Received: 27 February 2020 | Revised: 18 April 2020 | Accepted: 24 April 2020

DOI: 10.1111/tbed.13606

REVIEW

The risk of viral transmission in feed: What do we know, what

do we do?

Scott A. Dee1 | Megan C. Niederwerder2 | Gil Patterson3 | Roger Cochrane1 |

Cassie Jones4 | Diego Diel5 | Egan Brockhoff6 | Eric Nelson7 | Gordon Spronk1 |
Paul Sundberg8

1
Pipestone Applied Research, Pipestone
Veterinary Services, Pipestone, MN, USA Abstract
2
Department of Diagnostic Medicine/ The role of animal feed as a vehicle for the transport and transmission of viral diseases
Pathobiology, College of Veterinary
was first identified in 2014 during the porcine epidemic diarrhoea virus epidemic in
Medicine, Kansas State University,
Manhattan, KS, USA North America. Since the identification of this novel risk factor, scientists have con-
3
Center for Animal Health in Appalachia, ducted numerous studies to understand its relevance. Over the past few years, the
Lincoln Memorial University, Harrogate,
TN, USA
body of scientific evidence supporting the reality of this risk has grown substantially.
4
Department of Animal Science and In addition, numerous papers describing actions and interventions designed to miti-
Industry, Kansas State University, gate this risk have been published. Therefore, the purpose of this paper is to review
Manhattan, KS, USA
5 the literature on the risk of feed (what do we know) and the protocols developed to
Department of Population Medicine and
Diagnostic Sciences, College of Veterinary reduce this risk (what do we do) in an effort to develop a comprehensive document to
Medicine, Cornell University, Ithaca, NY,
raise awareness, facilitate learning, improve the accuracy of risk assessments and to
USA
6
Prairie Swine Health Services, Red Deer, identify knowledge gaps for future studies.
AB, Canada
7
Department of Veterinary Science, South KEYWORDS
Dakota State University, Brookings, SD, USA African swine fever, animal feed, China, feed mitigation, swine viral diseases, transboundary
8
Swine Health Information Center, Ames,
IA, USA

Correspondence
Scott A. Dee, Pipestone Applied Research,
Pipestone Veterinary Services, 1300 Box
188, Hwy 75 South, Pipestone, MN 56164.
Email: [email protected]

1 | PA RT 1: W H AT D O W E K N OW ? in-shower out, transport sanitation, quarantine and testing of in-

coming genetics and the filtration of incoming air are commonplace
1.1 | Introduction throughout the US swine industry, particularly at the level of the
sow farm (Silva, Corbellini, Linhares, Baker, & Holtkamp, 2018). In
Effective biosecurity protocols are essential towards protecting the contrast, prior to the May 2013 entry of porcine epidemic diarrhoea
health status of swine farms. In the United States, tremendous re- virus (PEDV) into the US swine population (Chen et al., 2014) the
sources have been invested to reduce the risk of viral pathogens, role of swine feed as a vehicle for pathogen transport and transmis-
such as the entry of porcine reproductive and respiratory syndrome sion had not been considered, despite the fact that feed is delivered
virus into susceptible populations. Protocols including shower to swine farms on a daily basis in the absence of any biosecurity

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,
provided the original work is properly cited.
© 2020 The Authors. Transboundary and Emerging Diseases published by Blackwell Verlag GmbH

Transbound Emerg Dis. 2020;67:2365–2371.  wileyonlinelibrary.com/journal/tbed | 2365

 18651682, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/tbed.13606 by National Institutes Of Health Malaysia, Wiley Online Library on [27/05/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
2366 | DEE et al.

