Why must we rush to bury our dead (pigs): The option of excarnation by exposure

Abstract

The accepted paradigm of foreign animal disease preparedness in Canada, the emergency for which to prepare, starts with identification of the exotic viral agent in a Canadian farm animal population. This narrative focuses on the containment of the infectious agent, within diseased animals, on infected premises. Framing the emergency as a disease incursion limits rational imagination to only one version of one potential animal emergency. This framing of the problem directs the carcass disposal solutions to consider only methods to dispose of viral infected material. However, in all documented responses to catastrophic swine diseases in the past three decades, the number of uninfected animals caught up in movement control zones and killed greatly exceeds the number of infected animals killed. The temporary closures of slaughterhouses in spring 2020 due to COVID-19 transmission resulted in thousands of healthy market hogs surplus to market; an unanticipated emergency of healthy pigs. This paper proposes an alternate carcass disposal option for material from uninfected farms. “Excarnation by exposure” is a natural process of debulking and dehydrating carcasses by blow fly larvae, mitigating financial costs of final disposal. Excarnation by exposure is a reasonable and possibly necessary additional option for the management of uninfected carcasses in a catastrophic emergency response in commercial pigs.

“I much fear that flies will settle upon the son of Menoetius and breed worms about his wounds, so that his body, now he is dead, will be disfigured and the flesh will rot.”

The Iliad, Book 19 Homer

Introduction

In the veterinary literature, the clause “foreign animal disease” (FAD) carries a great deal of social, cultural, ethical, economic, and political meaning beyond a disease of animals. The term “swine catastrophic disease” (1) may better describe the incursion of a trade restricting disease, [foot-and-mouth disease (FMD), classical swine fever (CSF), swine vesicular disease (SVD), African swine fever (ASF)] into previous disease- free pork-producing regions. The documentation of recent eradication programs indicates most of the animals killed in these programs are uninfected and killed for animal welfare reasons secondary to movement restrictions. The carcasses of uninfected animals killed due to worsening conditions on farms compete with carcasses on infected premises for limited disposal resources.

The “Disposal of Dead Animals” chapter in the World Organisation for Animal Health (OIE) — Terrestrial Animal Health Code (2) mentions animal mortality due to natural disasters such as flooding. However, the chapter has a disease control focus and primarily describes the safe disposal of carcasses from infected, contact, and pre-emptive slaughter (potentially infected) premises. Authors of the Code did not anticipate the destruction of healthy animals due to supply chain interruption. In relation to carcass disposal, the final “decisions made should reflect a balance between the scientific, economic, and social issues at stake” (2). The United States Department of Agriculture (USDA) parallel document states, in relation to emergency carcass disposal, “The overall goal is to protect the agricultural and national economy through the control and containment of disease by conducting operations in a timely, safe, biosecure, aesthetically acceptable, and environmentally responsible manner” (3). These parallel directives clearly identify 2 non-technical modulators of carcass disposal decisions, aesthetically acceptable and environmentally responsible. Both are moral constructs reflecting societal expectation of the national veterinary infrastructure. Open pyre burning produces a visible marker on the rural landscape and is now prohibited in the European Union (EU), justified as an environmentally questionable carcass disposal option (4). Although deep burial has high cost and serious environmental challenges (5,6), deep burial remains the current and expected first choice method for (infected) carcass disposal (7).

Foreign animal disease response planning

The binding standards for resumption of market access, international trade in livestock and livestock products following an FAD incursion are outlined in the Sanitary and Phytosanitary agreement of the World Trade Organization. The OIE — Terrestrial Animal Health Code clarifies the details of requirements to recover recognition of freedom from exotic disease and normalize trade. The most dependable and predictable return to market access is by stamping-out, which is a suite of disease investigative and control actions directed at eliminating all infected animals and thus eradicating the introduced virus from the regional animal population (8). The primary action of stamping-out is comprehensive animal movement prohibition. In stamping-out, the number of animals killed due to infection may be as low as 5% of the animals killed as surplus to market (9). Before the year 2000, in every CSF incursion into the EU where more than 10 herds were infected on Day 1, the cost of welfare slaughter was greater than the cost of “stamping-out” (10). In the 1997/1998 epizootic of CSF in the Netherlands, of the 11 million animals disposed of by rendering, 1.828 million were from infected farms and pre-emptive culled premises; 9.229 million were killed for welfare reasons (11). In the Netherlands-2001-FMD outbreak, 118 786 clovenhoofed animals were killed on 211 farms as part of a purchase scheme (killed because of welfare problems). These comprised 24 173 calves (82 farms), 43 638 fattening pigs (99 farms), and 50 975 piglets (30 farms) (12).

