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. 2024 Jan 19;8:txae009. doi: 10.1093/tas/txae009

Postmanufacturing techniques for mitigation of viral pathogens in porcine-derived feed ingredients: a review

Olivia L Harrison 1, Chad B Paulk 2, Jason C Woodworth 3, Jordan T Gebhardt 4, Cassandra K Jones 5,✉
PMCID: PMC10858441  PMID: 38343389

Abstract

African swine fever virus (ASFV) is a highly infectious virus known to cause substantial mortality and morbidity in pigs. The transmissibility and severity of disease within pigs, as well as the potentially resultant catastrophic trade ramifications, warrant its status as a foreign animal disease of substantial concern to the United States. The ASFV virus can survive for extended periods of time outside its host, and its greatest concentration is often observed in blood and organs, products that are frequently used as raw materials to manufacture porcine-derived ingredients fed to animals in the United States. Unlike ruminant-based proteins that cannot be fed to ruminant animals, it is permissible to feed porcine-derived ingredients to pigs in the United States. However, the increased threat of ASFV entry into the United States and our evolving understanding of viral transmission by feedstuffs warrant further investigation into this practice. The objectives of this review are to describe the current knowledge of ASFV survival in raw materials used to produce porcine-based ingredients, identify priorities for future research, and summarize potential options for managing risk until additional knowledge can be gained. While limited data is available for ASFV-specific mitigation, the temperatures used in both spray-drying and rendering have proven to effectively reduce viral concentrations of multiple swine viruses below detectable limits. However, some of these procedures may not eliminate the risk of recontamination, which necessitates the need for additional prevention or mitigation measures. Most published research in this area relies on direct inoculation of raw ingredient, not the finished porcine-derived ingredient. Currently, three published studies report ASFV mitigation in either thermally processed conditions (>40 °C) or ingredient quarantine (<40 °C). Virus inactivation, or the reduction of viral concentrations below detectable levels, was observed in the thermally processed study and one of the two ingredient quarantine studies. In conclusion, there is little knowledge to eliminate the risk of recontamination in porcine-derived ingredients; therefore, future research should aim to support and validate the currently available literature for the continued and safe production of porcine-derived ingredients in the event of a foreign animal disease outbreak.

Keywords: ASFV, porcine, proteins, rendering, spray-drying

Introduction

Porcine epidemic diarrhea virus (PEDV) was first reported in the United States in 2013 with outbreak reports swiftly following in Canada (Huang et al., 2013; Pasick et al., 2014). During the outbreak, epidemiological studies linked PEDV to spray-dried porcine plasma (SDPP), which was later found to be infectious during a swine bioassay (Pasick et al., 2014). However, the resultant feed resulted in a negative bioassay. Initially interpreted as a conclusive negative, subsequent studies have revealed the substantial risk of statistical beta error in bioassay studies (Beecher-Monas, 1998; Halperin, 2005), including its likelihood to extend past the 20% accepted by most biological experiments due to the low sample size. Later work demonstrated the potential for PEDV to be transmitted through feed and dust (Dee et al., 2014; Gebhardt et al., 2018). The original source of plasma contamination reported by Pasick et al. (2014) remains unidentified as PEDV replication and transmission is typically associated with the gastrointestinal tract and feces, not blood or plasma (Jung et al., 2020). Together, the beta error and low level of PEDV in blood relative to other raw materials may explain the variability in feed-based bioassay (Gerber et al., 2014; Opriessnig et al., 2014) and why other routes of entry may have contributed to the spread of PEDV (Russell et al., 2020). Regardless, the identification of PEDV RNA in SDPP prompted further discussion and research into the safety of porcine-based ingredients, which has continued to expand in recent years.

Research focused on virus transmission in ingredients and feed quickly expanded to include more than just PEDV (Dee et al., 2018; Niederwerder et al., 2019; Stoian et al., 2020; Blazquez et al., 2022); however, as more viruses were found to be transmissible in different feed or ingredient matrices the inherent differences between viruses must be considered. The method of viral transmission and relevant raw material must be considered when evaluating product risk and safety of mitigation methods. For example, PEDV is transmitted through a fecal-oral route, so affected animal digestive tracts used in raw materials for porcine-based ingredients likely carry greater risk than other tissues. Alternatively, African swine fever virus (ASFV) is naturally found in blood (Guinat et al., 2014) and meat (Mazur-Panasiuk et al., 2019). Substantial epidemiological evidence supports the entry of ASFV into naïve regions by pigs ingesting contaminated pork products (Sánchez-Vizcaíno et al., 2012; Mazur-Panasiuk et al., 2019). Thus, there is a greater risk for ASFV transmission if affected animal blood or muscle is used as a raw material for porcine-based ingredients, such as meat and bone meal, meat meal, blood meal, or blood plasma. The United States requires hazards in raw materials to be addressed prior to use in animal feed (FDA, 2023), and the rendering industry has robust protocols to ensure the safety of resultant ingredients (Meeker and Meisinger, 2015). For example, both conventional renderings to produce porcine meat and bone meal and spray-drying to produce spray-dried porcine plasma have been reported to successfully destroy PEDV (Gerber et al., 2014; Opriessnig et al., 2014). However, different temperatures or retention times may be necessary for the destruction of blood- and tissue-borne viruses such as ASFV.

