Risk factors related to bacterial contamination by Enterobacteriaceae and fecal coliforms and the prevalence of Salmonella spp. in Algerian farms, slaughterhouses and butcheries: a two-year follow-up study

AIMS Agriculture and Food, 6(3): 768–785. DOI: 10.3934/agrfood.2021046 Received: 24 April 2021 Accepted: 06 July 2021 Published: 16 July 2021 http://www.aimspress.com/journal/agriculture Research article Risk factors related to bacterial contamination by Enterobacteriaceae and fecal coliforms and the prevalence of Salmonella spp. in Algerian farms, slaughterhouses and butcheries: a two-year follow-up study Khireddine Ghougal1, Amira Leila Dib1, Nedjoua Lakhdara1, Melisa Lamri2, Sameh Baghezza3, Abdennour Azizi3, Rayane Merrad1, Ahmed Zouikri4, Daoud Cheraitia4, Messaoud Trouni4, Hichem Soualah4, Elena Moreno5, Elena Espigares5 and Mohammed Gagaoua6,* 1 GSPA Research Laboratory, Institut des sciences vétérinaires, Université Frères Mentouri, Constantine 1, 05 Route de Batna, El-Khroub, Constantine, 25000, Algeria 2 Laboratoire de Qualité et Sécurité des Aliments, Université Mouloud Mammeri, Tizi-Ouzou 15000 Algeria 3 Department of Veterinary Science, Veterinary Sciences and Agricultural Sciences Institute, University of Batna, Algeria 4 Institut des sciences vétérinaires, Université Frères Mentouri, Constantine 1, 05 Route de Batna, El-Khroub, Constantine, 25000, Algeria 5 Department of Preventive Medicine and Public Health, Faculty of pharmacy, University of Granada, Campus Universitario de Cartuja, 18071, Granada, Spain 6 Teagasc Food Research Centre, Ashtown, Dublin 15, Ireland * Correspondence: Emails: [email protected]; [email protected] Tel: +35318059948. Abstract: This study was conducted to investigate first the bacterial contamination by Enterobacteriaceae, fecal coliforms and the prevalence of Salmonella spp. and second to identify the main associated risk factors in Algerian farms, slaughterhouses and butcheries during a two-years period. Thus, a cross-sectional study was performed using a simple random sampling method to target 20 farms, 10 slaughterhouses and 5 butcheries. A structured questionnaire was further used to assess hygienic status of the farms and slaughterhouses. A total of 265 samples were collected from wall, floor, litter, food, water and animals’ samples composed mainly of meat, neck skin and liver. Samples from walls and floors, from different sites were analyzed to evaluate the overall contamination and the hygiene of sites for Total viable bacteria, Enterobacteriaceae counts and Fecal coliforms counts. Furthermore, E.coli and salmonella spp. were identified in all samples. The overall 769 AIMS Agriculture and Food Volume 6, Issue 3, 768–785. contamination by sampling sites expressed as log10 CFU/g (mean ± SD) for Total Aerobic Microbial Count, Enterobacteriaceae count and fecal coliforms counts were around 4.71 ± 1.1, 4.73 ± 1.3 and 4.68 ± 1.2 respectively. The findings evidenced that the prevalence of E.coli and Salmonella spp. were 63.40% and 18.49% respectively. The highest rate of E.coli contamination was for poultry farms (70%), beef farms (64%) and butcheries (74.54%) followed by poultry meat slaughterhouses (60%) and sheep farms (48%) while beef slaughterhouses have the lowest rate of contamination (33.84%). For salmonella spp. the contamination was found to be mainly in poultry meat slaughterhouses (31.11%), butcheries (25.45%), followed by poultry farms (22%), beef farms (20%) and sheep farms (12%) while beef slaughterhouses have the lowest rate of contamination (4.61%). This study evidenced multifactor effects of microbial contamination in farms such as animal density, litter hygiene and scraping, manure storage, water and pest control, contact with other animals and decontamination process. Overall, this trial indicated a high rate of microbial contamination for which further