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J APPL POULT RES 2007. 16:502-508. doi:10.3382/japr.2006-00061
© 2007 Poultry Science Association
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Research Reports

Comparative Study of Microbiological Quality of Raw Poultry Meat at Various Seasons and for Different Slaughtering Processes in Casablanca (Morocco)

N. Cohen*,1, H. Ennaji*, B. Bouchrif*, M. Hassar* and H. Karib{dagger}

* Laboratoire de Microbiologie et d’Hygiène des Aliments et de l’Environnement Institut Pasteur du Maroc, 1 Place Louis Pasteur, Casablanca 20100, Morocco; and {dagger} Département Hygiène et Industrie des Denrées Alimentaires d’Origine Animale, Institut Hassan II d’Agronomie et de Médecine Vétérinaire, B.P. 6202-Madinat Al Irfane, Rabat 10101, Morocco

Correspondence: 1 Corresponding author: nozha.cohen{at}pasteur.ma


   SUMMARY
TOP
 SUMMARY
DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
The aim of the present study was to evaluate the bacterial quality of chicken (n = 96) and turkey (n = 96) marketed in Casablanca, Morocco. Poultry samples (n = 192) were collected randomly from traditional shops and supermarkets during 2 sampling periods (hot and cold seasons). The samples were analyzed for the presence and counts of various bacteria. Results indicated that aerobic plate counts and fecal coliforms were particularly high in all the samples analyzed. Escherichia coli, coagulase-positive Staphylococcus, Clostridium perfringens, Salmonella, and Listeria monocytogenes were detected, respectively, in 48.4, 10.4, 7.2, 1.6, and 0.5% of the poultry meat samples. The chicken and turkey samples contained, respectively, 25 and 33.3% of bacteria above the maximum limits established by the Moroccan regulatory standards. The highest bacterial counts in poultry meat product samples were recorded with the traditional slaughtering process during the hot season (P < 0.05). These high levels of microbial contamination and occurrence of pathogenic bacteria reflect the poor hygienic quality of poultry meat under these conditions.

Key Words: bacterial quality • chicken • turkey • slaughtering process • season


   DESCRIPTION OF PROBLEM
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
It is well documented that contamination of food with pathogens is a major public health concern worldwide [1]. Because of the relatively high frequency of contamination of poultry with pathogenic bacteria, raw poultry products are reported to be responsible for a significant number of cases of human food poisoning [2]. In the absence of hygienic conditions, the birds may be highly exposed to bacterial pathogens such as Listeria monocytogenes, Campylobacter, and other enteric bacteria [3]. In Morocco, Salmonella, Staphylococcus aureus, and Clostridium perfringens are reported to cause 42.8, 37, and 1.7% of food poisoning, respectively [4]. However, care is recommended in considering these numbers, because the incidence of foodborne diseases is underestimated, the number of viral gastroenteritidis has been inferred based on exclusion diagnostics, and there are no references on human listeriosis and campylobacteriosis [5].

Poultry meat contributes substantially to the human diet [6]. In Morocco, poultry meat is an important, low-cost source of animal protein. This encourages the consumption of poultry products by a large number of consumers. Poultry meat is increasingly used by the growing rural and urban populations. In 2004 the population of Casablanca alone consumed 338,000 tons, which represented 12.5% of total poultry meat consumption in Morocco [7].

Two kinds of poultry slaughtering are used in Morocco. One is an automated poultry slaughtering process established recently, whereby automated systems are used for scalding, plucking, eviscerating, rinsing, and packaging carcasses. Carcasses are then stored at 4°C before sale to supermarkets. The second is traditional slaughtering, which is commonly practiced in shops under poor hygienic conditions. More than 90% of poultry slaughtering in Morocco is done by traditional procedures [8]. In these shops the conditions are favorable for potential contamination by pathogens, which may originate from the animal itself and from environment factors (water, litter, air). Thus, controlling microbial contamination in poultry meat during slaughtering, processing, storage, handling, and preparation becomes a great challenge [9, 10, 11]. In the traditional shops, the broiler is slaughtered and scalded in hot water. After that, the carcasses are plucked and eviscerated mostly by hand. Before and after evisceration, broiler carcasses are subjected to washing and other operations, which may disseminate bacteria from localized sites to the rest of the carcass, as well as among carcasses. All parts of the broiler carcass may then be similarly contaminated. The trussed broiler is then displayed on the shelf, waiting to be sold. This kind of poultry is often sold in parts and the selling can take time, during which the carcasses are displayed at ambient temperatures during the day and put in the refrigerator for the night [12, 13]. Moreover, the storage temperature to which the carcasses are exposed may favor the proliferation of pathogenic bacteria for humans [11].

