Received: 16 August 2019 Accepted for publication: 10 June 2020 Slov Vet Res 2020: 57 (3): 115–21 DOI 10.26873/SVR-950-2020 UDC 636.3.09:579.63:637.513.1/.2:579.842.1/.2:612.428+612.35:57.083.1 Original Research Article Introduction Red meat is one of the important animal protein sources in human diet, and the meat under the skin of a healthy animal is considered sterile. However, carcass contamination is inevitable during the slaughtering process such as skinning and evisceration (1). Most of the microbial contamination on the carcass surface comes from different sources such as hide, intestinal contents, slaughterhouse equipment/tools and workers during the slaughtering. ASSESSMENT OF MICROBIOLOGICAL LOAD OF SMALL RUMINANT CARCASSES, LIVERS, SOME LYMPH NODES, TOOLS AND KNIFE SAMPLES IN SLAUGHTERHOUSE Halil Durmuşoğlu1, Gökhan Kürşad İncili2, Alper Güngören3, Osman İrfan İlhak4* 1Department of Food Hygiene and Technology, Faculty of Veterinary Medicine, Dicle University, Diyarbakır, 2Department of Food Hygiene and Technology, Faculty of Veterinary Medicine, Firat University, Elazığ, 3Department of Food Hygiene and Technology, Faculty of Veterinary Medicine, Bingol University, Bingöl, 4Department of Food Hygiene and Technology, Faculty of Veterinary Medicine, Balikesir University, Balikesir, Turkey *Corresponding author, E-mail: irfan.ilhak@balikesir.edu.tr Abstract: The aim of this study was to determine the microbiological loads of small animal carcasses, carcass lymph nodes, whole liver surface, liver lymph nodes and some tools contacting with carcass and offal. Total 630 samples taken from small ani- mal carcasses, livers, hepatic lymph nodes, subiliac and prescapular lymph nodes, staff knives and slaughterhouse tools sam- ples (stainless steel table, plastic crates, offal carts) were investigated for mesophilic aerobic bacteria, Enterobacteriaceae, Escherichia coli counts and Salmonella spp. The mean total aerobic mesophilic bacteria (TAMB), Enterobacteriaceae and E. coli numbers of the carcasses were 3.6, 0.6, and 0.1 log 10 CFU/cm2, respectively, and the most contaminated region among the carcass sampling points was flank. The mean TAMB, Enterobacteriaceae and E. coli counts of the liver surfaces were 6.0, 3.7, 2.9 log 10 CFU/liver, respectively. The average TAMB, Enterobacteriaceae and E. coli numbers of the knives were found as 6.3, 2.9 and 2.1 log 10 CFU/blade, and the average TAMB, Enterobacteriaceae and E. coli counts of the slaughterhouse surfaces were 5.1, 1.6, 0.5 log 10 CFU/cm2. Salmonella spp. was detected in 4% of the liver samples and 10% of the knives samples. Consequently, the presence of Salmonella on the surface of livers and blades, and high number of E. coli on the livers, blades and tools show that a public health risk may arise at any time, and staff should pay extra attention to the “Good Hygiene Practices” and Food Safety Management Systems (such as HACCP) applied in slaughterhouses. Key words: carcass; liver; lymph node; microbiological quality; Enterobacteriaceae; Escherichia coli; Salmonella spp. Salmonella is one of the pathogenic bacteria causing foodborne diseases (2). It is known that the animal skin, gastrointestinal tract and feces are the primary sources of Salmonella contamination for the carcass surface during the slaughter process (3). Besides, the studies conducted on carcass lymph nodes have shown that those nodes may harbor pathogenic microorganisms such as Salmonella spp. (4). It is known that completely removing lymph nodes from the carcass is impossible. The lymph nodes remaining in carcass meat become a part of the meat product after the mincing process of meat (5). Edible offal that is derived from carcass may be exposed to cross contamination with pathogen microorganisms in case of poor hygiene H. Durmuşoğlu, G. K. İncili, A. Güngören, O. İ. İlhak116 in slaughterhouse (6). Most of the studies related to the Salmonella prevalence in lymph nodes, edible offal, carcass and on slaughterhouse tools have been conducted in beef carcasses and beef slaughterhouses (3-5, 7, 8), however, the studies conducted in small animal carcasses are very limited (9-11). Hence, this study was conducted to investigate (i) the microbiological condition of small animal carcasses and liver surfaces in slaughterhouse, (ii) Salmonella prevalence of carcass lymph nodes and hepatic lymph nodes in small animals, and (iii) the bacterial load of staff blade and some slaughterhouse tools contacting with offal. Materials and methods The study was conducted in a slaughterhouse that has beef and sheep/goat slaughter-lines with a line speed of approximately 150 small animals per hour, and there was no automatic hide puller for small animal carcasses. Samples of the study were composed of total 630 samples taken from small animal carcasses (200 samples taken from 50 carcasses; four sampling sites including rump, flank, brisket ad neck regions were sampled for each carcass), livers (50), hepatic lymph nodes (taken from 100 livers), subiliac (100 pairs, one pair per carcass) and prescapular lymph nodes (100 pairs, one pair per carcass), staff knives (blade) (40) and some tools (stainless steel tables (15), plastic crates (15), offal carts (10)) used in slaughterhouse. The animals sampled were not separated as goat and sheep; they all were defined as small animal because the slaughterhouse was cutting them as mixed, and the staff was using the same blade, same plastic crates, offal carts and tables for both goat and sheep. The lymph nodes samples were collected as a pair per carcass. The samples were collected between February and May 2018, and the slaughterhouse was visited once a week during this period. Sampling procedures Carcass samples were taken from four sampling sites including rump, flank, brisket and neck regions indicated in the ISO 17604 (12) at the stage after washing but before chilling. Briefly, samples were taken from carcass regions by swabbing an area of 100 cm2 using sterilized stainless steel template (10 cm×10 cm) and sterile sponge (World bioproducts, EZ-ReachTM, US/Canada) which was premoistened with 25 ml sterile buffered peptone water (BPW) (Biokar, Beauvais/France). The entire liver surface was sampled by the sterile sponge premoistened with 25 ml sterile BPW. Samples from tools (stainless steel table, plastic crates, offal carts) were collected by swabbing an area of 100 cm2 using the sterilized template (10 cm×10 cm) and the premoistened sterile sponge. Staff knives were sampled by swabbing the both surfaces of the blade with the premoistened sterile sponge. Hepatic, subiliac and prescapular lymph nodes were taken using sterile scalpel. All visible hepatic lymph nodes on the liver surface were collected. Microbiological analysis All the samples were transported to the laboratory in a thermo cool box containing pre- frozen ice bags within 2-3 h. The sponge samples taken from carcasses, livers, blades and tools were homogenized in a stomacher (Bag mixer 400, Interscience, France) for 2 min. Analysis of aerobic plate counts, E. coli and Enterobacteriaceae in all the samples were conducted according to the methods described in ISO 4833, ISO 16649-2 and ISO 21528-2, respectively (13-15). Briefly, Plate Count Agar (PCA), Tryptone Bile X-glucuronide (TBX) agar and Violet Red Bile Glucose (VRBG) Agar (Biokar, Beauvais/France) were used for the detection of aerobic plate count (APC), E. coli and Enterobacteriaceae counts. TBX and VRBG plates were incubated at 37oC for 24 h, and PCA plates were incubated at 30oC for 72 h. The adipose tissues surrounding the each lymph nodes were removed as much as possible, and each lymph nodes were dipped into 70% alcohol for 5 min in order to disinfect the outside of the