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International Journal of Environmental Research and Public Health 17 (24): 9196 (2020)
Andrukonis, Allison
Hall, Nathaniel J
Protopopova, Alexandra
Animal shelter employees are in a unique position where they care for, and later kill, the same animals. The aim of our exploratory study was to assess whether “caring” and/or “killing” evokes physiological and psychometric indicators of stress in employees. Experiment 1 compared three careers that kill regularly, but involve varying degrees of husbandry (n = 28). Blood pressure (BP), salivary cortisol, heart rate (HR), and heart rate variability (HRV) were collected; data showed higher HR and lower HRV during the process of killing. Psychometric scales showed that burnout and Impact Event Scale-Revised (IES-R) scores were higher in careers with higher contact with animals. Experiment 2 compared three careers that involve husbandry, but varying exposure to killing (n = 41). BP, cortisol awakening response, HR, and HRV were measured as well as Professional Quality of Life Scale, IES-R, and Moral Injury Event Scale were administered. There were no significant differences across careers in any measures. The data suggest that the process of killing may be physiologically stressful to the person, and higher levels of animal contact in a euthanasia context may be associated with burnout and traumatic stress, but that the act of euthanasia is not a unique predictor of overall occupational distress.
International Journal ofEnvironmental Researchand Public HealthArticleThe Impact of Caring and Killing on Physiological andPsychometric Measures of Stress in Animal ShelterEmployees: A Pilot StudyAllison Andrukonis 1,*, Nathaniel J Hall 1 and Alexandra Protopopova 21 Department of Animal and Food Sciences, Texas Tech University, Lubbock, TX 79409, USA;Nathaniel.J.Hall@ttu.edu2 Department of Land and Food Systems, University of British Columbia, Vancouver, BC V6T 1Z4, Canada;a.protopopova@ubc.ca* Correspondence: allison.andrukonis@ttu.eduReceived: 10 November 2020; Accepted: 3 December 2020; Published: 9 December 2020Abstract: Animal shelter employees are in a unique position where they care for, and later kill, thesame animals. The aim of our exploratory study was to assess whether “caring” and/or “killing”evokes physiological and psychometric indicators of stress in employees. Experiment 1 comparedthree careers that kill regularly, but involve varying degrees of husbandry (n = 28). Blood pressure(BP), salivary cortisol, heart rate (HR), and heart rate variability (HRV) were collected; data showedhigher HR and lower HRV during the process of killing. Psychometric scales showed that burnout andImpact Event Scale-Revised (IES-R) scores were higher in careers with higher contact with animals.Experiment 2 compared three careers that involve husbandry, but varying exposure to killing (n = 41).BP, cortisol awakening response, HR, and HRV were measured as well as Professional Quality of LifeScale, IES-R, and Moral Injury Event Scale were administered. There were no significant differencesacross careers in any measures. The data suggest that the process of killing may be physiologicallystressful to the person, and higher levels of animal contact in a euthanasia context may be associatedwith burnout and traumatic stress, but that the act of euthanasia is not a unique predictor of overalloccupational distress.Keywords: animal-care employees; animal shelter; compassion fatigue; occupational stress1. IntroductionAnimal shelter employees euthanize approximately 1.5 million animals annually [1]. While someof the animals have significant health problems that may warrant a humane death, others are physicallyand behaviorally healthy. Animal shelter employees are in a unique position where they must providehusbandry for and subsequently euthanize the animals in their care. Arnold Arluke coined thephrase caring–killing paradox to highlight this specific challenge of caring for and later killing, in theanimal shelter environment [2]. A recent study suggested that annual incidence of Post-TraumaticStress Disorder (PTSD) in animal shelter employees is five times higher than the national average [3].Along with PTSD, animal shelter employees often suffer from secondary traumatic stress (STS) [4].STS is the reaction occurring in caregivers resulting from prolonged exposure to the stress associatedwith helping or wanting to help traumatized or suffering victims and differs from PTSD only in actualexposure to trauma [5,6].Occupational stress is thought to be an important contributor to animal control officers, along withothers in protective service occupations (e.g., police officers), having the highest workplace suiciderate, excluding military personnel, at 5.3 per 1 million people [7]. One hypothesized cause for such aInt. J. Environ. Res. Public Health 2020, 17, 9196; doi:10.3390/ijerph17249196 www.mdpi.com/journal/ijerphInt. J. Environ. Res. Public Health 2020, 17, 9196 2 of 18high suicide rate in animal control workers is the caring–killing paradox [8]. Animal shelter employeesprimarily enter the job because of their love of animals [9]. However, the reality of their job is oftenmore bleak than expected [10]. The contradiction between job expectations and the reality of having tokill can lead to moral stress [11,12]. Moral stress occurs when a person engages in, bears witness to,fails to prevent, or learns about acts that transgress that individual’s moral code [13]. Moral stress canlead to moral injury when that individual is unable to contextualize the experience and fit the actionsinto a pre-existing moral schema [13]. In the first empirical evaluation of moral injury in animal shelteremployees, Andrukonis and Protopopova (2020) found that moral injury was likely present in animalshelter employees and was significantly higher in individuals who euthanize. Further, Reeve andcolleagues (2005) found that animal shelter employees directly involved in euthanasia reportedsignificantly higher levels of work stress, stress-related somatic complaints, and lower levels of worksatisfaction compared to animal shelter employees not involved in euthanasia. This supports theargument that actual killing is an important precursor of occupational stress in animal-care employees.Participation in euthanasia activities has also been associated with higher incidence ofburnout [10,14–16]. In a 2015 survey of animal shelter managers, Anderson et al. found thatnearly 75% of managers strongly believed that participating in euthanasia activities contributedto