protocols. Since the identification of this novel risk factor, scientists discharged into bags using pilot-scale feed manufacturing equip-
across North America have conducted numerous studies to under- ment. Subsequent collection of environmental swabs demonstrated
stand its relevance. Therefore, the purpose of this paper is to review widespread distribution of virus via feed dust, with the presence
the literature on the risk of feed (what do we know?) and the proto- of PEDV ribonucleic acid (RNA) in 100% of dust samples collected
cols that have been developed to reduce this risk (what do we do?), in from animal food-contact surfaces and in 89% of dust samples from
an effort to develop a comprehensive document to raise awareness, non-animal food-contact surfaces. Once contamination of the feed
facilitate learning and identify knowledge gaps for future studies. mill environment was demonstrated, the question of whether viral
survival would differ across the various feed ingredients found in a
milling environment was investigated (Dee et al., 2015). A subset of
1.2 | PEDV changes the paradigm feed ingredients used in swine rations were inoculated with PEDV
and stored outdoors during the month of January in Minnesota.
Upon its entry to the United States, PEDV spread rapidly throughout Interestingly, viable PEDV was detected by virus isolation or swine
the country at an unprecedented rate (Niederwerder & Hesse, 2018). bioassay out to 180 days post-inoculation (DPI) in conventional (high
Following phylogenetic analysis, it was determined that the virus protein/low fat) soybean meal, as well as out to 30 DPI in DDGS,
most likely originated from China (Huang et al., 2013). During the meat and bone meal, RBCs, lysine HCL, D/L methionine, choice
initial outbreak, the American Association of Swine Veterinarians, white grease, choline chloride, and out to 7 DPI in limestone and 14
the National Pork Producers Council and the USDA Center for DPI in threonine. In contrast, viable PEDV was not present in several
Epidemiology and Animal Health conducted an epidemiological in- other ingredients, including corn, various animal protein sources and
vestigation involving porcine epidemic diarrhoea (PED) affected vitamin/trace mineral mixes (Dee et al., 2015).
case and control herds. Of the more than 100 variables surveyed These data, along with observations from the field, posed the
during the investigation, seven were significantly associated with question of whether certain ingredients could serve as vehicles for
acquiring PEDV during the process of feeding animals, including the movement of PEDV between countries. This issue was raised in
using sow feed that was custom mixed off-farm in the last 90 days January 2014, when PEDV was detected for the first time in Ontario,
prior to the questionnaire, how many meal/mash rations were fed Canada (Pasma, Furness, Alves, & Aubry, 2016). Following extensive
to nursery or finishers in the last 90 days, the total number of dif- epidemiologic investigation, the source of the virus appeared to be
ferent rations fed to finisher pigs in the last 90 days, the contents in contaminated samples of spray-dried plasma protein originating
terms of supplementation that was in the premix for the most recent from the United States (Perri, Poljak, Dewey, Harding, & O'Sullivan,
finisher diet and what type of grain mix was used for sow or fin- 2018, 2019). However, while infectious PEDV was demonstrated in
isher feed in the past 90 days (AASV, NPPC & USDA CEAH, 2015). samples of case-specific plasma by swine bioassay, transmission of
In 2014, the risk was confirmed when ingestion of contaminated the virus to pigs following consumption of feed containing PEDV-
complete feed was proven to be a vehicle for PEDV transmission to positive plasma was not successful (Pascik et al., 2014).
naïve pigs (Dee, Clement, et al., 2014). This study involved the detec- Building on the potential for transboundary movement of PEDV, a
tion of viral nucleic acid in feed dust samples from the interior walls Trans-Pacific model, simulating the movement of cargo from Beijing,
of feed bins that had provided feed for the index cases of PED in China, to the Anquing terminal in Shanghai, China to the port of San
sows across a subset of farms, followed by a demonstration of virus Francisco, CA, US, and then to Des Moines, IA, US, was developed
viability in a pig bioassay model through natural feeding behaviour (Dee et al., 2016). The model utilized transport times, environmental
(Dee, Clement, et al., 2014). Within 3–4 days after consumption, evi- conditions and feed ingredients representative of cargo transport
dence of PEDV infection was noted, including clinical signs of PED from China to the United States that were purposefully inoculated
(vomiting and diarrhoea), detection of PEDV RNA in rectal swabs with virus. Under the conditions of this study, PEDV survived the
and PED-consistent lesions in the gastrointestinal tract. This publi- trans-oceanic simulation in soy-based products, lysine, choline and
cation resulted in a series of laboratory experiments to validate the vitamin D (Scott et al., 2016). Surprisingly, the virus did not survive in
results and expand upon the concept of feed and feed ingredients the absence of a feed matrix, suggesting that survival is dependent
as risk factors for viral transport and transmission. It must be noted upon the presence of the ingredient, not the container (tote) per se.
that while the original study (Dee, Clement, et al., 2014) used natu-
rally contaminated feed, the majority of these follow up experiments
involved purposeful inoculation (spiking) of ingredients. 1.3 | Expanding the viral portfolio
Following the proof of concept study, the minimum infectious
dose of PEDV in feed was determined to be 5.6 × 101 TCID50/g using Based on these collective data involving PEDV, the transboundary ex-
the 10-day-old piglet bioassay (Schumacher et al., 2016). In addition, periment was repeated across 11 other viruses, including Senecavirus
the potential for widespread PEDV contamination of surfaces in A (SVA), a surrogate for foot-and-mouth disease virus (FMDV), bo-
an animal food manufacturing facility was evaluated (Schumacher vine viral diarrhoea Virus (BVDV), a surrogate for classical swine
et al., 2017). In this study, a U.S. virulent PEDV isolate was used to fever virus (CSFV), African swine fever virus (ASFV), influenza A virus
inoculate 50 kg of swine feed, which was then mixed, conveyed and of swine (IAV-S), bovine herpesvirus type 1 (BHV-1), a surrogate for
 18651682, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/tbed.13606 by National Institutes Of Health Malaysia, Wiley Online Library on [27/05/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
DEE et al. | 2367

