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<article xmlns:mml="http://www.w3.org/1998/Math/MathML" xmlns:xlink="http://www.w3.org/1999/xlink" dtd-version="1.3" xml:lang="en" article-type="research-article"><?properties manuscript?><processing-meta base-tagset="archiving" mathml-version="3.0" table-model="xhtml" tagset-family="jats"><restricted-by>pmc</restricted-by></processing-meta><front><journal-meta><journal-id journal-id-type="nlm-journal-id">0405525</journal-id><journal-id journal-id-type="pubmed-jr-id">4760</journal-id><journal-id journal-id-type="nlm-ta">J Environ Health</journal-id><journal-id journal-id-type="iso-abbrev">J Environ Health</journal-id><journal-title-group><journal-title>Journal of environmental health</journal-title></journal-title-group><issn pub-type="ppub">0022-0892</issn></journal-meta><article-meta><article-id pub-id-type="pmid">35979513</article-id><article-id pub-id-type="pmc">9380651</article-id><article-id pub-id-type="manuscript">HHSPA1791663</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>Tools and Techniques to Promote Proper Food Cooling in Restaurants</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Hedeen</surname><given-names>Nicole D.</given-names></name><degrees>MS, RS</degrees><aff id="A1">Environmental Health Division, Minnesota Department of Health</aff></contrib><contrib contrib-type="author"><name><surname>Schaffner</surname><given-names>Donald</given-names></name><degrees>PhD</degrees><aff id="A2">Food Science Department, Rutgers University</aff></contrib><contrib contrib-type="author"><name><surname>Brown</surname><given-names>Laura Green</given-names></name><degrees>PhD</degrees><aff id="A3">National Center for Environmental Health, Centers for Disease Control and Prevention</aff></contrib></contrib-group><author-notes><corresp id="CR1"><bold><italic toggle="yes">Corresponding Author:</italic></bold> Nicole D. Hedeen, Senior Epidemiologist, Environmental Health Division, Minnesota Department of Health, 625 Robert Street North, Saint Paul, MN 55164. <email>nicole.hedeen@state.mn.us</email>.</corresp></author-notes><pub-date pub-type="nihms-submitted"><day>31</day><month>3</month><year>2022</year></pub-date><pub-date pub-type="ppub"><month>3</month><year>2022</year></pub-date><pub-date pub-type="pmc-release"><day>16</day><month>8</month><year>2022</year></pub-date><volume>84</volume><issue>7</issue><fpage>8</fpage><lpage>11</lpage><abstract id="ABS1"><p id="P1">Slow cooling of hot foods is a common pathogen proliferation factor contributing to restaurant-related outbreaks. The Food and Drug Administration (FDA) model <italic toggle="yes">Food Code</italic> provides guidelines on the time and temperatures needed for proper cooling and recommends several methods to facilitate rapid food cooling. Restaurants continue to struggle with proper cooling even given these guidelines (<xref rid="R5" ref-type="bibr">Hedeen &#x00026; Smith, 2020</xref>). Research summarized in this guest commentary indicates that portioning foods into containers with a depth of &#x0003c;3 in. and ventilating the containers during the cooling process promote rapid cooling. Restaurant operators and health department inspectors could use these cooling methods to maximize cooling efforts. Additionally, a simple method (using a mathematical equation) could help restaurant operators and inspectors to estimate the cooling rates of foods. This simple method uses only two food temperatures taken at any two points in the cooling process (using the equation [Log(T<sub>1</sub> &#x02212; T<sub>df</sub>) &#x02212; Log(T<sub>2</sub> &#x02212; T<sub>df</sub>)]/&#x003b4;t) to estimate whether the food is expected to meet FDA cooling guidelines. This method allows operators and inspectors to identify foods unlikely to meet FDA guidelines and take corrective actions on those foods without having to monitor food temperatures for the entire cooling process, which typically takes 6 hr. More research is underway to further refine aspects of this method.</p></abstract></article-meta></front><body><sec id="S1"><title>Introduction</title><p id="P2">Improper cooling of hot food by restaurants is a significant cause of foodborne illness outbreaks (<xref rid="R1" ref-type="bibr">Brown et al., 2012</xref>). Cooling hot foods too slowly is one of the most common pathogen proliferation factors contributing to restaurant-related outbreaks (<xref rid="R3" ref-type="bibr">Gould et al., 2013</xref>). Of the 251 outbreaks that occurred during 2014&#x02013;2016, 10% had improper cooling as a contributing factor to the outbreak (<xref rid="R7" ref-type="bibr">Lipcsei et al., 2019</xref>). Hot foods should be cooled rapidly to minimize pathogen proliferation and subsequent foodborne illness risk.