Food Poisoning Microorganisms in Chicken Broiler Meat

Global Veterinaria 14 (2): 211-218, 2015 ISSN 1992-6197 © IDOSI Publications, 2015 DOI: 10.5829/idosi.gv.2015.14.02.9319 Food Poisoning Microorganisms in Chicken Broiler Meat 1 1 F.A. Khalafalla, 1N.S. Abdel-Atty, 2Soad A. Abdel-Wanis and 3Adel S. Hanafy Department of Food Hygiene and Control, Faculty of Veterinary Medicine, Beni Suef University, Egypt 2 Reference Lab for Veterinary Quality Control on Poultry Production, Animal Health Research Institute, Dokki, Egypt 3 Animal Health Research Institute, Fayoum Branch, Egypt Abstract: This study was carried out to investigate the prevalence of food poisoning microorganisms in chicken broilers in Fayoum city. Results showed that the mean count of coliforms (MPN), faecal coliforms (MPN), Escherichia coli (E.coli) (MPN) and Staphylococcus aureus (staph.aureus) count in fresh neck skin, breast skin, thigh skin, breast muscle and thigh muscle of chicken broiler samples was high when compared with frozen samples. There was a significant difference between fresh and frozen skin and muscle samples at P<0.01 in relation to coliforms count. There was a significant difference between fresh and frozen skin samples while there was no significant difference between fresh and frozen muscle samples at P<0.01 in relation to faecal coliforms count. Also there was a significant difference between fresh and frozen skin and muscle samples of chicken broilers at P<0.01 in relation to E.coli count. All the examined sites of fresh chicken broilers yield E.coli with total percentage was 100% while in frozen samples E.coli was isolated by 100%, 86.6%, 100%, 73.3% and 86.6% from neck skin, breast skin, thigh skin, breast muscle and thigh muscles respectively. On the other hand there was a significant difference between fresh and frozen skin and muscle samples at P< 0.01 in relation to staph.aureus count. Staph.aureus was isolated from 46.6%, 26.6%, 40%, 20% and 26.6% from neck skin, breast skin, thigh skin, breast muscle and thigh muscles respectively while in frozen samples it was isolated from 26.6%, 26.6%, 33.3%, 20% and 26.6% from neck skin, breast skin, thigh skin, breast muscle and thigh muscles respectively. Salmonella spp. were isolated from22.6%, 13.3%, 20%, 20% and 33.3% of neck skin, breast skin, thigh skin, breast muscle and thigh muscle, respectively with total percentage 22.6% of fresh chicken broiler samples while in frozen samples it was isolated from 13.3%, 13.3%, 6.6%, 6.6% and 6.6% of neck skin, breast skin, thigh skin, breast muscle and thigh muscle, respectively with total percentage 9.3%. The isolated serotypes were Salmonella infantis (S. infantis) and Salmonella enteritidis (S. enteritidis). Campylobacter jejuni was isolated from 80%, 73.3% and 66.6% of neck skin, breast skin and thigh skin, respectively with total percentage 44% in fresh chicken broiler samples while it was isolated from 33.3%, 46.6% and 53.3% of neck skin, breast skin and thigh skin, respectively with total percentage 26.6% from frozen samples of chicken broilers while it failed to be detected in muscle samples. Public health importance of the isolated bacteria and possible sources of chicken broiler meat contamination were discussed. Key words: Food poisoning Poultry meat Coliforms Salmonella Staph aureus Campylobacter jejuni entering slaughter processing are highly contaminated by microorganisms, including food borne pathogens such as Salmonella and Campylobacter spp. and these pathogens tend to be disseminated in the processing plant during processing [2]. Epidemiological reports suggest that poultry meat is still the primary cause of human food poisoning [3]. The presence of pathogenic and spoilage microorganisms in poultry meat and its by-products remains a significant concern for suppliers, INTRODUCTION Meat of chicken broilers are more popular to the consumers because of it's easy digestibility and acceptance by the majority of people, although it could be contaminated with a variety of potentially pathogenic food borne pathogens that may cause human illness such as Salmonella, Campylobacter, Staphylococcus aureus, Escherichia coli and Listeria [1]. Chicken broilers Corresponding Author: Adel Samir Hanafy, Animal Health