Efficacy of Two Hand Hygiene Interventions at Reducing Hand Contamination Among Produce Farmworkers in Northern Mexico Público

Abstract

Previous research has shown that produce can become contaminated through contact with farmworkers’ hands and that hand-hygiene interventions are important for reducing contamination. It is unknown whether hand-hygiene intervention results are produce-specific. Research exploring other produce commodities is needed to prevent farm-level contamination and reduce the number of U.S. produce-related outbreaks. This study aims to assess hand-hygiene intervention efficacy on melon farms and compare findings to previous research conducted on jalapeño farms.

Two studies assessed the efficacy of two hand-hygiene interventions; one among jalapeño farmworkers and one among melon farmworkers. 129 melon and 159 jalapeño farmworkers in Mexico were randomly assigned to one of three groups: handwashing, two-step alcohol-based hand sanitizer (SaniTwice), or no hand-hygiene (control). After harvesting, hand-hygiene interventions were performed, and hand rinsate samples were collected and tested for soil (absorbance A600nm) and bacterial indicators (coliforms, generic E. coli, Enterococcus spp., a universal Bacteroidales marker (AllBac), and a human-specific Bacteroidales marker (BFD). Melon groups were compared using linear and logistic regression models (a=0.05) and Tukey’s adjustment for multiple comparisons. Studies were compared using two-way, fixed-effects models. Spearman’s correlations described outcome measurement relationships. Surveys regarding farmworker perceptions on hand-hygiene were also summarized.

Compared to controls (geomean A600nm 0.138), handwashing (geomean A600nm 0.014; p<0.0001) and SaniTwice (geomean A600nm 0.043; p<0.0001) interventions yielded significantly lower absorbance levels on melon farmworkers’ hands, with the handwashing group having the lowest (p<0.0001). Bacterial indicator concentrations on melon farmworkers’ hands did not differ across intervention group (p=0.1238-0.4168). The efficacy of handwashing and SaniTwice, compared to controls, differed between melon and jalapeño farmworkers; fixed-effects interactions between intervention group and produce type were significant for absorbance (p=0.0018), E. coli (p=0.0050), and coliforms (p=0.0005), but not Enterococcus spp. (p=0.2797). Correlations between outcome measurements ranged from -0.14 to 0.56 for melon data and 0.06 to 0.49 for jalapeño data. Melon farmworker hand-hygiene perceptions varied.

Although handwashing and SaniTwice reduced soil on melon farmworkers’ hands after one 30-minute harvest, neither intervention reduced indicator bacteria. The efficacy of handwashing and SaniTwice interventions differed for melon and jalapeño farmworkers, suggesting it may be necessary to develop produce-specific hand-hygiene interventions in agricultural settings.

Table of Contents

TABLE OF CONTENTS

I. LITERATURE REVIEW ………………………………………………………………1

     Foodborne Illness and Outbreak Trends in the U.S. …………………………………..1

     Produce-Related Outbreak Trends …………………………………………………….1

     Pathogens Associated with Produce-Related Outbreaks ……………………………...4

     Microbial Indicators for Measuring Agricultural Contamination …………………….5

     Farm to Fork Produce Contamination ...………………………………………………7

     Agricultural Transmission via Human and Animal Pathogens …………………….…8

     Interventions to Reduce Produce Contamination ……………………………………10

     Hand Hygiene Practices Domestically and Internationally ……….…………………12

     Study Goals and Aims ……………………………………………………………….18

     Significance ………………………………………………………………………….18

II. MANUSCRIPT ……………………………………………………………………....20

     ROLES AND CONTRIBUTIONS …………………………………………………..20

     ABSTRACT ………………………………………………………………………….20

     INTRODUCTION …………………………………………………………………...22

          Produce-Related Outbreaks and Hand Contamination ……….…………………..22

          Alternatives to Handwashing with Soap and Water ……………………………...23

          Measurements of Hand Contamination …………………………………………..24

          Efficacy of Hand Hygiene Interventions by Produce Type ……………...……….25

          Farmworker Perceptions of Hand Hygiene ……………………………………….26

          Study Goals ……………………………………………………………………… 27

     MATERIALS AND METHODS …………………………………………………….28

          Study Location and Participants ………………………………………………….28

          Study Design ……………………………………………………………………...28

          Data Entry ………………………………………………………………………...31

          Statistical Analysis ………………………………………………………………..32

     RESULTS ……………………………………………………………………………34

          Participant Demographics ………………………………………………………...34

          Effect of Hygiene Interventions on Soil Contamination on Melon Farmworker Hands …………………………………………………………………………..…34

          Effect of Interventions on Indicator Bacteria Concentrations Among Farmworkers    Harvesting Melons ……………………………………………………………….35

          Correlations Between Absorbance, Bacterial Indicators, and Bacteroidales .….....36

          Comparison of Hand Contamination Between Melon and Jalapeño Farmworkers ……………………………………………………………………………………...38