burnout. While common in animal shelter employees, burnout has been reported in a varietyof animal-care careers [15,17–20]. Burnout, defined by three dimensions: exhaustion, cynicism,and inefficacy, is the result of chronic emotional and interpersonal stressors [21]. The reported highincidence of burnout in animal-care employees is not surprising given the emotional pull related toboth caring for and killing animals [22–24].Exposure to euthanasia has also been correlated with higher incidence of compassionfatigue [8,15,25]. Compassion fatigue was originally thought of as a unique form of burnout experiencedexclusively in caring professions [26]. While compassion fatigue has been conceptualized in thehuman-care professions, animal-care professions have been left out [27]. For the purpose of thispaper, we will refer to compassion fatigue as a state of emotional dysregulation, comprising secondarytraumatic stress and burnout, that negatively influences individuals in caring professions [28,29].Compassion satisfaction, or the gratification one gets from their work helping others, has beensuggested to be a protective factor against developing compassion fatigue, burnout, and secondarytraumatic stress [29–31]. Higher compassion satisfaction in animal-care workers has been correlatedwith increased human–animal interactions at work [17]. This suggests that providing care for animalsmay be a protective factor.However, research in veterinarians has found that knowing the animal prior to euthanasia makesthe process more stressful and that the degree of attachment to the animal may be an importantantecedent of euthanasia-related stress [32]. This contradicts the protective nature of caring andsuggests that animal shelter employees involved in animal care may experience higher levels ofeuthanasia-associated stress. There has been little research focused on whether providing care foran animal that later faces euthanasia increases the risk of negative occupational outcomes—perhapsbecause it is assumed that all animal-care work involves husbandry and, therefore, attachment toanimals is inevitable [33]. In fact, Arluke found that animal shelter employees could not conceive thenotion of not developing attachments to the animals in their care and that shelter employees foundthose attachments to be an important part of the job [33].There are several physiological measures indicative of occupational stress, such as heart rate,heart rate variability, blood pressure, and cortisol [34–36]. During a stressful event, two systems aretriggered: the autonomic nervous system and the hypothalamic-pituitary-adrenal (HPA) axis [37].Heart rate variability (HRV) has been used as a measure of the autonomic nervous system duringpsychoemotional stress [38]. Defined as the beat-to-beat variation in heart rate, lower HRV has beenassociated with stress and PTSD [39,40]. The activation of the sympathetic nervous system leads to therelease of epinephrine, which increases heart rate (HR) and blood pressure (BP). Following a stressor,the hypothalamus releases corticotropin-releasing hormone (CRH) [41]. CRH then stimulates theInt. J. Environ. Res. Public Health 2020, 17, 9196 3 of 18pituitary gland to release adrenocorticotropic hormone (ACTH), which then moves to adrenal glands,stimulating the release of cortisol. Increased cortisol levels have been associated with burnout [42].Interestingly, lower cortisol levels at the time of trauma have been shown to predict the developmentof PTSD after 6 weeks and 6 months [43].The aim of the current two-part exploratory study was to evaluate whether both caring for andkilling animals are necessary for the expression of physiological and psychometric indicators of stressin animal-care employees. We expected both the husbandry (Experiment 1) and killing (Experiment 2)aspects of animal-care work to be significant in eliciting physiological indicators of stress and developingburnout, secondary traumatic stress, and moral injury. Using both a quasi-experimental group andwithin-subject design, physiological and psychometric data were collected on animal-care professionswith (1) varying degrees of “caring” or husbandry duties: animal shelter employees, veterinarians,and university personnel who harvest livestock; and (2) exposure to killing: animal shelter employeeswho euthanize frequently, animal shelter employees who do not euthanize, and pet hotel employees.We hypothesized that PTSD indicators, burnout, secondary traumatic stress, and moral injury would behighest in animal shelter employees who euthanize regularly. We also hypothesized that compassionsatisfaction would be lowest in animal shelter employees who euthanize regularly. We expected to seea decrease in HRV during killing and an increase in BP following killing. We also expected to see thegreatest decrease in salivary cortisol in university personnel who harvest livestock.2. Materials and MethodsThe purposes of Experiment 1 and Experiment 2 were to evaluate “caring” (i.e., husbandry)and “killing” as predictors of physiological and psychological stress. Institutional Review Boardapproval was obtained from Texas Tech University (IRB2016-1014) for both experiments.2.1. Experiment 12.1.1. ParticipantsA convenience sample of sixteen animal shelter employees who currently euthanize,four veterinarians who euthanize, and eight university personnel who harvest livestock were selectedfrom across the United States (total n = 28). Participants were selected for their varying involvement inhusbandry tasks. Animal shelter employees see and interact with individual animals daily, veterinarianssee individual animals a few times per year but see them for many years, and university personnelwho harvest livestock typically do not have any involvement with the animals outside of harvest.See Table 1 for a breakdown of demographic information. Missing demographic information wasdue to omissions by the participants. Seventeen men and eleven women participated in Experiment1. Participants were contacted through their place of work and asked if they would be willing toparticipate in a study on occupational stress. All animal shelter employees and veterinarians wereworking in Texas, United States. Due to limited availability of universities that harvest livestock,university personnel were recruited from three states within the United States.Table 1. Shows the demographic information for Experiment 1.Animal Shelter Veterinarian University Employee Who HarvestsGenderMale 9 2 6Female 7 2 2No response 0 0 0Int. J. Environ. Res. Public Health 2020, 17, 9196 4 of 18Table 1. Cont.Animal Shelter