<?xml version="1.0" encoding="UTF-8"?><!DOCTYPE article PUBLIC "-//NLM//DTD Journal Publishing DTD v2.3 20070202//EN" "journalpublishing.dtd"><article article-type="research-article" dtd-version="2.3" xml:lang="EN" xmlns:mml="http://www.w3.org/1998/Math/MathML" xmlns:xlink="http://www.w3.org/1999/xlink"><front><journal-meta><journal-id journal-id-type="hwp">mmb</journal-id><journal-id journal-id-type="publisher-id">mmb</journal-id><journal-title>Meat and Muscle Biology</journal-title><abbrev-journal-title abbrev-type="full">MMB</abbrev-journal-title><issn pub-type="epub">2575-985X</issn><publisher><publisher-name>American Meat Science Association</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="publisher-id">2019-10-0043</article-id><article-id pub-id-type="doi">10.22175/mmb2019.10.0043</article-id><article-categories><subj-group subj-group-type="heading"><subject/></subj-group></article-categories><title-group><article-title>Consumer Practices and Risk Factors that Predispose to Premature Browning in Cooked Ground Beef<xref ref-type="fn" rid="fn1"><sup>1</sup></xref></article-title></title-group><contrib-group><contrib contrib-type="author" corresp="yes"><name><surname>Ramanathan</surname><given-names>R.</given-names></name><aff><label>2</label>Department of Animal and Food Sciences, Oklahoma State University, Stillwater, OK 74078, USA</aff></contrib><contrib contrib-type="author"><name><surname>Lusk</surname><given-names>J. L.</given-names></name><aff><label>3</label>Department of Agricultural Economics, Purdue University, West Lafayette, IN 47907, USA</aff></contrib><contrib contrib-type="author"><name><surname>Reuter</surname><given-names>R.</given-names></name><aff><label>2</label>Department of Animal and Food Sciences, Oklahoma State University, Stillwater, OK 74078, USA</aff></contrib><contrib contrib-type="author"><name><surname>Mafi</surname><given-names>G. G.</given-names></name><aff><label>2</label>Department of Animal and Food Sciences, Oklahoma State University, Stillwater, OK 74078, USA</aff></contrib><contrib contrib-type="author"><name><surname>VanOverbeke</surname><given-names>D. L.</given-names></name><aff><label>2</label>Department of Animal and Food Sciences, Oklahoma State University, Stillwater, OK 74078, USA</aff></contrib></contrib-group><author-notes><corresp id="cor1">&#x2a;Corresponding author. Email: <email>ranjith.ramanathan@okstate.edu</email> (R. Ramanathan)</corresp></author-notes><pub-date pub-type="epub-ppub"><month>12</month><year>2019</year></pub-date><volume>3</volume><issue>1</issue><fpage>526</fpage><lpage>531</lpage><history><date date-type="received"><day>04</day><month>10</month><year>2019</year></date><date date-type="accepted"><day>04</day><month>11</month><year>2019</year></date></history><permissions><copyright-year>2019</copyright-year><copyright-holder>American Meat Science Association</copyright-holder><license license-type="open-access"><p>This is an open access article distributed under the CC BY-NC-ND license (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc-nd/4.0/">http://creativecommons.org/licenses/by-nc-nd/4.0/</ext-link>)</p></license></permissions><abstract><p>Premature browning is a condition in which cooked ground beef patties turn brown before the USDA recommended temperature of 71&#xb0;C. This presents a potential food safety concern, as consumers may be eating undercooked meat. Although various intrinsic and extrinsic factors contribute to premature browning, the current knowledge indicates that the myoglobin form present within the interior of patties has a significant influence on cooked color. The objective of the study was to determine the consumer practices of cooking, methods to determine doneness, and type of packaging of their purchased ground beef. The data utilized in this study came from Food Demand Survey (FooDS), which tracks consumer preferences, food expenditures, price expectations, and awareness and concern for a variety of food issues. The sample size of FooDS on-line survey for this study was 1,030. The survey questions consisted of doneness of patties, cooking time, and packaging type of patties. Pictures of different packaging types such as a tray, vacuum package, film wrapped, butcher wrapped paper, frozen patties, and chub were also included. Approximately 67% of respondents indicated that they determine the doneness of ground beef patties by visual observation, 18% identify the doneness by a certain length of time for cooking, and 13.5% use a meat thermometer. Interestingly, 69% of respondents noted that they like a brown interior color of cooked patties. If the patties were prone to premature browning, the chances of consuming undercooked patties are higher. Only 5.7% of people bought patties packaged in a vacuum, while 60% of respondents bought patties packaged in film wrapped or in a tray. Even after 20 yr of attempt by the USDA to educate consumers about safe cooking, the current practices increase the likelihood of premature browning and food safety concerns.