic” or “food chain” approach that extends “from harvest toconsumption” and involves all the relevant actors (government of-ficials, food industry, local producers, researchers, academia, anal-ysis laboratories, the media, consumers and their organizations,and so on), within the framework of a predefined action plan suchas that proposed to the Middle East and North Africa (MENA)region by the FAO (2004). However, the implementation of suchan action plan appears to need greater financial and technical as-sistance from the governments and a longer transitional period toupgrade the quality of traditional food production while keepingtheir authenticity. A number of authors have suggested the trans-fer of traditional technologies to small or medium industrial scaleswhere the hygienic conditions and microbiological contaminationcould be better controlled than household production through theapplication of appropriate quality assurance programs such as GMPand HACCP (Fellows and others 1995; Motarjemi 2002; Benker-roum and Tamime 2004). In the case of traditional fermentedfoods, it has been suggested to adopt controlled fermentation us-ing selected industrial starter cultures and/or heat treatment ofthe raw materials, such as milk, as appropriate (Benkerroum andTamime 2004). According to Panagou and others (2013), the tran-sition from artisan practices in traditional food manufacturing towell-equipped industrial units under strict processing and hygienicconditions has resulted in drastic improvement in the microbio-logical quality of Greek foods similar to those reviewed herein(fermented meats, dairy products, and fermented vegetables), andhence their safety records. The addition of chemical preservativesincluding sorbates/benzoates or sulfites has also been suggested inthe 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 technologytransfer may lose their authenticity and uniqueness as the selectedstrains of the starter cultures cannot be representative of the com-plex and changing microflora involved in the different steps of thenatural fermentation. Alternatively, it has been suggested that safeand authentic traditional foods could be obtained by improving thesanitary conditions of the traditional technologies along the wholeproduction chain by the application of Good Agriculture Practices(GAP), Good Harvest practices (GHaP), GHP, HACCP, and theuse of adequate conditioning, packaging, and transportation facil-ities (Fellows and others 1995; Flamant 1996; Valyasevi and Rolle2002). However, the production of typical traditional foods mayalso include the acceptance of a “residual” risk. For example, theuse of raw milk to produce traditional cheese by application ofgood practices reduces risk of listeriosis, but it does not remove it,while initial sterilization of milk followed by controlled fermenta-tion with pure starter cultures can meet the “zero tolerance” status;however, the resulting cheese will loose its uniqueness and typi-cal gustatory quality. Therefore, though the residual risk could beaccepted, it has been recommended to prohibit the consumptionof such traditional foods by the high-risk groups: elderly, pregnantwomen, young children, and immunocompromised individuals.

Official food control measuresThe success of any strategy to promote food safety and quality

should involve all the relevant actors, with the government playinga central role in the coordination and supervision of the imple-mentation of the strategy. In this regard, the 27th FAO regionalconference for the Near East recommended a number of spe-cific measures that the governments of Middle Eastern and NorthAfrican (MENA) countries should take to improve food safetyand quality, and be prepared for the upcoming challenges relatedto the inspection and certification of food imports and exports andthe provisions of scientific risk assessment as needed (FAO 2004).According to these recommendations, government officials are re-sponsible for the establishment and management to enable institu-tional, policy, and regulatory frameworks for food safety, and carryout food control activities that protect consumers from risks aris-ing from unsafe food and fraudulent or deceptive practices. To thisend, government officials should work with interested parties atthe national and regional levels to build capacity and to strengthennational food control programs and activities. Among the mainrecommendations, the conference stressed the need to strengthenand modernize food control facilities and procedures through arisk-based approach. The conference also recommended creatingor reinforcing capacities for national foodborne disease surveil-lances accompanied by a rapid alert system and mechanism forcommunication with food control authorities along with an effi-cient means to implement corrective measures. The developmentof cooperation between the countries of the region to facilitatecommunication and exchange of information in foodborne dis-ease 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 assess-ment body(ies) that provides scientific advice to risk managers onissues of particular interest and to form interregional networks oflaboratories (FAO 2004).

However, efficient implementation of these measures is costlyand requires highly skilled personnel; therefore, financial and/ortechnical support from developed countries or international or-

ganizations is necessary for the execution of such an action planin North African countries. In addition, a transition period isneeded before all measures are operational. This period appears tobe particularly long for traditional foods, which have received lit-tle attention so far, partly due to the lack of political commitmentfrom the interested countries to act as partners having commonweaknesses and complementary assets.

Adequacy of current food control regulations and possiblealternatives

The nature and degree of sophistication of food control systemsvary widely among North African countries, which otherwisesuffer from common difficulties that limit the performance andefficiency of their food control and inspection systems. Theseinclude:

� Multiplicity of the food control systems—whereby modernsafety and quality assurance systems using GMP, GHP, andHACCP programs are used by certain enterprises to producefoods for export or urban retail sales, and to exist alongside aninformal food sector subject to minimal or no food safety orquality control. The latter situation applies to North Africantraditional foods generally sold in informal ways in rural mar-kets, shops, butcher shops (meat products), creameries (dairyproducts), and grocery stores or by street vendors.

