We investigated the effects of deep-frying or oven cooking on inactivation of Shiga toxin–producing cells of Escherichia coli (STEC) in meatballs. Finely ground veal and/or a finely ground beef-pork-veal mixture were inoculated (ca. 6.5 log CFU/g) with an eight-strain, genetically marked cocktail of rifampin-resistant STEC strains (STEC-8; O111:H, O45:H2, O103:H2, O104:H4, O121:H19, O145:NM, O26:H11, and O157:H7). Inoculated meat was mixed with liquid whole eggs and seasoned bread crumbs, shaped by hand into 40-g balls, and stored at −20°C (i.e., frozen) or at 4°C (i.e., fresh) for up to 18 h. Meatballs were deep-fried (canola oil) or baked (convection oven) for up to 9 or 20 min at 176.7°C (350°F), respectively. Cooked and uncooked samples were homogenized and plated onto sorbitol MacConkey agar with rifampin (100 μg/ml) followed by incubation of plates at 37°C for ca. 24 h. Up to four trials and three replications for each treatment for each trial were conducted. Deep-frying fresh meatballs for up to 5.5 min or frozen meatballs for up to 9.0 min resulted in reductions of STEC-8 ranging from ca. 0.7 to ≥6.1 log CFU/g. Likewise, reductions of ca. 0.7 to ≥6.1 log CFU/g were observed for frozen and fresh meatballs that were oven cooked for 7.5 to 20 min. This work provides new information on the effect of prior storage temperature (refrigerated or frozen), as well as subsequent cooking via deep-frying or baking, on inactivation of STEC-8 in meatballs prepared with beef, pork, and/or veal. These results will help establish guidelines and best practices for cooking raw meatballs at both food service establishments and in the home.

Ground beef is a staple food in the United States due to its relatively low cost and also due to its versatility for preparing a variety of lunch and/or dinner meals, such as hamburger patties, tacos, meatloaf, and meatballs. Annually, about 42% of all beef in the United States is consumed as ground beef (29). Whereas ground beef is mostly consumed as patties, ground veal is mostly consumed as meatballs, such as in spaghetti. Meatballs are typically made from ground veal, beef, pork, or lamb, as well as from blends of these various meats. Regardless of the specie of meat, meatballs also can contain nonmeat ingredients, such as cereal, bread crumbs, and/or eggs. According to the U.S. Department of Agriculture (USDA) Food Standards and Labeling Policy Book (40), meatballs must contain at least 65% meat, no more than 25% partially defatted chopped meat (i.e., beef or pork) of the meat block, and no more than 12% nonmeat ingredients, such as binders and extenders (i.e., soy protein concentrate). Meatballs can be prepared by consumers at home or by industry or food service establishments in a variety of styles, flavors, and sizes. Meatballs are usually stored frozen or refrigerated when prepared by consumers or are typically sold “frozen fully cooked,” “frozen partially cooked,” and/or “frozen raw” when manufactured commercially. As with other ground meat products, meatballs must be cooked to an internal temperature of 71.1°C (160°F), as measured by a food thermometer, to avoid foodborne illnesses that may be caused by the consumption of raw or undercooked meat contaminated with foodborne pathogens, such as Shiga toxin–producing cells of Escherichia coli (STEC (39, 47)).

Every year in the United States, ingestion of food contaminated with E. coli O157:H7 (STEC O157) and/or non-O157:H7 STEC results in ca. 175,900 illnesses, ca. 2,410 hospitalizations, and ca. 20 deaths (32), with associated economic costs estimated for both pathogens at ca. $300 million (17). Despite a concerted effort by food safety professionals from industry, professional organizations, and regulatory agencies to help identify and prioritize research needs to control STEC at various points along the beef chain, recent recalls and associated clusters of illnesses linked to STEC reinforce the need for additional research on validation of processing interventions for eliminating STEC in ground meat during manufacture, storage, and/or cooking. Over the last three decades, consumption of raw or undercooked nonintact meats, particularly ground beef patties, has resulted in numerous recalls and outbreaks attributed to STEC (4, 6, 11, 15, 38). Therefore, because of the elevated risks associated with the consumption of undercooked beef contaminated with STEC, the USDA Food Safety and Inspection Service (USDA-FSIS) has declared STEC O157 and a subset of six other STEC serogroups, denoted as the “Big Six” (serogroups O26, O45, O103, O111, O121, and/or O145), as adulterants in raw ground beef and/or veal and in raw whole muscle beef subjected to enhancement processes, such as tenderization (39, 41, 42).