One of the earliest studies describing the thermal mitigation of ASFV reported the virus was inactivated in cell culture medium exposed to 56 or 60 °C (Plowright and Parker, 1967). More recently, Kalmar et al. (2018) demonstrated inactivation at 48 °C using a similar technique. These temperatures are significantly lower than those used in either rendering or spray-drying, suggesting that the subsequent manufacturing steps are likely sufficient to inactivate ASFV in raw materials of porcine-based ingredients. However, a point-in-time thermal processing step may not be sufficient to eliminate the risk in porcine-based ingredients altogether. As reported by Elijah et al. (2021), ASFV introduced into a facility may be widely distributed throughout the manufacturing environment. Even if the mitigation step were successful at completely inactivating ASFV in raw material, the cooling, storage, loadout, and transportation of porcine-based ingredients to feed mills and farms may all pose potential opportunities for re-contamination from affected raw materials or cross-contamination from other fomites. If recontamination were to occur, Dee et al. (2018) found ASFV to be stable at or below room temperature (≤ 20 °C) for at least 30 d in a variety of feed matrices, which is similar to ASFV survival in meat, organs, and the environment (Mazur-Panasiuk et al., 2019; Mazur-Panasiuk and Wozniakowski, 2020). While few studies have researched ASFV persistence in porcine-derived ingredients, PEDV has remained stable in a variety of porcine-derived ingredients between 6 and 7 wk (Trudeau et al., 2017a).

Due to the stability of swine viruses in porcine-derived ingredients and the etiology of viruses like ASFV, it is important to consider both the efficacy of spray drying and rendering to inactivate pathogens and postmanufacturing mitigation in the event of recontamination. Therefore, the objectives of this review were to: 1) describe the current practices and efficacy of spray-drying and rendering regarding virus inactivation, 2) evaluate the available literature focused on mitigation of porcine-derived ingredients after manufacturing, and 3) identify knowledge gaps that need addressed for the continued and safe use of these protein sources in the event of a foreign animal disease outbreak.

Materials and Methods

A literature search was conducted using CAB Direct (www.cabdirect.org), Web of Science (www.webofscience.com), AGRICOLA (www.ebsco.com/products/research-databases/agricola), and Google Scholar (www.scholar.google.com). Keywords included a combination of the following: blood meal OR meat and bone meal OR meat meal OR spray-dried porcine plasma OR intestinal peptide products OR choice white grease AND virus inactivation OR thermal processing OR pelleting OR quarantine OR holding time.

Additionally, references from the generated papers were manually searched for relevant literature. Articles were restricted to those available in English with no restriction on publication year. Articles were separated based on the time of ingredient inoculation, either prior to manufacturing or postmanufacturing. Of those ingredients that were inoculated postmanufacturing, mitigation was classified as either thermally processed (>40 °C) or ingredient quarantine (<40 °C). No restrictions were placed on the porcine virus evaluated, but those evaluating foreign animal diseases, such as ASFV or classical swine fever virus (CSFV), were separated from those which evaluated viruses already present in the United States, mainly PEDV, porcine deltacoronavirus (PDCoV), and transmissible gastroenteritis virus (TGEV).

Results and Discussion

Manufacturing processes of porcine-derived ingredients

Rendering is the production of meal-based proteins and fats which serves as a recycling system for the unused and inedible trimmings from harvest facilities and disposal of carcasses from farms, through transport, and lairage. Rendering facilities can either be attached to harvest facilities, limiting the need for transport of raw materials, or independent off-site facilities which typically specialize in carcass disposal from farms (Meeker and Hamilton, 2006).

Rendering begins by reducing the particle size of the carcasses or trimmings from the production line of the harvest facility to a homogenous size for a more consistent cooking time. The majority of rendering plants utilize a continuous system that conveys the raw product into the cooker at a rate determined by the operator to not overfill the cooking system and thus decrease efficiency. The steam powered cooker, set between 115 and 145 °C, removes moisture from the raw material and creates a slurry of hydrolyzed protein and fat (Meeker and Hamilton, 2006). The slurry is discharged where liquid fat is centrifuged to remove solid impurities and the remaining solids are either returned to the cooker for further particle size reduction or pressed into cakes to remove any additional fat. The fats produced are either choice white grease, an animal feed grade fat source primarily composed of long chain fatty acids (NRC, 2012), or brown grease, which has a greater percentage of free fatty acids and is used in by-product industries such as biodiesel (Lopez et al., 2022). The choice white grease is stored in liquid form at approximately 95 °C following extraction while the meal-based protein cakes are milled into powder and stored in silos until loading (Meeker and Hamilton, 2006). Batch systems use heat (approximately 118 °C) to hydrolyze the raw products into protein meals and fat. Unlike the continuous cooker, this is a closed system, and will last between 2 and 3 h depending on the temperature and the contents of the batch cooker. Similar to a continuous system, both choice white and brown grease are separated from the protein meals and readied for storage or transport. Storage of rendered products and fats at rendering facilities varies based on the capacity of the facility and the demand for the product itself. Facilities may choose to store the meal-based proteins in silos or may directly load them into trailers or railcars for transport. Fats will be stored in heated silos at approximately 95 °C before transport in heated tankers to maintain a liquid consistency (Meeker and Hamilton, 2006).

