{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,11,12]],"date-time":"2025-11-12T20:43:22Z","timestamp":1762980202412,"version":"3.41.2"},"reference-count":21,"publisher":"American Society for Microbiology","issue":"5","license":[{"start":{"date-parts":[[2015,10,13]],"date-time":"2015-10-13T00:00:00Z","timestamp":1444694400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc-sa\/3.0\/"},{"start":{"date-parts":[[2015,10,30]],"date-time":"2015-10-30T00:00:00Z","timestamp":1446163200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/journals.asm.org\/non-commercial-tdm-license"}],"content-domain":{"domain":["journals.asm.org"],"crossmark-restriction":true},"short-container-title":["mBio"],"published-print":{"date-parts":[[2015,10,30]]},"abstract":"ABSTRACT<\/jats:title>\n \n A 2014 multistate listeriosis outbreak was linked to consumption of caramel-coated apples, an unexpected and previously unreported vehicle for\n Listeria monocytogenes<\/jats:named-content>\n . This outbreak was unanticipated because both the pH of apples (<4.0) and the water activity of the caramel coating (<0.80) are too low to support\n Listeria<\/jats:italic>\n growth. In this study, Granny Smith apples were inoculated with approximately 4 log\n 10<\/jats:sub>\n \u00a0CFU of\n L. monocytogenes<\/jats:named-content>\n (a cocktail of serotype 4b strains associated with the outbreak) on each apple's skin, stem, and calyx. Half of the apples had sticks inserted into the core, while the remaining apples were left intact. Apples were dipped into hot caramel and stored at either 7\u00b0C or 25\u00b0C for up to 11 or 28\u00a0days, respectively. Data revealed that apples with inserted sticks supported significantly more\n L. monocytogenes<\/jats:named-content>\n growth than apples without sticks under both storage conditions. Within 3\u00a0days at 25\u00b0C,\n L. monocytogenes<\/jats:named-content>\n populations increased >3 log\n 10<\/jats:sub>\n in apples with sticks, whereas only a 1-log\n 10<\/jats:sub>\n increase was observed even after 1\u00a0week for caramel-coated apples without sticks. When stored at 7\u00b0C, apples with sticks exhibited an approximately 1.5-log\n 10<\/jats:sub>\n increase in\n L. monocytogenes<\/jats:named-content>\n levels at 28\u00a0days, whereas no growth was observed in apples without sticks. We infer that insertion of a stick into the apple accelerates the transfer of juice from the interior of the apple to its surface, creating a microenvironment at the apple-caramel interface where\n L. monocytogenes<\/jats:named-content>\n can rapidly grow to levels sufficient to cause disease when stored at room temperature.\n <\/jats:p>\n \n IMPORTANCE<\/jats:bold>\n Neither caramel nor apples are a food where the pathogenic bacterium\n Listeria monocytogenes<\/jats:named-content>\n should grow, as caramel does not contain enough free water and apples are too acidic. Caramel-coated apples, however, were recently linked to a deadly outbreak of listeriosis. We hypothesized that inserting a stick into the apple releases juice to the interface between the apple and caramel, providing a more hospitable environment than either component alone. To test this hypothesis, apples were inoculated with\n L. monocytogenes<\/jats:named-content>\n prior to caramel dipping. Some apples had sticks inserted into them before dipping, while others did not. No growth of\n L. monocytogenes<\/jats:named-content>\n occurred on refrigerated caramel apples without sticks, whereas slow growth was observed on refrigerated caramel apples with sticks. In contrast, significant pathogen growth was observed within 3\u00a0days at room temperature on caramel apples with sticks inserted. Food producers should consider interfaces between components within foods as potential niches for pathogen growth.\n <\/jats:p>","DOI":"10.1128\/mbio.01232-15","type":"journal-article","created":{"date-parts":[[2015,10,14]],"date-time":"2015-10-14T01:47:18Z","timestamp":1444787238000},"update-policy":"https:\/\/doi.org\/10.1128\/asmj-crossmark-policy-page","source":"Crossref","is-referenced-by-count":46,"title":["Growth of Listeria monocytogenes within a Caramel-Coated Apple Microenvironment"],"prefix":"10.1128","volume":"6","author":[{"given":"Kathleen A.","family":"Glass","sequence":"first","affiliation":[{"name":"Food Research Institute, University of Wisconsin\u2014Madison, Madison, Wisconsin, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Max C.","family":"Golden","sequence":"additional","affiliation":[{"name":"Food Research Institute, University of