studies are needed to determine all the potential risk factors in order to evaluate the corrective effects. Keywords: farms; animals; abattoirs; meat safety; carcass; prevalence; Algeria; food safety 1. Introduction Algeria is believed to have the second livestock population in North Africa, with an estimated population of 1.9 million cattle, 26.4 million sheep and 4.8 million goats, with an estimated meat production of 4.7 million quintals [1]. The livestock sector contributes to about 12.3% of the national GDP in 2016, and constitutes the main source of industrial raw materials (milk, meat and skin) as well as a high source of animal proteins for consumers [1]. In Algeria, the consumption of animal products such as meat, milk and egg is rising due to rapid demographic expansion, growing rhythms of urbanization, and an obvious evolution in the consumption habits. This trend has induced a surge in the demand of animal products with emerging risks of a food dependency for the region [2]. In parallel, there may be defective processing practices at any point from the farm-to-fork chain, which increase the chances of contamination and spread of foodborne pathogens [3]. In fact, food products may become contaminated at different stages along the food chain [4], which might happen during production, processing, distribution, preparation, and/or final consumption. The risk of food getting contaminated depends largely on the health status of the food handlers, their personal hygiene, knowledge and practice of food hygiene among others [5]. According to Hoffmann et al. [6], more than 600 million persons globally, or nearly one out of ten people in the world, fall ill after consuming contaminated food in 2010. Among them, 420 000 people died, including 125 000 children under the age of 5 years and caused 33 million Disability Adjusted Life Years [6]. For example, food of animal origin can be contaminated with bacteria during food processing or slaughtering [7]. Further, these pathogens come also into contact with food during storage and packaging [4]. Foodborne pathogens are recognized as an important public health problem, and their impact on both health and economy is intensively investigated [8]. Among the bacteria that cause foodborne poisoning, some are particularly important in terms of frequency and/or of seriousness of the disease. Salmonella spp. and E. coli are the common causes of foodborne diseases and death in the world [8,9]. For example, E. coli is known as dangerous bacteria in the dairy farm 770 AIMS Agriculture and Food Volume 6, Issue 3, 768–785. sector worldwide as it causes significant economic losses [10]. There are several strains in E. coli, despite the fact that the majority of them are harmless, a few strains can cause serious foodborne infections in human [3]. More specifically and in cattle we can refer to shiga toxin-producing E. coli and enterohemorrhagic E. coli [11]. Currently, little is known about the critical points of Salmonella spp. and E. coli contamination from farm-to-fork in Algeria. The public health importance of several pathogenic enterobacteria associated with food of animal origin was highlighted in certain studies conducted in different parts of the country [12,13]. However, statistics on the hygienic status and handling practices of meat in slaughterhouses and butcheries are scarce due to poor or non-existent reporting systems. Despite the above-mentioned research, the prevalence of Salmonella spp. and E. coli and its risk factors associated has not been sufficiently studied. To the best of our knowledge, the risk factors from of Salmonella spp. and E. coli contamination particularly in farms, slaughterhouses and butcheries have never been investigated in Algeria. Thus, this study aimed to evaluate the potential risk factors favouring Salmonella spp. and E. coli contamination and to determine the contamination of food chain in the province of Oum El Bouaghi located in Eastern Algeria. 