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Microbial quality control of raw ground beef and fresh sausage in Casablanca (Morocco).


While foodborne diseases remain an important public health problem worldwide, one of the most significant food safety hazards is associated with foods of animal origin (Mead, 1994). In Morocco from 2000 to 2004, 7,118 cases of foodborne diseases were reported, among which 86% were of bacterial etiology (Cohen, Ennaji, Hassar, & Karib, 2006). According to the same references, 21.3% of the bacterial foodborne diseases were caused by the consumption of red meat and meat products, and 14.7% of cases occurred in the city of Casablanca.

Foodstuffs such as ground meat and fresh sausages are a significant portion of the diet of a large active population in Morocco. These products are highly perishable, with a pH value not lower than 5.5 and water activity ([a.sub.w]) equal to or higher than 0.97. Since no fermentation process takes place during storage at 4 [degrees]C, the hygienic quality of the raw materials is the main factor affecting the final value of the product (Casalinuovo, Cacia, Scognamiglio, & Bontempo, 2001).

In Moroccan traditions, ground meat product is made principally of beef and mutton, with or without the addition of salt, red chili, caraway, pepper, parsley, garlic, and onion, depending on local preparation and consumer order. The meat and the beef fat are ground together. The different spices and herbs are added after mixing. Fresh sausages are produced from beef and beef fat, and with or without the addition of salt, different aromas, spices, pepper, and garlic. The meat and fat are ground together in pieces, and after mixing, herbs are used to fill natural casings from sheep. The sausages are hand kneaded and stuffed without good aseptic techniques. These products are usually displayed for sale at room temperature or sometimes at refrigeration temperature. Fresh sausage products are often sold in parts displayed at ambient temperatures and are refrigerated overnight only.

Scientific experiments since the late 19th century have documented the antimicrobial properties of some spices, herbs, and their components (Mei-chin, & Wen-shen, 2002; Sara, 2004; Shelef, 1983; Zaika, 1980). Other studies have reported that spices and herbs themselves may be highly exposed to bacterial contamination, based on conditions in which they were ground and harvested. Moreover, contaminated spices have been reported to be causes of foodborne illness and spoilage (Kneifel & Berger, 1994; Pafumi, 1986).

In this paper, we describe the hygienic quality of ground beef and fresh sausages produced in Casablanca, with the following objectives: (i) to determine the prevalence and levels of pathogenic and nonpathogenic bacteria present in these products, (ii) to analyze the effect of spices and herbs; seasonality; and location distribution on the prevalence of such microorganisms, and (iii) to screen pathogenic strains of E. coli by molecular microbiology methods.


Sample Collection

Samples were collected during the period of April 2002 to March 2004. Two hundred and fifty samples of raw ground beef (n = 150) and fresh sausages (n = 100) were randomly collected from butchers (n = 84), supermarkets (n = 83), and fast-food shops (n = 83) in Casablanca, Morocco. Two sampling types of meat products were considered. Samples with spices (n = 115) were divided into ground meat (n = 71) and fresh sausages (n = 44), and samples without spices (n = 135) were divided into ground meat (n = 79) and fresh sausages (n = 56). Two sampling periods were used. The hot season (April to September) has temperatures varying between 25[degrees]C and 39[degrees]C and relative humidity between 32% and 72%. In this period, samples of ground meat (n = 75) and fresh sausages (n = 48) were collected. The cold season (November to March) has temperatures varying between 5[degrees]C and 20[degrees]C and relative humidity between 56% and 84%. In this period, samples of ground meat (n = 75) and fresh sausages (n = 52) were also collected.

At two-week intervals, approximately 200 grams of each product were collected in sterile plastic bags, labeled, kept on ice, and returned to the laboratory of Institut Pasteur du Maroc (Casablanca) within two hours. All samples were stored at 4[degrees]C upon arrival to the laboratory and processed the same day. A portion (25 g) of each sample was placed aseptically into a separate sterile stomacher bag containing 225 ml of 0.1% sterile peptone water, and homogenized with a MIX I[TM] mixer (AES Laboratory, Combourg, France). The suspension was then 10-fold serially diluted in 0.1% sterile peptone water for bacterial analyses.