node. After this procedure, the lymph nodes were kept in open air to remove the residual alcohol for 5 min. And then, hepatic, subiliac and prescapular lymph nodes were separately placed into sterile stomacher bags, and they were crushed with rubber mallet from outside of the stomacher bag. After this, 100 ml sterile BPW were added into stomacher bags and homogenized in a stomacher (BagMixer 400, Interscience, France) for 1 min, and the homogenized samples were incubated at 37oC for 24 h for Salmonella pre-enrichment procedure. Analysis of Salmonella spp., in all samples were conducted according to the methods described in ISO 6579 (16). Briefly; after pre-enrichment Assessment of microbiological load of small ruminant carcasses, livers, some lymph nodes, tools and knife samples in slaughterhouse 117 procedure, 0.1 ml of the sample was added to 10 ml Rappaport-Vassiliadis broth (RVS; Oxoid, Hampshire/England) and 10 ml Muller-Kauffmann tetrathionate novobiocin broth (MKTTn; Oxoid, Hampshire/England). RVS and MKTTn were incubated at 41.5oC and 37oC for 24 h, respectively. RVS and MKTTn enrichments cultures were streaked to Xylose-Lysine-Deoxycholate agar (XLD; Lab M, Lancashire/United Kingdom) and Xylose- Lysine-Tergitol agar (XLT4; Lab M, Lancashire/ United Kingdom), and the plates were incubated at 37oC for 24-48 h. At the end of the incubation, five suspected colonies with black center were transferred to tubes containing Triple Sugar Iron Agar and Lysine Iron Agar (Merck, Darmstadt/ Germany) and incubated at 37oC for 24 h. After incubation, presumptive positive Salmonella colonies were confirmed with Salmonella latex test (Oxoid, Hampshire/United Kingdom) and Microgen GN-ID A (Microgen, Camberley/United Kingdom). Statistical analysis Statistical analysis were made using SPSS version 22 (IBM SPSS, IBM Corporation, USA). The microbiological data were converted to Log10 CFU. One way analysis of variance (ANOVA) was used to compare samples taken from different regions (rump, flank, brisket and neck) of the carcasses. Statistical significance level was accepted as P<0.05. Results and discussion In Turkey, decontamination of carcasses with any chemicals is not allowed, but washing with water. Carcass samples were taken after carcass washing stage before chilling. In the present study, the highest APC count in the carcass regions was found in the flank by average APC number of 3.6 log10 CFU/cm 2 (Table 1), and significant difference was observed between the flank and neck regions (P<0.05). Similarly, the highest Enterobacteriaceae and E. coli numbers were found in the flank while the lowest numbers were in the rump and neck regions (P<0.05). Since the microbiological results were expressed as log10 CFU/cm 2 in the study, statistical analysis for E. coli numbers of the rump, brisket and neck regions was not performed (because some samples had E. coli number of <25 CFU/100 cm2 and negative logarithmic values). Gürbüz et al. (17) reported that the highest level of Enterobacteriaceae and APC were in rump and brisket regions after washing of sheep carcasses, respectively. However, unlike our study, they had chosen the three sampling points (rump, shoulder and brisket), not including flank region. In our study, the possible reason of the high microbial contamination of the flank compared to the other regions may be due to the dirty hands and blades of the staff. Staff hands and blades were frequently touching the flank region during the evisceration process. The average APC, Enterobacteriaceae and E.coli numbers of 50 carcasses were 3.6, 0.6 and 0.1 log10 CFU/cm 2, respectively. When the values obtained for E. coli in rump, brisket and neck regions of the carcasses were converted from CFU/100 cm2 to CFU/cm2, negative log values were obtained. Negative log value was used to imply that there was less than 1 bacterium in per cm2 (Table 