Thermal inactivation of Escherichia coli O157:H7 strains and Salmonella spp. in camel meat burgers

Thermal inactivation of Escherichia coli O157:H7 strains and Salmonella spp. in camel meat burgers

LWT - Food Science and Technology 120 (2020) 108914 Contents lists available at ScienceDirect LWT - Food Science and Technology journal homepage: ww...

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LWT - Food Science and Technology 120 (2020) 108914

Contents lists available at ScienceDirect

LWT - Food Science and Technology journal homepage: www.elsevier.com/locate/lwt

Thermal inactivation of Escherichia coli O157:H7 strains and Salmonella spp. in camel meat burgers

T

Tareq M. Osailia,b,c,∗, Fayeza Hasana,b, Dinesh Kumar Dhanasekaranb, Reyad S. Obaida,b, Anas A. Al-Nabulsic, Sowmya Raoa, Hera Fatimab, Mutamed Ayyashd, Ioannis Savvaidise, Richard Holleyf a

Department of Clinical Nutrition and Dietetics, College of Health Sciences, University of Sharjah, P. O. Box 27272, Sharjah, United Arab Emirates Research Institute of Medical and Health Sciences, University of Sharjah, P. O. Box 27272, Sharjah, United Arab Emirates c Department of Nutrition and Food Technology, Faculty of Agriculture, Jordan University of Science and Technology, P.O. Box 3030, Irbid, 22110, Jordan d Department of Food, Nutrition and Health, College of Food and Agriculture, United Arab Emirates University (UAEU), United Arab Emirates e Department of Chemistry, University of Ioannina, 45110, Ioannina, Greece f Department of Food Science and Human Nutrition, University of Manitoba, Winnipeg, Manitoba, R2J 3L8, Canada b

A R T I C LE I N FO

A B S T R A C T

Keywords: Camel meat D-value z-value Burger Fat Process validity

The study aimed to determine D and z-values of Escherichia coli O157:H7 strains and Salmonella spp. in camel lean meat burger (CM) and camel meat burger with hump fat (CMF). Two E. coli O157:H7 strains, S. Typhimurium and S. Copenhagen were mixed individually with CM and CMF samples, placed in sterile pouches and exposed to water bath heat treatment at 55, 57.5, 60, 62.5, 65, 67.5 °C for different time intervals. The Dvalues of E. coli O157:H7 161-84 in CM burgers at 60, 62.5, 65, 67.5 °C were 53.5, 20.1, 8.3, and 3.0 s, respectively, while the values in CMF samples were 76.0, 25.9, 9.9 and 4.1 s, respectively. The D-values of S. Typhimurium in CM burgers at 55, 57.5, 60, 62.5 °C were 349.2, 70.5, 18.4 and 6.7 s, respectively, while the values in CMF were 512.1, 77.1, 21.1 and 8.4 s, respectively. There was a significant (P < 0.05) difference in the D-values of E. coli O157:H7 strains and Salmonella spp. between the two formulations. The z-values of E. coli O157:H7 strains and Salmonella spp. ranged from 5.0 to 6.0 °C and 4.1–4.4 °C, respectively. This study provides preliminary data to the camel meat industry to validate thermal processes.

1. Introduction Recently, the market and demand for ready-to-eat (RTE) food products have increased due to changes in lifestyle. Meat burgers are one of the most common RTE products that are consumed extensively worldwide. Although beef is one of the most common types of meat used in the production of burgers and patties, pork, chicken and turkey meats are also used (Gurman, Ross, Holds, Jarrett, & Kiermeier, 2016; Murphy; Beard, Martin; Keener, & Osaili, 2004; Murphy, Duncan, Johnson, Davis, & Smith, 2002). Over the few last years, there has been an increasing trend, especially in Arab countries, to produce camel meat burger patties as a replacement for conventional beef patties, due to the regular availability of camel meat in the region and additionally to give a more ‘local and traditional touch’ to the food. Camel meat burgers are currently promoted to consumers as a food that contains a good source of protein, amino acids, and minerals, low levels of

intramuscular fat and a high proportion of polyunsaturated fatty acids (Kadim, Mahgoub, & Mbaga, 2014). The world camel meat market, if not the biggest, is acknowledged to be very large. Approximately 250,000 camels are slaughtered annually around the world (Kadim et al., 2014). Food and Agriculture organization (FAO) statistics state that the worldwide market of camel-based products is valued at > $10 billion US (Mirzaei, 2012). However, this potentially huge camel meat market is a risky issue, as meat provides a favourable substrate (medium) for the growth of various opportunistic pathogenic microorganisms, such as Salmonella spp. and Escherichia coli O157:H7, considered to be the leading causes of foodborne bacterial illnesses involving bovine meat (Niyonzima, Ongol, Kimonyo, & Sindic, 2015). Both E. coli O157:H7 and Salmonella spp. colonize the gastrointestinal tracts of animals and humans. During slaughter, the meat could potentially be contaminated if there is a rupture of the