Bacteriological Analysis

Viable cell counts were performed by the spread-plate method after 10-fold serial dilutions in 0.1% weight by volume (w/v) peptone solution as follows:

* Aerobic plate counts (APCs) were carried out on plate count agar and incubated at 30[degrees]C for 72 hours.

* Fecal coliforms (FC) counts were carried out on Violet Red Bile Lactose agar incubated at 44[degrees]C for 24 hours. Typical colonies were considered as round, red-to-pink, 0.5-2 mm in diameter, and surrounded with a red-to-pink halo.

* E. coli counts were carried out on RAPID'E. coli agar incubated at 37[degrees]C for 18 to 24 hours. Typical E. coli colonies were considered as violet-to-pink. Presumptive E.coli colonies were checked for Gram and were characterized by using Kligler test, then typical colonies (Gram-negative bacilli, lactose-positive, glucose-positive, and gas-positive) were confirmed by using Enterobacteriaceae API 20E, commercial kit (Biomerieux).

* S. aureus counts were carried out on Baird-Parker agar with egg yolk-potassium tellurite emulsion plates and incubated at 35[+ or -] l[degrees]C for 24 to 48 hours. Typical colonies (black surrounded by clear zones) were tested for coagulase activity using rabbit plasma after activation by overnight incubation in Brain Heart broth, at 35[degrees]C, and tested for deoxyribonuclease (DNAse) activities by using DNAse agar, and revealed by hydrochloric acid (HCl) at 2%. Presumptive colonies were confirmed by using API Staph, commercial commercial kit (Biomerieux).

* C. perfringens and other sulphite-reducing clostridia counts were carried out on tryptone-sulfite agar with Cyclocerine incubated anaerobically at 44 [+ or -] 1[degrees]C for 24 to 48 hours, followed by a confirmation on Lactose-Sulfite broth and Thioglycholate with Resazurine broth.

In addition to the above-mentioned enumerations, 25 grams of samples were analyzed for the presence or the absence of Salmonella spp. and Listeria monocytogenes using enrichment procedures. For confirmation of Salmonella, 25 grams of each of the samples were homogenized with 225 ml of 0.1% peptone water and incubated at 37[degrees]C for 24 hours. Portions of 1 ml and 0.1 ml of this pre-enrichment culture were transferred, for enrichment, to 9 ml of Muller Kauffman with added Tetrathionate broth, and to Rappaport Vassiliadis Soy Enrichment broth, respectively. Inoculated enrichment media were incubated at 37[degrees]C and 42[degrees] C, respectively. After 24 hours of incubation, a loopfull of each enrichment medium was steaked onto Xylose-Lysine-Desoxycholate agar, Edel and Kampelmarcher agar, and Hektoen agar and incubated at 35[degrees]C for another 24 hours. Presumptive colonies of Salmonella were picked from each plate and subjected individually to Kligler test. Typical colonies were then picked and confirmed using the Enterobacteriaceae API 20E, commercial kit. Salmonella isolates were serotyped using commercial antiserum according to the Kaufman and White protocol (Kauffman, 1964).

For confirmation of L. monocytogenes, a 25 gram sample was homogenized in a sterile bag with 225 ml of Half Fraser broth and incubated at 30[degrees]C for 24 h. A 1 ml portion from this pre-enrichment culture was transferred to 9 ml of enrichment broth (Complete Fraser broth, BIO-RAD), and incubated at 35[degrees]C for 24 hours. A loopful of the enrichment culture was streaked onto Palcam and Oxford agars (AES Laboratory) and incubated at 35[degrees]C for 24 to 48 hours. Typical colonies were characterized biochemically by the Listeria API commercial kit (Biomerieux).

Molecular Microbiology Analyses

The E. coli strains were characterized for virulence genes using polymerase chain reaction (PCR) and the different strains were subtyped by pulsed-field gel electrophoresis (PFGE) and Operon O PCR-RFLP (restriction fragment length polymorphism). These analyses were practiced in Centre National de Reference des E. coli et Shigella, Unite de Biodiversite des Bacteries Pathogenes Emergentes, Institut Pasteur, Paris.

