Introduction

The threat level of foreign pathogen introduction to the Unites States’ swine production supply chain has been increasing. Due to the growing global trade of swine-related products (e.g., pork products, feed ingredients, equipment, and personnel), the underlying risk for emerging disease outbreaks is increasing [1]. For instance, the imminent threat of African swine fever disease (ASV) has prompted an urgency to have response plans in place if ASV crosses onto U.S soil [2]. In addition, the aftermath of the recent supply chain disturbance including shutdown of meat processing plants during the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic, further necessitates response plans to mitigate potential negative impacts on the U.S swine industry caused by pathogens not based in the domestic swine population [3]. During disease response situations, swine producers will likely be instructed to temporarily stop animal movements and depopulate herds to prevent disease transmission. Performing depopulation methods currently approved by the American Veterinary Medical Association (AVMA) under field conditions can be challenging from the standpoint of timeliness, economic, logistic, and animal welfare [4]. For example, depopulating large numbers of animals using physical methods including captive bolt (nonpenetrative and penetrative), gunshot, electrocution, and manual blunt force trauma can be time consuming, labor intensive, and detrimental to personnel’s mental health. Other approved methods such as anesthetic overdose, carbon dioxide stunning or movement to slaughter have the potential to be less emotionally intense but can be difficult to implement due to logistic bottlenecks caused by temporary transport restrictions or shortage of local supplies [4, 5] or limitations on carcass disposal (in the case of anesthetic overdose). Furthermore, ventilation shutdown of ventilation shutdown plus (VSD+) have been approved since 2015 by the AVMA to be used under constrained circumstances such as during infectious disease outbreaks or supply chain breakdowns during the recent SARS-Cov-2 pandemic, when slaughter or humane euthanasia was not deemed possible [5]. However, although the use of VSD/VSD+ may facilitate large-scale depopulation events and reduce workforce pressure, the methodological approach of VSD/VSD+ has raised animal welfare concerns due to the conditions and time until induced death [6–12]. The second depopulation method listed in AVMA guidelines for depopulation is the use of sodium nitrate (NaNO₂) [4]. The administration of sodium nitrate induces methemoglobinemia due to the oxidation of ferrous ion (Fe²⁺) to ferric ion (Fe³⁺) in hemoglobin inflicting a reduction in the oxygen-carrying capacity in red blood cells leading to tissue hypoxia and death at lethal concentrations [13, 14]. The time to death after a lethal dose of NaNO₂ in baited feral pigs have been reported to be between 120–180 minutes [13, 15] but shorter (17–101 minutes) during controlled trials using up to 3 times the lethal dose [14]. To date, NaNO₂ has yet to be used for mass depopulation of pigs and additional research is needed to determine its efficacy during large scale implementation as well as associated welfare concerns due to the prolonged time to death.

A promising depopulation alternative for swine is the use of water-based foam (WBF), commonly used for depopulation of poultry in emergency circumstances [16]. The use of foam agents for depopulation of swine has not been investigated extensively, but the use of high expansion nitrogen gas-filled foam has recently been reported to be suitable for pigs [17, 18]. In addition, recent studies found WBF to be equally efficient in inducing cessation of movement and subsequent death in cull sows as CO₂ or compressed nitrogen foam (CAFN₂) [19], and that WBF could be a suitable and reliable depopulation method for pigs of different ages [20, 21]. From a personnel perspective, a possible benefit from using WBF is the reduction of both visual and handling elements during depopulation, which may help mitigate the risk of short- and long-term trauma especially during an extended depopulation scenario. Furthermore, details on the depopulation methods and plausible factors to the traumatic perceptions have not been well described, preventing a comprehensive understanding of which specific parts of the intense experience are responsible for causing the trauma. This information, if collected in a timely manner, could help justify depopulation method selection and facilitate timely interventions to prevent mental disorders in depopulation personnel.

The aim of this study was to assess the perception of swine industry stakeholders on the use of WBF in swine prior and post observation of the depopulation process in situ using a modified rendering trailer. The focus was on describing perceptions of methodology speed, likelihood of field success, swine welfare, and potential psychological and emotional impact of personnel performing the depopulation method. We hypothesized that stakeholders would perceive WBF as a better alternative for depopulation in terms of effectiveness, efficiency, and animal welfare, compared to existing approved methods following a direct observation of the process in situ. In addition, the study aimed to describe short-term psychological/emotional impacts to stakeholders after observing the WBF depopulation process.