∗ Corresponding author. Department of Clinical Nutrition and Dietetics, College of Health Sciences, University of Sharjah, P. O. Box 27272, Sharjah, United Arab Emirates.; E-mail addresses: [email protected], [email protected] (T.M. Osaili).

https://doi.org/10.1016/j.lwt.2019.108914 Received 30 June 2019; Received in revised form 16 October 2019; Accepted 1 December 2019 Available online 02 December 2019 0023-6438/ © 2019 Elsevier Ltd. All rights reserved.

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2.2. Camel meat burger formulation

gastrointestinal tract during carcass dressing. The presence of these microorganisms could also indicate faecal contamination of the meat from other sources (Adeyanju & Ishola, 2014; Meyer, Thiel, Ullrich, & Stolle, 2010). There are various sources involved in the whole production process from the slaughterhouse to the retail shop, which provide ample opportunity for pathogenic contamination (Nortje et al., 1990). During meat processing, improper handling of the carcass could result in contamination of the meat products. In addition, hide, cleaning tools and moisture from the carcass can contaminate the meat (Tuttle et al., 1999). Generic E. coli and S. Typhi, S. Kentucky, S. Enteritidis and S. Anatum were isolated from camel meat samples obtained from different abattoirs in Egypt at rates of 40, 2, 8, 8, and 8%, respectively (AlSharary, 2014). In Iran, Hajian, Rahimi, and Mommtaz (2011) and Rahimi, Kazemeini, and Salajegheh (2012) reported the prevalence of E. coli O157:H7 in camel meat to be 1.3 and 2%, respectively, while Momtaz, Dehkordi, Rahimi, Ezadi, and Arab (2013) reported the prevalence of Shiga toxin-producing E. coli serogroups to be 13%. Ingestion of E. coli O157:H7-contaminated food could potentially cause Shiga-like toxin producing E. coli (STEC) haemolytic uremic syndrome. E. coli (STEC) is also known to have a very low infective dose of < 100 organisms depending on the strain (Thorpe, 2004). Ingestion of Salmonella spp.-contaminated food might cause salmonellosis. Although the exact minimum dose depends on various factors, recent study of outbreak data showed that even 36 colony forming units are capable of triggering an infection/illness in humans (Niyonzima et al., 2015). There are no accurate data available in the Middle East area on the foodborne illnesses caused by foodborne pathogens. As per the Centres for Disease Control and Prevention (CDC), Salmonella spp. alone were responsible for causing 1.2 million illnesses and 450 deaths every year in the United States (USA) with food being the major carrier in one million of these cases (CDC, 2018). Due to ever rising demand, ground meat burgers may be left partially uncooked before being served to consumers. Unlike intact meat cuts, microbial contamination of burgers with pathogens can occur internally (Gurman et al., 2016). This could be dangerous as more intense thermal treatment is required to eliminate E. coli O157:H7 and Salmonella spp. when they are not just on the outer meat surfaces. Thermal inactivation of foodborne pathogens in food depends on many factors including the microbial strains present and the composition of the food (Juneja & Eblen, 2000; Osaili et al., 2013). For example, fat has been found to increase the thermal resistance of E. coli O157:H7 and Salmonella in meat products (Juneja & Eblen, 2000; Smith, Maurer, Orta-Ramirez, Ryser, & Smith, 2001). While there have been several studies conducted on the thermal inactivation of foodborne pathogens in beef, chicken and pork burgers and patties with different fat content to obtain quantitative data (Murphy et al., 2002; Osaili, Griffis, Martin, Beard, Keener, & Marcy, 2006, 2007), there appears to be a lack of data published on the thermal inactivation of foodborne pathogens in camel meat burgers. Therefore, the objective of the study was to determine the thermal inactivation of E. coli O157:H7 and Salmonella spp. by establishing their D and z-values in burgers prepared from camel lean meat (CM) and in camel meat with hump fat (CMF).

