Salmonella inactivation and sponge/microfiber mediated cross-contamination during papaya wash with chlorine or peracetic acid as sanitizer
Introduction
Papaya is an important tropical fruit rich in antioxidant nutrients, vitamins, minerals, and fibers (Krishna et al., 2008; Septembre-Malaterre et al., 2016). The United States is the largest papaya importer, consuming over half of the global exports between 2007 and 2017 (FAOSTAT, 2017). About 75% of papayas imported into the US are from Mexico (Evans et al., 2012).
Salmonella enterica is one of the leading contaminants of fresh produce and causes of bacterial foodborne outbreaks in the United States (CDC, 2018; CDC, 2020). Salmonella contamination can occur at any stage of food production and distribution, including produce growth, harvest, postharvest processing, and food distribution and service (Hanning et al., 2009; Alum et al., 2016; Iwu and Okoh, 2019). Although Salmonella contamination of fresh produce are often linked to animal farming operations, there are evidences that many serovars have increased fitness for survival and growth in the natural environments independent of animal hosts (Brandl and Mandrell, 2002; Brandl et al., 2013).
In the past decade, multiple salmonellosis outbreaks involving a variety of serovars (including Agona, Anatum, Gaminara, Infatis, Kiambu, Newport, Thompson, Uganda, and Urbana) have been linked to imported papayas from Mexico, which were marketed in US and Canada as whole fruits. These outbreaks caused hundreds of cases of illnesses, hospitalizations, and sometimes deaths in US, which also resulted in numerous recalls of implicated papayas in the US and Canada (CDC, 2019; Hassan et al., 2019; Mba-Jonas et al., 2018; CDC, 2011; FDA, 2020). Maradol papaya, a common variety grown in Mexico, was implicated in these reported outbreaks.
The US Food and Drug Administration (FDA) requires papaya producers exporting to the US to meet standards for the safe growing, harvesting, packing, processing and holding of produce outlined in FSMA Produce Safety Rule (FDA, 2016; FDA, 2018), and recently issued a letter of call to action urging papaya industry to “improve practices to better protect consumers” (FDA, 2019). Meanwhile, the papaya industry has engaged in renewed efforts re-examining papaya growing, harvesting, packaging, and distribution processes for vulnerabilities of Salmonella contamination. United Fresh Produce Association (UFPA, Washington, DC.) and Texas International Produce Association (TIPA, Mission, TX.), in collaboration with papaya industry professionals, research institutions, regulatory agencies, and other commodity and trading groups, have recently drafted and started to implement a guideline on “Best practices for the growing and handling of Mexican papaya”, which provides recommended food safety practices to minimize the microbiological hazards associated with fresh papaya from Mexico. (UFPA, 2020).
However, it is recognized that knowledge on the cause and confounding factors of Salmonella contamination on papaya, and on the means of effectively preventing and reducing contamination risks during production is still limited. Despite repeated outbreaks, there are very limited data on Salmonella contamination, survival, and transference on Mexican papayas that is available in the literature. Previous studies mostly focused on the survival and growth of Salmonella on fresh-cut papaya. It has been reported that Salmonella could grow on papaya pulp at 10–30 °C, and survive on frozen cut papayas for at least 180 days (Penteado and Leitao, 2004; Strawn and Danyluk, 2010), highlighting the importance of preventing and controlling Salmonella contamination during papaya production and packing house handling.
