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Assessing vegetable producers' beliefs regarding food safety issues

Authors:
Vegetable producersperceptions of food safety hazards in the Midwestern USA
Melanie L. Lewis Ivey
a
, Jeffrey T. LeJeune
b
, Sally A. Miller
a
,
*
a
Department of Plant Pathology, The Ohio Agricultural Research and Development Center, The Ohio State University, 1680 Madison Avenue, Wooster, OH 44691, USA
b
Food Animal Health Research Program, The Ohio Agricultural Research and Development Center, The Ohio State University, 1680 Madison Avenue, Wooster, OH 44691, USA
article info
Article history:
Received 11 November 2011
Received in revised form
19 January 2012
Accepted 20 January 2012
Keywords:
Food safety
Pre-harvest contamination
Post-harvest contamination
Mental models
Producer perceptions
Science-based management decisions
Risk communication
abstract
The perspectives, practices and potential gaps in knowledge regarding fresh produce safety hazards
among Midwestern US vegetable producers were measured using a survey-based conrmatory assess-
ment. Although the majority of vegetable producers considered themselves familiar with national Good
Agricultural Practices (GAPs) and agreed that implementing GAPs could reduce the risk of produce
contamination, they were not consistently practicing GAPs. Irrigation and run-off water, worker hygiene,
raw and composted animal manure, wildlife droppings, eld proximity to livestock or wildlife habitats,
plant diseases and insects were acknowledged as important potential sources of pre-harvest microbial
contamination of produce, but paradoxically, producers disagreed that contamination most frequently
originated on-farm. There was signicant variation in producerslevel of agreement with regard to the
importance and economic feasibility of various management practices for the prevention of on-farm food
contamination. In general, vegetable producers did not declare an immediate need for more information
on food safety, but did nevertheless, indicate that they would like more information on the sources of
produce contamination, how contamination occurs, and GAPs guidelines. Vegetable producers preferred
in-person modes of communication over mass media, fact sheets or electronic modes, with only 17%
having a preference for Internet or email based information. These ndings aid in the development and
delivery of targeted, science-based, farm management guidelines and knowledge translation programs
aimed at enhancing the safety of produce on the farm.
Ó2012 Elsevier Ltd. All rights reserved.
1. Introduction
Recent years have been marked by an increase in foodborne
disease outbreaks caused by the consumption of fresh produce
contaminated with pathogenic bacteria and these outbreaks
currently account for more illnesses than outbreaks caused by beef,
poultry and seafood (DeWaal, Tian, & Plunkett, 2009). Much of the
current research emphasis is directed toward identifying the
sources and mechanisms of pre- and post-harvest contamination
(Lynch, Tauxe, & Herberg, 2009), understanding plant pathogen/
human pathogen interactions (Aruscavage, Lee, Miller, & LeJeune,
2006; Parish et al., 2003), and assessing the efcacy of post-
harvest decontamination practices (Teplitski, Barak, & Schneider,
2009) with the long-term goal of reducing the number of food-
borne illnesses and deaths related to these illnesses. Long-term
research outcomes of such studies are to develop improved
science-based guidelines for pre- and post-harvest protection of
fresh produce from microbial threats. However, in the short-term,
there is a need to transfer and translate generated knowledge to
the end-users and to provide producers with the tools they may
need to integrate vegetable food safety practices into daily
management of food production systems.
Historically, information transfer in agriculture is a top-down
process, from expertsource (i.e. scientist or academic) to inex-
pertrecipient (i.e. practitioner or layperson). Experts often provide
information that is inuenced by their own perceptions, biases,
preferences, beliefs and knowledge, often without rst identifying
these same attributes in the recipients of the information (Morgan,
Fischhoff, Bostrom, & Atman, 2002). As a result, the recipients often
miss the intended message and become confused, annoyed or
disinterested (Morgan et al., 2002) while the communicator
becomes frustrated that the message is not being accepted or
adopted (Francis, 2009).
Effective risk communication is grounded in an understanding
of the mental models of communicators and target audiences
(Morgan et al., 2002). The mental models methodology has been
previously applied in risk communications related to natural
disasters (Zaksek & Arvai, 2004), global climate change (Bostrom,
Fischhoff, & Morgan, 1994), public health concerns (Atman,
Bostrom, Fischhoff, & Granger Morgan, 1994; Cox et al., 2003;
*Corresponding author. Tel.: þ1 330 263 3678; fax: þ1 330 263 3841.
E-mail address: miller.769@osu.edu (S.A. Miller).
Contents lists available at SciVerse ScienceDirect
Food Control
journal homepage: www.elsevier.com/locate/foodcont
0956-7135/$ esee front matter Ó2012 Elsevier Ltd. All rights reserved.
doi:10.1016/j.foodcont.2012.01.065
Food Control 26 (2012) 453e465
Jungerman, Shutz, & Thuring, 1988; Marik & Fischhoff, 1992),
hazardous processes (Bostrom, Fischhoff, & Morgan, 1992) and
most recently in agriculture-related disciplines (Cattaneo, Wislon,
Doohan, & LeJeune, 2009; Wilson, Parker, Kovacs, Doohan, &
LeJeune, 2009; Wilson, Tucker, Hooker, LeJeune, & Doohan, 2008).
The mental models approach (Morgan et al., 2002)isave-stage
formal analysis that can provide insight into ways of broadening
the deeply held beliefs of a particular audience through rst
identifying individualsbeliefs, then addressing them with highly
specic and targeted risk communication messages (Atman et al.,
1994; Morgan et al., 2002). Classically, the rst two stages of
a mental models approach are the elucidation and description of
thought patterns, or mental models, of the problem and associated
decision-making process held by 1) experts in the eld and 2)
practitioners or routine decision-makers. The third stage is the
development and implementation of a survey-based conrmatory
and quantitative assessment of the rst two models. The last two
stages involve the development and evaluation of risk communi-
cation messages.
In this and companion studies, expert-based mental models
depicting expected inuences on farmersdecision-making
regarding the safety of fresh produce were developed (Parker,
Wilson, LeJeune, Rivers III & Doohan, 2012; Wilson et al., 2009).
The primary goal of this study was to determine the extent to which
the beliefs, attitudes, perceptions and practices identied in these
previously described mental models were shared among producers
in the Midwestern United States. The results of this study will be
used to prioritize the development and delivery of risk communi-
cation materials about pre-harvest vegetable food safety hazards so
that producers can make more informed, science-based manage-
ment decisions.