In the UK-2001-FMD outbreak (6 million animals killed), although deep burial was preferred, open pyre burning was also used. Negative public opinion resulted in the prohibition of the open pyre option in the future (4). Emergency managers treated carcass disposal as “extremely urgent” and opted for centralized burial on 6 large landfill operations (13). Korea eradicated FMD in 2010, primarily using the on-farm deep burial option of over 3 million pigs and 155 000 cattle from 6268 affected farms, generating 4583 separate burial sites (14) presenting a geographically widely distributed concern for groundwater contamination by carcass leachate.

The COVID-19 pandemic caused temporary slaughterhouse closures in the US and subsequent slowdowns resulting in mass killing of an estimated 1 000 000 healthy surplus to market pigs. The extensive State-Federal FAD eradication plans currently in place were not activated, as widespread livestock emergency in the absence of a FAD was not anticipated (15). In response to this crisis, the industry in some cases adopted “above ground burial” for the carcasses of healthy animals (16). This technique is more accurately described as shallow grave burial, in which, a pit is constructed about 20 cm deeper than the carcass width, and 20 cm of absorbent plant material is placed under the carcasses and the carcass is covered over with the original pit origin soil (17).

The killing and disposal of large numbers of uninfected animals is an unintended but expected consequence of FAD eradication efforts in export dependent countries. The USDA standard comprehensive FAD operational manual on (infected) carcass disposal is 253 pages describing high resource dependent and technological solutions (3). This paper challenges the assumption that uninfected carcasses represent an “extremely urgent” risk that requires disposal by one of the recognized bio-secure methods appropriate for infected carcass disposal. This paper promotes the inclusion of excarnation by exposure in emergency planning for swine carcass management — specifically, by placing carcasses outdoors to maximize access by blow flies and other necrophagous insects. Exposure will decrease the mass and water content of uninfected carcasses of pigs and thereby free up resources for disease control activities and minimise the environmental hazards inherent in the burial of fresh carcasses.

Technical summary

In the years following 9/11, there was considerable awareness of the vulnerability of the modern food system and concern with the potential of intentional FAD introduction (18) resulting in an increase in preparation plans including carcass disposal. In 2004, the Kansas State (University) Research Exchange e-published comprehensive reference guides: Carcass Disposal: A Comprehensive Review (19) which provides an extensive summary of the scientific, technical, and social aspects of various carcass disposal technologies, and serves as a resource for veterinary and other officials tasked with planning for the safe and timely disposal of (infected) animal carcasses. This reference includes chapters that address burial (including landfill), incineration (air curtain incineration), composting, rendering, lactic acid fermentation, alkaline hydrolysis, anaerobic digestion, as well as Chapter 8, on novel technologies.

The Terrestrial Animal Health Code (Chapter 4.13) identifies 11 acceptable methods of (infected) carcass disposal (2); rendering, incineration in a dedicated facility, rendering and subsequent incineration, air curtain incineration, pyre burning, composting, burial, biogas production, alkaline hydrolysis, bio-refining, and disposal at sea. Of this group of options, half are not scalable under emergencies and some, such as disposal at sea, are limited in opportunity. The current published reviews of FAD carcass disposal do not differentiate between carcasses from infected and high-risk farms and surplus to market, uninfected animals. Guidance focuses on “infected carcass” as a vector for the disease to be eradicated and rely on deep burial, rendering, incineration, composting, and open-air cremation on a pyre, with deep burial having the greatest flexibility in field application (5,20). These methods operate with green carcasses < 7 d post-mortem and effectively protect carcasses from necrophagous insects.

In flooding resulting in livestock death, there is some urgency placed on agencies tasked with collection and disposal of carcasses, as by Day 7–8 post-mortem, carcasses are friable and break apart on mechanical handling (21). This sense of “extreme urgency” to dispose of animals killed in disease control operations was instrumental to the decision to develop 6 massive deep burial projects in the 2001 UK response to FMD (13).

There are several well-documented myths associated with emergency response to natural disasters (22). The belief that dead human bodies are a human disease hazard is in error (23). Disaster victims generally die of trauma, burns, or drowning. Any contagious disease risk the victim posed ante-mortem is greatly diminished post-mortem. Death of the victim immediately stops any viral replication and the bacteria of putrefaction inhibit the further replication of bacterial pathogens of the living (24). The myth that post-disaster epidemics are caused by dead bodies is extremely resilient to scientific counter-evidence (25). A possible explanation is that the progressive physical deterioration of human bodies left in the open triggers a feeling of disgust. Conflating disgust with contagion is a common error and the experience of disgust may be manifest in public demand for protection from the dead (pigs) (26). Ebola virus in human cadavers and African Swine Fever virus in pig carcasses are exceptions to the “dead are generally safe” rule.