Research Institute, Fayoum Branch. E-mail : Vet_adel2010@yahoo.com 211 Global Veterinaria, 14 (2): 211-218, 2015 consumers and public health officials worldwide [4]. Outbreaks of food borne illness occur following ingestion of undercooked meat, handling of raw meat, cross contamination of ready-to-eat products with microbial contaminants from the raw poultry or others introduced during preparation of food [5]. Poultry and poultry products are frequently contaminated with Salmonellae that can be transmitted to humans either through the handling of raw poultry carcasses and products or through consumption of undercooked poultry meat [6]. Because salmonella typically is found in poultry, this type of meat has been an important vehicle in food borne diseases rendering Salmonellosis is one of the most frequently reported food borne diseases worldwide [7]. Campylobacteriosis in man is mainly a food borne infection in which foods of animal origin, particularly poultry, play an important role. In the last 10 years Campylobacter jejuni has emerged as the most frequent cause of bacterial gastroenteritis in man in United States and reported as the most common bacterial cause of food borne infection [8]. Coliforms level, Mesophiles, psychrotrophs, Escherichia coli and Staphylococcus aureus in poultry carcasses can be routinely used to assess microbiological safety, improper hygiene methods and sanitation conditions during processing, keeping quality of products and incorrect storage conditions which can lead to the proliferation of pathogens [9]. Therefore the aim of this study was to investigate the prevalence of food poisoning microorganisms in chicken broiler meat as well as discuss the public health importance of the isolated microorganisms. Ten grams from all samples were aseptically removed and stomached in a sterile stomacher bag containing 90 ml of sterile peptone water (Oxoid CM0009 Ltd., Hampshire, England) for 2 min. this represent the original food homogenate from which ten-fold serial dilutions were prepared using the same diluents. The prepared samples were subjected to the following examination: Bacterial Count: By using the technique recommended by APHA [11]: Coliforms Most Probable Number (MPN): by using the 3 tubes protocol, faecal coliforms most probable number (MPN), E.coli most probable number (MPN) and staph aureus count. Bacterial Isolation: salmonella isolation according to ISO 6579:2002 [12], E.coli isolation according to APHA [11], staph.aureus isolation according to APHA [11] and campylobacter isolation according to ISO 10272-1: 2006 [13]. Statistical Analyses: analysis of variance was conducted and means were compared according to Knapp and Miller [14]. RESULTS AND DISCUSSION Results obtained in tables (1,2) showed that there was a significant difference between fresh and frozen skin and muscle samples at P<0.01 in relation to coliforms count. Nearly similar result was reported by Northcutt et al. [15] while higher value was recorded by Bhandari et al. [16] on the other hand lower coliform counts were reported by Buhr et al. [17] in breast skin, Abu-Ruwaida et al. [18] in neck skin, Gad [19] in breast and thigh muscles of chickens also Daoud et al. [20] in frozen chicken breast and thigh muscles. Higher coliforms count may be attributed to the fact that live birds and animals are hosts to a large number of different microorganisms residing on their skin, feathers or in the alimentary tract. Birds admitted to slaughtering generally highly contaminated with bacteria, especially with potential human pathogenic bacteria, such as Coliforms. During slaughter most of these microorganisms are eliminated, but subsequent contamination is possible at any stage of the production process, from feather plucking, evisceration and washing to storage by cooling or freezing also microorganisms from the environment, equipment and operator’s hands can contaminate meat this agreed with Kotula and Pandya [21] and Geornaras et al. [22]. MATERIALS AND METHODS Samples Collection: A total of 30 carcasses from chicken broiler (15 fresh and 15 frozen) were purchased from different grocery stores and poultry shops in Fayoum city. Each carcass was wrapped in a sterile polyethylene bag and identified. The collected