pseudorabies virus (PRV), canine distemper virus (CDV), a surrogate ASFV half-life in feed ingredients. Original estimates based on limited
for Nipah virus (NiV), porcine reproductive and respiratory syndrome (n = 2) data points derived from the trans-Atlantic model indicated that
virus (PRRSV), porcine sapelovirus, (PSV) a surrogate for swine ve- half-life ranged from 4.1 to 5.1 days across all nine of the virus-positive
sicular disease virus (SVDV), vesicular stomatitis virus (VSV), porcine ingredients (Dee et al., 2019). In subsequent work, Niederwerder and
circovirus type 2 (PCV2), and feline calicivirus (FCV), a surrogate for others again used the Trans-Atlantic model to conduct a more compre-
vesicular exanthema of swine virus (VESV) (Dee et al., 2018). hensive half-life evaluation, incorporating data from all four sampling
Under the conditions of this study, SVA (representing FMDV), points in the model and increasing the number of replicates. This work
FCV (representing VESV), BHV-1 (representing PRV), PRRSV, PSV resulted in half-life values that ranged from 9.6 to 14.2 days across all
(representing SVDV), ASFV and PCV2 maintained infectivity as de- nine supportive ingredients following purposeful inoculation (Stoian
termined by virus isolation or swine bioassay, while BVDV (repre- et al., 2019), suggesting that ASFV survival could occur far beyond the
senting CSFV), VSV, CDV (representing Nipah Virus) and IAV-S did 30-day transport period used in the model.
not. Since ASFV had not been reported in China at the time of the In conclusion, there appears to be a growing body of experimental
study and was actively circulating in Eastern Europe, a Trans-Atlantic evidence that specific viruses in combination with the proper ingredi-
model was developed involving representative feed ingredients, ent can survive long-distance transport under simulated transboundary
transport times and environmental conditions simulating shipment conditions. This evidence corroborates field observations, suggesting
from Warsaw, Poland, to the port of Le Havre, France, to the port that the spread of PEDV had occurred in novel ways, despite the fact
of New York City, NY, US, and then to Des Moines, IA, US (Dee that multiple interventions were already in place. This may also be the
et al., 2018). As before, following purposeful inoculation of ingredi- case for ASFV, although at this time we have no evidence of this is
ents, the majority of viruses survived in conventional soybean meal, North America. It is now clear that under experimental conditions,
lysine hydrochloride, choline chloride, vitamin D and pork sausage pathogens such as PEDV and ASFV can be transmitted through feed,
casings. These collective results led to the development of the con- and the minimum oral infectious doses have been calculated. Finally, in
cept of ‘high-risk combination’ (i.e. specific ingredients promote the further support of feed as a risk factor, a recent publication by Stoian
stability of certain viruses) and contributed to the growing body of and others documented that following purposeful inoculation of the
evidence that contaminated feed ingredients may represent a risk actual viruses, PRV and CSFV survived throughout the Trans-Pacific
for the transport of pathogens at domestic and global levels. model in feed ingredients (Stoian et al., 2020). Surprisingly, viable PRV
These findings became significant following the announcement was recovered from 9 ingredients (conventional soybean meal, organic
of the initial cases of ASFV in China's pig population during August soybean meal, lysine, choline, vitamin D, moist and dry pet food, and
2018 for several reasons: pork sausage casings) while in contrast, viable CSFV was only recov-
ered from conventional soybean meal and pork sausage casings.
1. Fifty per cent of the world's pigs were in China at the time.
2. The Chinese national herd was naïve to ASFV.
3. Purposeful inoculation of ASFV in 12 feed ingredients resulted 2 | PA RT 2 : W H AT D O W E D O?
in the survival of the virus in nine of the ingredients, including
three varieties of soy-based products, choline chloride, three Since the discovery of PEDV in the United States and the role that
types of pet food, pork sausage casings and complete feed (Dee feed may have played in the epidemiology of the disease, there has
et al., 2018). been extensive effort put forth to evaluate the efficacy of multi-
4. The United States imported approximately 2 M metric tons of ple protocols and products to reduce risk. Reviewing the literature,
agricultural products, including 55,000 metric tons of soy-based current publications have centred on one of four approaches: me-
products from China, along with 45,000 metric tons and 3,000 chanical reduction (flushing and sequencing of feed batches), heat
metric tons of soy-based products from the Ukraine and Russia, treatment, chemical mitigation and/or storage time of feed. As a
respectively, in 2018. complement to this work, a validated sampling method has been
developed (Jones, Stewart, Woodworth, Dritz, & Paulk, 2019). This
The ASFV outbreak in China accelerated the research efforts to publication indicated that the sampling of bulk ingredients for PEDV
better understand the risk of feed, specifically as it pertained to ASFV. should include compositing of least 10 individual samples and that
This resulted in the work of Niederwerder and others who docu- the ability to detect is dependent upon dose and loss of viral load
mented transmission of ASFV to naïve pigs following natural consump- (~10 Ct) during the extraction methods involving feed.
tion of purposefully contaminated feed and liquid (Niederwerder et al.,
2019). This study determined the minimum infectious dose of ASFV in
liquid (100 TCID50) and in feed (104 TCID50) following a one-time expo- 2.1 | Strategy 1: Mechanical reduction (flushing and
sure. However, further analysis indicated that the more frequent the sequencing)
exposure (3×, 10×, 30×) to ASFV in small volumes of feed or liquid, the
higher the probability of infection, even in the presence of lower doses Several experiments have been conducted to assess the efficacy
such as 102 TCID50. Another significant finding was the calculation of of decontaminating feed and feed manufacturing facilities through
 18651682, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/tbed.13606 by National Institutes Of Health Malaysia, Wiley Online Library on [27/05/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
2368 | DEE et al.

