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eye, such as hand-colored soil. We recommend that the
Visible Hand Dirtiness Score may be a useful alternative
to assess visible hand soil in the field or in settings where
it is not possible to measure the turbidity of a hand rinse.
Visible Hand Dirtiness Score may also be a better indicator
of perception of soil on farmworker hands than turbidity,
because it is based on visible soil instead of soil picked up in
a hand rinse.
The Visible Hand Dirtiness Score was weakly associated
with Enterococcus (rho = 0.273), but not significantly
correlated with E. coli and coliforms. Because Visible
Hand Dirtiness score was correlated to turbidity (rho =
0.549), we also expected a correlation between turbidity
and Enterococcus (rho = 0.352) and a lack of a significant
correlation between turbidity with E. coli and coliforms,
which we found. One hypothesis to explain the difference
in relationships between Visible Hand Dirtiness Score
and turbidity with each indicator organism may be that
different indicator organisms differ in their biology and their
prevalence in the environment (8). For example, Enterococcus
may have been correlated with visible soil because this
bacterium is commonly found in the soil environment and
could be transferred to farmworker hands along with the
soil during harvest (3). Our previous studies on bacterial
concentrations on fresh produce confirm that Enterococcus
is highly prevalent in the agricultural environment. In one
study, performed in 2000-2003, in which 923 produce
samples were collected from 15 farms and 8 packing sheds
(1), we found that Enterococcus was detected on 78% of all
produce samples, whereas E. coli was detected on 16% of
produce samples (1). In a second study, performed between
November 2002 and December 2003, 466 produce samples
were collected from 8 packing sheds, and the level of
Enterococcus found on produce samples ranged from less than
1.0 log10 to 5.4 log10 CFU/g (14).
This study has several strengths and limitations. One
strength was that the Visible Hand Dirtiness Score was a
valid and reproducible measure, as evidenced by two pilot
tests in which two independent reviewers scored hands
with > 90% agreement on each category. We also were
able to perform the experiments in real life conditions,
on a farm rather than using simulated conditions. One
limitation of this study is the low prevalence of specific
indicators (i.e., E. coli), suggesting that a larger sample
size would have provided greater statistical power and
ability to detect possible relationships. Another limitation
is that we utilized indicator bacteria as a measure of

contamination rather than pathogen contamination,
which also would have required a larger sample size to
detect the relatively low prevalence of pathogens (5).
Based on these results, visible hand soil may be a moderate
proxy for hand rinse turbidity, but it is not a strong indicator
of bacterial load on farmworker hands. First, the Visible
Hand Dirtiness Score may be a better indicator of perception
of soil on farmworker hands than turbidity is, because
the score is based on soil seen by the eye. Therefore, we
recommend that the Visible Hand Dirtiness Score can be
used as a research-based teaching tool to demonstrate to farm
workers the areas commonly missed during handwashing,
especially in the field, where a turbidimeter is not accessible.
Second, farmworkers or managers cannot depend on visible
cleanliness alone in assessing the microbiological cleanliness
of hands. Therefore, regardless of whether hands look
"clean," to minimize the risk of pathogen contamination on
fresh produce, we recommend that growers follow Good
Agricultural Practices (GAPs) as recommended in the US
FDA Produce Rule (9) and newer, innovative hand hygiene
recommendations that are proven and evidence based, such
as well-formulated ABHS interventions (6).
ACKNOWLEDGMENTS
We thank the farmworkers for their collaboration. We also
thank Dr. Lee-Ann Jaykus for the conception of the study
and Dr. Ben Lopman for guidance on the analysis. Additionally, we thank Nereida Rivera, Roberto Blancas, and Aldo
Galvan from Universidad Autonoma de Nuevo Leon for the
collection and processing of samples and Manasa Bhatta at
Emory University for data entry. This material is based upon
work that is supported by the National Institute of Food and
Agriculture, U.S. Department of Agriculture, under award
number 2015-67017-23080.
This project was financially sponsored by GOJO
Industries, Inc., through an unrestricted research grant to
cover partial salary for the effort of the study team, study
supplies, and communication of results. Emory University
and UANL covered the remainder of staff salary through
internal funding, government fellowships and subsidies.
UANL-affiliated authors provided significant input into
the overall study design, data collection, and editing of the
manuscript. Emory-affiliated authors provided significant
input into the overall study design, data analysis, and
writing of the manuscript. Mention of trade names or
commercial products does not constitute endorsement or
recommendation for use.

REFERENCES
1. Ailes, E. C., J. S. Leon, L.-A. Jaykus,
L. M. Johnston, H. A. Clayton, S. Blanding,
D. G. Kleinbaum, L. C. Backer, and C. L.
Moe. 2008. Microbial concentrations on
fresh produce are affected by postharvest
processing, importation, and season. J. Food
Prot. 71:2389-2397.

2. Bartz, F. E., D. W. Hodge, N. Heredia,
A. Fabiszewski de Aceituno, L. Solís,
L.-A. Jaykus, S. Garcia, and J. S. Leon.
2016. Somatic coliphage profiles of produce
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in northern México. Food Environ. Virol.
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3. Byappanahalli, M. N., M. B. Nevers,
A. Korajkic, Z. R. Staley, and V. J. Harwood.
2012. Enterococci in the environment.
Microbiol. Molecul. Biol. Rev. 76:685-706.

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