Veterinarian University Employee Who HarvestsAge<20 0 0 020–40 10 2 840–60 6 1 060+ 0 1 0No response 0 0 0SmokeYes 4 0 0No 12 2 8No response 0 2 0SpiritualYes 14 4 8No 2 0 0No response 0 0 0MarriedYes 8 4 1No 8 0 7No response 0 0 0Pets at homeYes 15 3 5No 1 0 3No response 0 1 0Contact with animalsNone 0 0 5Not much 3 0 3Some 0 0 0Moderate 1 0 0A lot 12 2 0No response 0 2 0Months on the jobRange: 3–312 12–60 12–216Mean: 96.81 36.00 70.50Median: 84 36 42No response 0 2 0Total euthanized/harvested:<100 0 0 3100–1000 4 2 31001–10,000 6 0 210,001–100,000 3 0 0>100,000 1 0 0No response 2 2 0Frequency of euthanasia/harvest:Never 0 0 0<1/month 0 0 21/month 0 0 12/month 0 1 21/week 2 0 32/week 1 0 0>3/week 4 0 0Daily 8 0 0No response 1 3 0Int. J. Environ. Res. Public Health 2020, 17, 9196 5 of 18Table 1. Cont.Animal Shelter Veterinarian University Employee Who HarvestsEuthanized/harvested at a time:Range: 5–90 1 3–13Mean: 21.13 1.00 6.50Median: 15.5 1 6.5No response 0 3 02.1.2. General ProcedureFigure 1 is a visual representation of the procedure for Experiment 1. Participants were giventhe Polar H7 (Polar Polar Electro Oy, Kempele, Finland) band to put around their chest. Once theband was in place, the researcher would check the connection with the V800 watch and then startdata collection. Next, blood pressure and a saliva sample were taken. Then the euthanasia/harvestingbegan. Immediately following the euthanasia/harvest, the V800 watch was turned off and bloodpressure and a saliva sample were collected again. If time allowed, the participant then completed thesurveys and answered the additional questionnaire. Researchers attempted to make data collection asunobtrusive as possible, so if necessary, the participant was able to answer the surveys and questionslater in their shift.Int. J. Environ. Res. Public Health 2020, 17, x 5 of 18 2.1.2. General Procedure Figure 1 is a visual representation of the procedure for Experiment 1. Participants were given the Polar H7 (Polar Polar Electro Oy, Kempele, Finland) band to put around their chest. Once the band was in place, the researcher would check the connection with the V800 watch and then start data collection. Next, blood pressure and a saliva sample were taken. Then the euthanasia/harvesting began. Immediately following the euthanasia/harvest, the V800 watch was turned off and blood pressure and a s liva sample were coll cted again. If tim llowed, the participant then completed the surveys and answered the additional questionnaire. Researchers attempted to make data collection as unobtrusive as possible, so if necessary, the participant w s able to answer the surveys and questions later in their shift. Figure 1. shows a visual representation of methods for Experiment 1. BP: blood pressure; HRV: heart rate variability. 2.1.3. Physiological Measures Heart rate variability (HRV) was collected throughout euthanasia/harvest using Polar V800 and H7. Participants were instructed to get the sensors of the H7 band damp using water from the sink and then strap the band around their chest, with the sensor positioned just below their sternum. The author (AA) confirmed that there was skin-to-sensor contact and that the band was positioned properly. Correct location was confirmed by initiating the R-R testing function (interval between heart beats) on the polar watch. Once the V800 watch successfully connected with the H7 band, HRV data collection began. The duration of the euthanasia/harvest varied by participant, depending on the number of animals killed (range: 26 min to 8.6 h, mean: 2.6 h). There are a variety of time domain HRV calculations. SDNN, or the standard deviation of NN intervals, is the most common way to analyze HRV in 24 h frames [44]. NN intervals are the interbeat intervals from which artifacts have been removed [45]. However, it is not good for short-term (~5 min intervals) evaluation [45]. rMSSD, or the root-mean-square of successive differences of NN intervals, and pNN50, or the percentage of adjacent NN intervals that differ from each other by more than 50 ms, are common short-term HRV measures [45] and were therefore used for data analysis in this study. Both rMSSD and pNN50 are also controlled by the parasympathetic nervous system [45,46]. On a day when participants were not actively euthanizing or harvesting, they wore the heart rate monitor for the same amount of time as they did for the euthanasia/harvest. Due to the varying durations for euthanasia/harvest, the duration of the control period varied equivalently. Blood Pressure (BP) was measured by a trained researcher (AA) pre- and post- euthanasia/harvest using an ADC 760 sphygmomanometer (American Diagnostic Corporation, Hauppauge, NY, USA) and 3M Littmann 5870 Classic III stethoscope (Littmann, St. Paul, MN , USA). The researcher followed the BP measuring protocol described in the Guyton and Hall Textbook of Medical Terminology [47]. Due to organizational policies and the sensitive nature of the work, the Pre-euthanasia/Harvest-Sign consent-BP collected-Salivary cortisol collectedEuthanasia/ Harvest-HRV collectedPost-euthanasia/Harvest-BP collected-Salivary cortisol collected-Scales and additional questions Active Day- Euthanasia/harvestBase day- No euthanasia/harvestNormal workday-HRV collectedFigure 1. Shows a visual representation of methods for Experiment 1. BP: blood pressure;HRV: heart rate variability.2.1.3. Physiological MeasuresHeart rate variability (HRV) was collected throughout euthanasia/harvest using Polar V800 andH7. Participants were instructed to get the sensors of the H7 band damp using water from the sinkand then strap the band around their chest, with the sensor positioned just below their sternum.The author (AA) confirmed that there was skin-to-sensor contact and that the band was positionedproperly. Correct location was confirmed by initiating the R-R testing function (interval between heartbeats) on the polar watch. Once the V800 watch successfully connected with the H7 band, HRV datacollection began. The duration of the euthanasia/harvest varied by participant, depending on thenumber of animals killed (range: 26 min to 8.6 h, mean: 2.6 h). There are a variety of time domain HRVcalculations. SDNN, or the standard deviation of NN intervals, is the most common way to analyzeHRV in 24 h frames [44]. NN intervals are the interbeat intervals from which artifacts have beenInt. J. Environ. Res. Public Health 2020, 17, 9196 6 of 18removed [45]. However, it is not good for short-term (~5 min intervals) evaluation [45]. rMSSD, or theroot-mean-square of successive differences of NN