the physical process of mixing, using repeated sequencing of clean of feed contaminated with PEDV (Cochrane et al., 2019). Results in-
feed following known contaminated batches or through the use of dicated that feed treated with individual MCFA, 1% MCFA blend or
chemically treated rice hulls (Gebhardt et al., 2018; Schumacher formaldehyde had less detectable viral RNA than other treatments,
et al., 2018) In regards to sequencing, results demonstrated that such as canola oil, coconut oil, palm kernel oil and choice white
sequenced batches of feed had reduced quantities of PEDV RNA, grease. In addition, PEDV-contaminated feed treated with formal-
although sequenced feed without detectible PEDV RNA was still dehyde, 1% MCFA, 0.66% caproic, 0.66% caprylic and 0.66% capric
infectious (Schumacher et al., 2018). Therefore, this protocol can re- significantly reduced infectivity, in contrast to feed treated with C12
duce but not eliminate the risk of producing infectious PEDV carryo- or longer chain fatty acid sources.
ver from the first batch of feed. In regards to the use of chemically In regards to the elimination of PEDV from a contaminated animal
treated rice hulls, flushes treated with formaldehyde or medium- feed manufacturing facility, the combined application of a quaternary
chain fatty acid (MCFA) blends reduced the quantity of detectible ammonium-glutaraldehyde blend cleaner, followed by a sodium hypo-
RNA present after mixing a batch of PEDV-positive feed (Gebhardt chlorite sanitizing solution, along with a facility heat-up to 60°C for 48 hr
et al., 2018). was effective at reducing PEDV genomic material, but did not com-
pletely eliminate it, demonstrating the residual risk of this virus at the
feed mill level following purposeful contamination (Huss et al., 2017).
2.2 | Strategy 2: Heat treatment

Several studies have demonstrated a positive effect of temperature 2.4 | Strategy 4: Responsible Imports
on the inactivation of PEDV in feed (Cochrane et al., 2017; Gerber
et al., 2014; Trudeau et al., 2016; Trudeau, Verma, Sampedro, et al., With the generation of new knowledge on viral half-life in feed, the
2017; Trudeau, Verma, Urriola, et al., 2017). Early work on the ef- application of a ‘Responsible Imports’ approach has been adapted
fect of heat treatment by Trudeau et al indicated that heating swine across the US industry (Patterson, Niederwerder, & Dee, 2019).
feed at temperatures over 130°C effectively reduced PEDV sur- Responsible Imports, a science-based protocol to safely introduce
vival (Trudeau et al., 2016; Trudeau, Verma, Sampedro, et al., 2017; essential feed ingredients from high-risk countries using extended
Trudeau, Verma, Urriola, et al., 2017). Furthermore, the spray drying periods of storage, is based on the following principles:
process also was effective in inactivating infectious PEDV in plasma
protein (Gerber et al., 2014). Finally, in regards to pelleting, condition- Necessity: is importation of the ingredient an absolute necessity?
ing and pelleting temperatures above 54.4°C were effective in re- Alternatives: can the ingredient be obtained from a country free
ducing the quantity and infectivity of PEDV in swine feed (Cochrane from foreign animal diseases?
et al., 2017). In contrast, viable virus was present following exposure Virus: which virus is causing the concern?
to lower (37.8°C and 46.1°C) conditioning temperatures. Viral half-life: is there published information on the half-life of
the virus in the designated ingredient?
Transport time: what is the projected time for delivery of the
2.3 | Strategy 3: Chemical mitigation ingredient from the source to its destination?
Mitigation: are there safe products that can be added to the in-
Extensive studies have been conducted to evaluate the effect gredient to reduce viral load during transport?
of chemical mitigation on PEDV-contaminated feed (Cochrane Storage period: is there published information on storage time
et al., 2019; Dee, Neill, Clement, Christopher-Hennings, & Nelson, and temperature that will eliminate residual virus from the ingre-
2014; Huss et al., 2017; Trudeau et al., 2016). The initial work re- dient prior to use?
volved around Sal CURB® (Kemin Industries), an FDA-approved Therefore, as production companies across the United States de-
liquid anti-microbial used to control Salmonella contamination in velop storage facilities for incoming products, a new way of thinking
poultry and swine diets. In groups of pigs fed Sal CURB®-treated is taking shape, one that is based on ‘feed quarantine’ that brings to-
feed spiked with PEDV versus non-treated feed, clinical signs of gether information across several disciplines including feed science,
PEDV infection (vomiting and diarrhoea) and viral shedding in fae- microbiology and oceanic transport logistics to understand how to
ces were observed 2–3 days post-consumption of non-treated feed. minimize risk. This approach is intriguing as it is non-regulatory in
In contrast, no evidence of infection was observed in pigs fed Sal nature and does not negatively impact trade.
CURB®-treated feed (Dee, Neill, et al., 2014). In another study, feed
samples were spiked with PEDV and mixed with either organic acid
mixtures, sugar or salt and were incubated at room temperature for 3 | CO N C LU S I O N S A N D N E X T S TE P S
up to 21 days. All additives tested were effective in reducing the
survival of PEDV as compared to non-treated controls (Trudeau In summary, there is a growing body of scientific evidence suggest-
et al., 2016). Recent work by Cochrane and others compared the ef- ing that contaminated feed and feed ingredients purposefully inocu-
ficacy of MCFA to other common fat sources to minimize infectivity lated with viruses may be risk factors for the spread of viral diseases
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DEE et al. | 2369