Spray-drying is a process used on a multitude of ingredients throughout the food and feed industries including whey, coffee, spices, and in the case of porcine-derived ingredients, plasma. Blazquez et al. (2020) describe the plasma spray-drying process beginning with swine passing visual inspection by a United States Department of Agriculture (USDA) veterinarian, where blood is then collected following exsanguination and an anticoagulant is added, either sodium citrate or sodium tripolyphosphate, to prevent blood clotting. Depending on the harvest facility, blood can either be centrifuged prior to transport or after arrival at the spray-drying facility to separate the red blood cells from plasma. Either whole blood or plasma is transported at 4 °C in stainless steel tankers to the spray-drying facility (Blazquez et al., 2020).

Plasma will undergo an additional concentration step via nanofiltration, reverse osmosis, or vacuum evaporation before entering the spray-dryer (Blazquez et al., 2020). Plasma is atomized into the drying chamber which controls the size of the liquid droplets and the rate of dispersion into the dryer. Concurrently, hot air (inlet temperature ~ 200 °C) is released into the dryer, rapidly evaporating more than 95% of the moisture in the droplet (Patel et al., 2009). Approximately 20 to 90 s after atomization, the spray-dried particles are separated from the circulating air and exit the chamber at an outlet temperature of ≥80 °C and are packaged in either 25 kg paper bags or metric ton polyethylene totes.

Following the PEDV outbreak in 2013, some facilities implemented additional mitigation steps to further protect SDPP. Ultraviolet irradiation (UV-C) equipment can be installed prior to the concentration step as a redundant biosafety measure. Given the opaque nature of liquid plasma, the plasma must be agitated to expose all particles to the UV-C for efficacious mitigation (Blazquez et al., 2020). After SDPP production, some facilities also chose to store SDPP at room temperature (20 °C) for a minimum of 14 d prior to shipping and loading (Blazquez et al., 2020). These additional steps are not required for SDPP production, and their implementation varies based on facility capabilities and cost.

Viral mitigation during manufacturing of porcine-derived ingredients

Inactivation of bacteria and viruses in porcine-derived ingredients has focused primarily on the manufacturing process itself as the critical control point for inactivation of pathogens in order to control production costs. The time and temperature parameters used in rendering have been proven to effectively reduce the presence of bacteria such as Salmonella, Escherichia coli, Listeria, Campylobacter, and Clostridium (Shurson et al., 2022b). Prior to the PEDV outbreak in the United States, the primary virus of concern in porcine-derived ingredients was porcine circovirus type 2 (PCV2) due to its high heat resistance (Welch et al., 2006). Shen et al. (2011) found natural levels of PCV2 DNA in 78.1% of manufactured SDPP samples, which was only slightly less than the 82.7% of PCV2-positive samples found in the fresh porcine plasma itself. When inoculated with the naturally contaminated SDPP, pigs showed no signs of infection and remained seronegative for PCV2 for the duration of the bioassay indicating that the RNA that was present and detectable was not infective (Shen et al., 2011). Pigs fed artificially contaminated levels of PCV2 in SDPP were able to seroconvert PCV2 with clinical signs of infection (Patterson et al., 2010); however, the artificially contaminated SDPP was manufactured at lower temperatures with a shorter retention time than commercially produced SDPP, thus reducing the degree of viral inactivation during manufacturing. Similar to the results found by Shen et al. (2011) in PCV2-contaminated SDPP, pseudorabies (PRV) and porcine reproductive and respiratory virus (PRRSV) infectivity was reduced when plasma was spray-dried (Polo et al., 2005). After PEDV RNA was identified in SDPP and proven to be infectious (Pasick et al., 2014), research continued to evaluate the efficacy of spray-drying as a viral inactivation step (Table 1). Furthermore, biosafety measures, such as UV-C and product quarantine were researched as additional mitigation steps to reduce PEDV and other swine pathogens presence.

Table 1.