intervals, and pNN50, or the percentage of adjacentNN intervals that differ from each other by more than 50 ms, are common short-term HRV measures [45]and were therefore used for data analysis in this study. Both rMSSD and pNN50 are also controlled bythe parasympathetic nervous system [45,46].On a day when participants were not actively euthanizing or harvesting, they wore the heartrate monitor for the same amount of time as they did for the euthanasia/harvest. Due to the varyingdurations for euthanasia/harvest, the duration of the control period varied equivalently.Blood Pressure (BP) was measured by a trained researcher (AA) pre- and post- euthanasia/harvestusing an ADC 760 sphygmomanometer (American Diagnostic Corporation, Hauppauge, NY, USA)and 3M Littmann 5870 Classic III stethoscope (Littmann, St. Paul, MN, USA). The researcher followedthe BP measuring protocol described in the Guyton and Hall Textbook of Medical Terminology [47].Due to organizational policies and the sensitive nature of the work, the researcher (AA) was not alwayspresent for the euthanasia/slaughter. Therefore, the time between killing and the post-blood pressurereading was variable.Saliva samples were collected pre- and post-euthanasia/slaughter using the Salimetrics ChildSwabs (Salimetrics, State College, PA, USA) to be assayed for salivary cortisol. The Salimetricsprotocol [48] was followed. Due to the variation in time of day of euthanasia/harvest, the change insalivary cortisol across jobs was dropped from the analysis [49]. Individual changes in salivary cortisolwere included in the analysis.2.1.4. Psychometric ScalesImpact of Event Scale-Revised (IES-R) [50]: This 22-item scale is an indicator of Post-TraumaticStress Disorder (PTSD). Respondents are asked to think about the past seven days, with respect to atraumatic experience, and indicate how much on a scale of 0 (not at all) to 4 (extremely) they havebeen distressed by certain difficulties. For Experiment 1, participants were asked to think about aparticularly difficult euthanasia or harvest when answering the questions to focus on job-relatedtrauma. Possible scores on this scale range from 0 to 88. A score of 24 or more indicates that PTSDis a clinical concern, and a score of 33 and above indicates the best probable cutoff for a diagnosis ofPTSD [50,51]. The Cronbach’s alpha for this experiment was 0.94.Professional Quality of Life Scale (ProQOL) [52]: This 30-item scale consists of three subscales:compassion satisfaction—the enjoyment one gains from helping others through their work,burnout—the feeling that one’s work is no longer making a difference, and secondary traumaticstress—trauma experienced through someone or something else [29]. Compassion fatigue has beenreferred to as the combination of burnout and secondary traumatic stress [29]. Each subscale consistsof 10 questions which ask respondents to indicate how often they feel a certain way or exhibit certainbehaviors on a scale from 1 (Never) to 5 (Very often). Scores on each of the subscales range from 10 to50. The Cronbach’s alpha for compassion satisfaction, burnout, and secondary traumatic stress in thisstudy was 0.84, 0.75, and 0.85, respectively.2.1.5. Additional QuestionsParticipants were asked the 11 questions regarding work and euthanasia/harvest history, marriage,spirituality, and pets at home by the researcher (AA).2.2. Experiment 2The purpose of Experiment 2 was to evaluate whether physically participating in killing isnecessary to see a decline in occupational health in animal-care employees. Previous researchsuggested that moral injury was higher in animal shelter employees who euthanize, so the MoralInjury Event Scale was added to this study [3].Int. J. Environ. Res. Public Health 2020, 17, 9196 7 of 182.2.1. ParticipantsA convenience sample of thirteen animal shelter employees who regularly euthanize,thirteen animal shelter employees who do not regularly euthanize, and fifteen pet hotel employeeswere selected (total n = 41). Participants were selected for their varying exposures to euthanasia.Euthanizing regularly was defined as at least once per week. Participants were contacted through theirplace of work. The thirteen animal shelter employees who euthanize regularly were recruited fromExperiment 1. All animal shelter employees were currently working in Texas animal shelters. The pethotel employees were currently working at a large pet hotel in Virginia. Experiment 2 included 20 menand 21 women. See Table 2 for a breakdown of the demographic information.Table 2. The demographic information for Experiment 2.Animal Shelter–Regular Euthanasia Animal Shelter–Irregular or No Euthanasia Pet HotelGenderMale 6 6 8Female 7 7 7No response 0 0 0Age<20 0 1 420–40 7 5 1040–60 6 4 060+ 0 3 1No response 0 0 0SmokeYes 3 1 7No 10 11 7No response 0 1 1SpiritualYes 12 11 10No 1 0 4No response 0 2 1MarriedYes 6 6 1No 7 5 13No response 0 2 1Pets at homeYes 13 11 10No 0 1 3No response 0 1 2Contact with animalsNone 0 0 0Not much 3 5 0Some 0 1 0Moderate 1 1 0A lot 9 5 15No response 0 0 1Months on the jobRange: 3–312 0.5–132 6–132Mean: 97.96 65.08 39.08Median: 84 48 24No response 0 0 12.2.2. Physiological MeasuresHeart rate variability was collected during an entire workday using Polar V800 and H7.Animal shelter employees who euthanize were recorded on a day when they were not euthanizing toInt. J. Environ. Res. Public Health 2020, 17, 9196 8 of 18reflect the other jobs’ lack of euthanasia. Average shift duration was 8 h, but ranged from 5 to 12 h.The V800 and H7 were fit and synched using the same method as Experiment 1. Blood Pressure wasmeasured at the beginning of the participant’s shift using the same method as in Experiment 1.Cortisol Awakening Response was measured using saliva samples collected first thing in themorning using the Salimetrics Child Swabs (Salimetrics) [53]. Cortisol awakening response is a reliableindicator of an individual’s adrenocortical activity and is subject to less variance than salivary cortisolsampled later in the day [54]. The night before, participants were sent home with a swab, a vial,an icepack, and an insulated envelope. They were instructed to follow the Salimetrics protocol [48].They were then told to put the swab in the tube and place the tube, along with the activated icepack,in the envelope and bring the entire package to work. The first author (AA) then met the participant atwork and collected the sample.2.2.3. Psychometric ScalesThe Impact of Event Scale-Revised (IES-R) and Professional Quality of Life Scale (ProQOL)were administered. Participants were instructed to think about