Preliminary data from the USDA-FSIS Beef and Veal Carcass Baseline Survey for the first semester of 2015 estimated the prevalence of STEC O157 on beef carcasses at 5 (1.08%) of 463 samples at the prechill carcass processing stage, whereas a percent positive of one (1.04%) of 96 samples was reported for veal carcasses sampled at the prechill stage (48). Likewise, testing of raw ground beef component samples in federal plants during the same period established a prevalence of one (0.31%) of 325 samples and 0 (0.0%) of 59 samples for STEC O157 in beef and veal, respectively. For non-O157 STEC (the “Big Six” sero-groups), similar prevalence was observed for non-O157 STEC on beef carcass samples, whereas a higher percent positive for non-O157 STEC on veal carcass samples and from samples of raw ground beef component and of veal was reported in comparison with the percent positive for STEC O157. At the prechill carcass processing stage, one (0.21%) of 465 samples and nine (9.27%) of 97 samples of beef and veal samples tested, respectively, were positive for non-O157 STEC. In the raw ground beef component samples, the percent positive samples for non-O157 STEC in beef and veal were three (0.99%) of 303 samples and five (10.42%) of 48 samples, respectively.

In addition to the higher prevalence of non-O157 STEC on prechill veal carcasses, veal trimmings, and ground veal than on similar beef products (43), over the past 5 years, veal products have frequently been recalled due to possible contamination with STEC O157 or non-O157 STEC. For example, ca. 770 lb (349 kg) of veal harvested from nine carcasses was recalled in Ohio in 2009 due to possible contamination with STEC O157 (18). In 2013, ca. 1,260 lb (571.5 kg) of boneless veal trimmings was recalled in California due to potential contamination with STEC O157 (2). In that same year, the USDA-FSIS recalled ca. 12,600 lb (5,715 kg) of boneless veal products due to potential contamination with serotype O157:H7, O145, and O45 strains of E. coli (44). In 2014, there was a recall of an undetermined amount of lean ground veal due to potential contamination with E. coli O157:NM in Canada (9). As final examples, in 2015, a federally inspected establishment in Washington recalled ca. 2,520 lb (1,143 kg) of boneless veal trimmings and whole muscle products that tested positive for STEC O157, whereas another recall of an undetermined amount of boneless trimmings was issued by an establishment in Illinois due to potential contamination with both STEC O157 and non-O157 STEC serotypes (45, 46). Although veal has not caused any reported human illnesses in the United States, the consumption of veal liver and beef and veal tartare in Canada was associated with outbreaks of STEC O157 in 2012 and 2013, respectively (8, 9, 13). Thus, given the recovery of STEC O157 and non-O157 STEC from veal and beef products, the numerous outbreaks linked to both pathogens due to the consumption of raw and/or undercooked ground beef, and the scarcity of information about thermal inactivation of STEC in formed ground meat products, the objective of this study was to validate the effects of deep-frying or oven cooking on inactivation of STEC in meatballs to establish the potential risk to public health related to preparation and cooking of these products.

Bacterial strains.

The following eight rifampin-resistant (100 μg/ml; Sigma Chemical Company, St. Louis, MO) strains of Shiga toxin–producing cells of E. coli (STEC-8) were maintained and subsequently prepared as a cocktail for this study as previously described (25, 26, 27): H30 (serotype O26:H11), JB1-95 (serotype O111:H-), CDC 96-3285 (serotype O45:H2), CDC 90-3128 (serotype O103:H2), ATCC BAA-2326 (serotype O104:H4), CDC 97-3068 (serotype O121:H19), 83-75 (serotype O145:NM), and USDA-FSIS 011-82 (serotype O157:H7).

Inoculation and preparation of meatballs.