2. Materials and methods 2.1. Study area and target population Figure 1. Map showing the geographical locations of the farms, slaughterhouses, and butcheries investigated from the province of Oum El Bouaghi, Algeria. 771 AIMS Agriculture and Food Volume 6, Issue 3, 768–785. A cross-sectional study was conducted using a simple random sampling over a period time of two years from December 2017 to February 2020. A total, of 20 specialised farms (5 cattle, 5 sheep and 10 poultry), 10 slaughterhouses (with slaughtering capacity ranges from 500 to 6000 chickens per day, 10 to 80 for cattle and 45 to 1200 for sheep), 5 private butcheries were selected in the province of Oum El Bouaghi from the Eastern of Algeria (Figure 1). 2.2. Data collection at the farm and slaughterhouse levels Observation worksheets were used to collect information on management, facilities, equipment and hygienic practices at farms and slaughterhouses. A structural questionnaire was prepared and designed for farms and slaughterhouses, which contains twenty closed type questions. The questionnaire focused on live animal management, biosecurity measures, data on the farms and slaughterhouses including information of the personnel, cleaning and disinfection methods. 2.3. Sample collection A total of 265 samples including wall, floor, litter, food, water and animal samples composed mainly of meat (chicken, beef and lamb), neck skin and liver, were collected. The meat samples were collected aseptically in sterile bags, stored on ice packs and transported to the laboratory under refrigerated conditions. Poultry and livestock feed (1pool of 5g x5), litter with droppings or faeces (1pool of 5g x5), neck skin and liver (1pool of 5g x5) placed in sterile bags were further considered. In addition, wall and floor swabs were collected aseptically in sterile tubes containing 9 mL of buffered peptone water (BPW) and transported directly from the sampling location to the laboratory under refrigerated conditions using wet ice. All samples were analyzed in the same microbiological laboratory to avoid any additional effects. Table 1 shows the nature, type and method of sampling, the amount and the number of samples taken from each farm, slaughterhouses and butcheries. 2.4. Hygienic evaluation The notation of cleanliness was evaluated according to the guide of good farming practices for animal production and food safety [14]. 2.5. Microbiological analysis The standard ISO 6887:1999 designed for samples preparation, stock suspension and dilutions for microbiological examination was used in this study. Briefly, under aseptic conditions, 10 g and 25 g of beef and chicken meat samples were weighted and homogenized in a sterile blender for 2 min using 90 mL and 225 mL respectively of 0.1% BPW (pH 7.0 ± 0.2). The swabs from farms and slaughterhouses were directly seeded on surface (streaks) and in depth (count) on selective agar. All samples were tested for the different groups of bacteria consisting of Total Count Bacteria, Enterobacteriaceae counts, fecal coliforms and presence of E. coli and Salmonella. The culture methods for the detection of different organisms were based on international standards: - Bacterial counts: ISO 4833: 2003 for Total Count Bacteria, where 1 mL of each dilution (10−1, 10−2, and 10−3) of the bacterial suspension was seeded in Plate Count Agar and incubated at 30 ± 1 ℃ 772 AIMS Agriculture and Food Volume 6, Issue 3, 768–785. for 72 h ± 3 h. Following incubation, bacteria colonies on plates were counted. - Enterobacteriaceae enumeration was performed following ISO 21528-2: 2004 guidelines. Inoculation was done on Violet Red Bile Glucose agar and incubated between 18–24 h at 37 ℃. - Enumeration of thermotolerant coliforms was performed using NF