their current job when answeringthe questions. The Cronbach’s alpha for IES-R for Experiment 2 was 0.94. The Cronbach’s alpha forcompassion satisfaction, burnout, and secondary traumatic stress for Experiment 2 were 0.87, 0.71,and 0.85, respectively.The Moral Injury Event Scale (MIES), originally formulated for military personnel in 2013, assessesthe impact of moral stress in both personal offenses and perceived betrayals [55]. A higher score onthe MIES indicates lower moral injury. This scale has also been used in animal shelter employees todetect moral injury [3]. Questions 7–9 were adapted to reflect animal shelter and pet hotel employees.Question 7 originally read “I feel betrayed by leaders who I once trusted” and was changed to “I feelbetrayed by superiors who I once trusted” for both animal shelter and pet hotel employees. Question8 originally read “I feel betrayed by fellow service members who I once trusted” and was changedto “I feel betrayed by fellow employees who I once trusted” for both animal shelter and pet hotelemployees. Question 9 originally read “I feel betrayed by others outside the U.S. military who I oncetrusted” and was changed to “I feel betrayed by others outside the animal shelter who I once trusted”and “I feel betrayed by others outside the pet hotel who I once trusted” for animal shelter and pet hotelemployees, respectively. The Cronbach’s alpha for the nine-item, adapted, scale in this study was 0.86.Participants were instructed to think about their job at animal services / pet hotel when answeringthe scale.2.2.4. Additional QuestionsMethods were the same as in Experiment 1.2.2.5. Data AnalysisTable 3 presents the averages of the psychometric measures across jobs for Experiments 1 and 2.Analyses were performed using R (R Core Team, Vienna, Austria, 2016). HRV data were analyzedusing RHRV [56]. A principle component analysis (PCA) was run on the physiological measuresin both Experiments 1 and 2. Due to the small amount of variance explained by the componentsin Experiment 1, each variable was analyzed separately. In Experiment 2, 71% of the variance wasexplained by two components. PC1 showed highest loadings (loadings > 0.3) for heart rate variabilitymeasures: rMSSD and pNN50, heart rate, and waking salivary cortisol. PC2 showed highest loadingsfor systolic and diastolic blood pressure. The premise of Experiment 1 was to test the impact ofproviding husbandry on occupational stress; therefore, contact with animals was used as the mainindependent variable. Linear regression models were run on each of the dependent variables bycontact with animals, controlling for gender, age, smoking, marriage, spirituality, pet ownership,job, months on the job, total euthanasia, average number of euthanasias per session, and frequencyof euthanasia. Each model was reduced through nest model comparison using the F test in R [57].Int. J. Environ. Res. Public Health 2020, 17, 9196 9 of 18The variables remaining in the model are reported in Table 4. Paired t-tests were run on pre- versuspost-euthanasia for blood pressure, heart rate, and saliva as well as on base versus active average heartrate, pNN50, rMSSD. In Experiment 2, linear regression models were run on each of the dependentvariables by job, controlling for gender, age, smoking, marriage, spirituality, pet ownership, job,contact with animals, and months on the job. Each model was reduced similarly to Experiment 1.The variables retained variables are reported in Table 5.Table 3. The averages of the psychometric measures across jobs for Experiments 1 and 2.Impact of Event Scale Scores Compassion Satisfaction Burnout Secondary Traumatic Stress Moral Injury *Experiment 1Animal shelterMean 26.88 37.94 27.06 23.75SE 4.36 1.23 1.40 1.73Range 5:61 30:47 18:37 13:38University employee who harvests livestockMean 9.38 42.00 19.75 17.25SE 3.86 2.15 1.62 1.63Range 0:35 33:50 13:27 13:27VeterinarianMean 11.00 38.50 21.50 22.50SE 4.60 2.25 2.10 1.32Range 0:20 32:42 17:27 20:26Experiment 2Pet hotelMean 18.14 38.07 23.00 20.50 35.86SE 3.60 2.12 1.48 1.11 2.68Range 0:46 25:50 10:32 16:29 18:50Animal shelter: irregular euthanasiaMean 21.54 39.85 23.54 22.69 36.69SE 5.39 1.62 1.60 2.15 2.63Range 0:56 31:50 13:34 10:37 20:54Animal shelter: regular euthanasiaMean 23.69 37.77 27.00 23.15 38.77SE 4.49 1.26 1.36 1.95 3.10Range 5:61 30:47 21:36 13:38 22:54* Note. Higher moral injury scores indicate lower moral injury.Table 4. Shows the reduced linear model output for Experiment 1.Variable Df Sum Sq Mean Sq Estimate Std. Error F Value Pr(>F) SignificanceBurnout–reduced modelContact withanimals 1 130.72 130.72 −1.70 0.75 12.41 0.00 *Gender 1 70.13 70.13 −3.92 1.54 6.66 0.02 *Age 1 24.03 24.03 5.34 2.06 2.28 0.15Married 1 74.73 74.73 −8.741 1.98 7.09 0.02 ***Spiritual 1 262.16 262.16 −9.20 2.90 24.88 0.00 **Job 2 162.18 81.09 −15.22 3.27 7.70 0.00 ***Pets 1 76.34 76.34 −6.25 2.32 7.25 0.02 **Residuals 17 179.1 10.54 NA NA NA NACompassion satisfaction–reduced modelMarried 1 28.02 28.02 5.76 2.03 1.54 0.23Job 2 143.05 71.52 8.60 2.26 3.92 0.04 *Pets 1 148.00 148.00 7.61 2.67 8.11 0.01 **Residuals 22 401.61 18.26 NA NA NA NASecondary traumatic stress–reduced modelTotaleuthanasias/harvestperformed1 183.69 183.69 2.78 1.10 6.37 0.02 *Residuals 22 634.14 28.83 NA NA NA NAInt. J. Environ. Res. Public Health 2020, 17, 9196 10 of 18Table 4. Cont.Variable Df Sum Sq Mean Sq Estimate Std. Error F Value Pr(>F) SignificanceImpact of event scale score–reduced modelContact withanimals 1 1164.74 1164.74 6.00 1.53 10.01 0.01 **Age 1 21.28 21.28 −17.72 8.10 0.18 0.67Smoke 1 73.43 73.43 17.10 7.47 0.63 0.44Married 1 707.38 707.38 −19.21 5.51 6.08 0.02 *Spiritual 1 123.19 123.19 27.66 12.11 1.06 0.32Months on the job 1 1490.95 1490.95 0.14 0.04 12.82 0.00 **Average numberof euthanasias persession1 1548.92 1548.92 0.65 0.18 13.32 0.00 **Residuals 18 2093.99 116.33 NA NA NA NAChange in heart rate–reduced modelJob 2 2716.61 1358.30 27.76 5.09 12.54 0.00 ***Pets 1 594.83 594.83 14.60 6.23 5.49 0.03 *Residuals 17 1842.20 108.37 NA NA NA NAChange in systolic pressure–reduced modelMarried 1 303.60 303.60 6.06 2.51 8.54 0.01 **Average numberof euthanasias persession1 245.93 245.93 0.18 0.07 6.92 0.02 *Residuals 21 746.43 35.54 NA NA NA NAChange in diastolic pressure–reduced modelPets 1 330.98 330.98 −11.20 4.80 5.43 0.03 *Residuals 23 1401.26 60.92 NA NA NA NADifference in pNN50–reduced modelJob 2 322.17 161.09 −10.31 3.16 3.84 0.04 **Pets 1 442.55 442.55 −12.59 3.88 10.56 0.01 **Residuals 17 712.77 41.93 NA NA NA NANote: * p < 0.05, ** p < 0.01, *** p < 0.001.Table 5. Shows the reduced linear model