Freshly processed and finely ground veal (veal; ca. 97:3 [lean:fat]) and an approximately equal mixture of finely ground veal, beef, and pork (meat mix; ca. 90:10 [lean:fat]) were procured from a local butcher and stored at 4°C for up to 24 h before preparing and inoculating the meatballs. In brief, the ground veal or the ground meat mix was aseptically transferred to a sterile, stainless steel food processing bowl and separately inoculated with the rifampin-resistant STEC-8 cocktail (1 ml of inoculum to 100 g of ground meat) to achieve a target level on average of ca. 7.0 log CFU/g. The inoculated ground meat (ca. 4.5 kg) was mixed with pasteurized liquid whole eggs (900 ml; EggBeaters, ConAgra Foods Inc., Omaha, NE) and with flavored bread crumbs (850 g; Cento, Cento Fine Foods Inc., Thorofare, NJ) in a commercial mixer (Univex SRM12, Univex, Salem, NH) for 2 min at room temperature (21 ± 1°C) to ensure even distribution of the inoculum and ingredients. Portions (40 g each) of the inoculated batter were shaped into meatballs by hand and were placed onto sterile Styrofoam trays (1012S, Genpak, Glens Falls, NY). Each tray was placed individually into nylon-polyethylene bags (Koch Supplies, Kansas City, MO), heat sealed, and then stored either at −20°C (i.e., frozen) for up to 18 h (model 5145B42, Thomas Scientific, Swedesboro, NJ) or at 4°C (i.e., fresh) for up to 18 h (model PR505750R, Thermo Fisher Scientific, Waltham, MA).

Cooking meatballs.

Meatballs were baked in an electric convection oven (model XL HE650CO, Calphalon, Toledo, OH) or deep-fried in an electric fryer (model 0548812, Presto, Eau Claire, WI) filled with ca. 3.8 liters of canola oil (America's Choice, A&P Inc., Montvale, NJ). Based on an informal online search on cooking temperatures for meatballs and on cursory inspection of product labels at grocery stores, we selected a target cooking temperature of ca. 176.7°C (350°F) and cooking times that ranged from 2.5 to 9 min for meatballs cooked in the fryer and 7.5 to 20 min for meatballs cooked in the oven. Both the air temperature of the oven and the temperature of the oil in the fryer were preheated to ca. 176.7°C prior to cooking. When cooked in the oven (Fig. 1A and 1B), the top surface of a nonstick bake pan (Calphalon) was covered with a piece of aluminum foil and sprayed with cooking oil (PAM Grilling, ConAgra, Omaha, NE). Next, using an alcohol-sterilized stainless steel tong (Calphalon), 12 meatballs were placed side-by-side (three meatballs by four meatballs), with a ca. 3.5-cm space between each meatball, in a single layer on the bake pan for subsequent cooking in the oven. When cooked in the fryer (Fig. 2A and 2B), 12 meatballs were placed side-by-side without space between them, into the fryer basket just prior to cooking. Frozen meatballs were removed from the freezer and were cooked for 0.0, 15.0, 16.25, 17.5, or 20.0 min in the oven or for 0.0, 5.0, 6.0, 7.5, or 9.0 min in the fryer. Likewise, fresh meatballs were removed from the refrigerator and were cooked for 0.0, 7.5, 9.0, 10.5, or 12.5 min in the oven or for 0.0, 2.5, 3.5, 4.5, or 5.5 min in the fryer. The air temperature of the oven and the oil temperature in the fryer were monitored using calibrated stainless steel Type J thermocouples (Omega Engineering Inc., Stamford, CT), which were individually connected to an 8-channel data logger (model OM-CP-OCTTEMP, Omega Engineering). At each sampling time, three meatballs were removed from the oven or from the fryer with the aid of an alcohol-sterilized stainless steel tong (Calphalon), and the internal temperature of each meatball was measured using a calibrated handheld thermometer (model AccuTuff 340, Atkins Technical Inc., Gainesville, FL). Next, meatballs were weighed and then immediately transferred into separate sterile filter stomacher bags (type XX-C003, Microbiology International, Frederick, MD). Bagged meatballs were rapidly smashed by hand and then were quickly submerged in an ice-water bath. The time from removal from the oven or fryer to submersion in the ice bath was ca. 3 min. Each meatball was analyzed within 30 min after being placed in the ice-water bath. The experimental matrix consisted of one inoculation level × two meat types (veal versus meat mix) × two meat states (fresh versus frozen) × two cooking appliances (oven versus fryer) × five sampling times × three meatballs per sampling time, for a total of 120 meatballs sampled per trial.