</p></abstract><kwd-group><title>Keywords</title><kwd>cooking temperature</kwd><kwd><italic>Escherichia coli</italic> O157:H7</kwd><kwd>food safety</kwd><kwd>packaging</kwd><kwd>premature browning</kwd></kwd-group></article-meta></front><body><sec sec-type="introduction"><title>Introduction</title><p>Foodborne illness results in tremendous health and economic burden (<xref ref-type="bibr" rid="bib4">CDC, 2019</xref>). The Center for Disease Control and Prevention reported that ground beef had been associated with 56% of the <italic>Escherichia coli</italic> O157:H7 outbreaks in 2014 (<xref ref-type="bibr" rid="bib3">Andrews, 2014</xref>). Since ground beef is linked with outbreaks of <italic>E. coli</italic> O157:H7 and <italic>Salmonella</italic> contamination, effective pasteurization of ground beef by cooking to recommended temperatures is critical to avoid potential food safety concerns. Prior to the Jack-in-the-Box in the early 1990s, government agencies recommended &#x201c;brown&#x201d; as the doneness color for ground beef. Although the USDA-Food Safety Inspection Service has very long recommended using a food thermometer, reporting/detection of premature browning in 1995 has led to include ground beef in the safety guidelines and noted that visual color is not a reliable indicator of doneness (<xref ref-type="bibr" rid="bib26">USDA-ARS/FSIS, 1998</xref>).</p><p>Premature browning is a condition in which interior of cooked patties appear to have a dull brown or well-done appearance before the USDA recommended temperature of 71.1&#xb0;C to kill enterohemorrhagic <italic>E. coli</italic> and <italic>Salmonella</italic> spp. (<xref ref-type="bibr" rid="bib6">Hague et al., 1994</xref>; <xref ref-type="bibr" rid="bib28">Warren et al., 1996a</xref>, <xref ref-type="bibr" rid="bib29">1996b</xref>; <xref ref-type="bibr" rid="bib1">Amalaradjou et al., 2010</xref>; <xref ref-type="bibr" rid="bib16">Mancini et al., 2011</xref>). If consumers use brown visual color as an indicator of doneness, then premature browning may contribute to undercooking of ground beef. Previous research has noted that 70% of consumers did not use a meat thermometer to determine temperature has reached the recommended level (<xref ref-type="bibr" rid="bib21">Phang and Bruhn, 2011</xref>). Hence, it is critical to understand consumer cooking and temperature monitoring practices to formulate strategies to limit its undesirable consequences.</p><p>Cooked meat color is primarily due to myoglobin denaturation and the Maillard reaction (<xref ref-type="bibr" rid="bib10">King and Whyte, 2006</xref>). The interior cooked color of ground meat products is determined primarily by 3 intrinsic factors such as myoglobin form (the major driver), pH, and end-point temperature (<xref ref-type="fig" rid="fig1">Fig. 1</xref>; <xref ref-type="bibr" rid="bib7">Hunt et al., 1999</xref>; <xref ref-type="bibr" rid="bib8">Killinger et al., 2000</xref>). Myoglobin is the primary protein responsible for meat color and depending on the redox state, it can impart pinkish-purple (deoxymyoglobin), bright-red color (oxymyoglobin), or brown (metmyoglobin). The thermal stability of these 3 myoglobin forms differs with deoxymyoglobin being most heat stable and metmyoglobin the least stable, oxymyoglobin is intermediate in thermal stability. Myoglobin form present within the interior of patties is determined by the type of packaging, storage temperature, and time.</p><fig id="fig1"><label>Figure 1.</label><caption><p>Effects of myoglobin forms on cooked meat color. <sup>1</sup>Conversion from oxymyoglobin to metmyoglobin is not thermodynamically feasible. The arrow indicates visual color change seen during discoloration (<xref ref-type="bibr" rid="bib2">AMSA, 2012</xref>).<sup>2</sup>In premature browning, conversion of ferrohemochrome to ferrihemochrome is fast, although oxymyoglobin forms ferrohemochrome.