Relationships Between Microbial Indicators on Produce, Produce Processing Equipment, Worker Handrinses and Water Used for Growing and Processing Produce on Farms in the United States Open Access

Abstract

Foodborne pathogens, such as Escherichia coli, Salmonella and Norovirus, are not easy to detect in outbreak samples, but using indicator species allows for easier detection of foodborne disease risk. This study aims to assess the relationships between microbial indicator species contaminating produce, processing equipment, workers' hands and water. This cross-sectional study examined 1,912 samples including produce (cabbage, turnip greens, cilantro and parsley), swabs of processing and packing environments, worker handrinses and various sources of water (irrigation water, processing ice and processing water) collected in the southwest U.S. between November 2000 and December 2003. Produce and swab samples were analyzed for aerobic plate count (APC), coliforms, enterococci and Escherichia coli (E. coli). Water samples were analyzed for E.coli, fecal coliforms and somatic coliphages. Several indicator species had significantly different log10 means when means were compared amongst types of produce, amongst types of swabs, and amongst types of water samples. Among produce, APC had at least 2 pairs (cilantro vs. cabbage and parsley), coliforms had 2 pairs (parsley vs. cabbage and turnip greens) and enterococci had 4 pairs (cabbage vs. turnip greens, or cilantro and parsley vs. turnip greens or cilantro) that were significantly different. Among swabs, APC had 3 pairs (turnip greens vs. cabbage or cilantro and cilantro vs. parsley) and enterococci had 5 pairs (turnip greens vs. cabbage or parsley and cilantro vs. cabbage, turnip greens or parsley) that were significantly different. Among water, E. coli had 4 pairs (handrinse vs. ice or processing water and irrigation vs. ice or processing water) fecal coliforms had 5 pairs (handrinse vs. ice, irrigation or processing water and irrigation vs. ice or processing water) and somatic coliphages had 2 pairs (irrigation vs. ice or processing water) that were significantly different. Correlation values showed that several pairs of indicator species had significant associations among produce (r = 0.20- 0.69) and swabs (r = 0.20- 0.61) and among water samples (r = 0.70- 0.93). Among unadjusted prevalence odds ratios, coliforms were most frequently a significant exposure (OR= 2.11- 16.97) compared to other indicator species. Among linear regression models, APC and E. coli were the most frequently significant predictors compared to other indicator species. Among adjusted prevalence odds ratios, all indicator species were found to be significant predictors when combined in produce models. Among adjusted odds ratios from swab models, coliforms had significant odds of being present when enterococci or E. coli were present, but enterococci and E. coli had significant odds of being present when coliforms were present. In summary, among produce samples, swabs of harvesting and processing equipment, various types of water that contact produce and worker handrinses there were significant relationships among microbial indicator species.

Table of Contents

Literature Review...1

Prevalence of Foodborne Illness in U.S. Related to Vegetables...1

Food Safety Policies in the U.S....1

Routes of Vegetable Contamination...5

Pathogens and Indicator Species Relationships...8

Relationships Among Indicator Species...11

Study Goals and Aims...19

Significance...19

Methods...21

Population Description...21

Sample Microbial Testing Methods...22

Data Management...23

Statistical Analysis...24

Results...25

Discussion...32

Strengths and Limitations...37

Implications...37

Conclusions...38

Future Directions...39

References...40

Tables...44

Table 1. Microbial Indicators from Produce and Swabs of Produce Processing Equipment by Type of Sample...44

Table 2. Microbial Indicators from Water by Type of Sample...45

Table 3. Microbial Indicator Prevalence Odds Ratios for Produce, Swabs, and Water by Type of Sample...46

Table 4. Model Parameters of Concentrations of Indicator Species Adjusted± for Produce, Swab and Water...47

Table 5. Presence versus Absence of Indicator Species Adjusted± Odds Ratios for Produce, Swab and Water...48

Figures...49

Figure 1. Microbial Indicator Species Correlations from Produce and Swabs by Type of Sample. There is a table header for sample type and another header for indicator species. The column under sample type lists the various types of produce and swab samples (cabbage, turnip greens, cilantro or parsley). The column with indicator species is cross-referenced with an indicator species in the top row to locate a Pearson correlation value where r is significant if p < 0.05. The legend shows that colors (blue shades) indicate statistically significant positive correlations...50

Figure 2: Microbial Indicator Species Correlations from Water by Type of Sample. There is a table header for sample type and another header for indicator species. The column under sample type lists the various types of water samples (handrinse, ice, irrigation or processing water). The column with indicator species is cross-referenced with an indicator species in the top row to locate a Pearson correlation value where r is significant if p < 0.05. The legend shows that colors indicate statistically significant positive (blue shades) or negative (red shades) correlations...51

Appendix A: Additional Tables...52

Table 6. Associations of Microbial Indicator Species (Presence versus Absence) from Produce and Swabs by Type of Sample...52

Table 7. Associations of Microbial Indicator Species (Presence versus Absence) from Water by Type of Sample...53

About this Master's Thesis

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School	Rollins School of Public Health
Department	Epidemiology
Degree	MPH
Submission	Master's Thesis
Language	English
Research Field	Health Sciences, Public Health Health Sciences, Epidemiology
Keyword	Escherichia coli aerobic plate culture (APC) herbs produce coliforms enterococci somatic coliphage indicator species leafy greens handrinse
Committee Chair / Thesis Advisor	Leon, Juan, Emory University
Partnering Agencies	Emory University schools, faculty or affiliated programs

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