FIGURE 1.

Meatballs placed side-by-side with a ca. 3.5-cm space between each meatball, in a single layer on the bake pan (A) for subsequent cooking in the electric convection oven (B).

FIGURE 1.

Meatballs placed side-by-side with a ca. 3.5-cm space between each meatball, in a single layer on the bake pan (A) for subsequent cooking in the electric convection oven (B).

Close modal
FIGURE 2.

Meatballs placed side-by-side without space between them into the fryer basket (A) for subsequent cooking in the electric fryer (B).

FIGURE 2.

Meatballs placed side-by-side without space between them into the fryer basket (A) for subsequent cooking in the electric fryer (B).

Close modal

Enumeration of STEC.

The pathogen was recovered from meatballs by adding 60 ml of sterile 0.1% peptone water (Difco, BD, Sparks, MD) to each sterile filter stomacher bag and macerating for 2 min (Stomacher 400, Seward, Cincinnati, OH), as described by Luchansky et al. (26). A 10-ml aliquot of the macerate was transferred to a sterile 15-ml screw-cap conical centrifuge tube, and the resulting slurry was serially diluted in 0.1% peptone water and surface plated onto sorbitol MacConkey agar (Difco, BD) plates plus rifampin (100 μg/ml; Sigma). Plates were incubated at 37°C for 24 h and surviving cells were enumerated. Samples that tested negative for the pathogen by direct plating (≤0.36 log CFU/g) were enriched as described previously (23, 26).

Physicochemical analyses.

Prior to cooking, the proximate composition analysis of a composite sample (200 g total) of raw ground veal and of the ground raw veal-beef-pork mix, as well as 200 g of the ground veal and ground meat mix after the addition of eggs and seasoned bread crumbs, from each of two trials was determined by a commercial laboratory using methods approved and described by the Association of Official Analytical Chemists (5).

Statistical analyses.

Means and standard deviations were calculated from individual sets of data for each of the three or four separate trials by using the statistical function option that is provided with Microsoft Excel 2003 software (Redmond, WA). Analysis of variance was used to determine the effects and interactions of the factors on the log reduction values. Pairwise differences in lethality observed for each combination of meat type, meat state, and cooking appliance were considered significant (α = 0.05) using SAS PROC MIXED with the Adjust=Sidak option in the least-squares means statement to prevent inflation of false-positive probability (SAS Version 9.4, SAS Institute, Cary, NC).

Thermal inactivation of STEC O157 and/or non-O157 STEC in ground beef patties and various nonintact beef products has been widely investigated (1, 12, 14, 24–26, 28, 33, 34, 36, 37); however, considerably fewer studies have addressed thermal inactivation of these pathogens in non-intact veal products (21, 27). In fact, to our knowledge, this is the only published study to quantify thermal inactivation of STEC in meatballs containing veal. In related studies, Luchansky et al. (27) reported ca. 2.0- to 6.7-log CFU/g reductions of STEC O157 when nonbreaded veal cutlets were cooked in 15 ml of canola oil on a flat-surface, electric skillet heated at 191.5°C on a ceramic hot plate for 0.75 to 2.25 min per side, whereas reductions of ca. 1.1 to 3.5 log CFU/g were observed when breaded cutlets were cooked under the same conditions. However, when breaded cutlets were cooked in 30 ml of canola oil, pathogen numbers decreased by ca. 2.6 to 6.4 log CFU/g. Kulas et al. (21) also quantified thermal inactivation of STEC-8 in veal cordon bleu, a meal prepared by placing a slice of cheese and a slice of ham between two (tenderized) veal cutlets and then coating or breading the resulting product. The authors reported ca. 1.5- to 3.5-log CFU/g reductions of STEC-8 in cordon bleu cooked on a griddle for ≤6 min per side in 45 ml of extra virgin olive oil preheated to 191.5°C, whereas reductions of ≥6.2 log CFU/g were achieved when the meat was cooked for 7 to 10 min per side. Lastly, Li (22) reported that cooking veal patties (ca. 175 g each; ca. 2.2% fat) on a double broiler pan in a griller set at 177°C to a target internal temperature of 55 to 76°C for 5 to 7 min with a 3-min rest resulted in a 5.7- to ≥6.6-log reduction in STEC O157 numbers.