V08-060. Tenfold serial dilution for each sample for up to 10−3 were prepared, seeded on VRBL and incubated at 44 ℃ for 48h. Five suspected colonies per sample were randomly isolated from VRBL and identified with an API 20E biochemical tests (BioMérieux, France). - Salmonella identification was performed using ISO 6579:2007. Briefly, 25g of samples were separately pre-enriched with 225 mL of peptone water (Condalab, Spain). All the samples were incubated at 37 ℃ for 18–24 h. From each pre-enrichment solution, 0.1 mL were transferred into 10 mL of Rappaport Soy Broth Vassiliadis (Condalab, Spain) and incubated at 42 ℃ for 18–24 h. Enriched samples were then seeded on Xylose Lysine Desoxycholate Agar (Condalab, Spain) and incubated at 37 ℃ for 18h–24 h. Red colonies with black centers were re-isolated on nutrient Broth (Condalab, Spain) for purification. Five suspected colonies per sample were randomly identified with an API 20E biochemical tests (BioMérieux, France). Table 1. Organization of sampling at the farm, slaughterhouse and butchery levels. Number and site of sampling Type of samples Type and mode of sampling Location and quantity of samples Number of samples 5 Cattle farms Floor, wall Swab Floor and wall surface 10 Litter with faeces Litter pots 1 pool of 5g x5 05 Feed Feed pots 1 pool of 5g x5 05 Water Bottle of water 250mL of water 05 5 Sheep farms Floor, wall Swab Floor and wall surface 10 Litter with faeces Litter pots 1 pool of 5g x5 05 Feed Feed pots 1 pool of 5g x5 05 Water bottle of water 250 mL of water 05 10 Poultry farms Floor, wall Swab Floor and wall surface 20 Litter with droppings Litter pots 1 pool of 5g x5 10 Feed Feed pots 1 pool of 5g x5 10 Water Bottle of water 250mL of water 10 5 Red meat slaughterhouses Floor, wall Swab Floor and wall surface 1 Water Bottle of water 250 mL of water 05 Meat Pieces 30g of carcass 50 5 Chicken meat slaughterhouses Floor, wall Swab Floor and wall surface 10 Water Bottle of water 250 mL of water 05 Neck skin Pieces 3 pools of 5x5g 15 Liver Pieces 3 pools of 5x5 g 15 5 Butcheries Red meat Pieces 30g of carcass 30 Chicken meat Pieces 30g of carcass 25 Total samples 265 773 AIMS Agriculture and Food Volume 6, Issue 3, 768–785. 2.6. Statistical analysis Data were entered into Excel spreadsheet, cleaned, and exported to Statistical Package for Social Sciences (SPSS) program version 24 (IBM, USA) for statistical analysis. Descriptive statistics like mean, frequency, and percentage were performed on different variables. Univariate analysis and logistic regression were performed to identify factors associated with bacterial contamination. Univariate analysis for binary variables consisted of either Fisher exact test or chi-square (χ2) test as appropriate at 95% Confidence Interval (CI) and a significant level of 5%. The calculation of odds ratios (OR) was performed using the method of Woolf (method of logit) with a 95% confidence interval. Fisher’s exact test was performed if n ≤ than 20 or n ≤ 5 to test the relationships between each explanatory variable and the variable “presence/absence of E. coli and Salmonella spp.” 3. Results 3.1. Characteristics of the farms and slaughterhouses and overall contamination Our survey at the farm level allowed to observe that cattle are kept in tie-stall in all the surveyed farms. From this, 60% of the floors were found to be constructed from concrete, covered with straw while the remaining were made by clay (Table 2). Moreover, 65% of the buildings and sheepfolds are old constructions. The rest of the buildings are in a deteriorated state (cracks, holes in the roof). The hygiene in the buildings and sheepfolds is often poorly controlled, with only 35% in good hygienic conditions; however, the rest vary from fair to dirty. The distribution of germs per site, collected from cattle, sheep, poultry and slaughterhouses indicated that the wall