One loopful of each isolated colony was grown overnight at 37[degrees]C on tryptic soy agar plates. The chromosomal DNA of the stains was extracted with the instaGene "Matrix" extraction kit (BIO-RAD) according to the manufacturer's instructions. Specific primers were used: uidA (Bej, McCarty, & Atlas, 1991), Stx (Lin, Kurazono, Yamazaki, & Takeda, 1993), eaeA (Beaudry, Zhu, Fairbrother, & Harel, 1996), LT (Osek, Gallien, Truszezynski, & Protz, 1999), EAST1 (Yamamoto & Nakazawa, 1997), ehxA (Schmidt, Scheeff, Huppertz, Frosch, & Karch, 1999), and AAF1 (Monteiro-Neto, Campos, Ferreira, Gomes, & Trabulsi, 1996). Reference E. coli strains used as controls were EDL933 (O157:H7, stx1, stx2, ehxA, eae), Ec 10-407 (EAST, LT, STIa, [beta]-glu), and Hafnia alvei (negative control). Strains using amplified products were resolved by electrophoresis in 1.7 % agarose gels in TBE buffer at 100 V for 40 minutes. The gels were stained with ethidium bromide and bands were visualized under UV light. A 100bp DNA ladder was used as a size marker (New Englands Biolabs, Beverly, Massachusetts).

The identification of O-serogroups was carried by restriction of the amplified O-antigen gene cluster (rfb-RFLP) by the method described by Coimbra and co-authors (1999).

E. coli strains were subtyped using the PFGE method. Strains were resuspended in 10x TE buffer (100mM Tris, 10mM EDTA, pH 8.0) to O[D.sub.610] nml. 1.35-1.4. DNA plugs were prepared using standard PFGE procedures (Centers for Disease Control and Prevention, 1998). BioNumerics software (Applied Maths, Kortrijk, Belgium) was used to compare the PFGE profile. The bands generated were analyzed by using the Dice coefficient and the unweighted pair group method with an optimization of 5% and a tolerance of 5%.

Data Analysis

For each organism, duplicate plates were enumerated and the means calculated. All bacterial counts were expressed as log CFU per g (log CFU [g.sup.-1]). The mean log(X) value and standard deviation (SD) were calculated on the assumption of a log normal distribution.

Data of counts from raw ground beef and fresh sausages were analyzed. Preliminary analysis of fixed effects of data from raw meat product type (ground beef and fresh sausages) was performed using the GLM procedure of SAS [R] v.82 (Statistical Analysis Systems, 2002). Data for raw ground beef and fresh sausages were separated by organism and evaluated using a 2 x 2 (meat product type x added spices); (meat product type x season); (meat product type x distribution location) factorial design. Data for ground beef and fresh sausages, individual fixed effects, and up to two-way interactions were evaluated with ANOVA using the model

y = a + [x.sub.1] + [x.sub.2] + [x.sub.1][x.sub.2]

in the GLM procedures of SAS [R] where [x.sub.1] represents type of meat product and [x.sub.2] represents spices, season, and distribution location, respectively. Least-squares measures means were separated using a protected pair wise t-test of SAS [R]. All differences were reported at a significance level of alpha = .05.


Tables 1, 2, and 3 summarize the results of microbiological enumerations of APC, fecal coliforms, E. coli, S. aureus, and C. perfringens in raw ground beef and fresh sausages at different conditions, with or without added spices, in hot or cold season, and from different distribution locations.

Microbiological Profile of Raw Ground Beef and Fresh Sausage
With and Without Spices

                      Ground Beef                Fresh Sausage

                 With Spices    Spices      With Spices  Without Spices
                   (n = 71)    (n = 79)       (n = 44)       (n = 56)

Aerobic plate   7.5 [+ or -]  7.3 [+ or -]  7.4 [+ or -]   6.8 [+ or -]
counts          0.3 (a)       0.3 (a)       0.4 (a)        0.4 (b)

Fecal           3.8 [+ or -]  3.3[+ or -]   4.1 [+ or -]   2.9 [+ or -]
coliforms       0.3 (a)       0.3 (b)       0.5 (a)        0.5 (b)

Escherichia     2.8 [+ or -]  2.4 [+ or -]  3.7 [+ or -]   2.6 [+ or -]
coli            0.4 (a)       0.4 (b)       0.5 (a)        0.5 (b)

Staphylococcus  2.5 [+ or -]  2.3 [+ or -]  2.7 [+ or -]   2.2 [+ or -]
aureus          0.3 (a)       0.3 (a)       0.3 (b)        0.3 (a)

Clostridium     1.6 [+ or -]  1.3 [+ or -]  2.0 [+ or -]   1.0 [+ or -]
perfringens     0.3 (a)       0.3 (a)       0.3 (b)        0.3 (a)

Note: Mean log CFU g-1 [+ or -] standard deviation.
(a), (b) Means in the same row with different superscript letters
are different (p < .05).