Meat burgers were prepared as described by Abdel-Naeem and Mohamed (2016). Two formulations were prepared, generating CM and CMF burgers. The composition of CM burgers consisted on a weight basis of 82% lean camel meat, 11% water, 5% starch, 1.8% NaCl, 0.3% sodium tripolyphosphate (STPP) and 0.05% seasoning mix (turmeric, coriander, red chili, cumin, black pepper, ginger, cloves, cinnamon and cardamom), while CMF burgers were composed of 65% lean camel meat, 17% camel hump fat, 11% water, 5% starch, 1.8% NaCl, 0.3% STPP and 0.05% seasoning mix. The ingredients of each formulation were thoroughly mixed manually in disinfected stainless-steel bowls and units of 100 g were placed in polyethylene bags and kept at −80 °C. 2.3. Bacterial strains and culture preparation Two E. coli O157:H7 strains positive for stx1 and/or stx2 (E. coli O157:H7 1934, and E. coli O157:H7 161-84) from the Canadian Science Centre for Human and Animal Health, National Microbiology Laboratory, Ottawa, and two Salmonella spp. (S. Copenhagen PT 99, and S. Typhimurium 02–8423) isolated from animal and human sources (Agriculture and Agri-Food Canada, Food Research Institute, Ottawa, and Health Canada, Microbial Hazards Laboratory, Ottawa, Canada), respectively were used in the current study. The frozen cultures were activated individually in Tryptic Soy Broth (Oxoid, Basingstoke, UK) at 37 °C for 24 h. Three subsequent transfers were performed to activate the cultures. 2.4. Thermal inactivation studies One ml of fresh E. coli O157:H7 or Salmonella cultures were individually mixed with 100 g 4 °C thawed CM or CMF burger samples to reach inoculation levels of ~107 CFU/g. After that, the samples were mixed thoroughly with a sterile spatula for 2 min and left at 4 °C for 20 min to allow attachment of the cells to the burger substrate. Subsequently, 5 g of the burger samples were placed in sterile bags (5 × 10 cm) (Bag Light, Interscience, France) and compressed to ˂ 1 mm thickness with a roller to reduce come-up time during heating and were then sealed. Then, the samples were placed individually in wire metal holders and immersed in a circulating water bath (Thermo circulator SCT-HYDRO-14, Schichem Tech, Boston, USA) set at 55, 57.5, 60, 62.5, 65 or 67.5 °C for different intervals to achieve 3–4 log10 bacterial reductions. Upon completion of the time in the hot water bath, samples were immediately transferred to chilled water and kept at 4 °C until plating was performed (Osaili et al., 2013). All experiments were repeated three times on different days. 2.5. Microbial enumeration The bags were opened aseptically, combined with 45 ml of sterile 0.1% peptone water (Oxoid) and homogenized in a mixing machine (AES Chemunex®) for 2 min. To enumerate the survival of E. coli O157:H7 and Salmonella cells, 0.1 or 1 ml aliquots from appropriate decimal dilutions were plated in duplicate on 20-ml portions of Sorbitol MacConkey Agar (Oxoid) and Xylose Lysine Deoxycholate Agar (Oxoid), overlaid with 10 ml of Tryptone Soy Agar (Oxoid) respectively, to resuscitate injured cells from the thermal treatment (Osaili et al., 2013). After 48 h of incubation at 37 °C, typical colonies were enumerated.

2. Materials and methods 2.1. Camel meat and hump fat samples Fresh lean camel (leg) meat and hump fat were obtained from the local market and were ground separately through the 5 mm plate of a cleaned and 70% ethanol disinfected grinder. The samples were enclosed in polyethylene bags and transported in an icebox to the laboratory. All meat lots were examined to ensure they were free from E. coli O157:H7 strains and Salmonella spp. according to ISO (2001; 2002) and were found negative in 25 g.

2.6. D and z-values calculations D-values of E. coli O157:H7 strains and Salmonella spp. in CM and CMF burger samples at each temperature examined were calculated from the survival curves in which log10 of the surviving population was 2

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4. Discussion

plotted against the exposure time as described by Osaili, Martin, Beard, Keener, and Marcy (2006).