The main studies performed on chickens and turkeys have focused on evaluating their hygienic quality [12, 13, 14]. None of these studies has assessed the hygienic quality of raw poultry meat produced during various seasons and by different slaughtering processes. The objectives of the present studies were 1) to determine the occurrence and levels of pathogenic and non-pathogenic microorganisms present in chickens and turkeys produced in Casablanca, Morocco, and 2) to examine the effects of the hot and cold seasons and slaughtering processes on the incidence of such microorganisms.


   MATERIALS AND METHODS
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
Samples
Samples were collected between April 2002 and March 2004. A total of 192 poultry samples [chicken (n = 96) and turkey (n = 96)] were randomly collected in Casablanca, Morocco. Ninety-six samples were collected from 24 traditional shops, where the traditional slaughtering process is practiced, and from 24 supermarkets, with poultry from industrialized slaughterhouses. One sampling period was during the hot season (April to September), with temperatures varying from 25 to 39°C and RH between 32 and 72%. Turkey (n = 46) and chicken (n = 46) samples were collected during this period. A second sampling period was during the cold season (November to March), with temperatures varying from 5 to 20°C and RH between 56 and 84%. Samples of both turkey (n = 50) and chicken (n = 50) were collected.

At 2-wk intervals, approximately 200 g of whole muscle with neck skin were aseptically collected from the breastbone of poultry carcasses. All samples were sent to the laboratory in sterile bags at 4°C within ≤2 h. A portion (25 g) of each sample was placed into a separate sterile Stomacher bag with 225 mL of 0.1% sterile peptone water, and then pummeled with a Mix I mixer [15]. Samples were subsequently serially diluted in 0.1% sterile peptone water for bacterial analyses.

Bacteriological Analysis
The following viable cell counts were performed by the spread-plate method after 10-fold serial dilutions in 0.1% (wt/vol) peptone solution: 1) aerobic total counts on Bio-Rad plate count agar [16], 2) fecal coliform counts on Bio-Rad violet red bile lactose agar [17], 3) Escherichia coli counts, on Bio-Rad RAPID’E. coli agar, incubated at 37°C for 18 to 24 h (typical E. coli colonies were considered violet to pink), 4) Staph. aureus, on Bio-Rad Baird-Parker agar [18], and 5) C. perfringens and other sulfite-reducing clostridia on Bio-Rad tryptone-sulfite agar [19].

In addition to the above-mentioned counts, 25-g samples were analyzed for 1) the presence or absence of Salmonella spp. [20], and presumptive Salmonella isolates were serotyped by using commercial antiserum according to the Kauffman protocol [21], and for 2) the confirmation of L. monocytogenes by using enrichment procedures [22].

Data Analysis
The means were calculated for each organism from duplicate plate counts. All bacterial counts were expressed as log10 colony-forming units per gram (log10 cfu/g). The mean log10 (x) value and SD were calculated on the assumption of a log normal distribution. Data from chicken and turkey counts were analyzed separately. Preliminary analysis of fixed effects for data from chickens and turkeys using the GLM procedure of SAS [23] indicated that the bacterial populations were dependent on the season and slaughtering process. Data for chickens and turkeys were separated by organism and evaluated by using a 2 x 2 (distribution location x season, respectively) factorial design. For chickens and turkeys, individual fixed effect and 1-and 2-way interactions were evaluated with ANOVA by using the model


Formula

in the GLM procedure of SAS, where x1 represents the slaughtering process and x2 represents the season. Least squares means were separated by using the protected pairwise t-test of SAS. All differences were reported at a significance level of {alpha} = 0.05.


   RESULTS AND DISCUSSION
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
General Remarks
Bacteriological profiles of chickens and turkeys are reported in Tables 1Go and 2Go, respectively. Salmonella, L. monocytogenes, Staph. aureus, and C. perfringens are known to be important food safety hazards associated with raw poultry meat products [1]. Morocco has one legislative microbiological safety criterion for foods, including raw poultry meats [24]. For fresh poultry meat, acceptable upper limits are 6.7 log10 cfu/g for aerobic plate counts (APC), 4 log10 cfu/g for fecal coliforms, 3.7 log10 cfu/g for Staph. aureus, and 2.5 log10 cfu/g for C. perfringens. In addition, according to Moroccan regulations, Salmonella and L. monocytogenes should be undetectable in a 25-g poultry meat sample. There are, however, no safety criteria concerning E. coli in the Moroccan standard regulations. Therefore, for purposes of comparison, reference is made to other studies of this microorganism [13, 14].