1). In Europe, the studies conducted in Italy, Spain, Finland and Poland (18-21) reported that APC and Enterobacteriaceae counts on sheep carcasses were between 2.27-3.88 log10 and between 0.27-1.03 log10 CFU/cm 2, respectively. Small differences among the bacterial load of carcasses should be taken as normal. It should kept in mind that some factors such as slaughter practices, the number of animals cutting per hours, sampling time (season), sampling methods (sponge, excision or swabbing) and hygienic conditions and procedures in slaughterhouses can affect the bacterial load on carcasses. Salmonella spp. was not detected in 50 carcass samples collected in this study (Table 1). Similar to our result, some researchers reported no Salmonella spp. in sheep carcasses by excision and swabbing methods (17, 20-22). On the other hand, some researchers found that Salmonella spp. prevalence in small animal carcasses was between 0.62% and 14.1% (23-27). It is difficult to make comparison among the studies in point of the Salmonella prevalence. Since, some factors such as number of animals that harbor Salmonella spp. on their hide and in feces due to husbandry practices, sample numbers, sampling time (season) and frequency, sampling methods (sponge, excision or swabbing) and hygienic procedures in slaughterhouses should be taken into consideration. It should be noted that only 400 cm2 surface area was sampled for each carcass in this study, hence, actual Salmonella prevalence may be higher than 0%. H. Durmuşoğlu, G. K. İncili, A. Güngören, O. İ. İlhak118 Table 1: The mean Aerobic Plate Count (APC), Enterobacteriaceae, Escherichia coli counts and Salmonella spp. prevalence of the small animal carcasses and carcass regions (log10 CFU/cm 2±SD) (n=50) Carcass (general) Carcass regions Rump Flank Brisket Neck APC 3.6±0.8 3.1±1.2AB 3.6±0.9B 3.2±0.9AB 3.0±1.1A Enterobacteriaceae 0.6±0.8 0.3±0.9A 0.7±0.9B 0.4±0.9AB 0.1±0.8A Escherichia coli 0.1±0.9 -0.4±0.8 0.04±0.9 -0.2±0.9 -0.4±0.8 Salmonella spp.a 0/50 0/50 0/50 0/50 0/50 AB: The values with different superscript within the same row are significantly different (P<0.05) a: Salmonella positive sample/Total samples Bladea (n=40) Liverb (n=50) Slaughterhouse toolsc (n=40) APC 6.3±1.0 6.0±0.7 5.1±0.9 Enterobacteriaceae 2.9±1.3 3.7±0.9 1.6±0.8 Escherichia coli 2.1±1.1 2.9±0.9 0.5±0.9 Table 2: The average Aerobic Plate Count (APC), Enterobacteriaceae and Escherichia coli on the blade, liver and some slaughterhouse tools (plastic crates (15), stainless steel tables (15) and offal carts (10)) samples a: Log10 CFU/blade b: Log10 CFU/liver c:Log10 CFU/cm 2 Table 3: Salmonella spp. prevalence on the knife blade, liver, some slaughterhouse tools [plastic crates (15), stain- less steel tables (15) and offal carts (10)] and in lymph nodes. Samples Positive samples/Total samples Knife 4/40 Liver 2/50 Slaughterhouse surfaces 0/40 Portal (hepatic) lymph nodes 0/100 Prescapular lymph nodes 0/100 Subiliac lymph nodes 0/100 Knife blades and other tools (plastic crates, offal carts, working tables) used by the staff at the slaughterhouse can be one of the contamination sources of the carcass (1, 28). In the present study, the average numbers of APC, Enterobacteriaceae and E. coli on the blades were detected as 6.3, 2.9 and 2.1 log10 CFU/blade, respectively (Table 2). Salmonella spp. was detected in 4 (10%) out of 40 blades (Table 3). Bakhtiary et al. (29) reported that Salmonella enterica was found on knives in a sheep and beef slaughterhouse in Iran. In the samples taken from the stainless steel table, plastic crates and offal carts, the mean numbers of APC, Enterobacteriaceae and E. coli were 5.1, 1.6 and 0.5 log10 CFU/cm 2, respectively (Table 2). Salmonella spp. was not found on the surface samples taken from stainless steel table, plastic crates and offal carts. To our knowledge, there are limited studies