In agreement with the abovementioned studies, the results of the present study demonstrated that, regardless of meat type (veal versus meat mix), meat state (fresh versus frozen), or cooking appliance (oven versus fryer), the higher the internal meatball temperature, the greater the inactivation of STEC-8. Also, greater reductions of STEC were observed with increasing cooking times. In general, no significant differences (P ≥ 0.05) in pathogen inactivation were observed between meatballs prepared with veal and meatballs prepared with a mixture of veal, beef, and pork meat (Table 1). Our results demonstrated that deep-frying frozen veal or meat-mix meatballs in canola oil preheated at ca. 175.6 ± 2.0°C for 5.0, 6.0, 7.5, or 9.0 min resulted in total reductions of ca. 0.7, 1.1, 3.3, or 5.9 and ca. 0.7, 1.4, 1.9, or 5.9 log CFU/g, respectively. When fresh veal or meat-mix meatballs were deep-fried for 2.5, 3.5, 4.5, or 5.5 min, total reductions of ca. 1.1, 1.9, 4.3, or 6.1 and ca. 1.0, 2.5, 4.5, or ≥6.1 log CFU/g, respectively, were observed. Likewise, when frozen veal and meat-mix meatballs were heated in a convection oven set at ca. 176.7°C for 15.0, 16.25, 17.5, or 20.0 min, total reductions of ca. 1.0, 2.4, 4.5, or 6.0 and 1.0, 2.3, 4.6, or ≥6.1 log CFU/g, respectively, were achieved. Similar results were observed when fresh veal and meat-mix meatballs were heated for 7.5, 9.0, 10.5, or 12.5 min; total reductions of ca. 0.7, 1.4, 3.8, or 6.1 and 0.7, 2.0, 5.1, or ≥6.1 log CFU/g, respectively, were achieved. Subsequent enrichment of frozen meatballs that were heated in the oven for 20.0 min yielded no viable cells of STEC-8 (Table 2). In addition, regardless of the meat type or cooking method, to achieve similar internal meat temperatures, frozen meatballs required a cooking time nearly twofold longer than the time for fresh meatballs. The average final internal temperatures achieved in frozen meatballs cooked in the fryer for 5.0, 6.0, 7.5, or 9.0 min were 6.0 ± 6.1, 16.2 ± 8.6, 48.9 ± 14.1, and 68.4 ± 7.5°C, respectively; whereas, when frozen meatballs were cooked in the oven for 15.0, 16.25, 17.5, or 20.0 min, the average final internal temperatures were 41.9 ± 9.9, 54.5 ± 8.4, 68.4 ± 9.0, and 80.0 ± 8.0°C, respectively (Table 3). For fresh meatballs cooked in the fryer for 2.5, 3.5, 4.5, or 5.5 min, the average final internal temperatures were 21.7 ± 6.1, 35.7 ± 7.9, 52.0 ± 9.2, and 69.6 ± 10.1°C, respectively; whereas, when fresh meatballs were cooked in the oven for 7.5, 9.0, 10.5, or 12.5 min, the average final internal temperatures were 39.0 ± 4.1, 51.9 ± 5.2, 63.4 ± 5.0, and 72.1 ± 5.9°C, respectively (Table 3).

TABLE 1.

Recovery of STEC-8 from various types of meatballs cooked in a deep fryer or in a convection ovena

Recovery of STEC-8 from various types of meatballs cooked in a deep fryer or in a convection ovena
Recovery of STEC-8 from various types of meatballs cooked in a deep fryer or in a convection ovena
TABLE 2.