Wisconsin\u2014Madison, Madison, Wisconsin, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Brandon J.","family":"Wanless","sequence":"additional","affiliation":[{"name":"Food Research Institute, University of Wisconsin\u2014Madison, Madison, Wisconsin, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Wendy","family":"Bedale","sequence":"additional","affiliation":[{"name":"Food Research Institute, University of Wisconsin\u2014Madison, Madison, Wisconsin, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Charles","family":"Czuprynski","sequence":"additional","affiliation":[{"name":"Food Research Institute, University of Wisconsin\u2014Madison, Madison, Wisconsin, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"235","reference":[{"key":"e_1_3_3_2_2","unstructured":"Centers for Disease Control and Prevention. 2015. Multistate outbreak of listeriosis linked to commercially produced prepackaged caramel apples made from Bidart Bros. apples. http:\/\/www.cdc.gov\/listeria\/outbreaks\/caramel-apples-12-14\/. Accessed 9 March 2015."},{"key":"e_1_3_3_3_2","unstructured":"U.S. FDA. 2015. FDA investigated Listeria monocytogenes illnesses linked to caramel apples. http:\/\/www.fda.gov\/Food\/RecallsOutbreaksEmergencies\/Outbreaks\/ucm427573.htm. Accessed 9 June 2015."},{"key":"e_1_3_3_4_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.foodchem.2006.07.030"},{"key":"e_1_3_3_5_2","doi-asserted-by":"publisher","DOI":"10.1080\/10408390802248833"},{"key":"e_1_3_3_6_2","volume-title":"Food microbiology: fundamentals and frontiers","author":"Ryser ET","year":"2013","unstructured":"Ryser ET, Buchanan RL. 2013. Listeria monocytogenes. In Doyle MP, Buchanan RL (ed), Food microbiology: fundamentals and frontiers. ASM Press, Washington, DC."},{"key":"e_1_3_3_7_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.02831-13"},{"key":"e_1_3_3_8_2","doi-asserted-by":"publisher","DOI":"10.1080\/10408398309527372"},{"key":"e_1_3_3_9_2","doi-asserted-by":"publisher","DOI":"10.1016\/b978-0-12-404611-5.00013-0:291-312"},{"key":"e_1_3_3_10_2","doi-asserted-by":"publisher","DOI":"10.4315\/0362-028X-67.10.2342"},{"key":"e_1_3_3_11_2","doi-asserted-by":"publisher","DOI":"10.1016\/0168-1605(96)01107-5"},{"key":"e_1_3_3_12_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1539-6924.2009.01308.x"},{"key":"e_1_3_3_13_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.fm.2005.04.004"},{"key":"e_1_3_3_14_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.lwt.2013.10.034"},{"key":"e_1_3_3_15_2","doi-asserted-by":"publisher","DOI":"10.4315\/0362-028X-62.5.444"},{"key":"e_1_3_3_16_2","doi-asserted-by":"publisher","DOI":"10.1111\/1750-3841.12174"},{"key":"e_1_3_3_17_2","first-page":"157","volume-title":"Listeria, listeriosis, and food safety","author":"Lado BH","year":"2007","unstructured":"Lado BH, Yousef AE. 2007. Characteristics of Listeria monocytogenes important to food processors, p 157\u2013213. In Ryser ET, Marth EH (ed), Listeria, listeriosis, and food safety. CRC Press, Boca Raton, FL."},{"key":"e_1_3_3_18_2","doi-asserted-by":"publisher","DOI":"10.1094\/PDIS.2000.84.2.177"},{"key":"e_1_3_3_19_2","doi-asserted-by":"publisher","DOI":"10.1094\/PHYTO-97-11-1415"},{"key":"e_1_3_3_20_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.66.3.1077-1083.2000"},{"key":"e_1_3_3_21_2","doi-asserted-by":"publisher","DOI":"10.1086\/427803"},{"key":"e_1_3_3_22_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.00351-06"}],"container-title":["mBio"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/mBio.01232-15","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/mBio.01232-15","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,3,8]],"date-time":"2022-03-08T02:02:31Z","timestamp":1646704951000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.asm.org\/doi\/10.1128\/mBio.01232-15"}},"subtitle":[],"editor":[{"given":"Stefan H. E.","family":"Kaufmann","sequence":"additional","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2015,10,30]]},"references-count":21,"journal-issue":{"issue":"5","published-print":{"date-parts":[[2015,10,30]]}},"alternative-id":["10.1128\/mBio.01232-15"],"URL":"https:\/\/doi.org\/10.1128\/mbio.01232-15","relation":{},"ISSN":["2161-2129","2150-7511"],"issn-type":[{"type":"print","value":"2161-2129"},{"type":"electronic","value":"2150-7511"}],"subject":[],"published":{"date-parts":[[2015,10,30]]},"assertion":[{"value":"2015-07-21","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2015-09-14","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2015-10-13","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e01232-15"}}