output for Experiment 2.Variable Df Sum Sq Mean Sq Estimate Std. Error F Value Pr(>F) SignificanceCompassion satisfaction–reduced modelGender 1 214.520 214.52 5.28 1.75 9.70 0.01 **Married 1 122.800 122.80 4.72 1.89 5.55 0.03 *Pets 1 163.990 163.99 −6.91 2.54 7.42 0.01 *Residuals 25 552.820 22.11 NA NA NA NANote: * p < 0.05, ** p < 0.01.3. Results3.1. Experiment 1Table 4 reports the output from the reduced linear models. See Table S1 for the output from all theoriginal and reduced linear models. In the reduced linear model predicting burnout, higher burnoutwas significantly associated with less contact with animals (F (1) = 12.408, p = 0.003), male gender(F (1) = 6.657, p = 0.019), not being married (F (1) = 7.093 p = 0.016), not being spiritual (F (1) = 24.884,p < 0.001), having pets at home (F (1) = 7.246, p = 0.015), and working in an animal shelter (F (2) = 7.246,p = 0.004). See Figures 2A and 3A for a visual representation of the differences in burnout across joband contact with animals, respectively. In the reduced linear model predicting compassion satisfaction,not working as an animal shelter employee (F (2) = 3.918, p = 0.035) and owning a pet (F (1) = 8.107,Int. J. Environ. Res. Public Health 2020, 17, 9196 11 of 18p = 0.009) were statistically significantly associated with higher compassion satisfaction. See Figure 3Bfor a visual representation of the differences in compassion satisfaction across jobs. In the reduced linearmodel predicting IES-R scores, greater contact with animals (F (1) = 10.012, p = 0.005), not being married(F (1) = 6.081 p = 0.024), months on the job (F (1) = 12.816, p = 0.002), and greater average number ofeuthanasias per session (F (1) = 13.315, p = 0.002) were statistically significantly associated with higherIES-R scores (more likely to have PTSD). See Figure 2B for a visual representation of the differences inIES-R across contact with animals. In the reduced linear model predicting the difference in pNN50between active euthanasia and work with euthanasia, working in an animal shelter (F (2) = 3.842,p = 0.042) and not owning a pet (F (1) = 10.555, p = 0.005) were statistically significantly associatedwith less decrease in pNN50. See Figure 3D for a visual representation of the differences in change inpNN50 across jobs. In the reduced linear model predicting secondary traumatic stress, greater totalslaughter/euthanasias performed (F (1) = 6.373, p = 0.019) was statistically significantly associatedwith higher secondary traumatic stress. In the reduced linear model predicting the change in HR,not working in an animal shelter (F (2) = 12.535, p < 0.001) and owning a pet (F (1) = 5.489, p = 0.0312)were statistically significantly associated with a greater change in HR. See Figure 3C for a visualrepresentation of the differences in change in HR across jobs. In the reduced linear model predictingthe change in diastolic blood pressure, not owning a pet (F (1) = 5.433, p = 0.029) was statisticallysignificantly associated with greater change in diastolic blood pressure. In the reduced linear modelpredicting change in systolic blood pressure, being married (F (1) = 8.542, p = 0.008) and greater averagenumber of euthanasias per session (F (1) = 6.919, p = 0.016) were statistically significantly associatedwith greater change in systolic blood pressure. There was no statistically significant association in thereduced model predicting the difference in rMSSD.Systolic blood pressure (t (25) = −2.309, p = 0.029) was statistically significantly higher followingeuthanasia. Salivary cortisol (t (25) = 2.826, p = 0.009) was statistically significantly higher prior toeuthanasia. There were no significant differences in heart rate or diastolic blood pressure. Averageheart rate (t (20) = 3.785, p = 0.001) was statistically significantly higher and pNN50 (t (20) = −3.171,p = 0.005) was lower during killing. There were no significant differences in rMSSD. See Figure 4 for avisual representation.Int. J. Environ. Res. Public Health 2020, 17, x 11 of 18 Figure 2. The significant differences in Burnout (A) and IES-R (B) by contact with animals. Possible burnout scores ranged from 10 to 50 and possible IES-R scores ranged from 0 to 88. Greater contact with animals predicted lower burnout (F (1) = 12.408, p = 0.003) and higher IES-R scores (F (1) = 10.012, p = 0.005). IES-R: Impact of Event Scale-Revised. Figure 3. The significant differences in Burnout (A), Compassion Satisfaction (B), Change in HR (C), and Difference in HRV (D) by job. Possible burnout and compassion satisfaction scores range from 10 to 50 points. Animal shelter employees had significantly higher burnout (F (2) = 7.246, p = 0.004), lower compassion satisfaction (F (2) = 3.918, p = 0.035), and less change in HR (F (2) = 12.535, p < 0.001), and less difference in HRV (F (2) = 3.842, p = 0.042). HR: heart rate. Systolic blood pressure (t (25) = −2.309, p = 0.029) was statistically significantly higher following euthanasia. Salivary cortisol (t (25) = 2.826, p = 0.009) was statistically significantly higher prior to euthanasia. There were no significant differences in heart rate or diastolic blood pressure. Average heart rate (t (20) = 3.785, p = 0.001) was statistically significantly higher and pNN50 (t (20) = −3.171, p = 0.005) was lower during killing. There were no significant differences in rMSSD. See Figure 4 for a visual representation. Figure 2. The significant differences in Burnout (A) and IES-R (B) by contact with animals.Possible burnout scores ranged from 10 to 50 and possible IES-R scores ranged from 0 to 88.Greater contact with animals predicted lower burnout (F (1) = 12.408, p = 0.003) and higher IES-R scores(F (1) = 10.012, p = 0.005). IES-R: Impact of Event Scale-Revised.Int. J. Environ. Res. Public Health 2020, 17, 9196 12 of 18Figure 3. The significant differences in Burnout (A), Compassion Satisfaction (B), Change in HR (C),and Difference in HRV (D) by job. Possible burnout and compassion satisfaction scores range from10 to 50 points. Animal shelter employees had significantly higher burnout (F (2) = 7.246, p = 0.004),lower compassion satisfaction (F (2) = 3.918, p = 0.035), and less change in HR (F (2) = 12.535, p < 0.001),and less difference in HRV (F (2) = 3.842, p = 0.042). HR: heart rate.Int. J. Environ. Res. Public Health 2020, 17, x 12 of 18 Figure 4. The difference in HR (A) and HRV (B,C) measures during Active (euthanizing) vs. base (non-euthanizing) days. Average heart rate (t (20) = 3.785, p = 0.001) was statistically significantly higher and pNN50 (t (20) = −3.171, p = 0.005) was lower during killing. There were no significant differences in rMSSD. 