� The multiplicity of bodies involved in food safety andquality control, which are usually affiliated with differentministerial departments (agriculture, public health, interior,trade, industry, environment, energy, and possibly others)(http://www.reading.ac.uk/foodlaw/flip2000/tunisia.htm).Although these departments play, in principle, different andcomplementary roles and act to ensure the highest possiblelevel of consumer health protection, they have often been asource of problems and distortions due to the lack of clearboundaries between the specific tasks of each institution, andalso due to intrinsic competition to be the leading authorityin food safety and quality in the country.

� Management of food safety issues is considered as an exclusivegovernment mandate, and there is no or marginal inclusion ofother stakeholders (industry, research institutions, consumers,nongovernment organizations (NGOs), and so on) in thedecision-making process regarding the policy of food safety.

� In most North African countries, the current laws on foodcontrol are generally not specific to foods but cover all kinds ofgoods. Furthermore, many regulatory standards and thresholdvalues are obsolete and do not match with the recent advancesin food technology and the techniques used for the detectionof conventional or emerging microbial or chemical contami-nants, such as Creutzfeldt-Jakob prion, avian influenza virus,Ent. sakazakii, dioxin, and acrylamide. Furthermore, they donot meet the international trade requirements for accredita-tion, certification, traceability, and required high food safetystandards.

In fact, officials of North African countries are aware of theinadequacy and vulnerability of their food safety policies in viewof global trends. Therefore, they have been modifying, at differentrates, their food safety systems to meet WTO requirements andharmonize their standards with those of the CAC. However, thetransition from the conventional control and inspection systemsto a modern food safety framework requires profound institu-tional and legal changes in addition to substantial investment andtechnical needs. Morocco, for example, has been working on thisissue with the support of FAO since 2000, and has only recently



adopted a new law (Law 025-08) stipulating the creation of aNational Food Safety Office (ONSSA) (official bulletin N◦5714of 5 March 2009). This act has been designed to induce deepchanges in the Moroccan food safety policy and control practicesso as to meet the recommendations of regional and internationalorganizations including WTO (SPS, TBT), WHO and FAO (CA,IPPC), EU, OIE.

In view of these changes, traditional products should also beconsidered under the law 25-06 on “the distinguishing marks oforigin and quality of agricultural products and foodstuffs” to im-prove their safety and competitiveness. Under this law, traditionalfoods are subject to official food control and inspection. Indeed,standardization of traditional foods and protection of their originand quality through such legislations has been reported to moti-vate the small-scale production of traditional foods and to expandtheir export potential (Panagou and others 2013). Adoption of anadequate surveillance system is another crucial factor to accuratelyassess the health risk associated with the consumption of traditionalfoods, and consequently, design appropriate preventive measuresto reduce risks to as low levels as possible. This aspect was alsoemphasized in the new Moroccan food safety act.

Incentives to food producers and infrastructure improve-ments

To improve the safety of traditional North African food prod-ucts, it is necessary to adopt certain measures that would encouragefood producers, usually rural, including the provision of financialand technical incentives to help them upgrade the hygienic qualityof their products and be aware of the benefits of such an approachin the medium and long term. Some of these incentives may be:

� Preferential rates of water and electricity fees. The prices ofwater and electricity are relatively high in most North Africancountries due to the water shortage and limited capacity inthe production of electricity; a situation that deters rural foodproducers from using water and electric urban facilities to pre-pare traditional food products. Instead, they use wells or opensurface water as available; they thus expose the final productto various chemical and microbiological contaminants orig-inating from a polluted water supply. Also, the provision ofelectricity at a reduced rate would encourage rural food pro-ducers to use electric machines (dryers, churning machines,heated vats, meat cutters, refrigerators, and so on) for bettercontrol of the technological processes or for storage of thefinished product before sale.

� Provision of technical assistance at the farm level: Rural foodproducers are usually not aware of the critical steps in tra-ditional processes that may lead to defective final productsor inconsistent gustatory quality if not adequately controlled.Therefore, technical assistance by trained persons would drawthe attention of rural food producers to the critical steps of thetraditional processes, and help them ensure the production offoods with consistent quality. For example, the relevance ofcleaning/sanitation, as well as personal hygiene, to the qualityand safety of the final products is overlooked or even ignoredby rural food producers. The organization of adequate train-ing sessions would contribute to the sensitization of foodproducers to the impact of these practices on the quality ofthe finished food products.

� Facilitating technology transfer from the household level tosmall or medium industrial scale for traditional food productswhen such transfer is deemed viable and economically feasible

in the long run. To this end, the government could simplifythe administrative routine, reduce taxes, and provide technicalassistance to design a business plan and later implement it.

� Facilitating loans at reduced rates for the acquisition of smallequipment and machinery. Rural food producers usually lackthe basic capital to start producing foods for trade, and smallor medium loans with reduced rates would help them starta business either individually or within associations or coop-eratives. Many successful creameries in Moroccan cities havestarted in this way, which could be extended to traditionalmeat products (gueddid, khlia, mkila, and so on) or vegetableproducts.

