Growth of Listeria monocytogenes within a Caramel-Coated Apple Microenvironment

Abstract

A 2014 multistate listeriosis outbreak was linked to consumption of caramel-coated apples, an unexpected and previously unreported vehicle for Listeria monocytogenes. 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 Listeria growth. In this study, Granny Smith apples were inoculated with approximately 4 log10 CFU of L. monocytogenes (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°C or 25°C for up to 11 or 28 days, respectively. Data revealed that apples with inserted sticks supported significantly more L. monocytogenes growth than apples without sticks under both storage conditions. Within 3 days at 25°C, L. monocytogenes populations increased >3 log10 in apples with sticks, whereas only a 1-log10 increase was observed even after 1 week for caramel-coated apples without sticks. When stored at 7°C, apples with sticks exhibited an approximately 1.5-log10 increase in L. monocytogenes levels at 28 days, 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 L. monocytogenes can rapidly grow to levels sufficient to cause disease when stored at room temperature.

Fate of Listeria monocytogenes in Fresh Apples and Caramel Apples

“…The interface between the stem end of the apple and the caramel layer may produce a microenvironment with high water activity and high nutrient (apple and apple juices produced from the insertion of the stick) and sugar (caramel) concentrations (16). Specific microenvironments of multicomponent foods can affect the survival and thermal behavior of pathogens such as Salmonella enterica (21).…”

Singleton Sequence Type 382, an Emerging Clonal Group of Listeria monocytogenes Associated with Three Multistate Outbreaks Linked to Contaminated Stone Fruit, Caramel Apples, and Leafy Green Salad

“…In the caramel apple outbreak, most case-patients consumed caramel apples, but L. monocytogenes was isolated from whole apples produced in the implicated apple manufacturing facility. Whole apples do not support the growth of L. monocytogenes ( 27 , 28 ), but the production of caramel apples requires the insertion of a stick into the fruit, which may have facilitated the transfer of juice from the interior to the surface, thereby creating a microenvironment at the apple-caramel interface that enabled L. monocytogenes to multiply ( 27 ). Caramel apples are often given to children, which could partially explain why this outbreak involved 3 otherwise healthy children, aged between 5 and 15 years, a typically low-risk group ( 3 ).…”

Medical conditions revealed in fairy tales, folklore and literature

“…The pallor of Snow White may be a reference to albinism and the dwarves clearly had achrondroplasia . Snow White may have eaten an apple ‘poisoned’ with Listeria cytomonogenes which can induce coma . Alternatively, a piece of apple may have lodged in her airway ( foreign body ), Snow White recovering instantly when it was dislodged.…”