Summary of peer-reviewed, published literature which evaluate viral inactivation during the manufacturing stages of porcine-derived ingredients

Liquid plasma mitigation strategy Manufacturing mitigation strategy
Reference Virus evaluated1 Alkalization Increased temperature UV-C irradiation Spray-drying Ingredient quarantine
Polo et al. (2005) PRRSV, PRV − − − + −
Patterson et al. (2010) PCV2 − − − + −
Shen et al. (2011) PCV2 − − − + −
Gerber et al. (2014) PEDV − − − + −
Opriessnig et al. (2014) PEDV − − − + −
Pasick et al. (2014) PEDV − − − + −
Pillatzki et al. (2015) PEDV − − − + −
Quist-Rybachuk et al. (2015) PEDV + + − − −
Kalmar et al. (2018) ASFV + + − − −
Blazquez et al. (2019a) CSFV, BVDV, PCV2, PEDV, PPV, PRRSV, PRV, SIV, SVA, SVDV − − + − −
Blazquez et al. (2019b) HEV, PCV2, PPV, PRRSV, RVA, SIV − − + − −
Hulst et al. (2019) AdV, PCV2, PEDV, PSV1 + − − + +
Blazquez et al. (2021) ASFV, CSFV − − + + –
Blazquez et al. (2022) PCV2, PDCoV, PEDV, PPV, PRRSV, SIV, SVA, TGEV − − − + –
Blazquez et al. (2023) ASFV − − − + +
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1Classical swine fever virus (CSFV), bovine viral diarrhea virus (BVDV), porcine circovirus type 2 (PCV2), porcine epidemic diarrhea virus (PEDV), porcine parovirus (PPV), porcine reproductive and respiratory syndrome virus (PRRSV), pseudorabies virus (PRV), swine influenza virus (SIV), Senecavirus A (SVA), swine vesicular disease virus (SVDV), Hepatitis E virus (HEV), swine rotavirus A (RVA), African swine fever virus (ASFV), porcine deltacoronavirus (PDCoV), transmissible gastroenteritis virus (TGEV), adenovirus (AdV), porcine sapelovirus 1 PSV1).

+/– denotes the inclusion of the respective mitigation strategy in the study.

Ultraviolet irradiation can degrade or inactivate viruses in liquid plasma before the spray-drying process begins (Blazquez et al., 2020). Blazquez et al. (2019b) found that UV-C irradiation at either 3,000 or 9,000 J/L was able to inactivate PCV2 in naturally contaminated porcine plasma. Furthermore, multiple endemic viruses (Blazquez et al., 2019a) as well as ASFV and CSFV (Blazquez et al., 2021) underwent a 4-log virus reduction after UV-C irradiation of liquid porcine plasma. However, not all commercial facilities can implement UV-C irradiation in their current facilities and must therefore rely on the spray-drying process alone to inactivate any present pathogens.

Unlike the initial report by Pasick et al. (2014), the transmission of PEDV through SDPP was not replicated from either naturally contaminated SDPP (Opriessnig et al., 2014; Pillatzki et al., 2015) or experimentally inoculated SDPP (Gerber et al., 2014). Spray-drying alone reduced 95% of the infectious particles in inoculated porcine plasma which was further reduced beyond detectable limits when the SDPP was held at room temperature (20 °C) for more than 2 wk (Hulst et al., 2019). Spray-drying also decreased ASFV and CSFV concentrations, with the greatest reductions seen when SDPP was retained within the dryer for 60 s at 80 °C compared to the SDPP which was not retained for any additional time (Blazquez et al., 2021). Blazquez et al. (2023) also found ASFV concentrations to have the greatest reduction when the outlet temperature reached 80°C and retained at that temperature for 30 s vs. a lower temperature (70 °C) and shorter retention times (0 and 30 s).

Fewer studies have evaluated the efficacy of rendering compared to those that evaluated virus inactivation during spray-drying. A retrospective epidemiological investigation by Kim et al. (2008) linked improperly manufactured blood meal to the spread of CSFV vaccine antibodies in the Jeju Province off mainland Korea. However, blood meal manufacturing remains unregulated in Korea, so the rendering temperatures used to make the contaminated blood meal could be significantly different than what is commonly practiced in the United States (Kim et al., 2008). Lower temperatures (40 to 90 °C) than those used in rendering have been found to reduce viral concentrations given enough time for both PEDV (Quist-Rybachuk et al., 2015) and ASFV (Plowright and Parker, 1967; Knight et al., 2013; Kalmar et al., 2018) and while not validated using rendering parameters, implies rendering temperatures are adequate for viral inactivation.

Viral mitigation after manufacturing of porcine-derived ingredients

Cochrane et al. (2015) and Gebhardt et al. (2019) found that once SDPP and meat and bone meal (MBM) were contaminated with PEDV, the quantity of detectable RNA remained stable over the 6-wk study period. However, detectable RNA found in PCR assays is not synonymous with infectious particles. Hulst et al. (2019) estimated via virus isolation that spray-drying alone only inactivated 95% of PEDV infectious particles, which would increase the risk of product re-contamination. Therefore, postmanufacturing packaging, storage, and transport are critical steps in maintaining the biosafety of porcine-derived ingredients and reducing the risk of product contamination. Spray-dried porcine plasma is bagged in either 25 kg single-use bags or metric one ton polyethylene totes and some manufacturers have established and implemented additional protocols to store processed product in its final packaging for at least 2 wk at room temperature (Shurson et al., 2022a). Rendered ingredients, however, are either stored in bulk bins or directly loaded into trailers or railcars for transport. Previous research has demonstrated viral contamination is more prevalent in the transport vehicles than in the feed or ingredients (Greiner, 2016; Gebhardt et al., 2022) or within the storage bins on farms (Wu et al., 2022). Therefore, additional mitigation must be considered in case the porcine-derived ingredient was re-contaminated after leaving the production facility.