indicating bacterial load of staff knives in slaughterhouse. Hence, some references used in this study are old. Bell (30) detected APC number of 3.61 log10 CFU/cm 2 on the blade used for hide skinning. In another study, APC number on the blade was detected as 5.04 log10 CFU/cm 2 (31). Bell and Hathaway (31) and Bell (30) noted the bacterial load of the blade as per cm2. If it is assumed that the entire surface area of a blade is more than 10 cm2, then it can be said that the results of the studies are similar to each other. When the results obtained from tool and blades were evaluated, it was seen that the tool and blade samples had a high amount of microorganisms, Assessment of microbiological load of small ruminant carcasses, livers, some lymph nodes, tools and knife samples in slaughterhouse 119 and they could pose an important role in the cross contamination of carcass and offal. In addition, the presence of Salmonella spp. in 10% of the blades showed that hygienic condition of blades should be taken care. The Regulation (EC) 853/2004 reported that “they (slaughterhouses) must have facilities for disinfecting tools with hot water supplied at not less than 82°C, or an alternative system having an equivalent effect” (32). The slaughterhouse where this study was conducted has equipment for disinfecting blades with hot water at 82 °C, however, it was observed that the equipment were not used by the staff. The results show that it is extremely important that staffs are to be informed and educated about the hygiene rules and public health. Moreover, staffs who do not comply with the hygiene rules should be warned during the slaughter process. Liver surfaces can be contaminated with microorganisms during the production stage, and it can pose a risk for the public health. Woldemariam et al. (10) examined 107 small animals (sheep and goat) liver in Ethiopia and found that 5 (4.7%) of the livers were Salmonella spp. positive. In the present study, the average APC, Enterobacteriaceae and E. coli numbers of the 50 small animal livers collected from slaughterhouse were 6.0, 3.7 and 2.9 log10 CFU/ liver, respectively (Table 2). E. coli was detected in 90% of the livers collected (detection limit was ≥1.4 log10 CFU/liver). Salmonella spp. was detected in 2 (4%) livers surface, while it was not found in any of the hepatic lymph nodes collected from 50 livers, (Table 3). This result indicates that Salmonella that were detected on the surface of the livers most likely originates from the hands or knife blades of the staff or the surfaces contacting with the livers such as offal carts, plastic crates. The presence of high amount of microorganisms on the surfaces of tools and blades may have contributed to the contamination of the liver surfaces. In addition, the presence of Salmonella spp. in 10% of the blades suggests that blades may also play an important role in the contamination of liver surfaces with Salmonella spp. However, it should not be forgotten that staff hands may also play an important role in the contamination of carcasses and offal. There are limited studies on the Salmonella spp. prevalence of lymph nodes in small animal carcasses. El-Tom et al. (9) detected Salmonella spp. in 3 out of 78 mesenteric lymph nodes collected from goat carcasses. Hanlon et al. (11) collected mesenteric (223) and subiliac (223) lymph nodes from sheep and goat carcasses during 14 months, and they found Salmonella spp. prevalence as 5.8% in mesenteric and 7.6% in subiliac lymph nodes, respectively. It is almost impossible to use the mesenteric lymph nodes in the production of ground meat, however, removal of subiliac and prescapular lymph nodes from carcass can be forgotten; and they may probably be used in the production of ground meat. In the present study, Salmonella spp. was not found in any of the subiliac and prescapular lymph nodes