Food Protection Trends - September/October 2022 - 365

manure or feedlot surface material particles are more buoyant
than bacteria attached to soil particles. In laboratory studies,
Oni et al. (103) found that S. enterica remained viable for
longer when attached to smaller turkey manure dust particles
(125 μm) compared with larger particles (500 μm) and to
particles with lower moisture levels (5 > 10 > 15%). They also
reported that attachment to manure dust particles enhanced
Salmonella survival after exposure to UV light, indicating
that bacteria may benefit from their association with dust by
acquiring some protection from environmental stresses such as
UV light.
Because tree crops are grown off the ground and generally
have no direct contact with the ground, orchards are naturally
well suited for studying airborne pathogen transmission. Many
orchards have switched from sprinkler to microirrigation
systems, further reducing confounding factors from irrigation
water when studying pathogen transmission to crops via dust
and aerosolized particulates. Theofel et al. (130) sampled
leaves from an almond orchard next to and downwind from a
poultry operation. Both dust and bacteria (Staphylococcaceae)
on tree leaves decreased as sampling progressed from the rows
closest to the poultry operation (0 m) to rows 60 and 120 m
into the orchard and away from the poultry operation. E. coli
was present in significantly more air samples from orchards
near the poultry operation than in samples from orchards
farther away.
Row crops are also vulnerable to bacterial contamination
associated with aerosols, dust, and droplets, but because
particulates in these crops contact or are in close proximity to
the ground, particulate distribution may differ from that in tree
fruit and nut production. In their study of bacterial communities
of romaine lettuce leaves from commercial production
operations in Arizona and California, researchers from the
University of California (UC), Davis noted that a severe dust
storm during sampling in the Yuma area significantly affected
the bacterial communities identified on the lettuce leaf samples
collected that day (110). These researchers also found that
bacteria on leaves collected immediately after the dust storm
passed differed from those collected later that same day. Based
on this observation, they speculated that bacterial communities
on crop surfaces may be transient at times. Research
conducted in Salinas Valley fields over two growing seasons
by other UC Davis scientists revealed day-to-day variations
in native bacterial communities on romaine lettuce (142),
corroborating the previous findings in Yuma.
Bacteria attached to dust may also internalize if they attach at
locations on the plant surface that allows entry into the fruit or
vegetable interior. In a study exploring the role dust may play in
specialty crop contamination, researchers exposed tomato plants
in bloom to soil particulates contaminated with Salmonella
Newport and used compressed air to simulate wind currents.
One week after exposure, 29% of the blossoms were positive for
Salmonella Newport; sterilized fruit also tested positive, indicating
pathogen internalization within the tomatoes (37).
Insects
Similar to dust and particulates, insects may play a role in
pathogen transmission pathways between animal operations
and crops, but this possibility has not been widely studied.
We know human pathogens can survive in and on insects. The
FDA has identified 21 species of " filth flies " that represent
a potential human health threat as " scientifically proven
causative agents " of foodborne illness or as carriers of E. coli,
Salmonella, Shigella, and other foodborne pathogens (101).
Filth flies that breed in animal and human feces and decaying
food and vegetation can serve as vectors for transmitting
human pathogens. Efforts to control houseflies on military
bases have resulted in significant reductions of diarrheal
diseases caused by foodborne pathogens (e.g., Shigella and
pathogenic E. coli), and an upsurge in fly density was positively
associated with increased disease incidence in Bangladeshi
children (28, 46).
Studies in produce-growing regions have also provided
evidence that insects can pose a food safety risk in areas where
animals are present. Talley et al. (129) caught 34 filth flies in
a field of leafy greens adjacent to cattle-occupied rangeland in
the Salinas Valley. Of 18 flies tested with a PCR assay for the
E. coli O157:H7 gene eae, 61% were positive for the pathogen.
Other studies of flies in proximity to domesticated animals and
other sources of foodborne pathogens (e.g., landfills, compost
operations, and dumpsters) have revealed that flies can transfer
pathogens from contamination sources to other surfaces (19,
34, 53). Wasala et al. (137) found that filth flies that acquired
E. coli O157:H7 from contaminated cattle manure deposited
the pathogen by regurgitation onto spinach, where the E. coli
survived and multiplied. Janisiewicz et al. (68) used a fluorescently
labelled nonpathogenic E. coli strain to demonstrate that
fruit flies can transmit bacteria from refuse piles of decaying
fruit to uncontaminated apple wounds, indicating that the flies
were contaminated both externally and internally. In laboratory
experiments, Talley et al. (129) used a similar labeling method
to investigate E. coli O157:H7 transfer from flies to spinach
and found the fluorescently labelled bacteria on 50 to 100% of
leaves examined with a fluorescence microscope.
But not all insects are equal in the threat they pose as vectors
for transferring human pathogens. In their 2017 study of
houseflies and blow flies, Pace et al. (104) found that blow
flies were more efficient than houseflies at transmitting E. coli
O157:H7 and S. enterica from manure to leafy greens. The
risk to produce fields from insects may also be dependent on
the presence of risk factors in the surrounding environment
in addition to the insect species. Barreiro et al. (7) tested flies
from various rural areas in Portugal and reported that flies in
proximity to animals had higher human pathogen prevalence
than those collected from kitchens. USDA researchers
measured E. coli O157:H7 carriage rates in five different types
of flies (house, face, flesh, blow, and stable flies) collected at
their 6,000-head-capacity feedlot and adjacent leafy greens
research fields in Clay Center, NE during summer 2011 and
September/October Food Protection Trends 365
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