2. Methods
2.1. Research approach and survey design
In a companion study (Wilson et al., 2009), qualitative expert
and grower mental models depicting expert and grower
perspectives on decision-making regarding contamination
prevention and response for fresh and fresh-cut produce were
developed. In this study, major factors inuencing these growers
perspectives and practices, and potential gaps in knowledge were
identied from the qualitative companion models and a survey-
based conrmatory assessment was developed. The survey con-
sisted of four sections (Tab le 1) and the questions were either non-
weighted and discrete (yes or no, select one responseor select
all that apply), ranks, or Likert Scales. The survey was pre-tested
by various representative stakeholders (n ¼10) including vege-
table producers, Extension specialists and researchers from Ohio.
Survey pre-testers were asked to note the following as they per-
formed their validation: 1) approximate time needed to complete
the survey; 2) questions that were unclear or difcult to interpret;
3) terminology that was not understood or needed to be claried;
4) formatting concerns (i.e. font type and size, amount of content
per page, grammatical or spelling errors) and 5) any additional
comments about the survey. The reviewerscomments were
ascertained in a group via teleconference and the survey was
modied accordingly.
2.2. Participant recruitment
All survey and contact documents were reviewed by The Ohio
State University Ofce of Risk Protection and deemed exempt
from further review by the Institutional Review Board. Partici-
pants were selected from a mailing list from a commercial lay
publisher of farming magazines (Farm Journal Media Inc., Park
Ridge, IL). Individuals self-identied as vegetable growers were
randomly selected from 195, 416, 151, and 42 names available in
the states of Ohio (OH), Michigan (MI), Indiana (IN) and Kentucky
(KY), respectively. One hundred and fty-three OH growers, 318
MI growers, 119 IN growers and 31 KY growers were mailed
surveys, representing 76% of the qualied names provided from
each state on the mailing list. A ve-contact, Tailored Design
Sequence (TDS) (Dillman, 2007) was used, consisting of a pre-
notice letter, questionnaire, reminder postcard and a return
incentive postcard sent to selected participants. Participants who
returned the incentive postcard within 90 days received a thank
you letter and a $5 gift card as compensation. For surveys
returned as undeliverable, additional questionnaires were sent
to alternate, randomly selected participants from the same state.
The survey was conducted from December 2008 through March
2009.
2.3. Data analysis
The survey was manually coded by assigning a unique number
to each possible response and the response codes were entered into
a multivariate Excel spreadsheet (Microsoft Excel 2008, 2007
Microsoft Corp.). The PivotTable report function in Excel 2008 was
used to combine, summarize and identify trends in the participants
responses to each question. Descriptive statistics were determined
for the demographic and vegetable production responses and
research questions and hypotheses were tested using either the
KruskaleWallis (Kruskal, 1952; Kruskal & Wallis, 1952) or Mood
Table 1
Survey sections, question types and content of the vegetable food safety survey.
Section No. Question type Content
1 Production and management practices Years producing vegetables, acres produced, production locations, types of vegetables produced,
irrigation and wash water sources and practices, Good Agricultural Practices (GAP)
implementation, auditing procedures, Integrated Pest Management (IPM) practices,
production challenges
2 Knowledge and beliefs regarding
contamination threats
Organizations responsible for ensuring food safety, organizations that inuence management
practices, pathogens that contaminate fresh produce, sources of pre- and post-harvest
contamination, activities likely to cause contamination, management practices that prevent
contamination, economically feasible management practices to prevent contamination, stages
in the chain of custody where contamination occurs
3 Knowledge and beliefs regarding
contamination response
and communication
Opinions regarding producers preparedness for a contamination event, need for information
about food safety or GAP guidelines, preferred modes or sources of communication, types of
research that is needed to understand and respond to a contamination event and the impact
a contamination event would have on production
4 Demographics Age, gender, education, heritage, religious afliations, production sales
M.L. Lewis Ivey et al. / Food Control 26 (2012) 453e465454
one-way analysis of variance by ranks tests (Mood, 1954), or
Spearmans rank-order correlation coefcient (Spearman, 1904)as
appropriate. Medians were separated using the Dunn test (Dunn,
1964) with a Minitab macro (Orlich, 2000) in combination with
the KruskaleWallis test. Data were considered to be statistically
signicant at a 95% condence level (
a
¼0.05) unless otherwise
noted. All statistical tests were conducted using Minitab 15.1.20.0
(2007 Minitab Inc.).
3. Results
3.1. Survey response rate and respondent demographics
Of the 621 surveys mailed, 210 were returned (33.8% response
rate) within 90 days. At least 50% of the questions were answered
for 164 (26.4%) of the surveys, and 46 (21.9%) were returned with no
responses. Fifty-two percent (52.4%) of the respondents grew
vegetables in MI, 33.5% in OH, 20.1% in IN and 8.5% in KY. One
percent (1.2%) of the respondents grew vegetables in Florida (FL)
and Illinois (IL) and less than one percent grew vegetables in
Pennsylvania (PA) and Georgia (GA). Respondentsdemographic
information including age, level of education, gender, vegetable
sales (for 2007) and number of acres and years of vegetable
production is summarized in Table 2.
3.2. Production practices
The majority (95%) of the respondents produced vegetables
using conventional farming practices. One respondent from OH and
one from MI (1%) produced certied organic vegetables, 4% used
both certied organic and conventional management practices
(mixed farming practices) and 2% indicated transitional organic
production systems. Ten (6%) respondents grew vegetables under
high tunnels (hoop houses) with two of those respondents indi-
cating that more than 21% of their production was under high
tunnels.
Cucurbits, sweet corn and tomato were most often listed as the
top three vegetables produced in terms of total acres of production.
In OH, 31% of the respondents listed cucurbits and tomato as the
most cropped vegetables. In MI, cucurbits and asparagus were top
ranked and in IN and KY tomato and sweet corn were ranked rst.
3.3. Growersperspectives on management decisions regarding
produce food safety
The distribution of producer responses as to the types of
groups or organizations that inuence their management decisions
varied signicantly regarding produce food safety (
c
2
¼183.4,
DF ¼9, p0.001). Over 68% of producers either strongly or
somewhat agreed that consumers, crop consultants, retailers,
government regulators and university representatives inuence
their management decisions regarding produce food safety (Fig. 1).