Microbiological Profile of Raw Ground Beef and Fresh Sausage in Hot and
Cold Seasons

                         Ground Beef              Fresh Sausage

                   Hot Season   Cold Season    Hot Season   Cold Season
                    (n = 75)      (n = 75)      (n = 48)      (n = 52)

Aerobic plate     7.6 [+ or -]  7.1 [+ or -]  7.6 [+ or -]  6.7 [+ or -]
counts            0.3 (a)       0.3 (b)       0.4 (a)       0.4 (b)

Fecal coliforms   3.7 [+ or -]  3.3 [+ or -]  3.7 [+ or -]  3.2 [+ or -]
                  0.3 (a)       0.3 (b)       0.5 (a)       0.5 (b)

Escherichia coli  2.8 [+ or -]  2.4 [+ or -]  3.4 [+ or -]  2.7 [+ or -]
                  0.4 (a)       0.4 (a)       0.5 (a)       0.5 (b)

Staphylococcus    2.5 [+ or -]  2.3 [+ or -]  2.4 [+ or -]  2.5 [+ or -]
aureus            0.3 (a)       0.3 (a)       0.3 (a)       0.3 (a)

Clostridium       1.5 [+ or -]  1.4 [+ or -]  1.5 [+ or -]  1.4 [+ or -]
perfringens       0.3 (a)       0.3 (a)       0.3 (a)       0.3 (a)

Note. Mean log CFU g-1 [+ or -] standard deviation.
(a), (b) Means in the same row with different superscript letters are
different (p < .05).


Microbiological Profile of Raw Ground Beef and Fresh Sausage in
Different Sampling Locations

                                    Ground Beef

                      Butcher        Supermarket       Fast-Food
                      (n = 50)         (n = 50)       Shop (n = 50)

Aerobic plate     7.3 [+ or -] 0.3  7.3 [+ or -] 0.3  7.6 [+ or -] 0.3
counts            (a)               (a)               (a)

Fecal coliforms   3.5 [+ or -] 0.4  3.3 [+ or -] 0.4  3.8 [+ or -] 0.4
                  (a)               (a)               (b)

Escherichia coli  2.5 [+ or -] 0.5  2.6 [+ or -] 0.5  2.7 [+ or -] 0.5
                  (a)               (a)               (a)

Staphylococcus    2.3 [+ or -] 0.3  2.4 [+ or -] 0.3  2.5 [+ or -] 0.3
aureus            (a)               (a)               (a)

Clostridium       1.4 [+ or -] 0.3  1.3 [+ or -] 0.3  1.7 [+ or -] 0.3
perfringens       (a)               (a)               (b)

                                    Fresh Sausage

                      Butcher        Supermarket     Fast-Food Shop
                      (n = 34)         (n = 33)         (n = 33)

Aerobic plate     7.2 [+ or -] 0.4  7.1 [+ or -] 0.4  7.3 [+ or -] 0.4
counts            (a)               (a)               (a)

Fecal coliforms   3.7 [+ or -] 0.5  3.6 [+ or -] 0.5  3.2 [+ or -] 0.5
                  (b)               (b)               (a)

Escherichia coli  3.4 [+ or -] 0.5  3.3 [+ or -] 0.5  2.8 [+ or -] 0.5
                  (b)               (b)               (a)

Staphylococcus    2.5 [+ or -] 0.3  2.7 [+ or -] 0.3  2.2 [+ or -] 0.3
aureus            (a)               (a)               (a)

Clostridium       1.5 [+ or -] 0.3  1.5 [+ or -] 0.3  1.4 [+ or -] 0.3
perfringens       (a)               (a)               (a)

Note. Mean log CFU g-1 [+ or -] standard deviation.
(a), (b) Means in the same row with different superscript letters are
different (p < .05).