� Subsidizing traditional food products, especially those pro-duced in cooperatives or professional associations as an en-couragement during a limited period.

� Encouraging women associations to produce traditionalfoods. It is of paramount importance for women in NorthAfrican countries to know that the foods they produce at thehousehold level have financial value and constitute a signifi-cant source of income for their own autonomy and financialindependence. This also represents a means to support thegender policies now being recognized as a limiting factor tobalanced economic growth in developing countries; this isusually better achieved by a group of women within associa-tions.

� Organizing training sessions for all the personnel involved inthe production process including technicians and food han-dlers on a regular basis under the supervision of official agen-cies or NGOs, and at no fees for targeted participants.

� Organizing yearly prizes for individuals or associations pro-ducing the most competitive traditional food products thatalso meet the safety standards.

It is worth mentioning, however, that these measures can onlybe effective if the other basic requirements for such technologytransfer (infrastructure, transportation vehicles, electricity, potablewater, 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 awhole.

The role of NGOsThe role of NGOs in the promotion of the safety and quality

of foods is no longer questionable and should be further encour-aged by the governments. Depending on the objectives of theseorganizations, they may play critical roles at many levels for thepromotion of the safety of foods in general and specifically of tra-ditional foods. According to the approach of risk analysis, NGOsshould work closely with other stakeholders, by virtue of the riskcommunication component of the approach, to defend the con-sumers’ right to safe foods as was recommended by the CAC inthe 1990s. They should therefore be involved in the definitionof national food safety policies to request appropriate standards offood safety, and also at the production level to ensure that foods arehandled, stored, and prepared in accordance with good hygienicpractices (GHPs). Furthermore, NGOs that focus particularly onrural development would provide valuable technical assistance torural individuals or associations to develop economic activitiesadapted to their environment including the production of tradi-tional foods, so they can be formally marketed through the countryor the region. Such organizations are being increasingly active inall aspects of development in North African countries and maybe an asset for the modernization of the traditional food produc-tion sector. Indeed, subsequent to the CAC recommendation to



promote consumers’ participation in food-related decision-making at national and international levels, North African coun-tries have encouraged the organization of independent consumerassociations and their representation in all food safety-related issuesincluding those debated within the National Codex Committees(NCC) and subsidiary bodies. In Tunisia, the Consumers Protec-tion Defense Organization (CPDO), for example, plays an activerole alongside with technical committees in preparing standards asa member of the Tunisian NCC and in all the affiliated techni-cal committees. In Morocco, there are more than 20 associationsorganized under 2 federations (Federation Nationale des Associ-ations de Consommateurs, FNAC; and Confederation des Asso-ciations des Consommateurs; CAC-Maroc), which participate inthe work of the NCC and working groups. Among other activ-ities, they include consumer protection from deceptive practicesin commerce and the provision of technical and legal advice toindividuals or groups of consumers. In Egypt, there are more than60 consumer protection associations, which are represented in theNCC and in the various technical committees established by theEgyptian Organization for Standardization (ESO). In Algeria andLibya, the contribution of independent consumers’ associationsto food safety has started only recently and is still in its infancy;however, it is expected to grow and play an increasing role in con-sumers’ protection from illicit or fraudulent practice in foods. Infact, an Algerian Federation of Consumers (FACs) encompassingmany local associations has been created recently, but its actionsare rather diffuse including many goods, which may limit its ef-ficacy as regards food safety, especially in a developing countrycontext.

In addition, other stakeholder such as NGOs including produc-ers associations of farmers and processors may play a significantrole in the promotion of food safety awareness or in technologytransfer implementation. Although the primary role of such orga-nizations is to defend the producers’ interest, they also endeavorto promote the quality of their produce and ensure that they meetgovernment requirements and consumer expectations to be com-petitive. Such a trend has been officially encouraged in all NorthAfrican countries since the 1980s in response to the foreseen foodmarket and trade liberalization (Desrues 2005). Therefore, manyprofessional organizations and associations have been created indifferent food production fields including citrus, olives, red meat,poultry, viticulture, fisheries, dairy, fruits and vegetables, and soon, as well as in food processing industries. However, in spite ofthe fact that the role of such organizations and their impact on thepromotion of food safety and quality has been evident in recentyears, a critical analysis of their actual input in Moroccan agricul-ture, for example, suggested that they are of benefit to influentialand the biggest farmers/producers more so than to consumersor small-producer members (Desrues 2005); a situation that allNorth African countries may share. Yet, further development ofprofessional organizations and associations in North African coun-tries to fulfill adequately their role in economic development andcontinual upgrading of food safety is necessary (Ayad and oth-ers 2011) despite the present limitations that may be regarded asstimulatory factors for future developments. The role of these or-ganizations/associations, as professional representatives and also asmediators between professionals and officials, has been recognizedas an essential tool for the implementation of any balanced strategyfor sustainable development. Their involvement in risk analysis andinteraction with risk assessors and risk managers, for the purposeof risk communication, has been specifically mentioned among“the interested Parties” in the CA (WHO/FAO 2007).