Only 32% of producers were in agreement that media inuenced
their produce food safety management practices (Fig. 1). However,
55% agreed that news reports or stories specic to disease
outbreaks associated with fresh produce changed their manage-
ment practices. Producers strongly or somewhat disagreed (72%)
that farm management practices should be regulated by govern-
ment agencies. When asked to rank six groups or organizations
(consumer, producer, retailer, processor, government agencies and
universities) from most to least important with regard to which
should be responsible for ensuring food safety, producers ranked
themselves rst followed by processors, retailers, and consumers
(
c
2
¼411.3, DF ¼5, p0.001). Government agencies and university
extension were equally ranked last.
3.4. Producer familiarity with and implementation of good
agricultural practices
Specic survey questions were included to determine
producersself-perception of compliance with GAPs. Questions
were also asked about their specic management practices. These
questions permitted a comparison of how producers thought
they were complying with GAPs and actual management prac-
tices employed on the farm. Producers agreed (83%) that
following GAPs could reduce the risk of produce contamination,
however less than two thirds (60%) indicated that they practiced
GAPs all or most of the time. Approximately one quarter of
respondents (23%) were not at all familiar with GAPs and of those
respondents 89% indicated that they didnt know if they were
practicing GAPs, 3% indicated they never practiced GAPs, and 8%
indicated that they practiced GAPs all of the time. There was
a positive correlation between producersfamiliarity with GAPs
and their implementation of them, but only amongst those who
Table 2
Descriptive summary of Midwestern vegetable producer demographics.
Variable Variable
description
Distribution of responses (%)
Ohio Michigan Indiana Kentucky All
Age 35 12.2 5.1 3.4 0.0 6.3
36e65 75.5 79.7 86.2 90.0 80.5
66 12.2 15.2 10.3 10.0 13.2
Gender Male 93.9 98.8 89.7 70.0 94.4
Female 6.1 1.2 10.3 30.0 5.6
Education High school
or less
40.8 43.8 41.4 30.0 42.5
College
or higher
59.2 56.2 58.6 70.0 57.5
Years in
vegetable
production
1e20 28.0 22.5 36.7 45.5 28.8
21e30 14.0 23.8 23.3 9.0 20.9
>30 58.0 53.7 40.0 45.5 50.3
Acres in
vegetable
production
<10 18.0 3.7 16.7 63.6 14.6
10e50 12.0 13.6 10.0 27.3 14.0
51e100 16.0 17.3 6.7 0.0 14.0
>100 54.0 65.4 66.7 9.1 57.3
Vegetable sales
a
100 36.7 31.3 34.5 80.0 37.5
100 <500 30.6 37.5 27.5 10.0 33.8
500 32.7 31.3 37.9 10.0 28.8
a
Vegetable production sales (X 10
3
) in 2007.
Fig. 1. Response percentage of Midwestern vegetable producers who indicated that
they strongly or somewhat agree that various groups or organizations inuence their
management decisions regarding produce food safety. The line on the graph represents
the top ve groups or organizations that inuenced producersmanagement decisions
regarding produce food safety.
M.L. Lewis Ivey et al. / Food Control 26 (2012) 453e465 455
were very familiar, somewhat familiar or indifferent to GAPs
(
r
¼0.347, p0.001; Fig. 2A). For those producers who ranked
(in terms of acreage) a fresh market vegetable as their top ranked
crop the correlation between producer familiarity and GAPs
implementation increased (
r
¼0.394, p¼0.006; Fig. 2B).
No associations between the frequency with which producers
cleaned or sanitized packaging equipment and the extent to which
they practiced GAPs were identied. Over half (55%) of the
producers who packaged produce on the farm cleaned and sani-
tized their packaging equipment (bins, totes etc.) at least once
a week (Fig. 3A). However, 29% never cleaned or sanitized pack-
aging equipment and of those producers, 18% indicated that they
practiced GAPs all or most of the time.
There was a positive correlation between the frequency of
testing water (
r
¼0.343, p0.001) or testing wash water for
residual disinfectants (
r
¼0.227, p¼0.013) and the extent to which
producers indicated that they practiced GAPs. The majority (70%) of
growers who washed produce on the farm tested their water at
least once per year (Fig. 3B). However, 20% never tested their water
(Fig. 3B) and 67% did not test for residual disinfectant in their wash
water (Fig. 3C). Only 16% of the producers who washed produce on
the farm considered themselves to be very familiar with GAPs and
indicated that they practiced them all of the time. An additional
30% indicated that they were somewhat familiar with GAPs and
practiced them most of the time. The level of practice of GAPs
indicated by producers was associated with on-farm packaging of
produce (
r
¼0.161, p¼0.045) but not with the washing of produce
on the farm.
Fig. 2. Box plots showing Midwestern vegetable producersreported familiarity and
implementation of national Good Agricultural Practices (GAPs). A: All vegetable
producers who responded to both of the questions Are you familiar with GAPs?and
To what extent does your farm practice national GAPs?. B: Includes only those
producers that indicated a fresh market vegetable as their top ranked crop in terms of
acreage and responded to both of the questions listed in A. Gray boxes represent the
interquartile range where the top of the box is at third quartile, the bottom of the box
is the rst quartile and the middle line is placed at the second quartile, or median.
Lines extending from the boxes represent the range of data from the rst and third
quartiles to their respective extremes.
A
B
C
Fig. 3. Reported frequency of cleaning or sanitizing packaging equipment (A); testing
produce wash water (B) and testing residual disinfectant in wash water (C) by Mid-
western vegetable producers who wash produce on their farm.
M.L. Lewis Ivey et al. / Food Control 26 (2012) 453e465456
3.5. Producer beliefs regarding sources and prevention of the
contamination of fresh produce
Producers ranked the importance of some microorganisms
higher than others (
c
2
¼253.0, DF ¼9, p0.001; Fig. 4). Producers
considered Escherichia coli (E.coli; pathogenic or non-pathogenic)
and Salmonella to be signicantly more important contaminants of
fresh produce than coliforms, Listeria, parasites, Clostridium,
viruses, Cyclosporia,Cryptosporidium or the mad cow disease
agent.