D − value =

It is widely known that the microbial safety of fresh meat and its products varies and the final microbiota on the meat product may be both attributed to: a) the form of meat cut from the carcass (e.g. steak, ribs, fillets, strips etc.) and b) the “in house premises” microbiota, as well as and the handling/processing (e.g. grinding) steps in the preparation of a meat product. Camel burgers, as also with other types of meat burgers may pose a greater microbial safety risk, as compared to steaks, fillets or meat strips. Apart from microbial deterioration affecting meat quality, chemical oxidation of myoglobin (e.g. due to grinding) may cause premature browning during cooking (Nair et al., 2016). Premature browning may pose a risk of illness, as it could affect consumers’ judgement (if meat is fully or not adequately cooked). The relative risk for illness was estimated to increase by about 300 fold due to premature browning of hamburger (Boqvist, Fernström, Alsanius, & Lindqvist, 2015). In a study conducted by Lahou et al. (2015), although consumers concluded that hamburgers look cooked, it was subsequently found that 46% of cases had viable pathogens present, surviving after cooking, as a core temperature of 70 °C was not attained. Thus, an appropriate combination of temperature and time would be of paramount importance in achieving microbial safety of camel meat burgers. However, extra care must be given to ensure that the taste should not be compromised and because high cooking (especially charcoal grilling) temperatures may lead to the formation of carcinogenic heterocyclic amines (Salmon et al., 2000). In a study conducted by Line et al. (1991) on ground beef with 2% fat content, the D-value of E. coli O157:H7 at 62.8 °C was found to be 18 s while the z-value was 8.3 °C. In the present study camel meat burgers contained NaCl and phosphate, whereas the beef patties contained no additives. It can be clearly seen that there was a very subtle difference between the D-values obtained at 62 °C in ground beef (18 s) and camel meat (20 s and 16.7 s for E. coli O157:H7 161-84 and strain 1934, respectively). This difference might have been due to the additives in camel meat; however, Mukherjee et al. (2009) found that the addition of 1.4% NaCl and 0.32% STPP to ground beef containing 5% fat, caused no significant difference in terms of thermal inactivation of E. coli O157:H7 between the salt/phosphate and the control groups. As for the camel meat burger to which hump fat was added (fat content 7.9%), the D-values of E. coli O157:H7 at 62.5 °C were similar to those obtained by (Doyle & Schoeni, 1984; Line et al., 1991; OrtaRamirez Price, Hsu, Veeramuthu, Cherry-Merritt, & Smith, 1997) at similar temperatures. They recorded D-values of 24, 28.2 and 25.8 s at 62.5 °C in ground beef with a fat content varying from 3.8% to 30.5% (Table 2). However, in a study conducted by Ahmed, Conner, and Huffman (1995) on ground beef and pork, the D-values at 60 °C for both products (28.2 and 33 s, respectively) were lower than the values reported in the present study. In comparison, Clavero, Beuchat, and Doyle (1998) reported higher D-values both at 60 and 62.5 °C in ground beef. This could possibly be attributed to the cocktail of strains that were used, resulting in overall higher resistance. It was also seen that the choice of agar used for plating made a difference in the cell numbers of E. coli O157:H7 recovered (Clavero et al., 1998). As for the z-values, the camel meat patty had similar z-values compared to ground beef and ground pork (Ahmed et al., 1995; Doyle & Schoeni, 1984; Orta-Ramirez et al., 1997) (Table 2). Comparing the D-values of E. coli O157:H7 16184 and E. coli O157:H7 1934 between CM and CMF, it was found that the D-values in CMF burgers were higher than those in CM burgers. These results are in accordance with Smith, Maurer, Orta-Ramirez, Ryser, and Smith (2001); Faith et al. (1998); and Ahmed et al. (1995) who found that the D-values of E. coli O157:H7 increased as the fat content was elevated. The formulations used in the present study to develop the burgers may also have played a role in determining thermal inactivation. The mode that is used when meat is stored, prior to thermal treatment/cooking, may also play a role in determining the thermal inactivation rates. It was seen that refrigeration, freezing or

t2 − t1 , log N1 − log N2

where N1 and N2 represent the survivor numbers after heating for times t1 and t2, respectively. z-values were calculated for each E. coli O157:H7 strain and Salmonella spp. as the negative reciprocal of the slope of the line created by linear regression of a plot of log10 D-values against the temperatures range tested as described by Osaili et al. (2006).