          Melon Farmworkers’ Hand Hygiene Perceptions ……….………………………..40

     DISCUSSION ………………………………………………………………………..40

     REFERENCES ………………………………………………………………………50

     TABLES ……………………………………………………………………………..62

          Table 1: Demographics of 129 Farmworkers by Hand Hygiene Intervention Group at Melon Farms in Nuevo Leon, Mexico ……………………...………..………..62

          Table 2a: Concentrations of Absorbance, Indicator Bacteria, and Bacteroidales from Farmworker Control and Intervention Group Hand Rinsate Samples Collected on Melon Farms in Nuevo Leon, Mexico ……………….……...……..63

          Table 2b: Proportions of Positive Samples of Absorbance, Indicator Bacteria, and Bacteroidales from Farmworker Control and Intervention Group Hand Rinsate Samples Collected on Melon Farms in Nuevo Leon, Mexico …………………...63

          Table 3. Correlations Between Concentrations of Absorbance, Indicator Bacteria, and Bacteroidales in Melon Farmworker Hand Rinsate Samples (n=128)^a ...…...64

          Table 4. Correlations Between Concentrations of Absorbance, Indicator Bacteria, and Bacteroidales in Melon Control Group Hand Rinsate Samples (n=41)^a …….64

          Table 5. Correlations Between Concentrations of Absorbance, Indicator Bacteria, and Bacteroidales in Melon Handwashing Group Hand Rinsate Samples (n=42)^a …………………………………………………………………………………….65

          Table 6. Correlations Between Concentrations of Absorbance, Indicator Bacteria, and Bacteroidales in Melon SaniTwice Group Hand Rinsate Samples (n=45)^a ....65

          Table 7. Correlations Between Concentrations of Absorbance and Indicator Bacteria in Jalapeño Farmworker Hand Rinsate Samples (n=89)^a...............….….65

          Table 8. Mean Difference in Concentrations of Absorbance and Indicator Bacteria by Intervention Group Between Melon and Jalapeño Farmworker Hand Rinsate Samples …………………………………………………………………….…….66

          Table 9. Perceptions of Hand Hygiene Intervention Methods Reported by 39 Farmworkers Harvesting Melons in Nuevo Leon, Mexico..………………...……67

     FIGURES……………………………………………………………………….…….69

          Figure 1. Absorbance (600 nm) levels measured from melon farmworker hand rinsate samples differ significantly across both intervention groups and the control group. The boxes display the 25^th, 50^th, and 75^th percentiles and diamonds denote the mean for absorbance data. Whiskers depict minimum and maximum values. Subscripts identify significant differences in log-transformed absorbance values across intervention group from a linear regression model controlling for farmworker age (a=significantly different from the SaniTwice group, b=significantly different from the control group). Tukey’s procedure was used to adjust for multiple comparisons ………………………………………………….69

          Figure 2. Absorbance (600 nm) levels measured from control group hand rinsate samples are significantly lower among farmworkers harvesting melons compared to farmworkers harvesting jalapeños. The boxes display the 25^th, 50^th, and 75^th percentiles and diamonds denote the mean for absorbance data. Whiskers depict minimum and maximum values. Linear regression was used to compare mean log10 absorbance by produce group, controlling for farm location, gender, harvest time, and age ………………………..…………………………………...………..70

          Figure 3. Concentrations of E. coli and Enterococcus spp. measured from control group hand rinsate samples are significantly lower among farmworkers harvesting jalapeños than farmworkers harvesting melons. The boxes display the 25^th, 50^th, and 75^th percentiles and circles and plus signs denote the mean for absorbance data. Whiskers depict minimum and maximum values. Linear regression was used to compare mean log10 CFU/hand concentrations for E. coli, Enterococcus spp., and coliforms by produce group, controlling for farm location, gender, harvest time, and age ……………………………………………………………..……….71

          Figure 4. The effect of each intervention group on absorbance, E. coli, and coliform concentrations differs significantly by produce type. (4a) Absorbance interaction plot (4b) E. coli interaction plot (4c) Enterococcus spp. interaction plot (4d) coliforms interaction plot. Two-way fixed-effects models were used to identify significant interaction between intervention group and produce type for absorbance and bacterial indicators. Models controlled for farm location, gender, harvest time, and age ………………………………...…………………………...72

III. PUBLIC HEALTH IMPLICATIONS ……………………………………………....73    

About this Master's Thesis

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School	Rollins School of Public Health
Department	Epidemiology
Degree	M.P.H.
Submission	Master's Thesis
Language	English
Research Field	Health Sciences, Public Health Health Sciences, Epidemiology Agriculture, Food Science and Technology
Palavra-chave	produce outbreaks melons Mexico foodborne outbreaks hand hygiene fresh produce
Committee Chair / Thesis Advisor	Leon, Juan S., Emory University
Committee Members	Prince-Guerra, Jessica, Emory University
Partnering Agencies	Does not apply (no collaborating organization)

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