Producers had signicant differences in their level of agreement
as to where in the food chain produce contamination is most likely
to occur (
c
2
¼95.8, DF ¼6, p0.001; Fig. 5). Producers believed
that the home (50%), processing (43%) and wholesale or retail
operations (38%) were the most common sites of produce
contamination and that contamination was least likely to occur on
the farm (19%).
The majority of producers agreed that certain vegetables are
more likely to become contaminated than others (89%;
c
2
¼227.7,
DF ¼2, p0.001) and that knowing the source of contamination is
important to making management decisions (94%;
c
2
¼269.0,
DF ¼2, p0.001). Only 11% of producers disagreed with the
statement organic farms are more likely to produce contaminated
vegetables than conventional farms. Forty-four percent agreed
with the statement and the remaining 45% were of neutral opinion.
The two organic producers who responded to the surveysomewhat
disagreed that organic farms are more likely to produce contami-
nated vegetables.
Producerslevel of agreement regarding potential sources of
pre- and post-harvest contamination (
c
2
¼259.5, DF ¼18,
p0.001 and
c
2
¼83.4, DF ¼14, p0.001 respectively) of fresh
produce varied signicantly. At least one third of the respondents
strongly agreed that animal and bird droppings, raw manure,
handling by workers and criminal acts or terrorism could
contribute to both pre- and post-harvest contamination (Fig. 6).
Producers also strongly agreed that wash water (42%) and raw
animal manure (50%) were potential sources of contamination.
Producers somewhat agreed (median response ¼2) that insects
(pre- and post-harvest) and pre-harvest plant pests could be
sources of contamination and they were indifferent (median
response ¼3) to whether or not post-harvest plant diseases and
weeds were sources of contamination (Fig. 6). Producers who
strongly agreed that pests could be sources of contamination
believed insect infestations (pre- and post harvest) were more
likely to be a source of contamination than plant diseases or weed
infestations (
c
2
¼17.5, p¼0.002, DF ¼4).
3.6. Producer beliefs regarding the importance and economic
feasibility of management practices for the prevention of on-farm
food contamination
Producerslevel of agreement regarding the importance
(
c
2
¼765.3, DF ¼27, p0.0001) and economic feasibility
(
c
2
¼696.3, DF ¼26, p0.0001) of management practices for the
prevention of on-farm food contamination varied signicantly.
Producers equally believed that the control of plant diseases and
insect infestations is somewhat important in the prevention of
produce contamination and they somewhat agreed that the control
of these pests is an economically feasible practice (Table 3).
Producers were indifferent as to whether or not minimizing contact
between irrigation water and edible plant parts would be an
important management practice to reduce food contamination and
somewhat disagreed that eliminating overhead irrigation would be
economically feasible (Table 3). More producers believed that the
treatment of wash water would be very important for the
prevention of food contamination than would treatment of surface
water or well water used for irrigation (Fig. 7). Producers equally
believed that the routine testing of wash water and irrigation water
could be somewhat important in the prevention of produce
contamination but only somewhat agreed that testing wash water
would be economically feasible and were indifferent as to the
extent to which testing irrigation water would be economically
feasible. Routine on-farm inspections by trained upper manage-
ment employees were thought to be more important and
economically feasible than inspections by government agents or
third party auditors. Over one third (33%) of producers thought that
banning raw manure as an amendment would be very important
for the prevention of food contamination and 24% strongly agreed
Fig. 4. Percentages of Midwestern vegetable growers who believed that various
foodborne microorganisms were very importantor somewhat important
contaminants of fresh produce.
Fig. 5. Cumulative distribution of Midwestern vegetable producersreported
responses as to where contamination of fresh produce most likely occurs.
M.L. Lewis Ivey et al. / Food Control 26 (2012) 453e465 457
that it would be economically feasible (Fig. 7). Producers also
believed that the appropriate timing of both raw and composted
animal manure would be a very important management practice
for the prevention of produce contamination (56 and 43% respec-
tively; Fig. 7). While producers believed that separating livestock
and poultry farms (38%) from vegetable producing areas and the
use of barriers to restrict animal movement in the eld (35%) were
very important in the prevention of food contamination, only 17%
and 8% strongly agreed that these practices were economically
feasible, respectively (Fig. 7).
3.7. Food safety information needs of producers
The majority (82%) of producers declared that they had no
immediate need for food safety information, that they knew where
to nd information regarding food safety (77%) and that they were
content with the quality of information provided by university
extension (70%). Producers most frequently indicated that they
wanted more information on the sources of contamination (41%)
and GAPs guidelines (40%; Fig. 8).
3.8. Producer perspectives on contamination response
There was signicant variation in the distribution of responses
as to the type of impact that the occurrence of an on-farm food
safety contamination event might have on a producersfarm
(
c
2
¼218.3, DF ¼8, p0.001; Fig. 9). The perceived impacts
separated into three groups based on the frequency of responses.
Poor reputation, adoption of additional food safety practices and
loss of market share (Group 3) were most frequently selected, fol-
lowed by additional inspections, changes to the type of commodity
being produced, going out of business, lower product pricing and
worker layoffs (Group 2). Group 1 contained three producers (1.8%)
that selected the othercategory with two producers specifying
the type of impact (1: an on-farm contamination event would be
highly unlikelybecause the commodity that they produce is
processed and 2: a loss of buyerswould also be an impact). Most
producers (80%) indicated that a contamination event on a neigh-
boring farm could impact their own farms operations (
c
2
¼56.0,
DF ¼1, p0.001) and that their farms would be prepared to deal
with a contamination event should one occur (71%;
c
2
¼27.9,
Fig. 6. Midwestern vegetable producersreported level of agreement about potential sources of pre- and post-harvest microbial contaminants.
M.L. Lewis Ivey et al. / Food Control 26 (2012) 453e465458
DF ¼1, p0.001). Producers (83%) also believed that their
employees are very or somewhat knowledgeable about food safety
hazards (
c
2
¼68.4, DF ¼1, p0.001).
Vegetable producers most frequently selected university
extension (66%) as the group or organization that they would
contact in response to an on-farm contamination event (
c
2
¼284.3,
DF ¼8, p0.001; Fig. 10). Producerssecond choice was crop
consultants (42%) followed by food safety consultants (29%),
commodity group representatives (27%), government agency
representatives (20%), retailer (16%), third party auditors (10%), no
group or organization (7%) and media (2%).