Promotion of food safety awarenessThe increased dissemination of information worldwide re-

garding foodborne illnesses through mass media (written andaudio–visual) has greatly contributed to raising food safety aware-ness among North African citizens of the relevance of food safetyto the welfare of consumers and to sustainable development. Also,government officials are increasingly aware of the cost of food-borne diseases in terms of medical care, labor days-off, and foodslosses. However, greater efforts are yet to be made to raise suchawareness to a level where consumers, food producers, as wellas government leaders and heads of concerned agencies are con-vinced of the economic, social, and health benefits resulting fromupgrading the safety and quality of foods among which traditionalfoods constitute a substantial part. Consumer organizations have animportant role to play in the promotion of food safety awarenessand the need to strengthen food control among North Africancountries. For example, Tunisian CPDO plays an active role inconsumer awareness and guidance through audio–visual and writ-ten mass media. The Moroccan consumer associations affiliatedwith each of the 2 consumer protection federations are also in-volved in the enhancement of consumer awareness through variousmass media and the organization and participation in/of seminarsand meetings at universities, high schools, or in local communi-ties to disseminate information related to food safety. Similarly,in Egypt, a Consumer Protection Unit (CPU) has been createdwithin ESO to undertake consumer-related activities in additionto issuing a newsletter on a regular basis, among other means,to disseminate information on food safety. However, despite theofficial trend to encourage these associations in North Africancountries and their contribution to raise food safety awarenessamong consumers, all efforts may be hampered by limited data onthe incidence and prevalence of foodborne diseases among NorthAfrican traditional foods. In addition, the weak food control ca-pacity of these countries makes it difficult to demonstrate the riskassociated with the consumption of such foods on human healthand the impact on economic development. Indeed, in the absenceof risk assessment or profiling studies, and with the lack of epi-demiological data and reports on intoxication/infection cases, it isdifficult to convince consumers who do not question the whole-someness of traditional foods and firmly consider that these foodshave been part of their diets through generations without repre-senting a threat to health. It is even more difficult to convince mostconsumers about the risk for chronic diseases such as those causedby mycotoxins. Incidentally, traditional and homemade foods haverecently been identified as important nonconventional exposuresources for OTA, due to the widespread of this toxin among suchfoods (Duarte and others 2009). Nonetheless, traditional foods, es-pecially the fermented types, have been recognized to have goodsafety records worldwide, including developing countries wherethey are usually manufactured by people without training in mi-crobiology or chemistry. According to Steinkraus (2002), the safetyof such foods is related to different intrinsic protecting “princi-ples” that discourage the growth of undesirable microorganismsand may also contribute to reduce the levels of mycotoxins. How-ever, the same author emphasized that these “principles” wouldnot indefinitely guarantee a high degree of food’s safety, as theywould not compensate for unsanitary conditions such as improperstorage and handling, use of contaminated water supply, prepa-ration in environments heavily contaminated with human waste,improper personal hygiene by food handlers, infestation with in-sects spreading disease organisms, and raw materials carrying foodpoisoning or human pathogens.



Effective contribution to the implementation of food safetyregulations and control of traditional foods

Over the last 2 decades, risk analysis has emerged as a powerfultool that can be used by national food safety authorities to makeproportionate and scientifically based decisions on food safety is-sues. Also, as an integral part of Codex Alimentarius, risk analysiscan support and improve the development of standards and reg-ulations on a scientific basis and address food safety issues thatresult from emerging hazards or breakdowns in food control sys-tems. The relevance of risk analysis to all the food safety issueshas become increasingly important since its adoption within theSPS agreement. While risk analysis and its scientific componentrisk assessment are now widely applied in developed countries inEurope, America, and Australia, its extension to developing coun-tries is hindered by many limitations, the most important of whichare:

� General lack of awareness among officials, manufacturers, sci-entists, and consumers of the real gain that the implementa-tion of risk analysis approaches would represent to nationalfood safety status compared with the conventional food safetyand food control measures.

� Lack of infrastructure, technical and financial resources, ad-equate institutional framework, and necessary expertise toeffectively respond to existing and emerging food safety andquality problems.

� Insufficient information about the hazards and risks associatedwith traditional foods due to the lack or poorly documentedepidemiological, intoxication records, and scientific investi-gations.

� Lack of data on consumption patterns and insufficient knowl-edge about levels and occurrence of hazards (chemical andbiological) in foods.