3.2. Experiment 2 Table 5 reports the output from all the linear models. Compassion satisfaction was the only dependent variable that remained significant following the model reduction. See Table S2 for the output from all the original and reduced linear models. In the reduced linear model predicting compassion satisfaction, female gender (F (1) = 9.701, p = 0.005), being married (F (1) = 5.553, p = 0.027), and not owning a pet (F (1) = 7.416, p = 0.012) were statistically significantly associated with a higher score. Contrary to our hypothesis, there were no statistically significant associations in the reduced models predicting burnout, moral injury, IES-R scores, secondary traumatic stress, PC1, and PC2 by job. 4. Discussion 4.1. Experiment 1 A greater change in HR and less of a decrease in HRV (pNN50) was significantly related to not working in an animal shelter. HR was significantly higher and pNN50 was significantly lower on killing days compared to a non-killing days across jobs. Increased heart rate is associated with decreased HRV and indicates arousal, and both are often associated with emotional stress [58–61]. This suggests that killing, no matter the contact with animals prior, may be emotionally stressful. Interestingly, HRV hyporeactivity has been used as an indicator of both depression [62] and PTSD [63]. HRV biofeedback training has been successfully implemented as a treatment for individuals with anxiety, depression, and PTSD [64–66]. A study using biofeedback training as a predeployment protocol found that participants with the biofeedback training experienced less arousal during postdeployment combat situations [67]. This indicates that it may be beneficial for animal-care organizations that engage in killing to incorporate biofeedback training into protocols to decrease the arousal associated with killing. The statistically significant decrease in salivary cortisol levels between pre- and post-euthanasia/slaughter can be explained by the diurnal nature of salivary cortisol levels [49]. It should be noted that time of day was not controlled for; all harvesting began prior to 9:00 a.m., whereas the majority of animal shelter and veterinary euthanasia occurred in the afternoon and evening. Cortisol Figure 4. The difference in HR (A) and HRV (B,C) measures during Active (euthanizing)vs. base (non-euthanizing) days. Average heart rate (t (20) = 3.785, p = 0.001) was statisticallysignificantly higher and pNN50 (t (20) = −3.171, p = 0.005) was lower during killing. There were nosignificant differences in rMSSD.Int. J. Environ. Res. Public Health 2020, 17, 9196 13 of 183.2. Experiment 2Table 5 reports the output from all the linear models. Compassion satisfaction was the onlydependent variable that remained significant following the model reduction. See Table S2 for the outputfrom all the original and reduced linear models. In the reduced linear model predicting compassionsatisfaction, female gender (F (1) = 9.701, p = 0.005), being married (F (1) = 5.553, p = 0.027), and notowning a pet (F (1) = 7.416, p = 0.012) were statistically significantly associated with a higher score.Contrary to our hypothesis, there were no statistically significant associations in the reduced modelspredicting burnout, moral injury, IES-R scores, secondary traumatic stress, PC1, and PC2 by job.4. Discussion4.1. Experiment 1A greater change in HR and less of a decrease in HRV (pNN50) was significantly related tonot working in an animal shelter. HR was significantly higher and pNN50 was significantly loweron killing days compared to a non-killing days across jobs. Increased heart rate is associated withdecreased HRV and indicates arousal, and both are often associated with emotional stress [58–61].This suggests that killing, no matter the contact with animals prior, may be emotionally stressful.Interestingly, HRV hyporeactivity has been used as an indicator of both depression [62] and PTSD [63].HRV biofeedback training has been successfully implemented as a treatment for individuals withanxiety, depression, and PTSD [64–66]. A study using biofeedback training as a predeployment protocolfound that participants with the biofeedback training experienced less arousal during postdeploymentcombat situations [67]. This indicates that it may be beneficial for animal-care organizations thatengage in killing to incorporate biofeedback training into protocols to decrease the arousal associatedwith killing.The statistically significant decrease in salivary cortisol levels between pre- andpost-euthanasia/slaughter can be explained by the diurnal nature of salivary cortisol levels [49].It should be noted that time of day was not controlled for; all harvesting began prior to 9:00 a.m.,whereas the majority of animal shelter and veterinary euthanasia occurred in the afternoon and evening.Cortisol spikes approximately 30 min after awakening and then continues to decline throughout theday, with the biggest decline occurring in the morning [54,68]. It continues to decrease throughout theday, so a plateau or slight decrease may indicate stress. The duration of killing was also not controlledfor; therefore, the difference in pre- and post-salivary cortisol could not be compared across jobs.Previous research has shown that BP increases during acute stress; however, we only saw anincrease in systolic pressure following killing [69]. An increase in systolic reactivity during a stressor iscommonly associated with hypertension [70]. Occupational as well as psychosocial stress have beencorrelated with hypertension [71,72]. We did not ask participants about comorbid disorders, so thissuggestion of hypertension is speculative. One potential explanation for the inconsistency and lack ofincrease in diastolic BP is that BP was taken as close to the cessation of killing as possible, but it wasnot always feasible. Due to the sensitive nature of euthanasia and harvest, the author (AA) was notalways able to be present during the actual process and did not know the time between last killingand the post BP measurement. It is possible that BP did increase during killing, but had returned tobaseline before the author had the opportunity to measure this change.Increased contact with animals predicted higher IES-R scores. More than one third (n= 6) of animalshelter employees scored at or above a 33, which represents the cutoff for a probable diagnosis ofPTSD [51]. This is higher than previous research in shelter employees, which found that approximatelyone-fifth of the population scored high enough for a probable