at the domestic and the transboundary levels. This information has (Proceedings, 1st International Symposium of prevention of ASF,
stimulated collaborative efforts across North America between live- Henan, China, 2019). To compound this problem, a universally val-
stock and grain commodity groups, governmental agencies, and the idated method to test feed is not available and routine surveillance
veterinary profession in an effort to manage this risk. For example, testing of feed and feed ingredients is not permitted in the United
the Canadian Food Inspection Agency has already implemented a States. Furthermore, there are no feed additives that are currently
national program using designated secondary control zones to man- approved by the US Food and Drug Administration to mitigate the
age the introduction of high-risk feed ingredients, such as grains, risk of viral-contaminated feed. Fortunately, research is ongoing to
oilseeds and meals from 44 ASFV-positive countries into Canada. identify additional mitigant candidates and conversations are under-
Activity in the United States includes the passage of resolutions way between feed companies and government officials regarding
from the National Pork Producers Council requesting collaborative the approval process.
efforts across North America to reduce the risk of foreign animal In closing, in a few short years, global agriculture has come a long
disease entry via the risk of feed ingredients, widespread use of feed way in recognizing and accepting the risk of feed and feed ingredi-
additives as chemical mitigants and the writing of policy to guide ents as vehicles for the domestic and transboundary spread of dis-
the implementation of the Responsible Imports approach. A US eases, based on the research efforts cited in this writing. It is hoped
feed safety task force involving representatives from governmental that these efforts will continue to stimulate communication and
agencies and multi-species stakeholder groups has been formed to collaboration between the feed and livestock industries, resulting
develop a national plan to manage this risk. Finally, requests to re- in further research into the emerging concept of ‘global feed biose-
strict the importation of high-risk feed ingredients such as soy-based curity’. Ideally, current and future information regarding the risk of
products from ASFV-positive countries are being made to key gov- pathogen spread in feed will enhance the accuracy of risk assess-
ernment officials. Collectively, representatives from Mexico, Canada ments, drive the continual development of efficacious feed-based
and the United States have begun the discussion of how to collabo- mitigation strategies and ultimately change the philosophy regarding
rate to reduce the risk of the introduction of ASFV and other foreign the global trade of feed ingredients from one that based on price
animal disease pathogens to North America, with focused discussion to one where the biosecurity of the feed supply chain is prioritized.
on all risk factors, including feed.
However, despite all the scientific evidence, there are still differ- AC K N OW L E D G E M E N T S
ences in opinion as it pertains to the risk of feed. While a recent re- Dr. Dee would like to recognize and thank Mr. Robert Dykhuis
view concluded that the current body of scientific knowledge lacks of the Michigan Pork Producers Association for his timely words
conclusive evidence of virus contamination of imported non-an- of encouragement and motivational comments while the studies
imal origin feed ingredients of commercial swine feed (Gordon evaluating the risk of viral transport and transmission in feed were
et al., 2019), another review concluded that there is a moderate risk under development. Dr. Dee would also like to acknowledge Dr.
for the introduction of ASFV and PEDV to the United States through Tom Burkgren of the American Association of Swine Veterinarians
contaminated feed (Jones, Woodworth, Dritz, & Paulk, 2019). Some for never losing faith in the risk of feed, despite the significant ex-
reason for this discrepancy is that the latter publication took into ternal pressures.
account all existing published studies on the transmission of ASFV
in feed (Niederwerder et al., 2019), as well as a recent report citing C O N FL I C T O F I N T E R E S T
the detection of Seneca Virus A in swine feed and feed ingredients The authors declare no conflict of interest.
in Brazil (Leme, Miyabe, Dall Agnol, Alfieri, & Alfieri, 2019), while
the former paper did not. Clearly, as the body of scientific evidence E T H I C A L A P P R OVA L
surrounding the risk of feed continues to grow, the accuracy of risk No ethical approval was required as this is a review article with no
analyses will improve. original research data.
However, despite the progress that has been made, significant
research gaps still exist regarding the risk of feed. For example, the DATA AVA I L A B I L I T Y S TAT E M E N T
vast majority of the published papers are based on experimental in- All references used to write this review were disclosed.
oculation and models. Further efforts to reproduce this work using
actual modes of transport, that is actual ocean freighters and com- ORCID
mercial transport vehicles trucks, are needed. In addition, it is argued Scott A. Dee https://orcid.org/0000-0001-8691-3887
that there is a lack of evidence documenting the presence of viral Cassie Jones https://orcid.org/0000-0002-0671-8879
pathogens in actual feed samples around the world. While the cur-
rent evidence is indeed limited, viable PEDV has been detected in REFERENCES
feed bins feeding index cases of PED on sow farms (Dee, Clement, American Association of Swine Practitioners, National Pork Producers
et al., 2014) and ASFV DNA has been detected in Chinese feed Council & USDA Center for Epidemiology and Animal Health (2015).
PEDV Investigation 2013. Retrieved from http://www.aasv.org
and feed dust from bulk grains stored on the ground post-harvest,
Chen, Q., Ganwu, L., Stasko, J., Thomas, J. T., Stensland, W. R., Pillatzki,
along with samples from feed mills, personnel and delivery vehicles A. E., … Zhang, J. (2014). Isolation and characterization of Porcine
 18651682, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/tbed.13606 by National Institutes Of Health Malaysia, Wiley Online Library on [27/05/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
2370 | DEE et al.