</p><p id="P3">The Food and Drug Administration (FDA) model <italic toggle="yes">Food Code</italic> (Section 3-501.14) provides guidelines for retail and foodservice establishments to cool foods classified as needing time and temperature control for safety. These guidelines state that foods must be cooled from 135 &#x000b0;F (57 &#x000b0;C) to 70 &#x000b0;F (21 &#x000b0;C) within 2 hr, and from 135 &#x000b0;F (57 &#x000b0;C) to 41 &#x000b0;F (5 &#x000b0;C) within a total of 6 hr or less (<xref rid="R9" ref-type="bibr">U.S. Department of Health and Human Services, 2017</xref>). To help reduce foodborne illness risk, the <italic toggle="yes">Food Code</italic> also recommends several methods to promote rapid food cooling. These methods include separating food into smaller portions; stirring food in a container placed in an ice water bath; adding ice as an ingredient; and placing food in shallow pans, in containers that promote heat transfer, and in rapid cooling equipment. Even with these guidelines, restaurants continue to struggle with proper cooling (<xref rid="R5" ref-type="bibr">Hedeen &#x00026; Smith, 2020</xref>). And as a model code for regulating retail and food service establishments, the <italic toggle="yes">Food Code</italic> does not specify how to apply cooling methods in varying situations or whether some methods are better than others.</p><p id="P4">The <italic toggle="yes">Food Code</italic> recommends that retail food establishments verify that their cooling practices are effective as well as monitor and record food temperatures during the cooling process, but research suggests that many establishments do not always engage in these practices (<xref rid="R1" ref-type="bibr">Brown et al., 2012</xref>; <xref rid="R5" ref-type="bibr">Hedeen &#x00026; Smith, 2020</xref>). A study by <xref rid="R2" ref-type="bibr">FDA (2018)</xref> found that cooling practices did not meet FDA guidelines at least once in 72% of 273 full-service restaurants where cooling was observed.</p><p id="P5">Cooling is difficult for operators and inspectors to assess because of the time required to adequately monitor the cooling process. Restaurant operators work in a dynamic and busy environment, and frequent monitoring of temperatures is not always feasible. Multiple factors influence an operator&#x02019;s ability to monitor food temperatures to ensure proper cooling. These factors can include insufficient staffing, the time of day foods are cooled (e.g., early or late shifts), and how busy a restaurant is throughout the day (<xref rid="R4" ref-type="bibr">Green &#x00026; Selman, 2005</xref>). Inspectors are typically in an establishment for fewer than the 6 hr needed to document proper cooling. Other options for assessing proper cooling include discussions with the restaurant manager, review of temperature logs to determine cooling start time, and subsequent comparison with food time and temperatures taken during the inspection. Use of thermocouples and data loggers for later retrieval or returning later in person to continue the inspection and check temperatures are other options, although inspectors cannot always conduct multiple visits to an establishment during a day. Focusing on specific cooling methods, rather than the full cooling process, might be another way to identify cooling issues during routine inspections.</p><p id="P6">Identification of practices that best promote proper food cooling can support operators and inspectors in their efforts to cool food properly. Research conducted by the Centers for Disease Control and Prevention&#x02019;s Environmental Health Specialists Network (EHS-Net), Rutgers University, and the Minnesota Department of Health has identified two common themes described next regarding cooling methods that ensure proper cooling (<xref rid="R5" ref-type="bibr">Hedeen &#x00026; Smith, 2020</xref>; <xref rid="R6" ref-type="bibr">Igo et al., 2021</xref>; <xref rid="R8" ref-type="bibr">Schaffner et al., 2015</xref>).</p></sec><sec id="S2"><title>Shallow Depth and Ventilation</title><p id="P7"><xref rid="R8" ref-type="bibr">Schaffner et al. (2015)</xref> examined 596 food items being cooled in refrigerators in 410 restaurants. They measured the temperature of these foods at two time points, approximately 80 min apart, and used modeling to determine the cooling rates and compliance with <italic toggle="yes">Food Code</italic> guidelines. Foods not actively monitored by food workers were more than twice as likely to cool more slowly than recommended in the <italic toggle="yes">Food Code</italic>. Foods stored at a container depth &#x0003e;3 in. were twice as likely to cool more slowly than specified in the <italic toggle="yes">Food Code</italic>. Moreover, unventilated foods were almost twice as likely to cool more slowly than specified in the <italic toggle="yes">Food Code</italic>.