carcasses were immediately transported to laboratory in ice box and examined up on arrival. Frozen samples were allowed to thaw in their original containers in the refrigerator for 8-10 hours. Sample Preparation: Skin and muscle samples from fresh and frozen chicken broiler carcasses were prepared. Skin samples include neck, breast and thigh skin while muscle samples include breast muscle and thigh muscle. All samples were prepared according to the technique recommended by ICMSF [10] as follows: 212 Global Veterinaria, 14 (2): 211-218, 2015 Table 1: Statistical analysis of the bacterial count of fresh and frozen skin of chicken broilers Coliforms MPN Faecal coliforms MPN E.coli MPN Staph aureus count Fresh --------------------------------------------------------------------Neck skin Breast skin Thigh skin Frozen -----------------------------------------------------------------Neck skin Breast skin Thigh skin 2×105 a±7×104 4×104 a±9×103 9×103 a±4×103 5×105 a±8×104 5.6×103 b±3×103 1.5×103 a±6×102 6×102 a±1.6×102 105 b±4×104 6×104 a,b±104 2.6×104 a±3×103 104 a±2×103 4×105 a±5×104 2×105 a± 4×104 8×104 b ± 2×104 3×104 b± 8×103 5×105 a ± 4×104 103 b±4×10 2 7×10 2 a±2×10 2 4×102 a± 16×10 2 105 b±3×104 3.5×10 4 b±1.5×10 4 2.6×10 4 a±10 4 2×10 3 a±3×10 2 1.5×10 5 b ± 3.5×10 4 a-b Means within the same raw with no common superscript are significantly different at p< 0.01 Results expressed as Mean ± S.E. Table 2: Statistical analysis of bacterial count of fresh and frozen muscle samples of chicken broilers Coliforms MPN Faecal coliforms MPN E.coli MPN Staph aureus count Fresh -------------------------------------------------Breast Thigh Frozen -----------------------------------------------Breast Thigh 4×104a±104 9×103a±2×103 2×103a±3×102 2×105a±7×104 1.5×103 b±7×102 7×102a±2×10 2 3×102 a±102 5×104b±104 5×104a±104 3×104a±1.5×104 6×103 b±2×103 3×105 a±5.5×104 4.5×103b±2×103 1.6×103 a±7×102 4×102a±1.7×102 5.5×104b±104 a-bMeans within the same raw with no common superscript are significantly different at p< 0.01 Results expressed as Mean ± S.E. Results in tables (1,2) showed that there was a significant difference between fresh and frozen skin samples while there was no significant difference between fresh and frozen muscle samples at P<0.01 in relation to faecal coliforms count. Lower figures of faecal coliforms counts were reported by Cohen et al. [23], Guergueb et al. [24], Chaiba et al. [4] and Daoud et al. [20]. Coliform bacteria, especially fecal coliforms, are good microbial indicators of the potential presence of disease causing bacteria and also showed the general sanitary quality of the food. Faecal coliforms had been used as indicator for faecal contamination. During the slaughter of poultry birds, there can be fecal contamination of the carcasses from the gut of these birds which means bacteria present in the spilled gut content is passed on as contaminants. Also improper evisceration (intestinal breakage) may significantly increase carcass contamination with bacteria from the intestinal tract of the bird. This agreed with that reported by Russell and Walker [25] and Adeyanju and Ishola [26]. Results obtained in tables (1,2) showed that there was a significant difference between fresh and frozen skin and muscle samples of chicken broilers at P<0.01 in relation to E.coli count. Nearly similar figures for E.coli count were obtained by Berrang et al. [27] and Berrang et al. [28] while lower figures were reported by Chaiba et al. [4], Cohen et al. [23] in chicken meat, Abu-Ruwaida et al. [18] in neck skin, Buhr et al. [17] in breast skin samples and Daoud et al. [20] in frozen chicken breast and thigh muscle samples. Concerning E.coli isolation, E.coli was isolated from 100% of neck skin, breast skin, thigh skin, breast muscle and thigh muscle while in frozen samples E.coli was isolated by 100%, 86.6%, 100%, 73.3% and 86.6% from neck skin, breast skin, thigh skin, breast muscle and thigh muscles respectively with total percentage 89.3% (table, 3). The isolated serotypes were O157 and O18 from chicken broiler samples. In this respect Adesiji et al. [29] reported that E. coli has been isolated worldwide from poultry meat. High figures of E.coli isolation were reported by Berrang et al. [30] who isolated