</p></caption><graphic xlink:href="526fig1"/></fig><p>Premature browning was first reported in the 1990s when the meat industry started using modified atmospheric packaging to improve color stability (<xref ref-type="bibr" rid="bib26">USDA-ARS/FSIS, 1998</xref>). A greater concentration of oxygen within a package can limit the migration of brown metmyoglobin form from the interior to surface and retain bright-red color for a longer time (<xref ref-type="bibr" rid="bib5">English et al., 2016</xref>; <xref ref-type="bibr" rid="bib22">Ramanathan and Mancini, 2018</xref>). Hence, beef purveyors started using high-oxygen (80% oxygen; 4 times greater oxygen content than atmospheric oxygen) in modified atmospheric packaging to maximize oxymyoglobin formation than traditional aerobic PVC packaging with 20% oxygen. Although modified atmospheric packaging minimized discoloration; this has led to food safety concerns (<xref ref-type="bibr" rid="bib11">Lien et al., 2002</xref>; <xref ref-type="bibr" rid="bib25">Suman et al., 2016</xref>).</p><p>Previous study noted that 47% of meat sold in retail is prone to premature browning (<xref ref-type="bibr" rid="bib9">Killinger et al., 2006</xref>). Even though the food safety messages and recommendations to consumers regarding the use of meat thermometer to assure safe cooking temperature are available, limited knowledge is currently available on consumer practices with respect to the type of packaging and cooking procedure. Therefore, the objective of current study was to determine consumer practices and risk factors that predispose to premature browning in cooked ground beef.</p></sec><sec sec-type="materials|methods"><title>Materials and Methods</title><p>The methodology utilized in research has been used in several published studies to determine consumer preferences, food expenditures, price expectations, and awareness and concern for a variety of food issues (<xref ref-type="bibr" rid="bib13">Lusk and Norwood, 2016</xref>; <xref ref-type="bibr" rid="bib18">McFadden and Lusk, 2016</xref>; <xref ref-type="bibr" rid="bib15">Lusk, 2017</xref>). The data utilized in this study came from a Food Demand Survey (FooDS) project that conducted in May of 2017. The FoodS is an online survey with a sample size of at least 1,000 individuals each month. The survey is delivered on the 10th of the month unless that date falls on a weekend, in which case it is moved to the next closest Monday. The requisite sample size is typically acquired within 3 d. The data collected do not constitute a panel because a new sample is drawn each month; however, precisely the same questions are posted each month. The survey is administered to an opt-in panel maintained by Survey Sampling International, and participants receive points worth about $1.50 for participating. The survey questions consisted of doneness of patties, cooking time, and packaging type of patties. Details of questions are included in <xref ref-type="table" rid="tbl1">Table 1</xref>. Pictures of different packaging types such as a tray, vacuum package, film wrapped, butcher wrapped paper, frozen patties, and chub were also included in the survey.</p><table-wrap id="tbl1"><label>Table 1.</label><caption><p>Questions included in the Food Demand Survey to determine consumer practices related to the doneness of patties, cooking time, and packaging type of patties</p></caption><table frame="hsides" rules="groups"><thead><tr><td>Question</td><td align="center">Choice options</td></tr></thead><tbody><tr><td>1: Do you eat ground beef patties (i.e. hamburgers)?</td><td align="center">Yes or no</td></tr><tr><td>2: How do you determine the doneness of ground beef patties when cooking a hamburger?</td><td align="center">A) By using a meat thermometer, B) By visual observation (i.e., looking at the color of meat in the center of the patty), C) By cooking a certain length of time, or D) Other ways</td></tr><tr><td>3: What is your preference for the cooked internal color of ground beef patties?</td><td align="center">Red, pink, brown, or another color<sup>1</sup> such as gray</td></tr><tr><td>4: To what internal temperature (degrees Fahrenheit) does the USDA recommend cooking ground beef patties?</td><td align="center">Respondents answered on a slider scale that ranged from 100 to 200 in 1&#xb0;F increments.</td></tr><tr><td>5: How is the ground beef you normally buy packaged?</td><td align="center">Vacuum sealed, in a box as frozen patties, in butcher wrapped paper, as a chub, and film wrapped in a tray</td></tr></tbody></table><table-wrap-foot><fn><p><sup>1</sup>Another color represents any personal preference such as gray.