Materials and methods

Statistical analysis

Surveys were manually entered into an Excel database (Microsoft Corp^®, Redmond, WA). Descriptive analysis was performed to describe demographics, including professional role and years of service in the swine industry. The frequency and percentage of responses were reported among categories for nominal questions, while numeric responses were summarized as means with standard deviations (SD). Where a range of numbers was provided, e.g., 30–50% of pigs, the upper bound of the ranges was used for analysis. Responses to multiple choice questions paired in PRE-Q and POST-Q (e.g., ensuring efficient depopulation, stress of animal loading, number of escape attempts) were compared using cumulative link mixed models (i.e., effects of the observation on stakeholders’ responses). Models were constructed by using the ordinal responses to questions paired in PRE-Q and POST-Q (Table 1) as the outcomes, observation status (pre/post) and trial (1/2) as fixed effects, and survey ID (anonymous participant identifier) as a random effect. Stakeholders’ PRE-Q predictions and POST-Q estimates of time to trailer fill, time to hearing the last animal movement, and percentage of unconscious animals were compared using a non-parametric paired Wilcoxon signed-rank test. Post-Q estimates were further compared with the exact average time to fill the trailer and to the animals’ cessation of movements using the one-sample Wilcoxon signed-rank test. In addition, the association between participants’ observation locations and their post-observation responses (Table 1) was investigated using a non-parametric Kruskal-Wallis one-way analysis of variance (ANOVA) for numerical predictions/estimates (e.g., time to trailer fill, time to last animal movement) and Fisher’s Exact Test for ordinal responses (e.g., ensuring efficient depopulation, number of escape attempts). Responses to the short-term impact assessment (FOLLOW-Q) were descriptively analyzed. Statistical significance was declared at P < 0.05; and all analysis and graphs were conducted using R 4.0.4 [25].

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Table 1. Swine industry stakeholders’ perception regarding logistic, speed, efficiency, and animal welfare of swine depopulation using the water-based foam before and after observing two field trials.

https://doi.org/10.1371/journal.pone.0290400.t001

Results

For Trial 1, the mean (±standard deviation) time (in mm:ss) to fill the trailer with WBF was 01:23 ± 00:12 and with the time to cessation of pig movements 02:11 ± 00:35 [21]. For Trial 2, the average time to fill the trailer with WBF was 01:27 ± 01:12 and the time to the cessation of swine movement was 02:46 ± 00:42. Across two trials, the trailer was filled in approximately 01:25 and the animals stopped moving at approximately 02:29. Vocalization was not identified during neither trial.

Follow-up questionnaire (FOLLOW-Q)

Among 41 stakeholders that returned both PRE-Q and POST-Q, 15 responded to the FOLLOW-Q one-month post-trial (response rate: 38.5%). Overall, stakeholders experienced none to minor post-traumatic stress disorder-like (PTSD-like) symptoms from the WBF swine depopulation trials that they observed (Table 2). Two respondents reported “a little” for the frequency of repeated, disturbing memories, thoughts, or images from the depopulation trials, and one experienced being upset upon being reminded about the trails. In addition, one respondent reported having difficulty in concentration.

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Table 2. Short-term mental effects on participated swine industry stakeholders one month after observing two water-based foam swine depopulation trials.

https://doi.org/10.1371/journal.pone.0290400.t002

Discussion

This manuscript adds to the body of knowledge on an important topic in veterinary medicine; the personnel perceptions regarding a novel WBF depopulation method for emergency situations. Social impacts to personnel that actively participates in and/or observes mass depopulation events should not be overlooked [26, 27]. These refer to indirect health consequences at the individual, family, or community level that could involve a wide range of swine stakeholders such as veterinarians, farm owners and animal caretakers, and first responders. Prolonged exposure to euthanasia or depopulation practices is known to incur both mental and physical fatigue [26, 28, 29], which may also increase risks of injury for both personnel and swine during animal handling and restraint, application of the depopulation methods, or due to improper equipment operation [4, 30]. Detrimental psychological and emotional impacts have been reported in field personnel during the eradication events of Foot and Mouth Disease in The Netherlands, the United Kingdom, and Japan, as well as eradication of bovine spongiform encephalopathy in Canada [27, 31, 32]. Of note, most of these publications reflect either expert opinion or perceptions on a method’s impact on personnel well-being [33] or assessments of post-traumatic stress symptoms conducted several years after the disasters [27, 31, 32], instead of directly measuring the impact. Furthermore, details on the depopulation methods and plausible factors to the traumatic perceptions were not described, preventing a comprehensive understanding of which specific parts of the intense experience are responsible for causing the trauma. This information, if collected in a timely manner, could help justify depopulation method selection and facilitate timely interventions to prevent mental disorders in depopulation personnel.