collected from 100 carcasses (Table 3). The reason of these differences among the results may be depend on the condition of the farms where animals are come from and health/disease situations of the animals brought to the slaughterhouse. It has been also noted that the prevalence of Salmonella spp. in animals shows seasonal differences (5). Conclusions Consequently, the presence of high amount of Enterobacteriaceae and E. coli on the surfaces of blades and livers, and the detection of Salmonella spp. on the surfaces of the blades and livers show that staff should pay extra attention to the “Good Hygiene Practices” and Food Safety Management Systems (such as HACCP) applied in slaughter- houses. In this context, disinfection of blades with the hot water of ≥82oC, taking care of the sanita- tion of the surfaces that are contact with livers, and washing liver surfaces with the clean water in slaughterhouse can significantly reduce the mi- crobial load on these surfaces. Although this study was conducted in one slaughterhouse, the samples were collected as many number as possible, and the study was continued for 4 months to reflect the general microbiological status of small animal carcasses and the surfaces contacting with offal in a slaughterhouse. 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Assessment of risk factors and prevalence of Salmonella in slaugh- Assessment of microbiological load of small ruminant carcasses, livers, some lymph nodes, tools and knife samples in slaughterhouse 121 OCENA MIKROBIOLOŠKE OBREMENITVE TRUPOV MALIH PREŽVEKOVALCEV, JETER IN NEKATERIH BEZGAVK TER ORODIJ IN NOŽEV V KLAVNICI H. Durmuşoğlu, G. K. İncili, A. Güngören, O. İ. İlhak Povzetek: Namen študije je bil določiti mikrobiološko obremenitev trupov malih živali, bezgavk na trupih, celotne površine jeter, jetrnih bezgavk in nekaterih orodij, ki prihajajo v stik s trupom ter drobovjem. Pregledanih je bilo 630 vzorcev trupel malih živali, jeter, bezgavk, jetrnih bezgavk, nožev in orodij za klavnice (mize iz nerjavečega jekla, plastični zaboji, zaboji za drobovino). Ugotavljali smo prisotnost mezofilnih aerobnih bakterij, Enterobacteriaceae ter število bakterij Escheria coli in Salmonella spp. Povprečna skupna količina aerobnih mezofilnih bakterij (TAMB), Enterobacteriaceae in E. coli je bila 3,6, 0,6 in 0,1 log10 CFU/cm2. Najbolj onesnaženo področje pri vzorčenju trupov je bilo na boku trupov. Povprečno število TAMB, Enterobacteriaceae in E. coli na površinah jeter je bilo 6,0, 3,7 in 2,9 log10 CFU/jetra. Povprečno število TAMB, Enterobacteriaceae in E. coli na nožih je bilo 6,3, 2,9 in 2,1 log10 log10 CFU/rezilo, povprečno število TAMB, Enterobacteriaceae in E. coli na klavniških površinah pa 5,1 in 1,6, 0,5 log10 CFU/cm2. Salmonello spp. smo odkrili v 4 odstotkih vzorcev jeter in na 10 odstotkih nožev. Prisotnost salmonele na površini jeter in rezil ter veliko število bakterij E. coli na jetrih, rezilih in orodju kažejo na to, da te bakterije lahko predstavljajo tveganje za jav- no zdravje. 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Villarreal-Silva M, Genho DP, Ilhak I, et al. Tracing surrogates for enteric pathogens inoculat- ed on hide through the beef harvesting process. J Food Prot 2016; 79: 1860–7. 29. Bakhtiary F, Sayevand HR, Remely M, Hippe B, Hosseini H, Haslberger AG. Evaluation of bacterial contamination sources in meat pro- duction line. J Food Qual 2016; 39: 750–6. 30. Bell RG. Distribution and sources of micro- bial contamination on beef carcasses. J Appl Mi- crobiol 1997; 82: 292–300. 31. Bell RG, Hathaway SC. The hygienic effi- ciency of conventional and inverted lamb dressing systems. J Appl Bacteriol 1996; 81: 225–34. 32. EC. Regulation (EC) No 853/2004 of The European Parliament and the Council of 29 April 2004 laying down specific hygiene rules for food of animal origin. Off J Eur Commun 2004; L139: 55–205.