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  		Table 1. Microbiological profile of chicken meat (mean log10 cfu/g ± SD)
 

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  		Table 2. Microbiological profile of turkey meat (mean log10 cfu/g ± SD)
 
APC
Aerobic plate counts are a widely accepted measure of the general degree of microbial contamination and the hygienic conditions of processing plants [24]. In our study, the mean APC in chicken meat collected in both traditional shops and supermarkets was below the value reported by Amara et al. (6.56 to 7.15 log10 cfu/g) [12]. However, the numbers were higher than those of Oumokhtar [14], who found a mean APC value of 4.46 log10 cfu/g. Our study results also showed that 29.2% of the total tested samples were beyond the safety limit in terms of APC [24]. The majority of these samples were recorded in the hot season, with 36 (18.8%) for traditional shops and 8 (4.2%) for supermarket samples. In the cold season, only 11 (5.7%) samples were beyond the safety limit and were found in traditional shops; none was recorded in supermarkets.

Fecal Coliforms and E. coli
In the current study, mean fecal coliform counts were higher than those reported by Oumokhtar [14], who found a mean coliform count of 2.08 log10 cfu/g, and were in accordance with that reported by Aymar [13] for chicken collected in the slaughterhouse at Rabat. On the other hand, the results obtained for fecal coliform counts in chickens were lower than those reported by Amara et al. (5.78 log10 cfu/g) [12].

Our results also showed that 22.4% of the total tested samples were beyond the safety limit in terms of fecal coliforms [24]. The majority of these samples were recorded in the hot season, with 26 (13.5%) from traditional shops and 11 (5.7%) from supermarket samples. In the cold season, only 6 (3.1%) samples were beyond the safety limit and were found in traditional shops; none was recorded in supermarkets.

Of all the samples analyzed, 93 (48.4%) tested positive for E. coli, 51 (52%) samples of turkey and 42 (43%) samples of chicken. This study showed that the mean value for E. coli in chicken samples collected in traditional shops was lower than the 3.1 log10 cfu/g reported by Aymar [13].

Staph. Aureus
In Morocco, Staph. aureus has been reported to cause 37% of food poisoning [25]. In the present study, the pathogen was isolated from 20 (10.4%) of the 192 poultry meat samples, 14 (7.3%) during the hot season and 6 (3.1%) during the cold season. The average count of Staph. aureus in poultry meat was below the number (5.36 log10 cfu/g) reported by Amara et al. [12]. Enumeration of Staph. aureus revealed that the pathogen count exceeded 5 log10 cfu/g in 12 of the 192 samples analyzed (6.2%). The reason for the high prevalence of Staph. aureus could have been the poor personal hygiene of the workers and the technique used for opening the abdomen. With the technique of hand evisceration predominantly practiced in the traditional shops under study and with infrequent hand washing, a high prevalence of bacteria related to human contact was expected in these samples. Such a high level of contamination with Staph. aureus has been associated with increased risk of staphylococcal food poisoning [26]. The primary factor contributing to staphylococcal food poisoning outbreaks is inadequate control of cold temperatures, with the initial contamination often being traced to poor personal hygiene by food handlers. Most Staph. aureus strains isolated from processed poultry in plants and farms produced staphylococcal enterotoxin D, whereas only a small number produced staphylococcal enterotoxin A. Staphylococcal enterotoxins are noted for their heat resistance, and typically they cannot be inactivated by the normal heat processing of food [27].

C. perfringens
Clostridium perfringens is one of the most widespread of all pathogenic bacteria in the environment and is commonly found (although in low numbers) in the gastrointestinal tract of healthy animals, from where it generally contaminates animal carcasses during slaughtering [28]. In the current study, the mean values for C. perfringens were beyond the tolerable limit [24] in only 3 samples (1.6%). This result is in agreement with that reported by Wen and McClane [29], (i.e., 2%), and the contamination level is similar to those reported by Amara et al. [12].

A correlation analysis among the 5 groups of microorganisms, namely, APC, fecal coliforms, E. coli, Staph. aureus, and C. perfringens, indicated high correlations between fecal coliforms and E. coli (r = 0.89, P < 0.05) and between APC and fecal coliforms (r = 0.71, P < 0.05). The high correlation between APC and fecal coliforms reflected the poor sanitary conditions of slaughtering, handling, and storage, and the high correlation between fecal coliforms and E. coli can be explained by the carcasses being contaminated with Enterobacteriaceae from the intestinal contents and by the same growing conditions for the 2 groups of bacteria.