z − value =

T2 −T1 , log D1 − log D2

where D1 and D2 are D-values at temperatures T1 and T2, respectively. 2.7. Chemical analyses and other measurements Proximate analysis of three different samples of CM or CMF burger (AOAC, 1995) yielded 74.1 ± 0.2% or 65.2 ± 0.2% moisture, 17.3 ± 0.1% or 14.8 ± 1.4% protein, 0.05 ± 0.03% or 7.9 ± 1.4% fat, 2.9 ± 0.0% or 2.3 ± 0.9% ash and 5.7 ± 0.1% or 9.8 ± 0.1% carbohydrate by difference, respectively. 2.8. Statistical analysis The difference between the D and z-values of E. coli O157:H7 strains and Salmonella spp. was tested using two-tailed, unpaired student t-tests using GraphPad Prism Version 7.0 (Graph Pad Software, Inc., La Jolla, CA, USA). Statistical significance was denoted at a P-value of < 0.05. 3. Results Representative survivor curves of E. coli O157:H7 strains and Salmonella spp. in CM and CMF burgers are shown in Figs. 1 and 2. No noticeable shoulders or concavities were detected in the survivor curves of the studied microorganisms. The determination coefficient (R2) of the regression curves was ˃ 0.90 at all studied temperatures. The Dvalues of E. coli O157:H7 (161-84 strain) in CM and CMF burgers at 60, 62.5, 65 and 67.5 °C were 53.5, 20.1, 8.3 and 3 s and 76.0, 25.9, 9.9 and 4.1 s, respectively (Table 1). Although the D-values of E. coli O157:H7 strain 161-84 were overall higher in CMF than in CM burgers, a significant difference (P < 0.05) was found between the two formulations only at 60 and 67.5 °C. z-values of 6.0 and 5.9 °C were obtained in CM and CMF burgers, respectively. No significant difference (P > 0.05) was found between the z-values. The D-values of E. coli O157:H7 (strain 1934) in CM and CMF burgers at 60, 62.5, 65 and 67.5 °C were 48.1, 16.7, 6.6 and 2.8 s, and 90.0, 31.2, 11.0, and 3.2 s, respectively (Table 1). A significant difference was found between the two formulations at all temperatures except 67.5 °C. The z-values were found to be 5.0 and 5.2 °C in CM and CMF burgers, respectively, and they were not significantly different. The D-values of S. Typhimurium in CM and CMF burgers at 55, 57.5, 60 and 62.5 °C were 349.2, 70.2, 18.4, and 6.7 s, and 512.1, 77.1, 21.1, and 8.4 s, respectively (Table 1). A significant difference in terms of D-values was found between the two burger formulations at all temperatures except at 60 °C. The z-values in CM and CMF burgers were 4.4 and 4.2 °C, respectively, and these were not significantly different. As for S. Copenhagen, the D-values obtained in CM and CMF burgers at 55, 57.5, 60 and 62.5 °C were 313.3, 64.8, 16.7, and 6.3 s, and 569.8, 107.1, 24.4, and 9.2 s, respectively (Table 1). There was a significant difference in D-values of S. Copenhagen between the two formulations at all temperatures. The z-values in CM and CMF burgers were 4.4 and 4.1 °C, respectively, and again, these were not significantly different. 3

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Fig. 1. Survival curves of (a) E. coli O157:H7 1934 (R2 = 0.988, correlation coefficient = −0.994) at 65 °C in camel meat burger; (b) E. coli O157:H7 161-84 (R2 = 0.9837, correlation coefficient t = −0.992) at 67.5 °C in camel meat burger; (c) E. coli O157:H7 1934 (R2 = 0.9761, correlation coefficient = −0.9879) at 67.5 °C in camel meat burger with fat and (d) E. coli O157:H7 161-84 (R2 = 0.9798, correlation coefficient = −0.9898) at 62.5 °C in camel meat burger with fat. Dotted line: confidence intervals.