Producers ranked university extension signicantly higher than
any other regarding the group or organization from which they
would seek help during an on-farm contamination event
(
c
2
¼114.3, DF ¼7, p0.001). Commodity group representatives,
crop consultants and food safety consultants ranked second, and
third party auditors ranked third. Producers ranked both retailers
and government agency employees fourth and media representa-
tives fth.
3.9. Communication of food safety risks
Producer responses to the question What modes of commu-
nication do you prefer to receive information regarding food safety
hazards?were combined into four groups: 1) mass media that
included newspapers, television or radio and magazines; 2) in-
person communication that included training sessions and
grower meetings; 3) electronic communication that included
internet or email; and 4) fact sheets or pamphlets. Producers
preferred in-person modes of communication to all other
communication modes (
c
2
¼62.1, DF ¼3, p0.001). However, for
their second most preferred mode of communication, the distri-
bution of responses varied depending on age (
c
2
¼21.3, DF ¼6,
p¼0.002) and level of education (
c
2
¼7.5, DF ¼3, p¼0.057).
Producers 35 years of age preferred electronic modes of
communication while those between the ages of 36e65 preferred
fact sheets or pamphlets and producers 66 years old preferred
mass media modes of communication. Post secondary school
educated producers preferred fact sheets or pamphlets and those
with any level less than post secondary preferred mass media.
Producers most frequently selected training sessions held in
the off-season (74%) as the most likely way to encourage producer
attendance or participation in learning programs or training
sessions (
c
2
¼300.2, p0.001, DF ¼7; Fig. 11). Off-season, short
training sessions (1e2 h) held close to the farm were preferred
over off-season, all day, on-farm training sessions (
c
2
¼49.4,
p0.001, DF ¼3). Nearly half of the producers (47%) indicated
that training sessions encompassing multiple topics such as food
safety, disease management, or soil fertility would encourage
attendance and participation. Producers who selected other
indicated that getting paid to be trained in issues regarding food
safety,training sessions leading to post test credits,being
trained by people who know what we need,andtraining
sessions required by the buyerwould encourage attendance and
participation.
4. Discussion
Based upon expert models and previous in-depth interviews
with vegetable producers we were able to determine the extent to
which beliefs and behaviors pertaining to pre- and post-harvest
food safety hazards were held among a wider population of vege-
table growers in the Midwest. The majority of surveyed vegetable
producers:
Table 3
Midwestern vegetable producersmedian responses regarding the importance and
economic feasibility of management practices for the prevention of on-farm food
contamination.
Management practice Median response
Prevention
a
Economic
feasibility
b
Control of crop pests
Plant diseases 2 eei
c
2fei
Insect infestations 2 hek2hek
Weeds 2 def2eeh
Irrigation
Minimizing plant and water contact 3 bc e
Use of drip or in-furrow irrigation e
d
2de
Eliminating overhead irrigation e4ab
Amendments
Excluding or banning the use of raw manure 2 eeg3cd
Appropriate timing of raw manure applications 1 lm e
Appropriate timing of composted manure
applications
2kl e
Use of composted manure e3c
Use of chemical fertilizers e2de
Wildlife
Separation of elds from livestock and poultry
farms
2iek2cd
Use of physical barriers to restrict animal
movement in elds
2eei4ab
Routine testing of:
Wash water 2 gei2eei
Irrigation water 2 de 3 cd
Produce 2 eeg2def
Compost e2deg
Treatment of:
Wash water 2 iek2eeh
Irrigation surface water 2 cd 3 b
f
Irrigation well water 3 b
Routine on-farm inspections by:
Government agents 3 a 4 a
Trained upper management employees 2 eeh2def
Third party auditors 3 b 3 b
Employee training in:
Personal hygiene 1 m 2 jk
Hand washing techniques 1 m 2 jk
Sanitation
Machinery and equipment Providing convenient 2 jk 2 gek
Restrooms and hand washing stations 1 m 2 k
Proper disposal of sewage 1 n 1 l
Documentation and signage
Posting personal hygiene signs in multiple
languages
e
2kl 2jk
Food safety standard operating procedures (SOP) 2 fei
Access to food safety SOP 2 hek2eeg
Other
Neighboring farms participation in food safety
prevention practices
2eege
Controlling movement of on-farm visitors 2 de e
c
2
¼765.3,
DF ¼27,
p0.0001
c
2
¼696.3,
DF ¼26,
p0.0001
a
Median response to the question To what extent do you consider the following
management practices to be important in the prevention of food contamination?
where 1 ¼very important; 2 ¼somewhat important; 3 ¼indifferent; 4 ¼somewhat
unimportant and 5 ¼not important.
b
Median response to the questions To what extent do you agree or
disagree that the following on-farm management practices are economically
feasible options to prevent food contamination?where 1 ¼strongly agree;
2¼somewhat agree; 3 ¼neither agree nor disagree; 4 ¼somewhat disagree and
5¼disagree.
c
Differences were tested and medians separated using KruskaleWallis one-way
analysis test on ranks. Medians followed by the same letter within a column are not
statistically signicant at a 95% condence level (
a
¼0.05).
d
Indicates that the management practice was not a choice for the relevant
question on the survey.
e
Question on the survey actually reads as posting of hand washing techniques in
all languages spoken by all workers.
f
Question on the survey did not distinguish between surface and well water.
M.L. Lewis Ivey et al. / Food Control 26 (2012) 453e465 459
Believe that they are practicing national GAPs all or most of the
time and that GAPs can reduce the risk of produce contami-
nation. However, their responses indicated that many do not
implement GAPs at a level of consistency needed to effectively
minimize the risk of contamination.
Do not believe that contamination is most likely to occur on the
farm.
Believe that many preventative management practices are
economically feasible.
Believe (amongst conventional producers) that contaminated
vegetables are more likely to originate from organic farms than
non-organic farms.
Do not want GAPs or other management guidelines to be
government-regulated.
Did not declare an immediate need for food safety information
and thought that the majority of their employees were
somewhator very knowledgeableabout food safety
hazards. Nevertheless, if they were to obtain more information
Fig. 7. Percentage of Midwestern vegetable producers who strongly agreed that various management practices were important for the prevention of fresh produce contamination
or were economically feasible.
Fig. 8. Midwestern vegetable producersreported preference for food safety-related topics for which they would like to receive more information.
M.L. Lewis Ivey et al. / Food Control 26 (2012) 453e465460
on food safety, they wanted to learn more about sources of
produce contamination.