Salmonella contamination on fresh produce could occur both pre- and post-harvest (Brandl, 2006; Franz and van Bruggen, 2008). For postharvest handling, producers in Mexico usually wash freshly harvested papayas in single or double flume wash tanks. During the growth and harvest, a milky white liquid (latex) released from the wound tissue often dry of the fruit surface, creating a contamination that can negatively impact both the quality and safety of the product. Sponges, microfiber wash mitts, or other types of rubbing tools are commonly used to remove latex, dirt, or other contaminants from fruit surface before paper wrapping and packing. Chlorine and peracetic acid (PAA) are two commonly used antimicrobials applied in the flume tanks. Significant data gaps exist concerning the risk of Salmonella contamination and cross-contamination during postharvest washing. The extensive use of sponges and other rubbing tools for papaya cleaning has been often perceived as a major risk for Salmonella cross-contamination (UFPA, 2020). Although brushing or wiping were also used for cleaning fruits such as cantaloupe, apple, mango, and tomato at commercial packing (Prusky et al., 1999; Annous et al., 2001; Sreedharan et al., 2014; Balaguero et al., 2015; Fu et al., 2020), the risks of these cleaning tools to mediate cross-contamination by foodborne pathogens need to be further assessed. To better understand and mitigate the contamination risks of Salmonella during papaya washing and cleaning, research data about the probability of Salmonella cross-contamination and the efficacy of different levels of free chlorine (FC) and PAA on Salmonella reduction is needed.
This study was primarily designed to examine the risks of Salmonella contamination on whole papaya during postharvest washing and cleaning, especially the plausibility of sponge or microfiber wash mitt mediating Salmonella cross-contamination during papaya washing in the presence of varying levels of sanitizers. We also examined the efficacy of free chlorine and PAA against Salmonella on papaya, and on sponges/microfiber. Data generated from this study can be used to support and improve the food safety guidelines for papaya production.
Section snippets
Papaya, sponges, and microfiber wash mitts
Experiments were performed to evaluate the contamination risk of Salmonella during papaya washing using sponges and microfiber wash mitts. Freshly packaged and imported papayas (Carica papaya; cultivar Maradol; grown and packed in Colima, Mexico) were expressly shipped by a collaborating importer to Beltsville Agricultural Research Center laboratory in Maryland for the experiments. The papaya fruits received were consistent with maturity stages 2–3 (with occasional 4) descriptions of the
Papaya wash water quality characterization
Wash water was prepared with the intention of simulating that used for commercial operations. Released papaya latex (and some juice) was considered as the primary source of organic load in the wash water. TDS, UVA254, and COD in the batches of wash water were assessed as the primary quality parameters. The measurements of these parameters were comparable for both batches of the wash water: for sponge wash TDS, 67.3 mg/L; UVA254, 0.08; COD, 341.85 mg/L, and microfiber wash TDS, 70 mg/L; UVA254,
Discussion
Salmonella contamination of papaya fruits could occur via different routes at various production stages, however, the role of sponge or microfiber wash mitts in postharvest cleaning in propagating Salmonella cross-contamination has specifically been questioned (UFPA, 2020). Unlike for other fruits such as cantaloupe, where sponge or tissue wiping is also used for cleaning, a major source of organic load in a papaya washing system is assumedly papaya latex. Sponges and other forms of soft
Conclusion
Papaya washing and cleaning were simulated using papayas and sponges or microfiber wash mitts that were differentially inoculated with Salmonella strains carrying different antibiotic markers. While Salmonella populations were significantly reduced both on inoculated sponge/microfiber (>5.37 log) and on inoculated papayas (0.69–2.66 log) after washing in FC (25–100 mg/L) or PAA (20–80 mg/L), the reduction on inoculated papayas showed low efficacy and poor correlation to sanitizer
Credit author statement
GG: Experiment planning and coordination, data analyses, manuscript draft; SB, GM, BZ: Experimentation-Microbiology; TZ, DP: Experimentation-Water quality; YL, PM, XN: Study design, data interpretation, industry interaction; XN: Supervision, manuscript writing. All co-authors contributed to manuscript revision.
Declaration of competing interest
All the listed authors declared no conflict of interest and approved the submitted manuscript.
Acknowledgements
Authors wish to thank United Fresh Produce Association, Texas International Produce Association, and Sungwon Distribution for providing information and materials used in this study.
This project was partially supported by a research grant from USDA-NIFA Specialty Crop Research Initiative, Award No. 2016-51181-25403, and by appointments to ARS Research Participation Program administered by the Oak Ridge Institute for Science and Education (ORISE) through an interagency agreement between DOE and
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Participant of Oak Ridge Institute for Science and Education (ORISE) Research Participation Program.
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Current affiliation: Cornell University, Department of Food Science, Ithaca, NY. 14853.