Epidemic Diarrhea Viruses associated with the 2013 disease outbreak porcine epidemic diarrhea virus in an animal feed manufacturing
among swine in the United States. Journal of Clinical Microbiology, 52, facility. PLoS One. 12(1), e0169612. https://doi.org/10.1371/journ​
234–243. https://doi.org/10.1128/JCM.02820 ​-13 al.pone.0169612
Chinese Pig Producers Association, Henan, China (2019). Retrieved from Jones, C. K., Stewart, S., Woodworth, J. C., Dritz, S. S., & Paulk, C. (2019).
the Proceedings of the 1st International Symposium on the Prevention Validation of sampling methods in bulk feed ingredients for detection
of ASFV. of swine viruses. Transboundary and Emerging Diseases, 67(1), 1–5.
Cochrane, R. A., Dritz, S. S., Woodworth, J. C., Stark, C. R., https://doi.org/10.1111/tbed.13326
Saensukjaroenphon, M., & Gebhardt, J. T. … Jones, C. K. T. (2019). Jones, C. K., Woodworth, J. C., Dritz, S. S., & Paulk, C. B. (2019).
Journal of Animal Science, 4(2), txz179. https://doi.org/10.1093/tas/ Reviewing the risk of feed as a vehicle for swine pathogen trans-
txz179 mission. Veterinary Medicine and Science. https://doi.org/10.1002/
Cochrane, R. A., Schumacher, L. L., Dritz, S. S., Woodworth, J. C., Huss, A. vms3.227
R., Stark, C. R., … Jones, C. K. (2017). Effect of pelleting on survival of Leme, R. A., Miyabe, F. M., Dall Agnol, A. M., Alfieri, A. F., & Alfieri, A.
porcine epidemic diarrhea virus-contaminated feed. Journal of Animal A. (2019). Seneca Valley virus RNA detection in pig feed and feed
Science, 95(3), 1170–1178. https://doi.org/10.2527/jas.2016.0961 ingredients in Brazil. Transboundary and Emerging Diseases, 66(4),
Dee, S. A., Bauermann, F. V., Niederwerder, M. C., Singrey, A., Clement, T., 1449–1453. https://doi.org/10.1111/tbed.13215
de Lima, M., … Diel, D. G. (2018). Survival of viral pathogens in animal Niederwerder, M. C., & Hesse, R. A. (2018). Swine enteric coronavirus
feed ingredients under transboundary shipping models. PLoS One, disease: A review of 4 years with porcine epidemic diarrhea virus
13(3), e0194509. https://doi.org/10.1371/journ​al.pone.0194509 and porcine deltacoronavirus in the United States and Canada.
Dee, S. A., Bauermann, F. V., Niederwerder, M. C., Singrey, A., Clement, Transboundary and Emerging Diseases, 65(3), 660–675. https://doi.
T., de Lima, M., … Diel, D. G. (2019). Correction: Survival of viral org/10.1111/tbed.12823
pathogens in animal feed ingredients under transboundary ship- Niederwerder, M. C., Stoian, A. M. M., Rowland, R. R. R., Dritz, S. S.,
ping models. PLoS One, 14, e0214529. https://doi.org/10.1371/journ​ Petrovan, V., Constance, L. A., … Hefley, T. J. (2019). Infectious
al.pone.0214529 dose of African Swine fever virus when consumed naturally in liq-
Dee, S., Clement, T., Schelkopf, A., Nerem, J., Knudsen, D., Hennings, J., uid or feed. Emerging Infectious Diseases. 25(5), 891–897. https://doi.
& Nelson, E. (2014). An evaluation of contaminated complete feed org/10.3201/eid25​05.181495
as a vehicle for porcine epidemic diarrhea virus infection of naïve Pascik, J., Berhane, Y., Ojkic, D., Maxie, G., Embury-Hyatt, C., Swekla,
pigs following consumption via natural feeding behavior: Proof of K., … Alexandersen, S. (2014). Investigation into the role of poten-
concept. BMC Veterinary Research, 10, 176. https://doi.org/10.1186/ tially contaminated feed as a source of the first-detected outbreaks
s1291​7-014-0176-9 of porcine epidemic diarrhea in Canada. Transboundary and Emerging
Dee, S., Neill, C., Clement, T., Christopher-Hennings, J., & Nelson, E. Diseases, 61, 397–410. https://doi.org/10.1111/tbed.12269
(2014). An evaluation of a liquid antimicrobial (Sal CURB®) for reduc- Pasma, T., Furness, M. C., Alves, D., & Aubry, P. (2016). Outbreak inves-
ing the risk of porcine epidemic diarrhea virus infection of naïve pigs tigation of porcine epidemic diarrhea in swine in Ontario. Canadian
during consumption of contaminated feed. BMC Veterinary Research, Veterinary Journal, 57(1), 84–89.
10, 220. https://doi.org/10.1186/s1291​7-014-0220-9 Patterson, G., Niederwerder, M. C., & Dee, S. A. (2019). Risks to animal