In total, there are only nine studies that have evaluated the mitigation of porcine-derived ingredients postmanufacturing (Tables 2 and 3). Limited information is available for thermal processing parameters required for viral inactivation. Trudeau et al. (2017b) determined at least 30 min at 90 °C were required for a 4-log reduction of PEDV contaminated SDPP. In comparison, the supplemental calculator by Songkasupa et al. (2022) predicts a mean time of only 3.1 min is necessary for a 4-log reduction at 90 °C, although a longer time with an added safety margin is recommended. As there are no other studies evaluating porcine-derived ingredients under these parameters, it is difficult to understand which study is the most accurate; however, the inactivation models for these studies may explain the discrepancies noted and will be discussed in greater detail later in this article.

Table 2.

Summary of peer-reviewed, published literature which evaluates African swine fever virus (ASFV) inactivation in manufactured porcine-derived ingredients by either thermal processing (>40 °C) or ingredient quarantine (<40 °C).

Reference Ingredient Duration1, min Temperature, °C Chemical mitigants applied
Thermal processing (>40 °C) Songkasupa et al. (2022) Meat and bone meal 20 60, 70, 80, and 85 N/A
Reference Ingredient Duration1, day Temperature, °C
Ingredient quarantine (<40 °C) Fischer et al. (2021) Spray-dried porcine plasma 35 4 and 21 N/A
McOrist et al. (2022) Meat and bone meal 7 23 Formic acid
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1Duration refers to the total time the study was conducted. Virus concentrations were evaluated at multiple time points throughout the study duration.

Table 3.

Summary of peer-reviewed, published literature that evaluate porcine epidemic diarrhoea virus (PEDV) inactivation in manufactured porcine-derived ingredients by either thermal processing (>40 °C) or ingredient quarantine (<40 °C)

Reference Ingredient2 Duration3, min Temperature, °C Chemical mitigants applied
Thermal processing
(>40 °C)		 Trudeau et al. (2017b) BM, MBM, MM, SDPP 30 60, 70, 80, and 90 N/A
Reference Ingredient Duration3, day Temperature, °C
Ingredient quarantine
(<40 °C)		 Cochrane et al. (2015) BM, MBM, SDPP 42 23 Essential oils, formaldehyde, medium chain fatty acids, organic acids, sodium bisulfate, or sodium chlorate
Dee et al. (2015) MBM, MM, SDPP, CWG, IM, PP, RBC 30 −18 to −9 Formaldehyde
Gebhardt et al. (2019) SDPP 42 23 Essential oils or benzoic acid
Pujols and Segales (2014) SDBP 21 4, 12, and 22 N/A
Trudeau et al. (2017a) 1 BM, MBM, MM, SDPP 25 56 N/A
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1 Trudeau et al. (2017a) also evaluated porcine deltacoronavirus (PDCoV) and transmissible gastroenteritis virus (TGEV) under the same parameters.

2BM, bone meal; MBM, meat and bone meal; MM, meat meal; SDPP, spray-dried porcine plasma; CWG, choice white grease; IM, intestinal mucosa; PP, purified plasma; RBC, red blood cells; SDBP, spray-dried bovine plasma.

3Duration refers to the total time the study was conducted. Virus concentrations were evaluated at multiple time points throughout the study duration.

More studies evaluated the time needed for virus inactivation in quarantine scenarios than thermal processing. Infectious ASFV particles were still present when MBM was held at 22 °C for 7 d and SDPP at 4 °C for 14 d (Fischer et al., 2021; McOrist et al., 2022). Fischer et al. (2021) noted ASFV particles failed to cause infection in SDPP from days 14 to 35 when held at 22 °C (Figure 1), but this is the only study where ASFV inactivation has been documented in porcine-derived ingredients under quarantine conditions. The number of days PEDV particles remained detectable differed based on the porcine-derived ingredient (Figure 2). Blood meal, MBM, and meat meal held at 25 °C (Trudeau et al., 2017a) maintained detectable levels of infectious viral particles longer than SDPP in multiple studies (Pujols and Segales, 2014; Trudeau et al., 2017a; Gebhardt et al., 2019). Trudeau et al. (2017a) observed a similar pattern for PDCoV (Figure 3) and TGEV (Figure 4). Infectious PEDV particles also remained detectable for more time as the temperature decreased (Pujols and Segales, 2014). Interestingly, Dee et al. (2015) did not find detectable PEDV particles in SDPP, intestinal mucosa, or purified plasma at the start of the study, which may be due to unknown interference when testing feed or ingredients in laboratory analyses. Dee et al. (2015) also found infectious PEDV particles in choice white grease via virus isolation only until day 7; however, the days 14 and 30 samples caused clinical infections during a swine bioassay. While not always feasible, bioassays are the preferred method to evaluate virus inactivation as they are typically more sensitive than virus isolation alone (Niederwerder et al., 2022). While a positive bioassay is considered to be conclusive evidence of infectivity, a negative bioassay result should be interpreted as inconclusive (Beecher-Monas, 1998; Halperin, 2005) due to the wide variance and small sample size necessitated by the nature of bioassays. Furthermore, care should be taken when sourcing pigs for the bioassay to ensure they are both disease free (Niederwerder et al., 2021, 2022) and lacking any neutralizing antibodies which can interfere with the bioassay itself (Gebhardt et al., 2018).