Believe that bacteria are the most important contaminants of
fresh produce.
Overwhelmingly prefer to receive their information in-person
and from university extension.
4.1. GAPs are not being implemented consistently by Midwestern
vegetable producers
Producer-proclaimed familiarity with GAPs correlated poorly
with producersusage of GAPs. Differences between knowledge
and behavior are not uncommon and research related to food safety
and other health risks indicates that there is often a discrepancy
between self-reported behavior and what is actually practiced
(Abbot, Byrd-Bredbenner, Schaffner, Bruhn, & Blalock, 2009; Patil,
Cates, & Morales, 2005; Rimal, Fletcher, McWatters, Misra, &
Deodhar, 2001). The discrepancy between knowledge and behavior
has been linked to a persons feelings, emotions, or degree of
acceptance or rejection of some concept (or an affective dimension,
Galli, 1978). It is therefore important for communicators to be
aware of the recipientsattitudes toward a subject or concept. We
posit several possible reasons for the inconsistency between
reported GAPs familiarity and implementation: 1) a lack of under-
standing of the specic practices required to be in compliance with
GAPs guidelines or a lack of clarity of the current guidelines; 2)
a belief among producers that they are unable to comply (self-
efcacy) or that following GAPs will not have an effect on the safety
of fresh produce (outcome expectancy); or 3) a conscious and
rational choice of the producer based on personal beliefs with
respect to issues related to on-farm food safety, including but not
Fig. 9. Distribution of producersreported perceptions of the type of impact a food safety contamination event would have on their farms.
Fig. 10. Outside group or organization most likely to be contacted by Midwestern
vegetable producers in response to an on-farm contamination event. Differences
among vegetable producersresponses were tested using the Mood one-way analysis
of variance by ranks test where
c
2
¼284.3, DF ¼8, and p0.001.
Fig. 11. Types of training sessions or learning programs geared toward on-farm food
safety that would encourage participation of Midwestern vegetable producers.
M.L. Lewis Ivey et al. / Food Control 26 (2012) 453e465 461
limited to the role producers believe they and others should play in
ensuring a safe food supply (fundamental attribution error).
Communicators of produce food safety information should
consider and attempt to integrate these possibilities in their
development of outreach materials. Ultimately, for a mechanism of
knowledge transfer to positively effect change, the GAPs guidelines
will need to be re-communicated in a way that encourages indi-
vidual empowerment and is sensitive to regional and geographical
differences in producer attitudes. Careful thought must also be
given to the content of the message. Wittwer, Nuckles, and Renkl
(2005) demonstrated that the negative effects of instructional
explanations could persist if the message is not adapted to accu-
rately reect the learnersknowledge. Therefore we propose that
the addition of the most current science-based information per-
taining to on-farm produce safety, the identication of reliable
metrics, providing producers with clear standards and emphasizing
the immediate production impacts and economic benets of safe
management practices, will have the potential to re-engage vege-
table producers and increase GAPs implementation. Although those
producers who thought themselves to be very familiar or some-
what familiar with GAPs have the potential to be impervious to
GAPs-related messages, nearly half of the respondents indicated no
familiarity at all with GAPs, suggesting that they may be receptive
to such messages.
4.2. Vegetable producers do not believe that contamination is most
likely occurring on the farm
Midwestern vegetable producers believed that contamination of
fresh produce most often occurred in the home and not on the farm.
This is not surprising since the majority of reported foodborne
disease outbreaks over the last decade have been associated with
food prepared or consumed in the home (Redmond & Grifth,
2003). Nonetheless, contamination can occur at any time during
growing, harvesting, packing, processing, distributing or handling
and outbreaks associated with on-farm contamination events have
been steadily increasing (Alliance for Food and Farming, 2010).
Many of the more recent outbreaks, especially those associated
with tomatoes contaminated with Salmonella, have been traced
back to the farm or packinghouses (CDC, 2007; Cummings et al.,
2001). For these reasons the successful prevention of foodborne
diseases associated with fresh produce must be a continuous chain
of prevention from the eld to the home and have the cooperation
of all participants in the chain of custody.
4.3. Vegetable producers believe that preventative food safety
management practices are economically feasible
Although Midwestern vegetable producers who responded to
this survey did not implement GAPs consistently; they indicated
that they believe most preventative management practices listed in
the survey were economically feasible. This could suggest that
economic potential outcome is not the primary driving force
for GAPs implementation, as has been found for the adoption
of sustainable agricultural practices (SAP); (DSouza, Cyphers,
& Phipps, 1993; Rodriguez, Molnar, Fazio, Sydnor, & Lowe, 2008;
Saltiel, Bauder, & Palakovich, 1994). However, the rationale
driving this conundrum is not known. Although some of the
management practices listed in the survey such as pest control and
the use of soil amendments are not new and are commonly used to
produce vegetables, many would need to be newly adopted and
may add substantial costs to producersoperations. The respon-
dents in this survey may have underestimated such costs.
4.4. Vegetable producers using conventional production practices
believe contaminated vegetables are more likely to originate from
organic farms than non-organic farms
Even though nearly 35% of the respondents using conventional
farming practices indicated that they used either manure or com-
posted manure to produce vegetables they believed organic farms
were more likely to produce contaminated vegetables than non-
organic farms. The risk of microbial contamination on organic
farms has been hotly debated both in the United States and United
Kingdom over the last decade. Proponents of organic farming
believe that organically produced foods are inherentlysafe (Powell,
Jacob, & Chapman, 2010; Soil Association, 2001), while critics assert
that organically produced foods are at higher risk of contamination
because of the use of animal manure (Avery, 1998; Stephenson,
1997). Although the microbial quality of organically grown
produce has been evaluated (Arthur, Jones, Fabri, & Odumeru,
2007; Bohaychuk et al., 2009; Oliveira et al., 2010), these studies
provide no evidence that organic production practices are linked to
higher microbial food safety risks than those practices used in
conventional production systems. This is not surprising since there
are numerous obstacles associated with conducting such studies,
especially at the pre-harvest level of production. For example,
because contamination rates are very low, large samples sizes are
needed in order to have adequate statistical power. In addition,
deliberate release of genetically modied (marked strains, for
example) or non-modied human pathogens in a eld setting such
as needed for pre-harvest studies is problematic. A better under-
standing of the risks, if any, associated with organic production
practices and a more practical means to identify these risks is
needed before adequate information translation can occur.