Dee, S., Neill, C., Clement, T., Singrey, A., Christopher-Hennings, J., & health associated with imported feed ingredients. Journal of the
Nelson, E. (2015). An evaluation of porcine epidemic diarrhea virus American Veterinary Medical Association, 254(7), 790–791. https://
survival in individual feed ingredients in the presence or absence of doi.org/10.2460/javma.254.7.790
a liquid antimicrobial. Porcine Health Management, 9(1), 9. https://doi. Perri, A. M., Poljak, Z., Dewey, C., Harding, J. C. S., & O'Sullivan, T. L.
org/10.1186/s4081​3-015-0003-0 (2018). An epidemiological investigation of the early phase of the
Dee, S., Neill, C., Singrey, A., Clement, T., Cochrane, R., Jones, C., … porcine epidemic diarrhea (PED) outbreak in Canadian swine herds
Nelson, E. (2016). Modeling the transboundary risk of feed ingre- in 2014: A case-control study. Preventive Veterinary Medicine, 1(150),
dients contaminated with porcine epidemic diarrhea virus. BMC 101–109. https://doi.org/10.1016/j.preve​tmed.2017.12.009
Veterinary Research, 12(12), 51. https://doi.org/10.1186/s1291​ Perri, A. M., Poljak, Z., Dewey, C., Harding, J. C. S., & O'Sullivan, T. L.
7-016-0674-z (2019). Network analyses using case-control data to describe and
Gebhardt, J. T., Cochrane, R. A., Woodworth, J. C., Jones, C. K., characterize the initial 2014 incursion of porcine epidemic diarrhea
Niederwerder, M. C., Muckey, M. B., … Dritz, S. S. (2018). Evaluation (PED) in Canadian swine herds. Preventative Veterinary Medicine,
of the effects of flushing feed manufacturing equipment with chem- 1(162), 18–28. https://doi.org/10.1016/j.preve​tmed.2018.11.001
ically treated rice hulls on porcine epidemic diarrhea virus cross-con- Schumacher, L. L., Cochrane, R. A., Huss, A. R., Gebhardt, J. T.,
tamination during feed manufacturing. Journal of Animal Science, Woodworth, J. C., Stark, C. R., … Dritz, S. S. (2018). Feed batch se-
96(10), 4149–4158. https://doi.org/10.1093/jas/sky295 quencing to decrease the risk of porcine epidemic diarrhea virus
Gerber, P. F., Xiao, C. T., Chen, Q., Zhang, J., Halbur, P. G., & Opriessnig, T. (PEDV) cross-contamination during feed manufacturing. Journal of
(2014). The spray-drying process is sufficient to inactivate infectious Animal Science, 96(11), 4562–4570. https://doi.org/10.1093/jas/
porcine epidemic diarrhea virus in plasma. Veterinary Microbiology, sky320
174(1–2), 86–92. https://doi.org/10.1016/j.vetmic.2014.09.008 Schumacher, L. L., Huss, A. R., Cochrane, R. A., Stark, C. R., Woodworth,
Gordon, R. K., Kotowski, I. K., Coulson, K. F., Link, D., MacKenzie, A., & J. C., Bai, J., … Jones, C. K. (2017). Characterizing the rapid spread
Bowling-Heyward, J. (2019). The role of non-animal origin feed in- of porcine epidemic diarrhea virus (PEDV) through an animal food
gredients in transmission of viral pathogens of swine: A review of manufacturing facility. PLoS One, 12(11), e0187309. https://doi.
scientific literature. Frontiers of Veterinary Science, 22(6), 273. https:// org/10.1371/journ​al.pone.0187309
doi.org/10.3389/fvets.2019.00273 Schumacher, L. L., Woodworth, J. C., Jones, C. K., Chen, Q., Zhang, J.,
Huang, Y. W., Dickerman, A., Pineyro, P., Long, L., Fang, L., Kiehne, R., Gauger, P. C., … Dritz, S. S. (2016). Evaluation of the minimum in-
… Meng, X. J. (2013). Origin, evolution and genotyping of emergent fectious dose of porcine epidemic diarrhea virus in virus-inoculated
porcine epidemic diarrhea virus strains in the United States. mBio, feed. American Journal of Veterinary Research, 77(10), 1108–1113.
4(5), e00737-13. https://doi.org/10.1128/mBio.00737​-13 https://doi.org/10.2460/ajvr.77.10.1108
Huss, A. R., Schumacher, L. L., Cochrane, R. A., Poulsen, E., Bai, Scott, A., McCluskey, B., Brown-Reid, M., Grear, D., Pitcher, P., Ramos,
J., Woodworth, J. C., … Jones, C. K. (2017). Elimination of G., … Singrey, A. (2016). Porcine epidemic diarrhea virus introduction
 18651682, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/tbed.13606 by National Institutes Of Health Malaysia, Wiley Online Library on [27/05/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
DEE et al. | 2371