Maggot apologetics

Large free-ranging ungulates and other mammals die and are efficiently removed from the landscape by ecosystems that have co-evolved for millions of years. Forensic entomology, especially the insect succession dynamics of the single human cadaver, allows for an estimate of time since death. Forensic research has been markedly advanced by the use of pig carcasses, both naked and fully clothed, to mimic the decomposition processes that a human cadaver would undergo in specific environmental conditions (27). Mass burial of pigs has also been used to better understand the process of deterioration of the human body in mass graves subsequent to genocide and crimes against humanity (28). Blow flies (Diptera; Calliphoridae) have world-wide distribution and are the predominant early insect scavenger contributing to excarnation of exposed vertebrate carcasses when temperatures exceed 10°C.

Mammal carcasses placed above ground and not protected from blow flies proceed through a rapid continuous decomposition process, recognizable as 5 visual stages. Fresh carcasses trigger almost immediate blow fly oviposition, followed by i) bloated (24 to 72 h, stage, ends with skin rupture); ii) active decay (3 to 5 d, massive assemblage of blow fly larvae which migrate away from the carcass to pupate); iii) advanced decay (subsequent to blow fly larval migration); iv) dry remains (skeleton remains with large joints attached with dry tendons and joint capsule); and v) skeleton (29). The carcass mass loss by the advanced decay (dry) stage is often 90% of the original mass and can occur within 8 d for small carcasses (29). Skin rupture, marking the transition from bloat to active decay is associated with some fluid leakage that is absorbed into porous substrate and/or evaporative loss. Excarnation, the nearly complete defleshing and dehydration of the carcass, represents the conversion of carcass carbon, nitrogen, and trace minerals into blow fly larval tissue with subsequent fly emergence and dispersal.

The rate of decomposition of exposed pig carcasses is highly temperature-dependent. Frozen carcasses are permanently stable as microbial and insect metabolism is blocked. It has been reported for piglets weighing 1000 to 1400 g that 10% body mass will remain by Day 5 of open exposure and the dry stage by Day 8 (29). Using larger pigs, 45 ± 5 kg in Tasmania and comparing urban to rural placement, bloat ended at Day 3 (skin rupture) in both settings, but active decay lasted 24 d in a rural setting compared to 10 d in an urban environment with daily temperatures ranging from 12 to 23°C (30). Blow flies are active between 10°C and 35°C (31) and accumulated degree days (ADD) is the prime factor in predictable speed of carcass mass disappearance by fly larvae (32). Large numbers of blow fly larvae in the decay stage create an exothermic mass (maggot-mass effect) which accelerates larval development and excarnation of the carcass (33). In contrast to the research on single pig models, there is limited research on exposure of multiple pig carcasses. A single report describes rapid mass carcass disposal by exposure. In this summer experiment, 2700 kg of feral swine carcasses were assembled in 5 piles at increasing pressure from 25 to 750 kg/20 m² plot. Blow fly larvae skeletonized all carcasses in just a few days (34).

Framing the concept

There are opposing frames represented in the scientific literature on the issue of natural carcass disposal by exposure. In ecologically framed discourse, natural excarnation of mammal carcass creates a temporary highly concentrated plant nutritional source, a cadaver decomposition island, which provides an opportunity for increased plant and insect diversity (35,36). The waste management and environmental hazard literature, however, frames the unnatural dead livestock animal as a thing of danger, contamination, or a technical or human failure (17,37). Emergency-related mass carcass disposal is not natural and usually presented as a technical challenge. There are few publications in veterinary journals dealing with carcass management, although it is a foundational issue for emergency animal disease response (3,38). Excarnation by exposure is not considered in current emergency management planning despite the extremely low input “technology” required and remarkable ability to scale up at relatively low financial cost compared to alternatives.

Burial is a method of preservation or greatly slowing the decomposition of human and non-human post-mortem material. Mass livestock burial results in decomposition by anaerobic bacterial activity leading to liquefaction and the production of leachate, which is difficult to contain, even with intensively purpose-engineered pit construction (39,40). As water is the predominant component of carcasses and leachate the primary challenge to environmental protection, other carcass mass reduction technologies have been investigated, such as using bacterial action within bio-reduction vessels (20). This process does accomplish a small volume reduction but primarily acts to convert semi-solid carcasses structure to a more easily handled fluid form. Composting is a technically feasible form of carcass reduction. Although input is intensive and costly, it effectively blocks carcass digestion by insects in favour of digestion by bacteria and organic heating (41). Blow fly access to a carcass is inhibited by 60 cm soil coverage in burial or less depending on the species of fly (42).

Barriers to adoption

There are several possible barriers to first-choice use of natural carcass excarnation. The 2 most obvious are risk of low public acceptance and regulatory isomorphism.