In view of these limitations, FAO and WHO have been work-ing together to increase the awareness and adoption of risk anal-ysis principles in developing countries, both as a tool for nationalfood safety authorities and the provision of scientific advice andevaluations. These United Nation organizations have also beenproviding technical and financial support to developing coun-tries to help them build capacities and strengthen national foodcontrol and inspection systems, and activities in order to adoptnew food safety frameworks based on risk analysis. Among NorthAfrican countries, Morocco has benefited from this assistance toreform its food safety policy, as confirmed by the promulgationof the new Law 25-08 on February 18th, 2009. Under this law,the ONSSA has been established as the only institution responsi-ble for protecting the consumer health as well as that of animalsand plants (http://www.onssa.gov.ma/onssa/fr/loi_creation.php).Nonetheless, risk assessment of North African traditional foods, atthe present, remains incomplete and inaccurate due to the lack ofnecessary data to produce credible and reliable risk assessment. Infact, this situation has been reported to be the main constraint fac-ing risk assessment worldwide regardless of the type of foods. Yet,the extent of shortage of relevant data and records to conduct riskassessment is variable depending on the country, with developingcountries being the most affected. In particular, the lack of thenecessary data to estimate exposure to hazards has been identifiedas one of the critical missing parts in a risk assessment process, as aninaccurate risk estimate would provide risk managers with a falseglobal picture of the situation, which may eventually lead them tomake inappropriate decisions (Luetzow 2003). The same authorhas recommended improving the collection and dissemination ofsuch data worldwide to progressively fill in the gaps for more

reliable estimates of exposure and specifically mentioned that aconsideration should be given to developing countries by provid-ing them with assistance and resources for generating meaningfulfood consumption data and subsequent exposure assessments. Al-ternatively, it has been suggested to perform risk profiling withthe available data, which should then be revised periodically andamended as new data are generated from scientific studies andsurveillance programs to ultimately allow quantitative risk assess-ment (FAO 2006; Bidlack and others 2009). Meanwhile, riskprofiling that categorizes food products into groups with high,moderate/medium, or low risk may be a useful tool to assist thedecision-making process and to set priority for action. In fact, un-der certain circumstances, including cases where risk assessment iseither unnecessary or not feasible to carry out, risk profiling mayserve as a basis to identify and select food control measures andrisk management decisions. Notable examples of such cases are: (i)the Canadian approach to regulating L. monocytogenes in ready-to-eat foods, (ii) the Swedish approach to regulating acrylamides inbaked and fried starchy foods, and (iii) the prohibition of certainantibiotics from veterinary care in many countries on the basis ofrisk profiling that suggests microbial resistance to some antibioticsused in both human medicine and animal health care (FAO 2006).

A systematic risk profiling approach would be appropriate andamply justified for North African traditional foods at the presenttime. It is generally admitted that the main risks associated withNorth African traditional food products are of microbial origin(pathogenic bacteria and their toxins, mold toxins, parasites, andviruses), although hazards of another nature, such as pesticideresidues and heavy metals (Zaida and others 2007), not discussedin this review, should not be overlooked. Depending on the natu-ral 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 samehazard may present different health risk patterns depending on theproduct (Larsen 2006; Bidlack and others 2009). Table 6 presentsdocumented hazards of microbial origin associated with NorthAfrican traditional dairy, meat, and vegetable food products. Ta-ble 12 shows various risk factors associated with North Africantraditional foods and the protective hurdles on which the tradi-tional technology relies to ensure their safety and stability. Correc-tive actions are proposed on the basis of harvest-to-consumptionapproach (Table 12). Taking into account the global situation ofNorth African traditional foods and the uncertainties regardingtheir wholesomeness, it appears urgent to start preliminary riskprofiling with the presently available knowledge on these products.Simultaneously, scientific studies and chemical and microbiologicalanalyses involving universities and research institutions along withsurveillance programs should be initiated to provide new infor-mation to progressively refine and update risk profiling. However,since traditional food products differ among North African coun-tries and even among localities of the same country, it is vital tofacilitate communication and information exchange in foodbornedisease surveillance as well as information about foodborne haz-ards between these countries according to the recommendationsof the 27th FAO regional conference (FAO 2004).

Ranking risk of North African traditional foodsIn order to compare microbiological risks associated with tra-

ditional foods from North Africa, the RCM developed by theFederal/Provincial/Territorial Committee on Food Safety Pol-icy (FPTCFSP 2007) was modified and used to profile selectedNorth African traditional foods. This model, originally designed to



Table 12–A general presentation of the risk factors related to hazards of microbial origin and the natural hurdles empirically used in traditionaltechnologies to reduce the health risk associated with the consumption of such foods. Corrective actions to upgrade the safety and quality of NorthAfrican traditional foods on a scientific basis are also proposed.