From all samples tested, S. aureus was isolated in 25 (16.7%) samples of ground meat and 18 (18%) in fresh sausages. Just two strains of all strains isolated (5%) were AD-Nase (antideoxyribonuclease) positive.

In our study, from all samples tested, C. perfringens was isolated in 47 samples (18.8%), 29 in ground meat (19.3%), and 18 in fresh sausages (18%). The majority of these positive samples were associated with added spices in ground beef (26.8%), as opposed to the 12.7% for ground meat without spices. For fresh sausage samples, the occurence of C. perfringens was in 32.1% of samples with spices and in only 2.3% of samples without spices.

The statistical analysis of the data obtained revealed that the effect of the hot season and the addition of spices were significant (p < .05) on the increasing charge of APCs, fecal coliforms, and E. coli in the two types of raw meat products, whereas no sampling location effect appeared.

Salmonella was found in seven samples of the raw meat products: in three of the 150 samples of ground meat (2%) and four in 100 samples of fresh sausage (4%). All strains of Salmonella were serotyped and showed two S. enterica serovar Typhimurium, two S. enterica serovar Enteritidis, two S. enterica serovar Anatum, and one S. enterica serovar Bareilly.

L. monocytogenes was isolated in eight samples of raw red meat products: three in ground meat (2%) and five in fresh sausage (5%).

The characterization of virulence genes by PCR identified only four strains containing virulence genes. Two strains presented the LT enterotoxin gene usually found in ETEC strains (strain V7 and S26). Two other strains presented the EAST1 gene, usually found in EaggEC (strains V3 and S20). No strain was found positive for Shiga toxin genes (Stx). Concerning the serogrouping of E. coli strains by the restriction method (rfb-RFLP) and the subtyping of the different E. coli strains by PFGE, the bands generated were analyzed.


To evaluate the hygienic quality of the samples studied, our results were compared to Moroccan regulatory standards setting the microbiological safety criteria for foods, including ground meats (Moroccan Department Order, 2004). According to these regulations, the aerobic plate counts, fecal coliforms, S. aureus, and anaerobic sulfitoreductor should not exceed 5.7, 2, 2, and 1.3 log CFU [g.sup.-1], respectively, in raw ground meats to be acceptable for human consumption. In addition, Salmonella spp. and L. monocytogenes should be undetectable in a 25 gram meat product sample. For comparison purposes, the same criteria were used to assess the hygienic quality of fresh sausages despite the absence of safety criteria of these products in the present Moroccan food safety regulations.

Our previous reports have indicated that 91.6% of meat product samples tested were above prescribed microbiological safety limits. The results showed that 80.7% of ground meat and 69% of fresh sausages samples were above safety limits in terms of APCs.

In our study, E. coli had an important prevalence in fecal coliforms flora (32%). E. coli were detected in 20% of total meat product samples. The average charge of E. coli in the total samples of ground meat was higher (1.4 [+ or -] 0.6 log CFU [g.sup.-1]) than previously reported (Scanga et al., 2000).

In the previous report, the prevalence of sorbitol-negative E. coli, presumptive O157:H7, is 1.2% in all samples. In the same way, the prevalence of the presumptive E. coli O157:H7 in ground meat is 1.3%, which is in agreement with 0.3% to 1.5% (Cassin, Lammerding, Todd, Ross, & McColl, 1998), and lower than 6% (Abdul-Raouf, Ammar, & Beuchat, 1995).

In Morocco, S. aureus reportedly causes 38% of food poisoning (Cohen & Karib, 2006). Our results showed that the average amount of S. aureus in ground meat was higher than 1.1 [+ or -] 0.2 log CFU [g.sup.-1] (Scanga et al., 2000), and the occurrence of S. aureus was much higher than the 2% reported by other studies (Aymerich, Martin, Garriga, & Hugas, 2003; Vivegnis, Mairy, Jacob, Piraus, & Decallonne, 1995). Enumeration of S. aureus revealed that the count of this pathogen exceeded 5 log CFU [g.sup.-1] in eight out of the 250 analyzed samples (3.2%).