Figure 1.

Figure 1.

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Summary of days infectious African swine fever virus (ASFV) was detectable in porcine-derived ingredients in quarantine conditions (<40 °C) as reported in peer-reviewed published literature.

Figure 2.

Figure 2.

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Summary of days infectious porcine epidemic diarrhea virus (PEDV) was detectable in porcine-derived ingredients in quarantine conditions (<40 °C) as reported in peer-reviewed published literature.

Figure 3.

Figure 3.

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Summary of days infectious porcine deltacoronavirus (PDCoV) was detectable in porcine-derived ingredients in quarantine conditions (<40 °C) as reported in peer-reviewed published literature.

Figure 4.

Figure 4.

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Summary of days infectious transmissible gastroenteritis virus (TGEV) was detectable in porcine-derived ingredients in quarantine conditions (<40 °C) as reported in peer-reviewed published literature.

There is limited information available on ASFV inactivation in porcine-derived ingredients, but studies that evaluated ASFV persistence and decay in complete feed can support our understanding of ASFV mitigation. African swine fever virus DNA has remained detectable for up to 375 d at 4 or 20 °C and 110 d at 35 °C (Elijah et al., 2022; Niederwerder et al., 2022). Niederwerder et al. (2022) further evaluated ASFV infectivity when complete feed was held at either 4, 20, or 35 °C and found ASFV was negative via tissue culture and bioassay by days 60, 3, and 1, respectively. Due to the risk of ASFV, they recommended longer storage times of at least 112, 21, and 7 d for each respective temperature (Niederwerder et al., 2022). At similar temperatures, Sindryakova et al. (2016), could not detect ASFV infectious particles on day 40 when held at 4 to 6 °C and on day 5 at 22 to 25 °C. The half-life for ASFV degradation in feed at temperatures ranging between 0 and 30 °C (mean 12.3 °C) is estimated to be at least 14.2 d (Stoian et al., 2019) which exceeds the previous estimate of only 4.3 d (Dee et al., 2018).

The feed in all the studies cited above did not contain porcine-derived products; however, studies that evaluated swill can provide greater context of ASFV degradation compared to complete feed. Swill has been a suspected transmission source in multiple ASFV outbreaks throughout the years (Mazur-Panasiuk et al., 2019; Song et al., 2022). The World Organization for Animal Health (OIE) states inactivation of ASFV occurs at 56 °C for 70 min or 60 °C for 20 min (OIE, 2019); however, they specifically state that swill should be held at 90 °C for 60 min with continuous stirring (OIE, 2022). Interestingly, the Food and Agriculture Organization of the United Nations (FAO) recommends heating swill at 70 °C for only 30 min (Beltran-Alcrudo et al., 2017). Utilizing these temperature parameters, Nuanualsuwan et al. (2022b) calculated that at least 4 h= was needed to inactivate high concentrations of ASFV (10.9 log PFU/g) at 60 °C and 2 h was necessary for inactivation at 70 °C. While Nuanualsuwan et al. (2022b) did not directly measure ASFV inactivation at 90 °C, they estimated it would take only 4 min for complete ASFV degradation, but this hypothesis would need further confirmation. While inactivation of ASFV in porcine-derived ingredients cannot be directly compared to complete feed or swill, these ingredients provide boundaries when considering time and temperature parameters which can be implemented in postmanufacturing mitigation.

One limitation to thermal mitigation processes is that they are point-in-time mitigants. This means that the combination of parameters such as time, temperature, and/or pressure serve as a “kill step” for pathogen destruction, but do not prevent subsequent cross-contamination or re-contamination. In similar industries that rely on thermal inactivation or point-in-time mitigation processes, regulatory and/or industry standards includes intensive sanitation controls to prevent postprocessing contamination. These types of cleaning, sanitizing, and environmental monitoring procedures are practiced in the production of some types of porcine-derived ingredients but are currently infeasible in others. In these cases, thermal inactivation should be considered as a method to reduce the likelihood and quantity of viral contamination in raw materials, but the risk for low-level cross- or recontamination must be considered.