Given the majority of respondents in our survey were educators, animal officials, and veterinarians, the moderate knowledge level and reference to the AVMA depopulation guidelines [4] was unexpected since they were likely trained by formal education programs and courses. This highlights the need for education on the existence of guidelines specifically for depopulation of animals. Such efforts have been conducted for euthanasia, so a similar model could be developed in future efforts [34–37].

After observing the trials, respondents became more optimistic in terms of efficiency and animal welfare of using the WBF for depopulation purposes when compared to existing approved methods, in contrast to their initial assessment. In addition, after observing the WBF trials, respondents perceived the logistics of moving and loading animals into the trailer to be more logistically efficient compared to logistics from currently approved depopulation methods. Respondents also became less concerned about potential additional stress to animals during the loading process compared to their initial expectations prior to observing the trials. Furthermore, respondents expected a higher number of animal escape attempts, animal vocalizations and a longer conscious time of potential suffering before death was induced, compared to their experience during the depopulation trial. In addition, the observed and reported time to trailer foam fill, cessation of vocalization, and cessation of movement were all significantly shorter than respondents’ pre-observation predictions. Although some participants reported concerns about resource accessibility for WBF depopulation when compared to captive bolt stunning and gunshot, respondents overall measured WBF as a better depopulation approach when it came to logistics, animal welfare, speed, personnel safety, and aesthetics.

Regarding personnel mental health, over 95% of respondents did not report common post-traumatic symptoms (irritation, distraction, and anxiety) after the observation, and less than half (42.1%) concerned WBF depopulation would weaken the mental fortitude of depopulation staff and caretakers. Minor short-term PTSD-like symptoms such as negative thoughts, flashback images, feeling upset and having difficulty concentrating were reported by four respondents. Performing animal euthanasia and depopulation can be a moral and ethical burden and introduce traumatic stress to practitioners and those involved with the activity [38, 39]. Symptoms of perpetration-induced traumatic stress, a consequence of actively participating in killing of healthy animals, including nightmares, intrusive memories, and avoidance, has been reported in farm caretakers that euthanized animals [29, 31, 40–42]. A recent study reported farm frontline culling workers (n = 200; 70.0% had worked with chicken, 53.0% with cows, 37.5% with pigs) suffered intensive guilt, distress, and irritation, and varied PTSD symptoms [43] that could be triggered by sights, sounds, and smells [44]. Although few respondents reported PTSD symptoms in this study, additional research is needed across a larger sample size and over a longer timeframe before any conclusive inferences regarding the impact of WBF on personnel can be drawn.

This study also comes with limitations. First, the findings of this study should be interpreted and generalized considering the small sample size and the fact that we took advantage of other on-going studies for this work. Although both trials were performed in May, animals and the depopulation process may be affected by the weather given two animal trials were performed at different locations with one year interval. In addition, since respondents were recruited on a voluntary basis, they may already be interested and willingly to observe the depopulation trials prior to the recruitment and could be more resilient to consequential negative perceptions. Furthermore, study results may also have limited extrapolation to different personnel populations given the limited inclusion of on-farm personnel (e.g., farm owner, farm staff/caretaker, truck driver). Although the top three recruited stakeholders (educator/researchers, animal health officials, veterinarians) will be involved in animal depopulation events, they are likely to play a role as a supervisor rather than practitioner. Farm personnel, on the other hand, may not have the opportunity to refrain from the depopulation process under urgent circumstances and may be more likely to develop aversive attitudes. The follow-up questionnaire response rate of 38.5% was low on an already limited sample size, but in line with previous findings on average response rates (34% - 41%) for online surveys/questionnaires [45–47]. Thus, future studies should aim for larger sample sizes and to investigate the perspective of farm personnel, and focus on describing and exploring both short- and long-term psychological impacts of WBF and to evaluate mental health using additional validated PTSD assessment instruments (e.g., 30-item Clinician-Administered PTSD Scale) [48]. They should also attempt to obtain qualitative data, for example using semi-structured interviews, which would likely provide richer and more detailed feedback. Nevertheless, this study provides an overall supportive sentiment for the field application of WBF depopulation from swine industry stakeholders and limited short-term personnel mental health implications.

Supporting information

Acknowledgments