</p></fn></table-wrap-foot></table-wrap><sec><title>Statistical analysis</title><p>The Food Demand Survey is a rapid response system to understand emerging policy or marketing issues (<xref ref-type="bibr" rid="bib12">Lusk and Murray, 2014</xref>). The FooDs is a national monthly online survey, and the current study had a sample size of 1,030 individuals. The results are weighted to match the US population in terms of age, gender, education, and region of residence (<xref ref-type="bibr" rid="bib14">Lusk and Tonsor, 2016</xref>). The survey consists of a series of questions that are asked in exactly the same way each month. The results are expressed as a percentage in each category. The margin of error, representing twice the standard error and thus a 95% confidence interval for the population proportion, was calculated for each sample proportion with the following equation:<disp-formula><inline-graphic xlink:href="526unequ1"/></disp-formula>where MoE is the margin of error, <inline-formula><inline-graphic xlink:href="526inf1"/></inline-formula> is the sample proportion, and <italic>n</italic> is the sample size (<italic>n</italic> &#x3d; 1,030). Two proportions were considered different if their margins of error did not overlap.</p></sec></sec><sec sec-type="results|discussion"><title>Results and Discussion</title><p>Consumer perception plays a significant role in the judgment of final product quality. This is particularly important in determining the safe cooking temperature of ground patties. In the current survey, out of 1,030 respondents, 88% responded yes to the first questions (do you eat ground beef or cook hamburger). Hence, 906 respondents&#x2019; observations were considered for the study.</p><p>Ground beef is a popular beef product sold in retail (<xref ref-type="bibr" rid="bib24">Shahbandeh, 2018</xref>). Most consumers are aware that ground beef is a potential source of pathogenic bacteria; hence adequate cooking is necessary to prevent foodborne outbreaks. A panel of food safety experts&#x2019; ranked use of meat thermometer offers the most critical opportunity to minimize the risk due to foodborne pathogens (<xref ref-type="bibr" rid="bib17">McCurdy et al., 2006</xref>). In previous research, although 64% of consumers had access to a thermometer, the majority of people looked for visual cues to determine doneness of patties. Popular magazines and cooking shows contradict the USDA recommendation for using a meat thermometer, instead recommending a fixed cooking time (<xref ref-type="bibr" rid="bib21">Phang and Bruhn, 2011</xref>; <xref ref-type="bibr" rid="bib20">Food Network, 2019</xref>). Likewise, in the current research 66.7% of respondents used visual observation, while 19.2% cooked patties to a certain length of time to determine doneness (<xref ref-type="fig" rid="fig2">Fig. 2</xref>). Only 13.5% of respondents used a meat thermometer to ascertain meat has reached pasteurization temperature. Previous study noted only 8.8% of consumers used a meat thermometer to determine the endpoint temperature (<xref ref-type="bibr" rid="bib23">Reynold, 2018</xref>). Interestingly, 69% of respondents indicated that they prefer a brown interior color for cooked patties (<xref ref-type="fig" rid="fig3">Fig. 3</xref>). If the patties were prone to premature browning, the chances of eating undercooked patties would be greater.</p><fig id="fig2"><label>Figure 2.</label><caption><p>Different ways to determine doneness of ground beef patties. Standard error bars are indicated. Responses with a different letter (a&#x2013;d) are different at 95% confidence interval.</p></caption><graphic xlink:href="526fig2"/></fig><fig id="fig3"><label>Figure 3.</label><caption><p>Responses for internal color preferences of cooked patties. Standard error bars are indicated. Responses with a different letter (a&#x2013;d) are different at 95% confidence interval. <sup>1</sup>Another color represents any personal preference such as gray.</p></caption><graphic xlink:href="526fig3"/></fig><p>Of the 13.5% of consumers that used a meat thermometer in the present study, the average and median cooking temperatures were 72.2 and 71.6&#xb0;C, respectively (<xref ref-type="table" rid="tbl2">Table 2</xref>). Interestingly, 28% of respondents cooked ground beef to &#x3c;68.3&#xb0;C (<xref ref-type="fig" rid="fig4">Fig. 4</xref>). In the current survey, approximately 25.8% of respondents preferred pink in the interior of patties. This suggests that personal preference or not knowing the USDA recommended temperature in ground beef patties can predispose to food safety challenges, especially when packaged in aerobic conditions that favor the formation of oxymyoglobin and metmyoglobin.</p><table-wrap id="tbl2"><label>Table 2.</label><caption><p>Summary of cooking temperature and percentage responses</p></caption><table frame="hsides" rules="groups"><thead><tr><td>Percentage of response</td><td align="center">Cooking temperature, &#xb0;C</td></tr></thead><tbody><tr><td>Average cooking temperature</td><td align="center">72.2</td></tr><tr><td>Median cooking temperature</td><td align="center">71.6</td></tr><tr><td>28%</td><td align="center">68 to 71.1</td></tr><tr><td>54%</td><td align="center">&#x3e; 71.1</td></tr><tr><td>32.5%</td><td align="center">&#x3c; 68.3</td></tr><tr><td>34%</td><td align="center">&#x3e; 73.8</td></tr></tbody></table></table-wrap><fig id="fig4"><label>Figure 4.