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strawberries to contamination is evident by the number of
reported foodborne disease outbreaks (44, 49). Between
1997 and 2017, 32 strawberry-related outbreaks were
reported, sickening 933 people in the United States (11).
Pathogens associated with these outbreaks included Shiga
toxin-producing Escherichia coli, nontyphoidal Salmonella,
cyclospora, norovirus, and hepatitis A virus (11).
Strawberries are susceptible to microbial contamination for
several reasons: they are hand harvested, not washed before
packing (i.e., if intended for the fresh market), and grown close
to the soil (3, 16, 33, 45, 49, 58, 60). In addition, the natural
openings on the external surfaces provide niches for pathogens
to hide, making pathogens difficult to remove by washing
before eating (18, 58, 76, 77). Strawberries can also become
contaminated through contact with animals, agricultural water,
biological soil amendments of animal origin (BSAAO), as well
as contaminated equipment, tools, and buildings at the farm
level (75). Importantly, strawberries are often eaten raw (71),
with no kill step to eliminate pathogens before consumption.
All these reasons illustrate the importance of proper implementation
of risk management practices (RMP).
Improving the safety of fresh produce, including strawberries,
is a priority of the Food Safety Modernization Act
standards for the growing, harvesting, packing, and holding
of produce for human consumption, commonly referred to
as the Produce Safety Rule (PSR) (75). The Produce Safety
Alliance, the only U.S. Food and Drug Administration-recognized
grower training program, delivers training aimed to
increase compliance with the PSR (58). At present, training
is not mandatory under the PSR for very small produce
farms, defined as farms earning less than US$25,000 in
annual sales (3-year average, adjusted for inflation), as well
as other qualified exempt farms (75). In 2017, 89% of U.S.
strawberry farms were less than 5 acres (20,234 m2
were less than 1 acre (4,047 m2) (67). The average strawberry
farm size in 36 U.S. states is less than 2 acres (8,094 m2
which is also the average for 8 (62%) of 13 southeastern
(SE) states (67). In 2017, the U.S. average value of utilized
production of strawberries (except California and Florida)
was US$21,572 per 2 acres (8,094 m2
) (70); hence, many
strawberry farms were exempt from the mandatory Produce
Safety Alliance grower training.
Even though researchers, produce industry members,
and government personnel have identified and communicate
RMP through training, produce-associated outbreaks
continue to occur (10). One explanation might be that small
farms (i.e., those that are exempt) are less likely to implement
RMP (1, 5, 50). Consequently, new approaches are
needed to improve implementation of RMP on small farms,
including strawberry farms. Implementation science methodology
could be used to inform training aimed to improve
on-farm implementation of RMP. One underlying principle
in implementation science is that understanding context,
such as availability of tools and adequate infrastructure, is
necessary for successful implementation of an intervention
(48), highlighting the importance of characterizing physical
attributes (PA) associated with RMP. To date, most published
studies conducted with produce growers, including
strawberry producers, have focused on directly and indirectly
assessing RMP and not PA associated with RMP (1, 39, 47,
59). A published review examined the relationship between
environmental attributes, including PA, and RMP on produce
farms (41). To the best of our knowledge, no studies have
specifically focused on characterizing PA associated with the
implementation of RMP on strawberry farms.
This descriptive study aimed to determine the PA associated
with implementation of RMP of a convenience sample
of 20 small strawberry farms in the SE United States. Within
the context of this study, we defined small farms as those that
are ≤ 2 acres (8,094 m2
). These findings can inform strawberry-specific
safety interventions aimed to increase RMP
implementation.
MATERIALS AND METHODS
Ethics statement
The study protocol was reviewed by the Clemson University
Institutional Review Board (2019-375) and determined
to be exempt. An informed consent form with a description
of the research background, procedures, risks, benefits, and
confidentiality was provided to growers or on-farm representatives,
and consent was obtained before site visits were
conducted. Farm identification information (e.g., farm name,
contact person name, farm address, phone number, and
e-mail address) was also collected. All data were kept confidential
and were only accessible to research team members.
), and 66%
),
Sample selection and recruitment of data collectors
Our target population was a convenience sample of small
strawberry farms, defined as ≤ 2 acres (8,094 m2
), across 13
SE states: Alabama, Arkansas, Florida, Georgia, Kentucky,
Louisiana, Mississippi, North Carolina, Oklahoma, South
Carolina, Tennessee, Texas, and Virginia. Two or more small
strawberry farms from each SE state were recruited.
Fourteen data collectors who work in horticulture and
food safety were recruited from 10 of 13 SE states. Data
collectors were expected to (i) recruit at least two small
strawberry farms in the state and (ii) conduct on-farm
assessments on those farms. A 30-min training Webinar
about data collection procedures was conducted before data
collection began. Of the 14 recruited data collectors, 10
completed on-farm assessments. Four data collectors did
not complete the on-farm assessments due to individual
state COVID-19 restrictions regarding university-sponsored
research activities.
Instrument development
Site visits were conducted by using an environmental
assessment (EA) checklist (Supplemental Material for the
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