freeze – thawing prior to cooking all had different effects in terms of thermal sensitivity of E. coli O157:H7 (Luchansky et al., 2013). It was observed that the D-values of E. coli O157:H7 were lower in ground beef, which was frozen prior to heat treatment, and as compared to its refrigerated counterparts (Zhao, Doyle, Kemp, Howell, & Zhao, 2004). Even during cooking, the number of times the patty is turned and whether the heating is provided from one turn-over during 10.9 min or multiturns over 6.6 min has also been shown to make a difference in the thermal inactivation of E. coli O157:H7 in ground beef (Rhee, Lee, Hillers, McCurdy, & Kang, 2003). If the meat is cooked at sub-lethal temperatures which usually happens in the case of slow cooking, heatshock proteins could be formed which could protect the cell from thermal destruction. If heat-shock proteins have been produced a higher than normal temperature would be required to destroy the microorganisms (Wiegand, Ingham, & Ingham, 2009). In our study, the D-values of CM burgers at 55, 57.5, 60, 62.5 °C for S. Typhimurium and S. Copenhagen were 349.2, 70.5, 18.4, and 6.7 s and 313.3, 64.8, 16.7, and 6.3 s, respectively; while in a study conducted by Velasquez et al. (2010) on ground pork with a fat content of 2.5% the D-values at 55, 58, 60, 62, 63 °C were 525, 90, 36.6, 28.2, and 16.8 s, respectively. The higher D-values of Salmonella spp. in ground pork compared to camel meat could be possibly due to both different types of meat and Salmonella strains used. However, in a study conducted by Juneja, Marks, and Mohr (2003), it was reported that salt and sodium pyrophosphate enhanced the heat resistivity of Salmonella. Thus, the higher D-values in ground pork could probably also be attributed to the higher NaCl content of 3.2% and the phosphate content

of 0.8% used in the formulation of the ground pork patties, as compared to the 1.8% NaCl and 0.3% STPP content, used in our study on camel meat burgers. Although the addition of NaCl to meat inhibits Salmonella multiplication (Gwak et al., 2016); if the salt is added in increasing amounts, it may enhance the heat resistance of Salmonella at temperatures below 63.5 °C (Juneja et al., 2003). The same effect could be seen with phosphates too, where increasing amounts also enhanced the heat resistance of Salmonella (Juneja et al., 2003). As for camel meat burgers, in which hump fat was added (fat content 7.9%), the D-values at 55, 57.5, 60, 62.5 °C for S. Typhimurium and S. Copenhagen were lower than those reported by Murphy et al. (2002) for Salmonella spp. in ground beef patties with a fat content of 18.6% fat, while the z-value was 9.1 °C. Juneja and Eblen (2000) found the D-value of Salmonella at 58 °C in ground beef with 18% fat to be 150 s and the z-value was 5.5 °C while Orta-Ramirez et al. (1997) found the D-values of Salmonella spp. in ground beef with 3.8% fat to be 910.2 and 126 s at 58 and 63 °C, respectively, and the z-value to be 6.3 °C (Table 3). The thermal resistance of Salmonella was higher in the beef studies most likely because it had more than 2 times the fat content compared to the camel burger formulations. In addition, neither Juneja and Eblen (2000), Murphy et al. (2002); nor Orta-Ramirez et al. (1997) incorporated phosphates or NaCl into their beef patties, while these ingredients were included in the present study. According to the study conducted by Juneja et al. (2003) on ground beef, the presence of these ingredients should have resulted in higher D-values in camel patties compared to the beef patties, but this was not the case. As per the current study, there was a significant difference between the D-values of CM and CMF for both S. 4

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Fig. 2. Survival curves of (a) S. Typhimurium 02–8423 (R2 = 0.9976, correlation coefficient = -0.996) at 62.5 °C in camel meat burger; (b) S. Copenhagen-99 (R2 = 0.9832), correlation coefficient = −0.992) at 62.5 °C in camel meat burger; (c) S. Typhimurium 02–8423 (R2 = 0.9943, correlation coefficient = −0.997) at 62.5 °C in camel meat burger with fat and (d) S. Copenhagen (R2 = 0.9931, correlation coefficient = −0.997) at 62.5 °C in camel meat burger with fat. Dotted line: confidence intervals.

this may happen because as the fat content increases, it provides more insulation to the microorganisms in the meat and consequently the time required to reach a specific internal temperature also increases. This may also have contributed to a lower moisture content as the fat level increased. Low moisture content would mean low water activity, which would result in less efficient heat transmission and hence would reduce the lethality toward microbes (Juneja & Eblen, 2000).