However, even with sound, reproducible scientic evidence it can
be very difcult to change individualsbeliefs and behavior with
regard to sustainable agricultural practices (Francis, 2009; Prokopy,
Floress, Klotthor-Weinkauf, & Baumgart-Getz, 2008; Rodriguez
et al., 2008; Vanclay & Lawrence, 1994). Francis (2009) argues that
studies that compare organic farming practices to conventional
practices are sometimes biased toward the researcherspersonal
beliefs resulting in cloudedconclusions that will not likely
convince stakeholders to change their taut beliefsabout either
type of production system. Francis (2009) goes on to suggest that
a better research approach to such a complex issue is to focus
resources on improving the agro-ecosystems as a whole and not
focusing on comparative studies that consider just one or two
factors between the systems. Leifert, Volakakis, and Cooper (2008)
made this same point and used a Hazards Analysis Critical Control
Points (HACCP)-like system to identify six Risk Reduction Points
(referred to as Critical Control Points for HACCP) where risks from
enteric pathogens could be reduced in organic and low-input
ready-to-eat vegetable crops. They also identied approaches that
could be used to minimize the risk of pathogen transfer onto these
crops. In a study by Franz, Semenov, and van Bruggen (2008),
probabilistic modeling was used to estimate the probability of
lettuce contamination with E.coli O157:H7 from manure-amended
soil and the effect of intervention strategies was determined.
Interestingly, a model developed by Franz et al. (2008) demon-
strated that traditionally produced organic manure (30-day storage
and applied at least 60 days prior to planting) was more risk-
reducing than manure produced using intensive conventional
practices. Regardless of the production method, all foods in the
United States, including fresh produce are covered under U.S. food
safety laws and must meet the minimal requirements of the United
States Food and Drug Administration (US-FDA). Until additional
science-based information is available on the added risks, if any, in
using organic management practices to produce vegetables the
M.L. Lewis Ivey et al. / Food Control 26 (2012) 453e465462
best approach may be to explain to conventional vegetable
producers how sustainable agriculture practices, such as those used
in organic farming, can and must be compatible with US-FDA food
safety guidelines.
4.5. Vegetable producers do not want GAPs or other management
guidelines to be government regulated
Public reaction to recent foodborne related outbreaks on fresh
produce has motivated the United States federal government to
increase its efforts to enhance food safety. In the past, the FDA has
issued non-mandatory food safety guidelines designed to prevent
microbial contamination. However there is increasing pressure
from consumers, buyers and retailers for the enactment of
mandatory state and federal regulations. While Midwestern vege-
table producers agreed that government agencies inuence their
management decisions regarding food safety hazards, they strongly
disagreed that management practices should be regulated.
Producersreasons for not wanting government-issued regulations
were not investigated in this study. Nonetheless, the process of
bringing federally mandated regulations for produce food safety
into law has already begun (see Food Safety Modernization Act,
Ofce of Information and Regulatory Affairs, Executive Ofce of the
President; www.reginfo.gov/public/). Palma, Ribera, Paggi, and
Knutson (2010) explored how government, producers, and others
in the private and public sectors could work together to share the
responsibility of assuring a safe food supply. While they provided
reasonable options, the analysis lacked a nuanced understanding of
farmersreluctance to mandated government regulations. Ascer-
taining Midwestern vegetable producersperceived burdens or
benets of mandatory food safety regulations, especially those
related to enforcement procedures and cost sharing, could provide
valuable insight into how to best work with producers to positively
inuence their adoption of unavoidable food safety regulations.
4.6. Vegetable producers want more information on the sources of
contamination
Academic and government researchers have not yet conrmed
the major sources of pre-harvest contamination nor have the
mechanisms of survival and persistence of human pathogens on
produce been deciphered. However, progress is being made in both
areas (Beuchat, 2006; Ng, Fleet, & Heard, 2005; Tyler & Triplett,
2008; Wachtel, Whitehand, & Mandrell, 2002). Identifying high-
risk sources of contamination will be essential to developing
effective preventative management strategies. National GAPs
guidelines focus on management practices pertaining to the Four
Wsewater, waste, worker health and hygiene and wildlife. For
each, guiding principles for crop production have been developed
based on the highest perceived risk factor in each category. In
addition to the Four Ws, vegetable producers indicated that pre-
harvest pests, specically plant pathogens and insects, were likely
sources of produce contamination.
Despite the fact that seed and transplants have long been known
sources of phytopathogens (Baker & Smith, 1966), most respon-
dents did not believe that they were potential sources of human
pathogen contamination. The role of plant pathogens (Aruscavage,
Lee, Phelan, & LeJeune, 2010; Aruscavage, Miller, Lewis Ivey, Lee, &
LeJeune, 2008; Barak & Liang, 2008; Brandl, 2008; Warriner &
Namvar, 2010) and insects (Sela, Nestel, Pinto, Nemny-Lavy, &
Bar-Joseph, 2005) as contaminants of fresh produce is currently
being investigated and there is great potential for this new
knowledge to be leveraged and added to the current GAP
guidelines.
4.7. Vegetable producers believe that bacteria are the most
important contaminants of fresh produce
Although viruses account for approximately 20 million cases of
foodborne illnesses in the United States (Scallan et al., 2011), more
than any other pathogenic group, the majority of vegetable
producers believed that the bacteria E. coli (pathogenic or generic,
non-pathogenic) and Salmonella spp. were the most important
pathogens of fresh produce. The origin of this belief was not
explored in this survey but could be explained by the mass media
campaigns ensuing recent foodborne disease outbreaks. While
recurrent and deadly multistate outbreaks caused by E. coli
O157:H7 and Salmonella continue to make national and interna-
tional news headlines, those caused by viruses such as Norovirus
(Norwalk-like virus) often do not. Since the public makes judg-
ments on an event based on how easily they can recall past
occurrences (Tversky & Kahneman, 1983), how memorable the
event or the likelihood of a fatal impact or catastrophe (Slovic,
1993; Slovic, Fischhoff, & Lichtenstein, 1981; Slovic, Finucane,
Peters, & MacGregor, 2004), it is reasonable that bacterial patho-
gens are in the forefront of producers minds. This belief may alsobe
explained by the fact that viruses, such as Calicivirus (Norwalk-like
virus) produce milder symptoms than other gastroenteric viruses
or bacteria, resulting in fewer hospital visits, less reporting to the
CDC and less media attention (Mead et al., 1999).