Recovery of STEC-8 from fresh and frozen meatballs by direct plating and enrichmenta

Recovery of STEC-8 from fresh and frozen meatballs by direct plating and enrichmenta
Recovery of STEC-8 from fresh and frozen meatballs by direct plating and enrichmenta
TABLE 3.

Average internal temperature in frozen and fresh veal and pork-beef-veal meatballs cooked in a deep fryer or a convection oven

Average internal temperature in frozen and fresh veal and pork-beef-veal meatballs cooked in a deep fryer or a convection oven
Average internal temperature in frozen and fresh veal and pork-beef-veal meatballs cooked in a deep fryer or a convection oven

Storage temperature (i.e., 4 versus −18°C) and/or thawing regimens may also have a direct impact on the response of STEC to subsequent heating, because freezing temperatures may increase the heat resistance of the pathogen (19, 20). More specifically, Jackson et al. (19) reported that storage of ground beef patties (ca. 22% fat; 114 g each) at refrigeration or freezing temperatures prior to cooking had a significant effect on thermal inactivation of STEC O157 strain ATCC 43895. These authors observed greater thermal inactivation for this strain when inoculated beef patties were stored at 3 or 15°C for up to 9 h as compared with otherwise similar patties that were stored at −18°C for 8 days and then cooked on a griddle to target internal temperatures of 62.8 or 68.3°C. Kotula and colleagues (20) found that nonpathogenic E. coli strains were more heat tolerant when inoculated into ground beef patties (85 g) that were stored at −45 or 4°C for 1 day and then grilled for 2 to 8 min to internal temperatures ranging from 149 to 232°C than when inoculated into otherwise similar patties that were previously stored at 4°C for 12 days. In contrast, Luchansky et al. (25) reported reductions of 2.5 to ≥7.0 log CFU/g for STEC O157 and non-O157 STEC after beef patties (300 g each; 7 or 30% fat) that were refrigerated, frozen, or frozen and then thawed at 4 or 21°C were cooked to 60.0 to 76.7°C on an open-flame gas grill or on an electric clam-shell grill. Although the authors did not observe significant differences in thermal inactivation of the pathogen related to the storage conditions prior to cooking, they concluded that cooking beef patties from a frozen state required twice the amount of time to reach the target internal temperature than otherwise similar patties that were placed on the grill in a refrigerated state.

Although STEC may not present atypical heat resistances in ground beef (10), the pathogen may survive for extended periods during storage at freezing temperatures (3, 10, 16, 25). Therefore, the practice of cooking meat directly from a frozen and/or a semifrozen state may present a serious risk to public health due to the higher probability for cold spots as a result of nonuniform internal heating and due to the presence of STEC that were not eliminated by freezing alone (25). Cooking frozen ground meats, such as meatballs and patties, prior to thawing is a common practice employed by consumers, restaurants, and/or food service establishments. Phang and Bruhn (31) conducted a survey to evaluate consumer practices for preparing ground beef patties at home and reported that 44 (ca. 22%) of 199 volunteer respondents did not defrost frozen beef patties before cooking. Likewise, Bogard et al. (7), in a multistate survey related to ground beef handling and preparation practices in restaurants, reported that 66 (26%) of 256 independent restaurants and 49 (39%) of 127 chain restaurants cooked ground beef patties starting from a frozen and/or a partially frozen state. The authors also reported that the same preparation practices were used by sit-down restaurants (58 [20%] of 289) and quick-service or fast food restaurants (44 [61%] of 72) for cooking beef patties. However, regardless of the ability of STEC to withstand extended storage at freezing temperatures, subsequent cooking and/or reheating regimens used by consumers at home or by cooks and chefs at restaurants or food service establishments should be effective to eliminate low levels of pathogens that may be present in ground beef and veal. Thus, validation of cooking regimens and the development of cooking guidelines for fresh and frozen meatballs are essential to lessen the likelihood of foodborne illnesses associated with the consumption of these products, which may, on occasion, be contaminated with low levels of STEC and which may not be adequately cooked, particularly if placed directly on the heating surface in a frozen state.

