Presence and Persistence of Salmonella in Dry Conditions
Traditionally, there are specific product groups that are associated with illnesses from foodborne pathogens. For example, retail deli meats are associated with Listeria monocytogenes, ground beef is associated with Escherichia coli O157:H7 and poultry products are associated with Salmonella spp. As such, specific interventions, practices and testing frequencies have been developed in order to reduce the risk for these product groups. Due to high frequencies, these product groups gain particular attention, however there have also been either emerging (within the last 10 years) product groups or products with consistent low levels of associated illness that are of concern also. Fresh and washed produce have emerged to be associated with foodborne illness events. Additionally, nuts and nut butters have also arisen to be of particular concern. Unlike the previous items (fresh produce, raw and RTE meat), nuts and nut butters have an intrinsic control factor (low water activity (a w) ) as well as an intervention kill step that provides an additional level of safety. Despite this, low moisture foods like nut butters, cocoa, dry milk powder, spices and dry cereals/grains have consistently been identified as sources related to foodborne disease (Finn et al. 2013). This consistency necessitates a further understanding of how Salmonella spp. are introduced and how this particular foodborne pathogen persists in dry conditions for both products and manufacturing environments.
The introduction of Salmonella spp. to finished products occurs through various routes including (i) in–coming raw ingredients that are contaminated with Salmonella coming into contact with finished product or food contact surfaces post–thermal treatment, (ii) Salmonella populations present within the production environment itself, and (iii) increased tolerance of Salmonella spp. in dry products to heat treatment. The Grocery Manufacturers Association (GMA) published a guidance document for the Control of Salmonella in Low–moisture Foods (GMA 2009). As is outlined in this document, there are efforts that can be taken to minimize the risk of Salmonella contamination of finished product. These efforts include the management of process and employee traffic to prevent Salmonella spread, subjecting the supply chain raw ingredient suppliers to control programs, the increase of hygienic and cleaning efforts, reassessment of the hygienic design of the manufacturing site and equipment, the control of Salmonella growth in the manufacturing site and the validation of interventions targeting the inactivation of Salmonella.
Despite the outlined efforts presented by GMA and other best approaches, there is still the possibility that Salmonella may persist within the dry conditions of the manufacturing site or within finished product. This persistence is, at least, in part due to the tolerance and resistance Salmonella spp. and other gram–negative bacteria have to harsh conditions.
In low moisture conditions, there is an initial stress placed on a gram–negative bacterial cell via turgor pressure that induces a response. Specifically, the dry conditions in the environment, drive a force for the available water from within the bacterial cell to equilibrate to the exterior of the cell. To resist this driving force, intracellular ions are either created or collected in order to equilibrate to the dry environment. The accumulation of these ions, or solutes, may also provide increased heat resistance by stabilizing crucial cell components to denaturation (Finn et al. 2013; Pleitner et al. 2012). With this in mind, the adjustment that occurs by Salmonella to dry conditions can lend increased tolerance to the kill step applied during processing (e.g. dry roasting for nuts and cocoa beans).
An additional action that Salmonella takes to persist within dry manufacturing environments is filamentation. Filamentation is a phenomena where only partial, not complete cell replication occurs and has been shown to be induced by dry conditions (Mattick et al. 2000). During filamentation, all cell components are replicated but the cell does not divide, making a long strand of partial cells. This results in a large accumulation of partial Salmonella cells which have been shown to have increased tolerance to dry and high temperature conditions. Furthermore, a population of Salmonella of which filamentation has occurred will not be enumerated accurately as ten partial cells that are filamented will only be enumerated as one cell. This can reduce the chances of identifying the presence of Salmonella in environments and products. It is important to note that when this population is introduced to a more favorable state (e.g. increased water) the filamented cells will separate and form individual cells, immediately increasing the Salmonella cell populations within the contaminated product.
Environmental and storage temperature conditions have also been shown to have an effect on tolerance and viability of Salmonella populations in dry conditions. Specifically, increased survival of Salmonella populations has been observed in peanut butter at lower temperatures (Burnett et al. 2000). Also, increased survival of Salmonella populations has been observed in environmental conditions on plastic surfaces at lowered temperatures (Gruzdev et al. 2012). This characteristic should be taken in to consideration for the storage of raw ingredient, processing environment temperatures and storage of finished product.
Moving forward in the process flow, from raw ingredient to manufacturing to finished product, the infective dose relating to the consumption of Salmonella populations in dry products is hypothesized to be effected as well. The surrounding theories behind this are that either (i) the adaptation to the dry conditions in the finished product can provide cell resistance to the harsh conditions present in the digestive system of the consumer and (ii) within a product of high lipid, low a w (e.g. peanut butter) pockets of high populations of bacterial cells occur that can also provide resistance to the harsh conditions in the digestive system of the consumer. Also, as mentioned, the occurrence of filamentation can to lead inaccurate enumeration and thus ineffective determination of low infective dose incidences.
The occurrence of foodborne illnesses related to dry, low aw products continues to occur in product types of peanut and tree nut butter, chocolate and cocoa, dry milk powder, and dry cereals. It is important to understand the ability that Salmonella has in persisting in dry conditions which allows for its presence within the food supply. Steps can be taken to mitigate the risk of finished product contamination including control requirements of raw ingredient specifications, proper GMPs and sanitation procedures, robust environmental monitoring program, validation and verification of the intervention kill steps, and management of process and employee traffic flow to limit post–process contamination.
- Burnett, S., Gehm, E., Weissinger, W., Beuchat, L. 2000. Survival of Salmonella in peanut butter and peanut butter spread. J. Appl. Microbiol. 89:472.
- Finn, S., Condell, O., McClure, P., Amezuita, A., Fanning, S. 2013. Mechanisms of survival, responses and sources of Salmonella in low–moisture environments. Front. Microbiol 4:331
- Grocery Manufacturers Association (GMA). 2009. Control of Salmonella in low–moisture foods. Available at: http://www.gmaonline.org/downloads/technical–guidance–and–tools/SalmonellaControlGuidance.pdf . Accessed: March 17, 2017.
- Gruzdev, N., Pinto, R., Sela Saldinger, S. 2012. Persistence of Salmonella enterica during dehydration and subsequent cold storage. Food Microbiol. 32:415.
- Mattick, K., Jorgensen, F., Legan, J., Cole, M., Porter, J., Lappin–Scott, H., Humphrey, T. 2000. Survival and filamentation of Salmonella enterica serovar Enteritidis PT4 and Salmonella enterica servar Typhimurium DT104 at low water activity. Appl. Environ. Microgiol. 66:1274.
- Pleitner, A., Zhai, Y., Winter, R., Ruan, L., McMullen, L., Ganzle, M. 2012. Compatible solutes contribute to heat resistance and ribosome stability in Escherichia coli AW 1.7. Biochimica et Biophysica Acta – Protein and Proteomics. 1824:1351.