Most producers also believed that coliforms were important
pathogens of fresh produce. Communications by experts should
better explain that these bacteria are not considered to be human
pathogens, generally do not present a health risk to consumers, and
when detected in water or on fresh produce, only indicate
a possible presence of harmful, disease-causing bacteria.
4.8. Vegetable producers prefer to receive their information in-
person and from university extension
Recognizing individual perceptions and beliefs is key to
successful message development (Lundgren, 1994). To effectively
disseminate information that target audiences self-report as being
most needed, audience-appropriate channels and trusted sources
(Morgan et al., 2002) for dissemination must be identied.
However, the number of choices available for information transfer
is extensive and leveraging the best and most preferred way to
reach desired audiences is a difcult challenge. Consumer prefer-
ence for mass media and internet tools has been documented in
recent studies (FDA, 2000; Cody & Hogue, 2003; Freimuth,
Linnman, & Potter, 2000; International Food Information Council
Foundation, 2010; Redmond & Grifth, 2006). However, Midwest-
ern vegetable producers overwhelmingly preferred personal
channels to receive information about food safety. Similar to other
farmer-targeted surveys throughout the United States (Ngathou,
Bukenya, & Chembezi, 2006; Riessenberg & Obel Gor, 1989;
Schnitkey, Batte, Jones, & Botomogno, 1992; Suvedi, Lapinski, &
Campo, 2000), our survey indicated that electronic modes of
communication were the least preferred. Given the decreased
funding of US Cooperative Extension Services (CES), emphasis has
been placed on electronic means of information transfer. While
there are obvious benets to electronic approaches, a substantial
portion of the target audience may be overlooked or unreached. For
example, the Amish, who are believed to be the fastest growing
population in the world (Ericksen, Ericksen, Hostetler, &
Huntington, 1979) and have an estimated population size of
249 500 in the United States (of which 48.7% are located in OH, MI,
KY and IN) (Young Center for Anabaptist and Pietist Studies, 2010)
voluntarily forego use of technologies such as television, radios and
personal computers (Kraybill & Nolt, 2004) and hence do not access
M.L. Lewis Ivey et al. / Food Control 26 (2012) 453e465 463
their information using on-line resources. In addition, ethnic
minority farmers (i.e. Blacks or African Americans, American
Indians and Asians) have less access to the Internet, especially high-
speed Internet, than non-minority farmers (USDA-NASS, 2007).
Overall, vegetable producers in the Midwest prefer to receive
food safety-related information from university extension. In other
studies conducted in OH, Oregon (OR), and FL, agricultural
producers and other clients also indicated a high level of satisfac-
tion with university extension (Meadowbrook & Fletcher, 1988;
Schnitkey et al., 1992; Warnock, 1992). In contrast, in an Internet-
based survey (International Food Information Council Foundation,
2010), consumers cited government agency/ofcials and health
professionals as their most trusted sources for food safety infor-
mation and CES as their least trusted source. However, consumers
are less likely than farmers to be aware of CES (Warner,
Christenson, Dillman, & Salant, 1996). The identication of CES as
a preferred source of information by Midwestern vegetable
producers should not be generalized to all vegetable producers nor
should it be considered as an either/orchoice. Producer prefer-
ences can be regionally biased and depend on other factors such as
accessibility to CES specialists and producer usage of CES (Lavis &
Blackburn, 1990). For example, vegetable CES Specialists in the
western United States have reported that for day-to-day concerns
growers mostly consult industry sources for their food safety
information but these sources typically obtain information from
university researchers or CES (S. Koike, personal communication).
In society the need for communication is heterogeneous (Renn,
2006), requires differentiation according to target groups (Yosie &
Herbst, 1998) and must therefore be accurately dened for each
group. It is critical that food safety educators in both the private and
public sectors recognize that there are clear differences between
consumers and producers with regard to how they prefer to receive
risk communications as they seek to develop the most effective
means of communication given current funding constraints.
5. Study limitations
As in similar survey-based research, the main limitations of
these types of studies pertain to survey data. These include,
coverage errors, non-response and measurement errors and
selection bias. The response rate in this study was low (26.4%) with
a high margin of error (6.6%). There was an unequal response rate
from each state with only 7.1% of KY producers responding to the
survey.
6. Conclusions
The dominant beliefs, perceptions and food safety practices of
vegetable producers in the Midwest were identied using a survey-
based conrmatory assessment. Having a better understanding of
the beliefs and management practices of vegetable producers, as
they pertain to produce safety, will allow us to develop risk
management and communication materials that specically target
the knowledge needs and wants of our stakeholders. Through the
development of highly targeted informational materials we hope to
provide vegetable producers accurate information on pre-harvest
vegetable food safety hazards so that they can make science-
based management decisions that will allow them to produce
fresh vegetables that are safe, sound and secure.
Acknowledgments
This work was supported by the National Integrated Food Safety
Initiative (NIFSI)-United States Department of Agriculture (Grant
No. 2007-51110-03817). We thank Pamela Schlegel for her
administrative expertise and liaisons with The Ohio State Univer-
sity Ofce of Responsible Research Practices. We thank Drs. Pierce
Paul and Laurence Madden for their invaluable suggestions on data
analyses. We also thank Drs. Sanja Ilic and Sunjeong Park for critical
reviews of this manuscript.
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... In order to better address this issue at the farm end of the chain of custody, we contend that both public policy and educational programming needs to be informed by grower perceptions and beliefs regarding food safety. In addition, this expert model was used as the analytical framework for subsequent companion studies (Ivey, LeJeune, & Miller, 2010;Parker, Wilson, LeJeune, & Doohan, in press) with fresh fruit and vegetable growers in Indiana, Kentucky, Michigan, and Ohio to describe and visualize how grower concepts map onto the framework an identify specific opportunities for future grower collaboration. ...
... In one study, farm scale and marketing relationships were explored in addition to grower preferences for information sources and channels, needs, and learning preferences (Parker et al., in press). In another companion study, researchers quantitatively evaluated this model in connection to produce grower perceptions and beliefs (Ivey et al., 2010). The information from these companion studies has supported the development of a tiered approach to food safety based on marketing practices, which was used in the development of an emerging three-tiered program called the Ohio Produce Marketing Agreement (http://opma.us). ...
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