and floor are relatively contaminated (Table 3). The total means bacterial count log10CFU/cm2/was found to be 4.71 ± 1.24. These resulted in 55% of the farms with a sparse litter. On another hand, the straw generally reserved for bedding was used for animals feeding (Table 2). It is important to mention that when it exists, the litter is poorly maintained (dirty, wet litter), because of its infrequent loading and renewal (reduced scraping per day). A high number of the farms (70%) regrouped several livestock buildings with enough distance (less than 500 m from each other). In addition, 60% of the farms allow access to domestic animals (dogs and cats). Further, the equipment is limited to the strict minimum (feeder and drinker) and the ventilation system was found to be static in all farms. In 70% of the farms, the storage of manure and feed was mainly performed inside the farm. The questionnaire allowed gathering information on the rearing practices applied by the farmers. In general, 70% of the farms use water from wells, which are not strictly controlled. Only 75 % of the farms surveyed are rat free (Table 2). The poultry have several origins and came namely from Oum El Bouaghi, Constantine and Batna. The hygienic control is ensured by the veterinary inspection of each province. Additionally, 60% of the slaughterhouses have walls lined with earthenware, with a satisfactory state of covering and a correct and non-slip concrete floor. Compared to cattle and sheep meat slaughterhouses, the chicken ones were in very poor conditions. The overall contamination for Total Aerobic Microbial Count, Enterobacteriaceae count and fecal coliforms counts were around 4.71 ± 1.1, 4.73 ± 1.3 and 4.68 ± 1.2 respectively (Table 3). 774 AIMS Agriculture and Food Volume 6, Issue 3, 768–785. Table 2. Characteristics of the farms visited and percentages of presence of salmonella spp. and E. coli strains. Parameters Characteristic Percentage of E. coli Percentage of Salmonella spp. Animal density Law 40 40 High 60 60 Building Old 70 70 New 30 30 General building hygiene Poor 75 75 Good 25 25 Litter Sparse 55 55 Exists 45 45 Scraping frequency One time 65 65 More than one time 35 35 Floor type Concrete 65 65 Clay 35 35 Storage of manure Indoors 70 70 Outdoors 30 30 Food storage Indoors 50 50 Outdoors 50 50 Water control Yes 30 30 No 70 70 Contact with other pets Yes 60 60 No 40 40 De-worming Yes 25 25 No 75 75 Diarrhea Yes 75 75 No 25 25 Pica Yes 50 50 No 50 50 Pest control Yes 75 75 No 25 25 Decontamination Yes 25 25 No 75 75 Table 3. Evaluation of the overall contamination by sampling sites expressed as log10 CFU/g. Flora Farms Slaughterhouses Cattle and sheep Poultry Red meat Chicken meat Wall Floor Wall Floor Wall Floor Wall Floor A 4.68 ± 1.08 4.74 ± 1.4 4.62 ± 0.8 4.74 ± 1.4 4.71 ± 1.2 4.74 ± 1.4 4.74 ± 1.4 4.69 ± 1.09 B 4.72 ± 1.02 4.74 ± 1.3 4.74 ± 1.3 4.74 ± 1.3 4.71 ± 1.2 4.74 ± 1.3 4.74 ± 1.3 4.71 ± 1.2 C 4.60 ± 1.08 4.64 ± 1.2 4.73 ± 1.4 4.58 ± 1.4 4.71 ± 1.3 4.74 ± 1.3 4.72 ± 1.4 4.71 ± 1.2 Flora A: Total Aerobic Microbial Count; Flora B: Enterobacteriaceae count; Flora C: Fecal Coliforms counts. 775 AIMS Agriculture and Food Volume 6, Issue 3, 768–785. 3.2. Prevalence of E. coli and Salmonella spp. The results showed that the prevalence for E. coli was 44.90% (119) for and 18.49% (49) for Salmonella spp. in the 235 collected samples (Table 4). Table 4. Characteristics of the farms visited and percentages of Salmonella spp. and E.coli strains. Sampling site Number of samples E. coli (%) Salmonella spp. (%/) Cattle farms 25 64 (16) 20 (4) Sheep farms 25 36 (09) 12 (3) Poultry farms 50 70 (35) 22 (11) Red meat slaughterhouses 65 29.23 (19) 4.61 (3) Chicken meat slaughterhouses 45 28.88 (13) 31.11(14) Butcheries 55 67.27 (27) 25.45 (14) Total 265 44.9 (119) 18.49 (49) 3.2.1. At the farm level Contamination by Salmonella spp. was found