E.coli from 90 and 100% of breast and thigh skin respectively, Saikia and Joshi [31] isolated E.coli by 98% from raw chicken meat samples and Odwar et al. [32] who found that contamination by E. coli in chicken meat samples was 78%.Lower figures of E.coli isolation were reported by Adeyanju and Ishola [26] and Cohen et al. [23]. E. coli, a natural inhabitant of the intestinal tracts of humans and warm-blooded animals, is used as an indicator bacterium. Its presence therefore reliably reflects faecal contamination, indicating a possible contamination by enteric pathogens. Raw or undercooked foodstuffs get contaminated either during primary production e.g. slaughtering or further processing and handling e.g. cross contamination during processing, human-to-food contamination via food handlers [26]. In traditional poultry shops after slaughtering poultry carcasses scalded in a common scaling tank, under poor conditions (stagnant water, excessive excreta and or non 213 Global Veterinaria, 14 (2): 211-218, 2015 Table 3: prevalence of isolated microorganisms in chicken broilers Neck skin --------------No. % Breast skin ------------No. % Thigh skin ---------------No. % Breast muscle -----------------No. % Thigh muscle ---------------No. % Total ------------No. % E.coli fresh frozen 15 15 100 100 15 13 100 86.6 15 15 100 100 15 11 100 73.3 15 13 100 86.6 75 67 100 89.3 Salmonellae fresh frozen 4 2 26.6 13.3 2 2 13.3 13.3 3 1 20 6.6 3 1 20 6.6 5 1 33.3 6.6 17 7 22.6 9.3 Staph aureus coagulase positive fresh frozen 7 4 46.6 26.6 4 4 26.6 26.6 6 5 40 33.3 3 3 20 20 4 4 26.6 26.6 24 20 32 26.6 Campylobacter jejuni. fresh frozen 12 5 80 33.3 11 7 73.3 46.6 10 8 66.6 53.3 0 0 0 0 0 0 0 0 33 20 44 26.6 bacteriocidal temperatures), the scalding tank can serve essentially as an enrichment system, through which pathogens are spread widely to all birds entering the tank [33]. Results in tables (1, 2) illustrated that there was a significant difference between fresh and frozen skin and muscle samples at P< 0.01 in relation to staph.aureus count. High figure of staph.aureus count was reported by Bhandari et al. [16] while nearly similar result was reported by Amara et al. [34] on the other hand lower results were reported by Chaiba et al. [4], Cohen et al. [23] and Guergueb et al. [24]. Staph aureus was isolated from 46.6%, 26.6%, 40%, 20% and 26.6% from neck skin, breast skin, thigh skin, breast muscle and thigh muscles respectively with total percentage 32% while in frozen samples it was isolated from 26.6%, 26.6%, 33.3%, 20% and 26.6% from neck skin, breast skin, thigh skin, breast muscle and thigh muscles respectively with total percentage 26.6% (Table, 3). In this respect nearly similar results were obtained by Guergueb et al. [24] and Karmi [35]. Higher figures were reported by Javadi and Safarmashaei [36] and Koza inski et al. [37] while lower figures were obtained by Akbar and Anal [38] and Shareef et al. [39]. The reason for the high prevalence of staph.aureus in this study may be attributed to 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 as reported by Cohen et al. [23]. In this respect Javadi et al. [40] stated that contamination of poultry meat with S. aureus can be occurred through non-hygienic practices during slaughter as well as contamination with intestinal contents and/or skin of the carcass and through contaminated work surfaces and Knives. Concerning salmonella isolation results illustrated in table (3) clarified that salmonella spp. were isolated from 22.6%, 13.3%, 20%, 20% and 33.3% of neck skin, breast skin, thigh skin, breast muscle and thigh muscle, respectively with total percentage 22.6% of fresh chicken broiler samples while in frozen samples it was isolated from 13.3%, 13.3%, 6.6%, 6.6% and 6.6% of neck skin, breast skin, thigh skin, breast muscle and thigh muscle, respectively with total percentage 9.3%. The isolated serotypes were S. infantis and S. enteritidis. Nearly similar figures were reported by Chaisatit et al. [41] and Jimenez et al. [42]. High prevalence was recorded by Boonmar et al. [43], Saeed et al. [44], and Hassanein et al. [45] while lower figures were recorded by Moussa et al. [46], Medeiros et al. [47], Saad et al. [48] and Rabie et al. [49]. Salmonella is of