Risk factorsType of commodities Microbial contaminants Mycotoxins Safety factors Corrective actions

Dairy products � Contaminated raw milk,� Poor sanitary conditions during

processing and handling� Opportunity for pathogens to grow

and produce toxins duringprocessing or storage

� Contaminated water supply� Usually ready-to-eat� High exposure� No application of any quality

assurance program

� Contaminated milk (carryover ofmycotoxins from feeds)

� Contamination and growth oftoxinogenic molds on finishedproduct or during storage

� Lactic fermentation� Predominance of safe or

health promotingmicroorganisms

� Reduced aw (dry-salted,brined cheeses, driedcheese)

� Addition of herbs andspices

� Veterinary care of dairyherd (control of mastitisdiseases)

� GHaP, GHP, GMPs,HACCP (from the farmto storage)

� Use of selected starter oradjunct starter cultures(controlledfermentation) withantimicrobial activities(for example, use ofbacteriocin-producinglactic starter cultures)

� Sourcing and potentialtesting of feed fromGAP producers

Meat products � Contaminated raw material� Poor sanitary conditions at

slaughter and processing� Postprocessing contaminations� Opportunity for pathogens to grow

during processing and/or storage� Poor veterinary care of livestock

(prevalence of zoonotic diseases)� No application of a quality

assurance program

� Mycotoxin-containing spices� Contamination and growth of

toxinogenic molds on finishedproduct during storage

� Presence in the liver and kidney ofanimals fed with contaminatedfeeds (meat products using offalmeat)

� Addition of herbs andspices

� Reduced aw (dry-salting,brining, drying)

� Heat treatment duringprocessing

� Usually cooked beforeconsumption

GHP, GMP, on-farmHACCP, improveanimal welfare GHP infood sale andpreparation to reducemicrobialcontamination

� Low exposure

Vegetable products � Contaminated raw material� Postprocessing� Contaminations� Opportunity to grow during

processing or storage� Poor hygiene during harvest,

processing, and storage� Cross-contamination� Human reservoirs� Contaminated raw material (use of

wastewater sewage or sludge forirrigations and fertilization

� Sanitary conditions duringmanufacture and storage

� Post- and cross-contaminations,� High exposure

� Presence in fresh vegetable productsand persistence during processing

� Growth of toxinogenic mold andopportunity to produce mycotoxinsduring processing or storage

� Use of spices and condimentscontaminated with variousmycotoxins

� Fermentation� Chemical acidification� Reduction of water

activity (dry-salting,brining, drying)

� Addition of herbs andspices withantimicrobial activities(occasionally)

� Inherent antimicrobialsubstances such aseuloropein andderivative substancesin olives

GAP, GHP, on-farmHACCP, adequateconditioning andstorage conditions,controlled fermentation

GHaP: Good harvest practices.GHP: Good hygiene practices.GMP: Good manufacture practices.HACCP: Hazard analysis critical control point.NA: Not available.

conduct risk profiling for food retail and food service establish-ments, takes into account 8 major risk factors each of which isscored according to the extent of risk it poses to consumers. Thetotal score of the 8 factors indicates the risk categorization of aproduct as per the following cutoff points: high risk (165 points ormore); moderate risk (between 110 and 160 points); low risk (105points or less). The RCM guide also provides an explanation foreach risk factor, along with directions on how to determine thecorresponding score. These risk factors were determined on thebasis of a previous study reviewing factors that contributed to food-borne illness in Canada in the period of 1973 to 1977 (Todd 1983)in addition to other factors used by some jurisdictions to deter-mine inspection frequency. The 8 factors used in this study were:

1. Types of food and intended uses: Scoring of this risk factor isbased on 2 main considerations: (i) the likelihood of a foodto contain pathogenic microorganisms above safety level andopportunities it provides for the microorganisms to growand/or produce toxins, and (ii) whether the food is ready-to-eat or undergoes further heat treatment or cooking beforeconsumption. For this risk factor, the RCM considers only

biological hazards based on the epidemiological evidence,showing that the most frequent foodborne diseases are ofmicrobial origin. In this study, we also omit microbial toxins,such as mycotoxins, or heat-stable E. coli or Staphylococcaltoxins, which may be produced during processing or storageand would not be removed by treatments such as cooking orfermentation. Omission to consider microbial toxins in riskscoring 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 traditionalfoods. Therefore, high- or medium-risk ready-to-eat foodsare scored higher than those which undergo additional treat-ments (cooking, marinating, addition of herbs, and spices) toreduce or control microbial load before consumption. Sim-ilarly, high- or medium-risk foods, which receive furtherheat treatment or undergo other methods to reduce micro-bial pathogens, are at reduced risk. Low-risk foods are thosethat represent a hostile environment (reduced water activity,low pH, contain known antimicrobial substances, and so on)for microbial contamination and growth.



Table 13–Risk categorization of traditional foods of North African countries based on the model developed by Health Canadaa using 8 risk factors(I to VIII).b

Score of each risk factorTotal score

Commodity I II III IV V VI VII VIII (risk category)c

Dairy productsLben 40 40 15 30 30 70d 10 15 250 (High)Jben 40 40 15 30 30 40 10 15 220 (High)Smen 25 25 15 30 30 20d 10 5e 160 (Medium)Semna 40 25 20d 30 30 40 10 10e 225 (High)Arish cheese 40 40 15 30 30 40 20 10e 225 (High)Klila 25 10 15 30 30 30 5e 5e 150 (Medium)Aoules 25 25 15 30 30 30 5e 5e 165 (High)Domiati cheese 30 25 30 30 30 40 20 15 220 (High)Mish cheese 40 40 30 30 30 40 10 15 235 (High)Kishk 30 25 30 30 30 40 10 15 210 (High)Rigouta 25 25 30 30 30 40 10 10 200 (High)Zabadi 40 40 15 30 30 40 20 15 230 (High)