During the hot season, the majority of samples were beyond the safety limits for all counted bacteria. The statistical analysis showed that the season and the slaughtering process had highly significant effects (P < 0.05). This may be due to poor hygienic conditions, contamination with Enterobacteriaceae from the intestinal contents, and inadequate temperature during slaughtering and storage, especially in the traditional shops. In these shops, the sanitary practices in the processing environments studied showed that certain conditions, especially the high ambient temperature in Morocco (18 to 30°C), were favorable for microbial contamination, indicating potential health hazards related to enteropathogens.

Salmonella
In this study, the prevalence of Salmonella was 1.56%. Salmonella was found in 1 sample of turkey meat (1%) and was serotyped as S. enterica serovar Hadar. This pathogen contaminated 2 samples of chicken meat (2.1%), and the serotypes were S. enterica serovar Anatum. The prevalence of Salmonella in chicken in the present study was higher than that reported by Amara et al. [12], which ranged from 0%, and was lower than the finding reported by Oumokhtar (i.e., 3.12%) [14]. Differences among the results of 3 Moroccan studies (Amara et al. [12], Oumokhtar [14], and the present study) and that reported by Swanenburg et al. [30] (i.e., 10.9 to 25%) can partly be explained by differences among countries in terms of poultry densities, environmental temperatures, husbandry technologies, and slaughtering processes.

In our study, the prevalence of Salmonella spp. was low. However, the health hazard from Salmonella must not be underestimated, as shown by the enumeration of microbial indicators of fecal contamination. The fact that Salmonella was also detected in samples from the supermarkets, where chicken are displayed under refrigeration, shows that the spread of infection is not only confined to seemingly unhygienic environments [31], but also that the animal itself may be initially contaminated [11].

L. monocytogenes
From all the samples of chicken meat analyzed in this study, L. monocytogenes was found in only 1 sample (0.5%). This is an appropriate indicator of the behavior of cold-tolerant pathogens in meat [32]. Its prevalence was lower than those (10 to 16% and 48.2%) reported by Uyttendaele et al. [33] and Gudbjörnsdottir et al. [34], respectively. One retrospective case-control study undertaken in 6 states in the United States suggested that approximately 20% of the 1,600 annual cases of L. monocytogenes were likely to have resulted from consuming undercooked hot dogs and undercooked chicken [35]. Actually, in Morocco, as in other countries, newer attitudes toward eating undercooked poultry meat are being acquired, which may increase the prevalence of L. monocytogenes. The incidence of human listeriosis in Morocco is low, and there is no evidence implicating poultry as a vehicle for this pathogen in the reported cases [24]. Although studies concerning the prevalence of L. monocytogenes in poultry meat are not available in Morocco, some studies have reported a 14.4% overall incidence of L. monocytogenes in red meat and meat product samples [36].


   CONCLUSIONS AND APPLICATIONS
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
REFERENCES AND NOTES
 

  1. Bacterial counts in 29.2% of all tested samples were beyond the Moroccan safety limits.
  2. The traditional slaughtering process and the hot season resulted in significantly increased incidences of bacterial flora.
  3. Fifteen percent of all poultry meat samples could be associated with food contamination by 1 or more pathogenic bacteria.
  4. Slaughterers need assistance in improving the quality of the products supplied to the consumer and in developing an appropriate Hazard Analysis Critical Control Point system as a means of identifying and controlling the hazards in poultry products, and to enhance food safety.


   ACKNOWLEDGMENTS
 
The authors are grateful to all collaborators in this study, especially B. Elamiri and D. Hadarbach from the Institut National de Recherche Agronomique (INRA) in Settat for their availability and participation in the data analysis. The authors also would like to thank the authorities of Casablanca for their help.


   REFERENCES AND NOTES
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 

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  14. Oumokhtar, B. 2000. Qualitébactériologique de viandes, d’abats, de préparations carnées et d’huîtres commercialisées à Rabat. Thése de Doctorat National, Université Chouaib Doukkali, Faculté des Sciences, El Jadida, Morocco.
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  20. NM 08.0.103 correspondante à la norme ISO 6579/2001: Directives générales concernant les méthodes de recherche des Salmonella. Service de normalisation Industrielle Marocaine (SNIMA), 2002. Broth and agar; Bio-Rad, Marnes la Coquette, France.
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