an increasing public health concern because they are the most incriminated pathogenic microorganisms of bacterial food poisoning especially present in poultry meat, with infection being through the handling of raw poultry carcasses and products, together with the consumption of undercooked poultry meat [50]. Poultry are the most important reservoir for salmonella. The high prevalence of salmonella in chicken meat may be a result of cross-contamination from intestines during processing and cutting or from cages, floor and workers during retailing or marketing. Also the water used for washing of carcasses is mostly from the same container and it could be contaminated with salmonella from feces or from the butcher’s hands during washing, this is in agreement with Shah and Korejo [51]. Contamination of poultry by salmonella may be occurred at different phases of poultry meat production and processing, i.e. on the farm, during transportation to the poultry-processing plant or during the steps involved in slaughtering, scalding, defeathering, plucking and chilling of the poultry carcasses [52, 53]. 214 Global Veterinaria, 14 (2): 211-218, 2015 In this respect Nde et al. [54] declared that Scald water may also contribute to the contamination of Salmonella-free flocks when they are processed following salmonella positive flock so scald water is considered a potential vehicle for the transfer of Salmonella between birds. Concerning Campylobacter isolation results shown in table (3) clarified that campylobacter jejuni was isolated from 80%, 73.3% and 66.6% of neck skin, breast skin and thigh skin, respectively with total percentage 44% in fresh chicken broiler samples while it was isolated from 33.3%, 46.6% and 53.3% of neck skin, breast skin and thigh skin, respectively with total percentage26.6% from frozen samples of chicken broilers. Campylobacter jejuni failed to be detected in muscle samples, this agreed with Berrang et al. [30], Koza inski et al. [37] and Gritti et al. [55] and disagreed with Stoyanchev [56], Grani et al. [57] and Rahimi and Tajbakhsh [58]. Nearly similar results for campylobacter isolation were obtained by Atanassova and Ring [59] and Stoyanchev [56]. High figures in chicken broilers were reported by Willis and Murray [60], Zhao et al. [61] and Jeffrey et al. [62]. Lower figures were reported by Jones et al. [63] and Giacoboni et al. [64]. Campylobacter jejuni is commonly found in the intestinal tract of chickens and is transferred to the skin during slaughter and processing [60]. Evisceration process is a potential source for poultry carcasses to become contaminated with Campylobacter from their intestinal contents during the slaughter process. Improper evisceration (intestinal breakage) may significantly increase carcass contamination with bacteria from the intestinal tract of the bird. Visceral rupture and intestinal breakage lead to escape of fecal content leading to the contamination of equipment, working surfaces, processing water, and air and increasing the opportunities for cross contamination of Campylobacter-free carcasses during processing. This agreed with that reported by Genigeorgis et al. [65] and Russell and Walker [25]. Crop contents may be an important source of campylobacter contamination during processing. The crop has been found to be a significant source of Campylobacter, thus potentially contributing to carcass contamination [66]. This agreed with that reported with Jeffrey et al. [62] who isolate campylobacter from crop by 48% suggesting that crop splitting during processing may be a potential source for contamination of carcass specially neck and breast skin. CONCLUSION Chicken broiler meat can be contaminated with a wide variety of pathogenic bacteria as salmonellae, E.coli, Staph.aureus and Campylobacter jejuni during processing, so it could be considered as a potential source for these pathogenic food poisoning microorganisms. Fresh carcasses have higher coliforms (MPN), faecal coliforms (MPN), E.coli (MPN) and staph.aureus count than the frozen ones. Lack of sanitary measures in traditional poultry shops lead to contamination of chicken broiler carcasses as cross contamination occurs during processing. 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