Meat productsGueddid 40 40 15 30 30 30 10 10 205 (High)Pastirma 40 40 30 30 30 40 10 10 230 (High)Khlii 10 10 15 30 0 15 10 15 105 (Medium)Naqaneq 40 40 15 30 30 40 10 5 210 (High)Merguez 40 25 5 30 30 40 20 15 205 (High)

Vegetable productsPickled green olive 40 40 15 30 30 40 10 15 220 (High)Pickled lemon 10 10 0 30 0 15 10 0 65 (Low)Dry figsf 10 10 15 30 0 15 10 15 105 (Low)Black ripe olives 25 40 15 30 30 30 10 15 195 (High)

aFederal/Provincial/Territorial Committee on Food Safety Policy (FPTCFSP) of health Canada; available fromhttp://www.hc-sc.gc.ca/ahc-asc/pubs/hpfb-dgpsa/fd-da/risk_categorization-categorisation_risques01-eng.php.bRisk factors as defined 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.cCutoff points: High risk (165 points or more); moderate risk (between 110 and 160 points); low risk (105 points or less).dThirty points were added to the original score because this product has been repeatedly associated with intoxications in Morocco during summer seasons.eRisk factors were assigned different scores from those proposed in the CRM taking into account the specific 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 refersto whether the food was minimally processed or has un-dergone a process designed to minimize the likelihood offood safety hazards (pasteurization, boiling, cooking, mari-nating, fermentation, and so on). In addition, the amountof handling that a food undergoes during preparation is adeterminant of the risk posed by a food. Indeed, extensivelyhandled foods, especially if they are uncooked and unpack-aged, are considered more likely to be subjected to microbialcontaminations, and hence they score highest.

3. Equipment and facilities: To determine the risk linked toa factor, RCM considers the layout and design of food es-tablishments, the way the flow of food goes from receptionto service or sale, whether or not raw materials and foodsof different risk categories are adequately separated in theestablishment, waste storage, and disposal as well as the sep-aration between nonfood activities from food preparationand processing areas. The water supply as food ingredientor for other needs (handwashing, warewashing, and sani-tizing), equipment for food preparation or processing (suit-ability, age, made from nontoxic materials, easily cleanable).As most traditional North African traditional foods are eitherhomemade or produced in small shops, scoring was basedmainly on the conditions where a given food is generallyprepared including the space, sanitary conditions of process-ing area, personal hygiene, access to drinkable water, andcleanliness of the utensils used.

4. Management and employee food safety knowledge: Accord-ing to RCM, scores of this risk factor are attributed de-pending on the extent of food safety knowledge of em-ployees, managers, and supervisors, which should be ade-

quate enough to ensure that safe food handling practicesare being followed with the possibility to undertake cor-rective actions when necessary. In addition to certificationthat the managers and employees should have from rec-ognized institutions, they must demonstrate to the regu-latory agency that they are following safe practices. Foodestablishments that do not have adequately trained em-ployees or practice safe food handling principles are atgreater risk of being implicated in a foodborne illness.North African traditional foods are generally not producedin modern establishments, by qualified personnel, and aftereffective training sessions on regular basis, but rather at thehousehold level or in shops, and generally by members of thesame family, usually with a low level of education. There-fore, this risk factor would score high for all North Africantraditional foods.

5. Food safety management program: Development and im-plementation of food safety management programs suchas Hazard Analysis Critical Control Point (HACCP) andits prerequisite support programs, including facility main-tenance and sanitation and personal hygiene of foodser-vice workers, contribute significantly to a better controlof food processing and preparation stages. RCM consid-ers that establishments that have such a program in placewould be at less risk than those that have no controls.As was discussed for the former risk factor, North Africantraditional foods are generally produced with untrainedpersonnel and in an environment where no food safetymanagement program could be appropriately applied.Therefore, this risk factor also scores high for all thesefoods.



6. Regulatory compliance: Determination of the risk associ-ated with the specific establishment as regards this factor isbased on historical information about regulatory compli-ance with critical items. The occurrence of an outbreak ata foodservice establishment is also taken into considerationwhen an indication exists that food safety principles werenot followed prior to the outbreak. Consumer complaintsand responsiveness of the management of the establishmentto act on previous advice are also considered to score this riskfactor. As the term “compliance” refers to past and currentcompliance to inspections, and North African traditionalfoods are not officially inspected, we relied on scientific pub-lications and reports to assess the microbiological complianceto known standards, either by the presence of pathogens orthe counts of groups of microorganisms of hygienic signif-icance (coliforms, fecal streptococci). Documented claimsabout implications of some North African traditional foodsin intoxications were also considered.