Alternatively, chemical mitigation has also been used to reduce viral concentrations of multiple swine viruses in contaminated feed and ingredients resulting in a residual, longer lasting effect compared to point-in-time mitigation such as thermal processing. These chemicals can include a formaldehyde-propionic acid blend, medium chain fatty acids (MCFA) either alone or blended, essential oils, or acidifiers. These chemical compounds have various modes of action which affect their efficacy based on the virus and its characteristics. Briefly, formaldehyde interacts with the proteins and genetic material of viruses, limiting their ability to replicate once inside the host (McDonnell and Russell, 1999), while acidifiers, as the name suggests, lower the overall pH of the ingredient or feed matrix which may limit the ability of the virus to survive the acidic environment of the stomach (Trudeau et al., 2016). Essential oils and MCFA are thought to be most effective against enveloped viruses as they are able to infiltrate the lipid envelope—this mechanism may act synergistically with acids where H + ions then are able to permeate across the lipid envelope and disrupt normal viral function (Cochrane et al., 2020; Zhai et al., 2021).

For viruses endemic to the United States, essential oils, MCFA, and formaldehyde were found to decrease the quantity of PEDV RNA in SDPP, MBM, and blood meal (Cochrane et al., 2015). However, essential oils and benzoic acid, either alone or in combination, did not decrease detectable RNA in SDPP over 6 wk and the combination from 7 d postinoculation caused clinical signs of PEDV in a swine bioassay (Gebhardt et al., 2019). Formaldehyde successfully decreased PEDV RNA and reduced infectious viral particles when added to porcine-derived ingredients held below freezing temperatures (Dee et al., 2015).

McOrist et al. (2022) saw an overall decrease in ASFV infectious particles in MBM over 7 d, but the inclusion of either 1 or 2% formic acid did not impact viral concentrations as compared to the ASFV-inoculated control. No other studies evaluated chemical mitigation in ASFV-contaminated porcine-derived ingredients, but anti-ASFV properties have been studied in other matrices. Tran et al., (2020a and 2021) noticed decreased detectable DNA when complete feed was treated with an equal C6:C8:C10 blend at all inclusion levels (0.125, 0.25, 0.375. and 0.50%). A C8:C10:C12 blend also decreased detectable ASFV DNA when included at 0.25, 0.375, and 0.5%, while C8 alone was most efficacious at the two highest inclusion levels (Tran et al., 2020a, 2021). However, neither the blended MCFA nor C8 alone were able to significantly reduce ASFV infectivity compared to the untreated control (Tran et al., 2021). When MCFA is applied to ASFV-contaminated water the C8:C10:C12 blend reduced detectable DNA at all inclusion levels while the C6:C8:C10 blend and C8 blend were most effective at the three and two highest inclusion levels, respectively (Tran et al., 2020a). Niederwerder et al. (2021) reported reduced infectivity of ASFV up to 0.70% inclusion of an equal C6:C8:C10 MCFA blend. At inclusion levels at or above 0.70%, ASFV was non-detectable via tissue culture (Niederwerder et al., 2021). African swine fever virus DNA was still detectable on d 30 in complete feed treated with 1% MCFA but did not cause infection in a swine bioassay (Niederwerder et al., 2021). In a similar study design, increased inclusion (0.25% to 2.0%) of a C8:C10:C12 (51:29:7 ratio) blend did not reduce ASFV concentrations compared to the untreated control; however, a 2.0% inclusion of glycerol monolaurate (C12 attached to a glycerol backbone), successfully reduced ASFV concentrations after only 30 min compared to the untreated control (Jackman et al., 2020).

Similar to PEDV, formaldehyde has also been found to decrease ASFV concentrations when added to complete feed. Le et al. (2022) noted that ASFV concentrations decreased below the detection threshold after 1 or 3 h when exposed to 0.2 or 0.05% to 0.1% formaldehyde concentrations, respectively. When included at 0.33% of the diet, formaldehyde decreased the quantity of detectable DNA over 30 d and did not cause clinical signs of ASFV infection in the following bioassay (Niederwerder et al., 2021). Ly et al. (2022) saw decreased detectable DNA from days 1 to 7 when formaldehyde was included in complete feed at either 1, 2, or 3 kg/ton (0.1% to 0.3%), where ASFV infectivity was reduced on days 1 and 3 with 3.0 kg/ton inclusion and on day 7 with 2 or 3 kg/ton inclusion of formaldehyde. When comparing formaldehyde-based products with an organic acid counterpart, Tran et al. (2020b) saw an increased antiviral effect with liquid formaldehyde on days 3 and 7 and dry formaldehyde only on day 7 (both included at 3 kg/ton); however the ASFV concentrations were decreased by less than one-log for both liquid and dry formaldehyde, so more time may be necessary for increased inactivation of either product.