into the United States: Root cause investigation. Preventative Trudeau, M. P., Verma, H., Sampedro, F., Urriola, P. E., Shurson, G. C.,
Veterinary Medicine, 1(123), 192–201. https://doi.org/10.1016/j. McKelvey, J., … Goyal, S. M. (2016). Comparison of thermal and
preve​tmed.2015.11.013 non-thermal processing of swine feed and the use of selected
Silva, G. S., Corbellini, L. G., Linhares, D. L. C., Baker, K. L., & Holtkamp, D. feed additives on inactivation of porcine epidemic diarrhea virus
J. (2018). Development and validation of a scoring system to assess (PEDV). PLoS One, 11(6), e0158128. https://doi.org/10.1371/journ​
the relative vulnerability of swine breeding herds to the introduc- al.pone.0158128
tion of PRRS virus. Preventative Veterinary Medicine, 160, 116–122. Trudeau, M. P., Verma, H., Urriola, P. E., Sampedro, F., Shurson, G. C.,
https://doi.org/10.1016/j.preve​tmed.2018.10.004 & Goyal, S. M. (2017). Survival of porcine epidemic diarrhea virus
Stoian, A. M. M., Petrovan, V., Constance, L. A., Olcha, M., Dee, S., Diel, (PEDV) in thermally treated feed ingredients and on surfaces.
D. G., … Niederwerder, M. (2020). Stability of classical swine fever Porcine Health Management, 3, 17. https://doi.org/10.1186/s4081​
virus and pseudorabies virus in animal feed ingredients exposed 3-017-0064-3
to transpacific shipping conditions. Transboundary and Emerging
Diseases., 2020(001), 1–10. https://doi.org/10.1111/tbed.13498
Stoian, A. M. M., Zimmerman, J., Ji, J., Hefley, T. J., Dee, S., Diel, D. G.,
How to cite this article: Dee SA, Niederwerder MC,
… Niederwerder, M. C. (2019). Half-life of African swine fever virus
Patterson G, et al. The risk of viral transmission in feed: What
in shipped feed. Emerging Infectious Diseases, 25(12), https://doi.
org/10.3201/eid25​12.191002 do we know, what do we do?. Transbound Emerg Dis.
Trudeau, M. P., Verma, H., Sampedro, F., Urriola, P. E., Shurson, G. C., 2020;67:2365–2371. https://doi.org/10.1111/tbed.13606
& Goyal, S. M. (2017). Environmental persistence of porcine coro-
naviruses in feed and feed ingredients. PLoS One, 12(5), e0178094.
https://doi.org/10.1371/journ​al.pone.0178094