</label><caption><p>Histogram showing the distribution of cooking temperature.</p></caption><graphic xlink:href="526fig4"/></fig><p>Premature browning depends on packaging, age of meat, postmortem muscle pH, and frozen/fresh conditions (<xref ref-type="bibr" rid="bib10">King and Whyte, 2006</xref>). Vacuum packaged patties will have predominant deoxymyoglobin form in the interior (myoglobin form resistant to premature browning), while film wrapped will have oxymyoglobin and possibly metmyoglobin in the center (form prone to premature browning). In the United States and United Kingdom, aerobic packaging is the most common type of packaging for ground beef (<xref ref-type="bibr" rid="bib19">McMillin, 2008</xref>). Consumers associate a bright-red color to freshness and wholesomeness. Both polyvinyl overwrap and high-oxygen packaging can form predominant oxymyoglobin on the surface. In addition, depending on the oxygen concentration within packages (as in high oxygen), oxygen can diffuse from the surface to interior, and results in the formation of oxymyoglobin in the center. Oxymyoglobin form has lower thermal stability than deoxymyoglobin. In this study, the majority of respondents purchased meat in a tray and overwrap (61%; <xref ref-type="fig" rid="fig5">Fig. 5</xref>). Myoglobin form within the interior of these patties can be oxy- or metmyoglobin. Furthermore, in patties that have been stored longer and in the central portion of thicker packages of ground beef, deoxymyoglobin can also be formed when the meat had deoxygenated and returned to a reduced state, thus these portions will form a normal pink color while the outer portions will premature brown. In the current research, only 5.7% of people bought patties packaged in vacuum, while 60% of respondents bought patties packaged in film wrapped or in the tray. Patties packaged in vacuum will have a pinkish-purple color of deoxymyoglobin (vs bright red or brown) and will be resistant to premature browning due to its greater stability to heat. In the current research, 6.4% respondents purchased patties in frozen state. Freeze-thawing can increase the incidence of premature browning (<xref ref-type="bibr" rid="bib27">Van Laack et al., 1996</xref>). The heat transfer to frozen patties can be different from unfrozen patties and the label recommendation on cooking time can lead to insufficient cooking.</p><fig id="fig5"><label>Figure 5.</label><caption><p>Different packaging types of purchased ground beef. Standard error bars are indicated. Responses with a different letter (a&#x2013;c) are different at 95% confidence interval.</p></caption><graphic xlink:href="526fig5"/></fig></sec><sec sec-type="conclusions"><title>Conclusions</title><p>Ground beef has been linked to the occurrence of foodborne illness and cooking is an important step in risk mediation. The survey results indicated that the majority of consumers prefer their cooked ground beef has a brown internal color and 86.5% of consumers did not use a meat thermometer to ensure safe recommended cooking temperature. The survey respondents were using packaging conditions that promote oxymyoglobin and can result in premature browning. The current study suggests that consumer practices increase the likelihood of premature browning and risk associated with eating undercooked patties. Increasing oxygen content in packaging has the potential to minimize wastage due to discoloration, but can lead to cooked color and safety concerns. Characterizing the factors that contribute to premature browning, developing strategies for predictable cooked internal color, and adopting novel consumer educational practices can limit foodborne outbreaks due to consumption of undercooked meat.</p></sec></body><back><fn-group><fn id="fn1"><label>1</label><p>This work was supported, in part, by the USDA National Institute of Food and Agriculture Hatch project and the Division of Agricultural Sciences and Natural Resources at Oklahoma State University.</p></fn></fn-group><ref-list><title>Literature Cited</title><ref id="bib1"><citation citation-type="journal"><person-group person-group-type="author"><name><surname>Amalaradjou</surname><given-names>M. A. R.</given-names></name><name><surname>Baskaran</surname><given-names>S. A.</given-names></name><name><surname>Ramanathan</surname><given-names>R.</given-names></name><name><surname>Johny</surname><given-names>A. K.</given-names></name><name><surname>Charles</surname><given-names>A. 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