on the walls (20%), in litter (20%) and in feed (20%) of the cattle farms. Interesting to note that no positive samples were observed at the sheep farms neither in wall and floor nor in water samples. Only feed (40%) and litter (20%) were contaminated. Contaminations at the poultry farms by Salmonella spp. of 40%, 10%, 20%, 30% and 10% were identified on walls, floors, litter, feed and water, respectively (Table 5). The highest presence of E. coli was observed at the poultry farms, mainly on the floors and feed (100%), litters (80%), walls (50%) and water (20 %). The presence of E. coli at sheep farms was 80 % on feed, 100 % on litter and no positive samples on walls, floors and water. The percentage of E. coli at cattle farms was 60% in walls and floors, and 100% in feed and litter and no positive samples in water (Table 5). 3.2.2. At the slaughterhouse level The percentage of E. coli in red meat slaughterhouses was 29.23%. The contamination was found to be mainly in walls (100%), beef samples (80%), sheep samples (80%) and floors (60%). Therefore, the prevalence of Salmonella spp. in red meat slaughterhouses was weak to be around 4.61% that is observed most frequently in samples of beef meat (40%) and sheep meat (20%). However, at the slaughterhouse level no positive samples to Salmonella spp. were found from walls and floors. In the chicken meat slaughterhouses, the contamination by E. coli and Salmonella spp. was 28.88% and 31.11%, respectively. The contamination by E. coli was found in walls (100%), floors (60%), water (40%), liver and neck skin (6.66%) samples, respectively. Salmonella spp. were mainly isolated from neck skin (60%), liver (33.33%), walls, water and floors (40%) (Table 5). 3.2.3. At the butcheries level The rates of samples contaminated by E. coli and salmonella spp. were 67.27% and 61.81%, respectively. The presence of E. coli in beef meat, sheep meat and chicken meat were 86.66%, 13.33% and 46.66%, respectively. In addition, 46.66% of the sheep meat and 28% of the chicken meat samples 776 AIMS Agriculture and Food Volume 6, Issue 3, 768–785. were contaminated with Salmonella spp. However, Salmonella spp. was not isolated from the beef samples (Table 5). 3.3. Univariate analyses to investigate the risk factors To identify risk factors that predict Salmonella spp. and E. coli contamination at the farms and slaughterhouses levels, univariate analyses were performed to assess the relationships between the outcome variable and each explanatory variable. The relations were expressed based on “odds ratio” (OR) and P-values. The results of the univariate analysis of the association between the explanatory variables and the variable (Salmonella spp.and E. coli status: absence/presence) are summarized in Table 6. Table 5. Prevalence of Salmonella spp. and E. coli by sampling sites. Type of sampling Prevalence (%) E. coli Salmonella spp. Cattle farms Wall (3) 60 (1) 20 Floor (3) 60 (1) 20 Litter (5) 100 (1) 20 Feed (5) 100 (1) 20 Water (0) 00 (0) 00 Sheep farms Wall (0) 00 (0) 00 Floor (0) 00 (0) 00 Litter (4) 80 (1) 20 Feed (5) 100 (2) 40 Water (0) 00 (0) 00 Poultry farms Wall (5) 50 (4) 40 Floor (10) 100 (1) 10 Litter (8) 80 (2) 20 Feed (10) 100 (3) 30 Water (2) 20 (1) 10 Red meat slaughterhouses Wall (5) 100 (0) 00 Floor (3) 60 (0) 00 Beef meat (4) 80 (2) 40 Sheep meat (4) 80 (1) 20 Water (3) 60 (0) 00 Chicken meat slaughterhouses Wall (5) 100 (2) 40 Floor (3) 60 (2) 40 Water (2) 40 (2) 40 Neck skin (2) 40 (3) 60 Liver (1) 6.66 (5) 33.33 Butcheries Beef meat (13) 86.66 (0) 00 Sheep meat (2) 13.33 (7) 46.66 Poultry meat (12) 48 (7) 28 783 AIMS Agriculture and Food Volume 6, Issue 3, 768–785. 4. Hemalata V, Virupakshaiah D (2016) Isolation and identification of food borne pathogens from spoiled food samples. Int J Curr Microbiol Appl Sci 5: 1017–1025. 5. 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