Table 1 D-values (s) of different strains in camel meat burger (CM) and camel meat with fat (CMF) burger. Temperature (°C) E. coli O157:H7 161-84 60 62.5 65 67.5 E. coli O157:H7 1934 60 62.5 65 67.5 S. Typhimurium 55 57.5 60 62.5 S. Copenhagen 55 57.5 60 62.5

CM burger

CMF burger

P-value

53.5a ± 3.4 20.1 ± 2.8 8.3 ± 0.6 3.0a ± 0.2

76.0b ± 2.6 25.9 ± 2.5 9.9 ± 1.0 4.1b ± 0.1

0.0008 0.06 0.07 0.0007

48.1a ± 1.7 16.7a ± 2.3 6.6a ± 0.3 2.8 ± 0.2

90.0b ± 4.7 31.2b ± 0.4 11.0b ± 1.0 3.2 ± 0.3

0.0001 0.0005 0.002 0.14

349.2a ± 13.7 70.5a ± 3.51 18.4 ± 1.2 6.7a ± 0.4

512.1b ± 52.0 77.1b ± 0.3 21.1 ± 3.9 8.4b ± 0.8

0.0063 0.0320 0.31 0.0313

313.3a ± 19.6 64.8a ± 1.7 16.7a ± 1.0 6.3a ± 0.2

569.8b ± 107.2 104.1b ± 13.8 24.4b ± 2.6 9.2b ± 1.6

0.0152 0.0076 0.0090 0.037

5. Conclusion Camel meat burgers are gaining popularity in the Middle East. Ensuring they are safe for consumption from a microbiological aspect is of paramount importance to prevent illness. E. coli O157:H7 strains and Salmonella spp. did not have unusual thermal resistance in camel meat burgers with or without fat as compared with beef burgers. The data gained from the current study could help camel meat burger producers, who use the same recipe, to validate thermal processes as a requirement for a HACCP system. Declaration of competing interest No potential conflict of interest was reported by the authors.

a,b

Means ± standard deviation in the same row differ significantly (P < 0.05).

Acknowledgments Copenhagen and S. Typhimurium. These results are in accordance with Juneja and Eblen (2000) where an increase in the fat content was associated with a respective increase of the D-values. It is speculated that

The authors thank the University of Sharjah for funding the project and Mr. Ismail Abdul Halim at United Arab Emirates University for conducting the chemical analysis. 5

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Table 2 D-values (s) and z-values (°C) of E. coli O157:H7 strains in beef and pork as available in the literature. Ground Beef

Pork Sausage

Parameter

Temperature (°C)

E. coli O157:H7

E. coli O157:H7

E. coli 204P O157:H7

E. coli O157:H7 932

E. coli O157:H7 ATCC 43894

E. coli O157:H7 cocktail (5 strains)

E. coli O157:H7 ATCC 43895

E. coli O157:H7 204P

D-value (s)

50.0 51.7 53.0 54.4 55.0 57.2 58.0 58.9 60.0 62.8 63.0 64.3 65.6 68.0

6930 318 28.2 8.3 30.5 Line et al. (1991)

4692 246 18 8.37 2 Line et al. (1991)

5560.2 1156 28.2 4.35 20 Ahmed et al. (1995)

2390 270 70 45 24 9.6 4.1 17–20 Doyle and Schoeni (1984)

2766 386.4 25.8 7.2 5.60 3.8 Orta - Ramirez et al. (1997)

7434 388.2 37.2 12 4 22 Clavero et al. (1998)

26 11.6 12–17 Kay Shipp (1989)

4838.4 677 33 4.61 30 Ahmed et al. (1995)

z-value (°C) Fat content (%) Authors

Table 3 D-values (s) and z-values (°C) of Salmonella spp. in beef as available in the literature. Ground Beef

Ground Pork

Parameter

Temperature (°C)

Salmonella Cocktail (6 serotypes)

Salmonella Cocktail (8 serotypes)

Salmonella Senftenberg (ATCC 43845)

Salmonella Cocktail (8 serotypes)

D-value (s)

53.0 55.0 57.5 58.0 60.0 62.5 62.0 63.0 65.0 67.5 68.0 70.0

545.4 462 288 144 58.2 34.2 15 9.14 18.6 Murphy et al. (2002)

149.4 28.8 118.8 24.6 5.47 18 (Juneja & Eblen, 2000)

3180 910.2 124.8 13.2 6.24 3.8 (Orta-Ramirez et al., 1997)

525 90 36.6 28.2 16.8 2.5 Velasquez et al. (2010)

z-value (°C) Fat content (%) Authors

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