The fat content, and the inclusion of nonmeat ingredients such as salt and bread crumbs, in meatballs and other nonintact meat products can protect bacterial cells against heat and/or affect the rate of heat penetration into the meat during cooking (28, 30). The proximate composition of the raw ground veal and raw ground meat mix, as well as the associated meatballs made therefrom, are presented in Table 4. Inclusion of liquid whole eggs and seasoned bread crumbs did not significantly (P ≥ 0.05) affect the pH, water activity, acidity, or the fat, salt, or protein levels of the uncooked veal meatballs. Likewise, inclusion of these ingredients to prepare ground meat-mix meatballs did not significantly (P ≥ 0.05) affect the pH, acidity, or the fat or moisture levels of the final raw product. A significant (P ≤ 0.05) difference in fat levels between the ground veal and the ground meat mix was observed. This result was somewhat expected, because veal is typically leaner than beef, and it is also even leaner than pork. These results are also in agreement with previous studies reporting that levels of fat in ground veal ranged from ca. 2.2 to 2.7% (22, 49). Although studies reported that the higher the fat content in the heating menstruum, the greater the protection afforded to microorganisms from heat during cooking (28, 30), our results revealed that, in general, significantly (P ≥ 0.05) fewer cells of STEC-8 were inactivated in frozen and fresh veal-beef-pork meatballs (ca. 10.8% fat) than in frozen and fresh veal meatballs (ca. 1.65% fat) that were cooked in the convection oven. Similarly, no significant (P ≥ 0.05) decrease in STEC-8 levels was observed in fresh and frozen veal-beef-pork meatballs compared with fresh and frozen veal meatballs that were cooked in the fryer.

TABLE 4.

Proximate composition of raw, finely ground veal and a mixture of finely ground veal, beef, and pork, as well as meatballs made from veal or the mixture of veal, beef, and porka

Proximate composition of raw, finely ground veal and a mixture of finely ground veal, beef, and pork, as well as meatballs made from veal or the mixture of veal, beef, and porka
Proximate composition of raw, finely ground veal and a mixture of finely ground veal, beef, and pork, as well as meatballs made from veal or the mixture of veal, beef, and porka

In addition to product composition (e.g., fat content, pH level, or inclusion of nonmeat ingredients), and the state of the meat prior to cooking (e.g., refrigerated versus frozen), the cooking method (e.g., deep-frying versus baking versus pan-frying) can also affect the extent of thermal inactivation of STEC in ground meat products (25, 35). More specifically, our results revealed that, regardless of the meat state, it took more time to achieve the same level of inactivation in the oven compared with the fryer. To achieve a 5-log reduction of STEC-8 in fresh or frozen meatballs cooked in the deep fryer, it was necessary to cook the meat for 5.5 or 9.0 min, respectively; whereas, to achieve similar reductions of STEC in fresh or frozen meatballs in the oven, meatballs needed to be cooked for 12.5 or 20 min.

In summary, our data validate that cooking veal or meat-mix meatballs in a deep fryer or in an electric convection oven is effective for eliminating STEC cells that may be present at low levels in naturally contaminated meat. In addition, parameters such as cooking method (e.g., deep-frying versus baking), state of the product prior to cooking (e.g., refrigerated versus frozen), and formulation must be taken into consideration when cooking ground beef products, because these variables may affect the thermal inactivation of STEC in meatballs. Results of this study will be helpful to consumers, restaurants, and food service operations to validate their time-temperature cooking regimens to lower any public health risk potentially associated with STEC due to consumption of undercooked ground veal, pork, and beef. Companion studies are also being conducted to evaluate the effectiveness of high pressure processing, alone or in combination with cooking, to inactivate STEC in meatballs. Future studies will optimize cooking time-temperature parameters for fully cooked and partially cooked meatballs and will evaluate the effect of binders and extenders in the formulation, as well as the size and compaction of meatballs, on thermal inactivation of STEC.

We extend our sincere appreciation to Manuela Osoria (USDA, Agricultural Research Service, Eastern Regional Research Center, Wynd-moor, PA) for her assistance on this project. We extend a special note of thanks to Dr. Bryan Vinyard (USDA, ARS, Beltsville Agricultural Research Center, Beltsville, MD) for statistically analyzing these data. This material is based upon work supported by the National Institute of Food and Agriculture, USDA, under award no. 2012-68003-30155. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA.

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