Disgust is a well-studied emotion that has some spillover into moralization of the object of disgust (26,43). The elicitation of strong disgust is supportive of the thing being morally wrong (44,45). Disgust should be irrelevant to moral judgement and legal decisions (46); for example, the historical error of legal sanction for sexual orientation or miscegenation or the use of disgust in dehumanizing for effect (43,46).

In the UK-2001-FMD outbreak, media coverage, especially visual images of open pyre carcass burning, resulted in subsequent prohibition. The moralization (justification) leading to prohibition was based on an assemblage of dubious environmental risks. Open pyre burning, although fossil fuel and labor intensive, has demonstrated safe disposal by burial of ash, negligible effect on soil, and emissions from pyres do not affect air quality beyond the immediate vicinity (6). The public has no reason to have a pre-existing opinion on carcass excarnation by exposure. It is a novel approach to emergency carcass disposal and exists as an idea at this time. In Canada, novel technologies such as cloning and genetically modified crops have not triggered a prohibition by populist moralization. Planned communication of new technology can result in public acceptance although the mental image of bodies consumed by maggots is repugnant and has been perceived as undesirable since the writings of Homer (8th century BCE).

The larger barrier to adoption is the result of institutional isomorphism. In a comparison of open access transboundary emergency animal disease response plans, such as the AUSVETPLAN, Animal Health Australia and The Red Book, United States Department of Agriculture, the goals, methods, and desired outcomes are very similar. Institutions of similar purpose tend to converge with similar structure and function over time. The pressure on institutions to mimic each other has been attributed to 3 distinct sources. The literature has described them as coercive isomorphism (in this case the quasi-regulatory role of the OIE and the Terrestrial Animal Health Code); normative isomorphism (the delivery of animal health by a professionalized group e.g., veterinarians with a standardized training and ongoing peer review reinforcing uniform thinking); and mimetic isomorphism (the adoption of lessons learned by the experience of others) (47). Disposal by excarnation has never been considered by the OIE or other science-based authorities such as the National Agriculture Biosecurity Center (NABC), Kansas State University (19). The NABC documents give full consideration to feeding surplus carcasses to alligators, but does not consider the opportunity to feed carcasses to blow fly larvae (48). Thinking outside the box and acting outside the box are not equivalent energetic actions. Stamping-out livestock disease has high public visibility and is at risk to transform from a primarily science-informed management structure to a politically informed management structure. Scientific innovation is unlikely under a politically driven emergency response where mimetic isomorphism is the primary determinate of decisionmaking. The 2010/2011 Korean FMD outbreak was recently reviewed in light of this dynamic (49).

Discussion

All currently recommended emergency carcass disposal methods effectively prevent degradation of the carcass by blow flies. The author could not identify scientific reports, comprehensive risk assessment, or cost-benefit analysis that would justify the enforced preference of burial and anaerobic bacterial degradation over openair insect degradation for presumed uninfected carcasses. There is a wealth of studies documenting the hazards of leachate from livestock mass burial sights to groundwater (5,39,50). It appears that the universal decision to ignore the option of disposal by exposure for uninfected livestock affected by mass mortality events reflects attitudes and paradigms of thought outside of rational choice theory. This begs the question of why the FAD preparedness community has universally embraced burial and composting, whereas excarnation by exposure is not currently considered.

The twentieth century has witnessed the escalation and industrialization of murder, crimes against humanity, and the practice of mass human burial. Arguably, the cultural distance between human and non-human animals has shortened in the past 2 centuries. It is possible the strong desire to recover livestock carcasses in floods and natural disasters and to urgently place carcasses of animals killed for disease control purposes where they cannot be seen is not based on rational risk minimization decisions but on a deeper imperative: treating the animals that they once were with respect, or to assuage the guilt of massive animal killing. If organizational decisions on carcass disposal are mainly based on morality, a belief that failure to bury dead livestock is inherently wrong, then the proposed technical innovation suggested in this paper could be interpreted as a form of blasphemy. This paper suggests that in the culture and professional norms of veterinary medicine, respectful disposal of carcasses may constitute both technical and moral work.

Conclusion

This paper contributes to the field of foreign animal disease emergency preparedness by exploring an extremely well-documented process in the forensic scientific literature and its possible application to emergency management. Future research in decision-making in animal emergency response should seek to identify if decisions are unconsciously moderated by deep socio-cultural understandings of the appropriate treatment of animal bodies both alive and dead. In summertime (average daily temperature above 20°C) livestock carcass handling, a delay or backup in the first-choice disposal process by as little as 7 d, excarnation by blow fly larvae will be well underway and mechanical handling of carcasses difficult.