</p><p id="P8"><xref rid="R5" ref-type="bibr">Hedeen and Smith (2020)</xref> used data loggers to collect time and temperature data points at 5-min intervals for 34 cooling food items. They plotted the data points to form a cooling curve for each food item. They then assessed the cooling curves of the foods and found that those cooled in containers with a depth &#x0003c;3 in. were more likely to meet the first cooling parameter (i.e., 140 &#x000b0;F to 70 &#x000b0;F within 2 hr) than those cooled in containers with a depth &#x02265;3 in. (<italic toggle="yes">p</italic> = .035). As almost all the food items in this study were ventilated, the relationship between ventilation and cooling rates was not evaluated. Using these same cooling curves, <xref rid="R6" ref-type="bibr">Igo et al. (2021)</xref> also found that food depth has a strong influence on cooling and verified that containers with a food depth &#x02265;3 in. were more likely to have cooling rates slower than the cooling rate specified in the <italic toggle="yes">Food Code</italic>.</p><p id="P9">Using containers with a depth of &#x0003c;3 in. and ventilating foods during refrigerated cooling (as recommended in Section 3-501.15 of the <italic toggle="yes">Food Code</italic>) are simple ways for operators to maximize cooling efforts. They also serve as indicators for inspectors to assess cooling at restaurants. The extra space needed to use shallow pans and ventilation is a potential drawback; to address this drawback, restaurants could small-batch recipes or use speed racks in walk-in coolers.</p></sec><sec id="S3"><title>Two-Point Temperature Monitoring</title><p id="P10"><xref rid="R8" ref-type="bibr">Schaffner et al. (2015)</xref> identified a simple two-point method to measure cooling rates in restaurants and identify cooling issues. This method was developed using on-site observations of cooling food times and temperatures. Operators and inspectors can use this method to quickly determine if the cooling method used is expected to cool foods properly before the entire 6-hr period has elapsed.</p><p id="P11">The equation to calculate the cooling rate of a food is [Log(T<sub>1</sub> &#x02212; T<sub><italic toggle="yes">df</italic></sub>) &#x02212; Log(T<sub>2</sub> &#x02212; T<sub><italic toggle="yes">df</italic></sub>)]/&#x003b4;t, where T<sub>1</sub> and T<sub>2</sub> are any two temperatures measured during the cooling process, T<sub><italic toggle="yes">df</italic></sub> is the driving force temperature (i.e., the temperature of the cooling environment), and &#x003b4;t is the time between the two temperature measurements (<xref rid="F1" ref-type="fig">Figure 1</xref>). When the temperature and time values from the <italic toggle="yes">Food Code</italic> guidelines for food cooling results are plugged into this equation, and a driving force of 37 &#x000b0;F is assumed, this produces the best fit (i.e., highest <italic toggle="yes">R</italic><sup>2</sup> value). The slope of this best-fit line equates to a cooling rate of 0.23 when time is measured in hours (or 0.0039 when time is measured in minutes). Thus, a food with a cooling rate faster or equal to 0.23 would meet <italic toggle="yes">Food Code</italic> recommendations, but a rate slower than 0.23 would not (<xref rid="R6" ref-type="bibr">Igo et al., 2021</xref>; <xref rid="R8" ref-type="bibr">Schaffner et al., 2015</xref>). Under some circumstances, the driving force will not be constant, which can influence the cooling rate estimate.</p><p id="P12"><xref rid="R6" ref-type="bibr">Igo et al. (2021)</xref> used cooling curves for 29 different foods that were collected in 25 different restaurants to verify the two-point rate calculation method. Cooling curves were divided into two categories: typical and atypical. Curves were considered atypical when they had many dips and peaks, which are typically caused by stirring the food or changing the cooling method. Most cooling curves (21 out of 29) were considered typical (i.e., log linear rate changes with time). Atypical cooling curves (8 of 29) had non-log linear rate changes with time resulting from stirring or other factors.</p><p id="P13">Almost all typical cooling curves identified had highly predictable cooling rates (<xref rid="R6" ref-type="bibr">Igo et al., 2021</xref>). Among 9 foods with typical cooling curves that did not meet the cooling times recommended in the <italic toggle="yes">Food Code</italic>, the two-point model identified 6 as having slow cooling rates and 3 as having marginal cooling rates; among 12 foods identified by the two-point model as having acceptable cooling rates, 10 met the cooling times recommended in the <italic toggle="yes">Food Code</italic>. Among 8 foods that were considered to have atypical cooling curves, 6 failed to meet the cooling times recommended in the <italic toggle="yes">Food Code</italic>. These findings indicate that for most foods that are cooling at a steady rate (e.g., not stirred, not moved to a different environment), taking only two temperature measurements at any point in the cooling process should reliably indicate whether the food is going to meet the cooling guidelines in the <italic toggle="yes">Food Code</italic>.