Future research considerations

There is currently limited research evaluating the viral inactivation of viruses in porcine-derived ingredients during and after conventional thermal processing activities, especially for foreign animal diseases such as ASFV. While not all research objectives can be easily answered, there are some that may elucidate the best course of action in the event of a foreign animal disease outbreak. New research, especially studies including positive swine bioassays, can support the current published literature to provide greater clarity for viral inactivation parameter estimates. Alternatively, a negative bioassay result likely provides no more clarity than there was prior to the experiment.

The combination of temperature and time used in conventional rendering and spray-drying processes can successfully reduce the quantity of infectious viruses, but the risk and subsequent practice to prevent cross- or re-contamination after processing risk has not been fully elucidated. The locations where recontamination is most likely to occur have not been identified which limits our ability to implement successful postmanufacturing mitigation. For example, if thermal processing or ingredient quarantine were to occur directly after manufacturing but the recontamination was most likely to occur further down the supply chain, the additional mitigation would be negated. It is therefore imperative that proper posthandling practices, such as segregation between raw and finished products, rodent and pest control, and covering trailers when they are not being loaded, are implemented to reduce the risk of recontamination until risk analysis studies have been conducted. Furthermore, the virus concentration of naturally re-contaminated products remains largely unknown. Blazquez et al. (2022) identified low levels of viral RNA and DNA of multiple viruses in SDPP, but the infectivity of those samples was not analyzed, which limits the ability for a risk analysis.

As noted previously, Songkasupa et al. (2022) predicted a shorter mean time to a 4-log reduction at 90 °C for ASFV than Trudeau et al. (2017b) predicted with PEDV. Since PEDV is typically considered a less resilient virus than ASFV (Dee et al., 2016, 2018) when ingredients are held under similar conditions it is surprising to see a shorter estimate for ASFV degradation. This discrepancy is largely driven by the different inactivation models used in each study. Songkasupa et al. (2022) used a first-order kinetic inactivation curve which assumes log-transformed virus concentrations will decrease at a constant rate. Trudeau et al. (2017b), however, modeled inactivation data using a Weibull distribution which assumes the rate of viral inactivation decreases over time. It is not clear which model best fits ASFV inactivation as both linear (Nuanualsuwan et al., 2022b; a) and non-linear (Mazur-Panasiuk and Wozniakowski, 2020) models have been used to describe ASFV degradation in different matrices. However, Blazquez et al. (2019a) modeled the inactivation of multiple viruses, including CSFV, when inoculated porcine plasma was exposed to UV-C and found non-linear models best represented the viral degradation for all viruses evaluated in the study. Understanding which model works best for ASFV inactivation in porcine-derived ingredients, and whether all porcine-derived ingredients can use the same model, will provide greater confidence in the estimates generated from past and future research.

Practical considerations of additional thermal processing and ingredient quarantine must also be considered. Thermal processing, typically implemented as pelleting in swine diets, has been known to decrease amino acid digestibility if conditioned to too high a temperature (Steidinger et al., 2000; Almeida, 2013). As porcine-derived ingredients are rarely thermally treated alone, it is unknown whether protein degradation would occur and to what degree. Logistically, it would also be difficult to thermally treat or quarantine large quantities of porcine-derived ingredients which would require large climate-controlled warehouses for storage and processing thus creating a bottleneck in the supply chain as demand for the mitigated product exceeds the available supply.

There is still a lot to learn about porcine-derived ingredients and their supply chain. Previous research has found that the processes used in porcine-derived ingredient manufacturing are capable of virus degradation in laboratory settings, but it’s unclear if porcine-derived ingredients still contain infectious viral particles following commercial production. Furthermore, if products are pathogen-free, the location and extent of product recontamination must be further defined. Thermal processing and ingredient quarantine are effective management strategies for porcine-derived ingredients, but the viral degradation characteristics in each porcine-derived ingredient and the time and temperatures needed for viral inactivation in each ingredient need more thorough investigation.

Conclusions

The production of porcine-derived feed ingredients is an intensive process that utilizes high temperatures to create a nutritious protein source for livestock and pet food industries. The combination of parameters used in United States rendering and spray-drying to produce porcine-derived ingredients can mitigate infectious viruses in affected raw materials. However, the risk of cross- or recontamination after this point-in-time mitigation method warrants additional study before affected raw materials should be used for the production of ingredients intended for pigs.

Contributor Information

Olivia L Harrison, Department of Animal Sciences and Industry, Kansas State University, Manhattan, KS, USA.

Chad B Paulk, Department of Grain Science and Industry, Kansas State University, Manhattan, KS, USA.

Jason C Woodworth, Department of Animal Sciences and Industry, Kansas State University, Manhattan, KS, USA.

Jordan T Gebhardt, Department of Diagnostic Medicine/Pathobiology, Kansas State University, Manhattan, KS, USA.

Cassandra K Jones, Department of Animal Sciences and Industry, Kansas State University, Manhattan, KS, USA.

Conflict Interest Statement

None declared.

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