7. Volume of food: In the RCM, this risk factor relates tothe volume of foods sold or prepared, as estimated by thenumber of people served or provided food, or the numberof 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, thefrequency and quantity a given traditional food is consumedat each meal, based on personal knowledge of the culinaryhabits of North African communities, were used to estimatethe volume of the food.

8. Typical patronage: Serving foods to subgroups of a popu-lation (the young, elderly, and immunocompromised) whoare the most vulnerable to foodborne disease will increasethe likelihood of occurrence of a foodborne illness outbreak.Some North African traditional foods, especially dairy prod-ucts such as zabadi and jben are served to young children orsick persons due to the believed health virtues; such productswere attributed high scores regarding this risk factor.

Table 13 presents a tentative risk profiling of selected NorthAfrican traditional foods using the FPTCFSP RCM after the ad-justments/interpretations mentioned above. The outcome of thisprofiling showed that the vast majority of North African traditionalfoods pose a high risk to consumers, few fall into the medium riskcategory, and only 2 of the profiled products (pickled lemon anddry figs) would be of low risk owing to their extreme intrinsicphysicochemical parameters and relatively low consumption pat-tern, and hence, low exposure. Pickled lemon is highly acidic andsalty, while dried figs have low water activity due to their lowmoisture and high sugar contents. As for the consumption pat-tern, lemon is used in the North African cuisine as an ingredientin some cooked meals, and dry figs are mainly consumed duringthe fasting month of Ramadan in Muslim communities as an ap-petizer. However, the risk associated with the latter product mayincrease if contamination with mycotoxins are also considered asa potential hazard. Table 13 shows that the risk factors IV (man-agement and employee food safety knowledge) and V (food safetymanagement program) scored highest for almost all the profiledfoods. This demonstrates the prominent impact, either directly orindirectly, of employee education and the management system onthe risk ranking of foods, and it implies that any improvementto reduce risks linked to these foods should first address theseaspects, which will, in turn, mitigate other risk factors. Indeed,there is general agreement that the standardization of technologiesfor these foods by transfer to small or medium scale is a neces-

sary means to improve the safety of traditional foods (Fellows andothers 1995; Rolle and Satin 2002; Steinkraus 2002; Valyasevi andRolle 2002; Benkerroum and Tamime 2004; Panagou and oth-ers 2013). According to this preliminary profiling, North Africantraditional foods that constitute an important part of the NorthAfrican diet warrant due attention to improve their safety. Riskprofiling should be officially conducted on a large scale throughfield surveys in order to prioritize government actions and de-fine specific regulations and control measures, which should bestrictly implemented. Meanwhile, accompanying measures shouldbe taken by the government to provide the necessary assistance,encouragements, and other incentives as was suggested in this re-view and elsewhere (Rolle and Satin 2002; Valyasevi and Rolle2002; Benkerroum and Tamime 2004) to gear all producers towarda voluntary adoption of quality assurance management systems toimprove the quality and competitiveness of the foods they pro-duce. Practical measures to improve the safety of North Africantraditional foods at the production level are suggested in Table 13.

ConclusionsWith the advent of globalization and involvement of North

African countries in many international, regional, subregional,or bilateral agreements (SPS, OIE, CA, European neighborhoodpartnership, FTA, and so on) and increasing demand in terms ofquality and safety of foods for trade, it becomes urgent to reshapethe food safety policies in North African countries, not only toupgrade the safety and quality of the foods they produce, butalso to protect consumers from fraudulent or unsafe importedfoods. The latter foods make up a very high percentage, up to75%, of the food supply in some of these countries (Mboungou2011). Any future food safety strategy should be based on a riskanalysis approach, and national food regulatory standards shouldbe aligned according to the CA. The standards, guidelines, andrecommendations adopted by the CAC are, indeed, referred toin the WTO agreement on the application of SPS agreement asbenchmarks for international harmonization of food regulations.Reliable risk assessment or profiling studies need to be conductedon different foods of North Africa (including traditional foods) inorder to set food control priorities.

Despite their different economic, demographic, and politicalpriorities, North African countries share much sociocultural speci-ficity that would be an asset for their common sustainable develop-ment and the differences could, in fact, be regarded as complemen-tarities that stimulate synergistic actions. Therefore, it is crucial tofacilitate the exchange of information on all food safety-relatedissues and perform common risk profiling and assessments whenpossible. Nonetheless, to make such profound changes in foodsafety policy, North African countries are facing various financial,technical, cultural, and political challenges that they may not over-come if they rely only on their own potentialities and resources;they require greater and concrete synergistic actions between eachother in addition to external assistance from international organi-zations (FAO, EU, OIE, OECD, WHO, and so on) and developedcountries.

AcknowledgmentDeep appreciation is expressed to Dr. Dennis Bittisnich of

the Australian Government Dept. of Agriculture, Fisheries andForestry, and Dr. Manfred Luetzow, international food safety con-sultant, for reviewing the prepublication manuscript and for theirexpert comments and suggestions. The author is also grateful



to Prof. Mohamed Dehhaoui for his helpful discussions on sta-tistical issues and for providing valuable documentation to thiswork.

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