Recommended laboratory criteria used in association with clinical presentation and epidemiological evidence needed to implicate C. perfingens in foodborne disease are > [10.sup.5] vegetative cells per gram of food (Tholozan, Carlin, Fach, & Poumeyrol, 1997). In this study, two of the total samples (0.8%) could be associated with food poisoning, and the detected level was beyond the tolerable limit in 29 samples (11.6%), and almost all were in the samples with spices (96.5%).

Nontyphoidal Salmonella spp. causes an estimated 42.8% cases of foodborne illness per year in Morocco (Cohen & Karib, 2006). In this study, Salmonella occurrence is higher than that reported by Scanga and co-authors (2000).

In our study, the occurrence of L monocytogenes in raw meat products was lower than that teported by other studies: 17.6% (Aymerich, Martin, Garriga, & Hugas, 2003) and 14.4% (Kriem, El Marrakchi, & Hamama, 1998).

In our study, ETEC and EaggEC with pathogenic genes LT and EAST1, respectively, were detected in four of all E. coli isolated strains (12%). According to the serogroups, diversity of the E. coli strains analysed by restriction of the amplified O-antigen gencluster, the results of subtyping with PFGE, demonstrated differences in the profiles of almost all isolates. This is a proof of the diversity of the strains found in nature. The high similitude between strains V15 and V16 (100%); S24 and S25 (97%); V8, V9, and VI (97%); and V3 and S22 (95%) can be explained by the same animal origin of meat products isolates.


Results from this study indicated that 4% of all tested samples could be associated with food poisoning by one or more pathogenic bacteria, 0.8% for ETEC or EAggEC, 0.8 % for S. aureus ADNase positive, 0.8% of C. perfringens, 2.8% for Salmonella, and 3.2% for L. monocytogenes. Our previous reports have indicated that in general, the addition of spices and the hot season significantly increased the amount of bacterial flora in the two kinds of meat products samples that were tested. Snyder reported that the addition of spices and herbs has inhibitory effects at approximately 0.5%-0.9% of essential oil content (Snyder, 1997). The antimicrobial activity varies widely, depending on the type of spices or herbs, test media, and microorganisms (Giese, 1994), and the normal amounts added to foods for flavor is not sufficient to completely inhibit microbial growth. For these reasons, antimicrobial spices should not be considered as a preservative method, and it is urgent to promote the prohibition of spices addition in advance in ground beef and fresh sausages, and the application of such programs as hazard analysis critical control point.

Acknowledgements: The authors are grateful to all collaborators in this study, especially Dr. F. Grimont, M. Lejay-Collin, and K. le Roux from Centre National de Reference des E. coli et Shigella, Unite de Biodiversite des Bacteries Pathogenes Emergentes, Institut Pasteur Paris for their collaboration of the molecular analyses, and Dr. B. Elamiri and Dr. D. Hadarbach from the Institut National de Recherche Agronomique (INRA) in Settat for their availability and participation on the data analysis. We would like to thank the authorities of Casablanca for their help.

Corresponding Author: Nozha Cohen, Director of the Microbiology and Food Safety Laboratory, Institut Pasteur Maroc, 1 Place Louis Pasteur, Casablanca, Morocco 20100.



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Although most of the information presented in the Journal refers to situations within the United States, environmental health and protection know no boundaries. The Journal periodically runs International Perspectives to ensure that issues relevant to our international constituency, representing over 60 countries worldwide, are addressed. Our goal is to raise diverse issues of interest to all our leaders, irrespective of origin.

Nozha Cohen, D.V.M., Ph.D.

Ingrid Filliol, D.Ph., Ph.D.

Bouchra Karraouan, Ph.D.

Samira Badri, Ph.D.

Isabelle Carle, Ph.D.

Hayat Ennaji, Ph.D.

Brahim Bouchrif, Ph.D.

Mohammed Hassar, D.H.M., M.D., Pr.

Hakim Karib, D.V.M., Ph.D., Pr.
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Author:Cohen, Nozha; Filliol, Ingrid; Karraouan, Bouchra; Badri, Samira; Carle, Isabelle; Ennaji, Hayat; Bo
Publication:Journal of Environmental Health
Article Type:Report
Geographic Code:6MORO
Date:Nov 1, 2008
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