</p><p id="P14">During routine inspections, this two-point method could help inspectors identify cooling issues. Specifically, when inspectors see a food item cooling, they could note an initial time and temperature of the food. Then they could take a second temperature reading, preferably at the end of their inspection to allow for the greatest elapsed time between the two temperature readings. The simple equation described previously would enable inspectors to estimate the cooling rate. They could use the calculated rate to determine whether the cooling rate of the food is predicted to follow the recommendations in the <italic toggle="yes">Food Code</italic>. Inspectors could use this tool to educate restaurant operators. If the equation predicts that a food will not cool within the guidelines of the <italic toggle="yes">Food Code</italic>, the inspector could discuss alternative cooling methods with operators and develop a plan for properly cooling the food. Operators could also use this method to help verify whether their cooling process is effective or to evaluate the effect of changes in their process.</p><p id="P15">Additional research is needed to potentially determine ideal times during the cooling process when inspectors should take the two temperature readings (i.e., between 135 &#x000b0;F and 70 &#x000b0;F and then again after the food is below 70 &#x000b0;F). Differences in time between the two temperature measurements also might affect the outcome (e.g., are measurements 60 min apart better than measurements 15 min apart?).</p><p id="P16">Foodborne disease outbreaks resulting from improper cooling continue to occur (<xref rid="R7" ref-type="bibr">Lipcsei et al., 2019</xref>). Proper cooling is sometimes difficult for restaurants to accomplish and for inspectors to verify. Although the <italic toggle="yes">Food Code</italic> provides valuable information on suggested cooling methods, beyond specifying to monitor temperatures, it does not provide guidance on determining how cooling is to take place. Logging continuous time and temperature data is an ideal way to determine if foods are cooled correctly, but this process is not always practical for operators or inspectors. Portioning foods into containers with a depth &#x0003c;3 in. and ventilating them during the cooling process are best practices that can promote rapid cooling and that restaurants can easily apply. As described in this study, calculating cooling rates to determine if foods meet FDA <italic toggle="yes">Food Code</italic> recommendations is one way that operators and inspectors can determine if a cooling method can be expected to work without having to monitor a food for the entire 6-hr cooling process. More research is underway to further refine aspects of this method.</p></sec></body><back><fn-group><fn id="FN1"><p id="P17" content-type="publisher-disclaimer"><bold><italic toggle="yes">Disclaimer:</italic></bold> The findings and conclusions in this guest commentary are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention or the Agency for Toxic Substances and Disease Registry.</p></fn></fn-group><ref-list><title>References</title><ref id="R1"><mixed-citation publication-type="journal"><name><surname>Brown</surname><given-names>LG</given-names></name>, <name><surname>Ripley</surname><given-names>D</given-names></name>, <name><surname>Blade</surname><given-names>H</given-names></name>, <name><surname>Reimann</surname><given-names>D</given-names></name>, <name><surname>Everstine</surname><given-names>K</given-names></name>, <name><surname>Nicholas</surname><given-names>D</given-names></name>, <name><surname>Egan</surname><given-names>J</given-names></name>, <name><surname>Koktavy</surname><given-names>N</given-names></name>, <name><surname>Quilliam</surname><given-names>DN</given-names></name>, &#x00026; <collab>EHS-Net Working Group</collab>. 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(<year>2017</year>). <source>Food code: 2017 recommendations of the United States Public Health Service</source>, <publisher-name>Food and Drug Administration</publisher-name>. <comment><ext-link xlink:href="https://www.fda.gov/media/110822/download" ext-link-type="uri">https://www.fda.gov/media/110822/download</ext-link></comment></mixed-citation></ref></ref-list></back><floats-group><fig position="float" id="F1"><label>FIGURE 1</label><caption><p id="P18">Equation to Calculate the Cooling Rate of a Food</p></caption><graphic xlink:href="nihms-1791663-f0001" position="float"/></fig></floats-group></article>