diagnosis of PTSD [3]. It is estimatedthat 3.5% of the population is suffering from PTSD in a 12 month period [73]. Data from this studysuggest that animal shelter employees may be more likely than the general population to have PTSD ina given year. While the average number of animals killed in each session did statistically significantlyinfluence the model predicting IES-R scores, neither frequency nor total number of animals killedInt. J. Environ. Res. Public Health 2020, 17, 9196 14 of 18statistically significantly predicted IES-R scores. This supports recent research in laboratory animalpersonnel [17] and animal-care professionals [18], which found that other job stressors contribute moreto occupational stress than euthanasia.Decreased contact with animals and job predicted burnout, but not secondary traumatic stress.While burnout was statistically significantly different across jobs, no participants scored a 42 or above,indicating high burnout. There were also no participants who scored in the high range of secondarytraumatic stress. The majority of participants scored in the average range for both burnout (n = 16)and secondary traumatic stress (n = 11), suggesting that both are still a concern. This supports previousstudies that also found very low rates of high employee burnout and secondary traumatic stress,but high rates of average burnout in animal-care employees [3,19].Contact with animals did not statistically significantly predict compassion satisfaction; however,marriage, job, and pet ownership were statistically significant in this model. This aligns with previousresearch that support from significant others [74] predicts compassion satisfaction. Lower compassionsatisfaction scores were associated with working in an animal shelter. A score of 23–41 indicatesaverage compassion satisfaction, and 42 or more indicates very high compassion satisfaction [52].All participants had average-to-high compassion satisfaction, indicating that they all felt like theywere making a difference through their work. The average-to-high compassion satisfaction scoresare similar to those found in previous studies, which found average compassion satisfaction scoresbetween 39 and 42 in animal shelter employees [3,18].4.2. Experiment 2There were no statistically significant differences in the reduced models predicting burnout,moral injury, secondary traumatic stress, PC1 and PC2 between animal shelter employees whoeuthanize regularly, those who do not euthanize regularly, and people who work in a pet hotel.This contradicts the hypothesis that the act of killing is necessary to develop compassion fatigueand moral injury. It also further supports the findings from Monaghan and colleagues (2020)that non-euthanasia related job demands are better predictors of burnout and secondary traumaticstress than euthanasia. In the context of the results from Experiment 1, these data suggest that simplyproviding husbandry and constant care for animals may be enough to develop compassion fatigue.This aligns with research that has found increased prevalence of compassion fatigue in a variety ofhuman care-giving careers in which death is not a typical outcome [75,76]. The lack of relationshipbetween euthanasia and moral injury contradicts previous research which found moral injury to behigher in individuals who do euthanize [3]. The average moral injury score across all jobs was 37,which is similar to previously reported data that found the median scores of 35 and 44 in shelteremployees who euthanize and who do not, respectively. The current data suggest that moral injurymay be a concern for many animal-care professionals.4.3. Limitations and Future DirectionsThis study was exploratory as physiological measures of compassion fatigue and moral injury inanimal-care employees had never been previously assessed. The recruitment of participants provedto be a great challenge due to the sensitive nature of the subject matter, which led to a small samplesize and incomplete data sets for the majority of the veterinarians, limiting interpretation of thedata. All animal shelter and veterinary participants were from Texas, pet hotel employees wereall from Virginia, and university personnel who harvest were from Texas, Oklahoma, and Virginia.There is a possibility that the geographic differences impacted the physiologic and psychometricmeasures. Comorbid disorders and/or previous experience may have also impacted the physiologicand psychometric measures.The lack of control for time of day and length of killing in Experiment 1 limited the comparisonsthat could be done. Due to the diurnal nature of salivary cortisol, and the variation of time of day ofInt. J. Environ. Res. Public Health 2020, 17, 9196 15 of 18killing, salivary cortisol could not be compared across jobs. Practically, it was not possible to controlfor this as shelters, veterinarians, and universities have set times when they euthanize and harvest.The time constraints associated with each job also led to some participants answering the surveyquestions following slaughter or euthanasia, while others answered the questions on another day. It ispossible that the time in between killing and answering the psychometric measures may have had animpact on scores.5. ConclusionsThe overall aim of these studies was to evaluate the physiological and psychometric correlates ofcaring and killing in animal-care work. Experiment 1 found that increased contact with animals priorto killing predicted higher burnout and traumatic stress and that killing caused an increase in HR anda decrease in HRV. Experiment 2 found that jobs with greater euthanasia frequency did not predict anyof the psychometric or physiological measures, suggesting that killing may not be the biggest uniquepredictor of occupational stress. Future research should focus on non-euthanasia-related job stressorsas well as interventions to combat those stressors in animal-care staff.Supplementary Materials: The following are available online at http://www.mdpi.com/1660-4601/17/24/9196/s1,Table S1: Experiment 1 Analysis, Table S2: Experiment 2 Analysis.Author Contributions: A.P. and A.A. conceived the idea for the study and devised the methods. A.A. collecteddata, and N.J.H. and A.A. performed the formal analysis and prepared the results and figures. A.A. prepared theoriginal draft, and all authors contributed to the final writing and editing. All authors have read and agreed to thepublished version of the manuscript.Funding: This research received no external funding.Acknowledgments: We would like to thank the anonymous reviewers for their helpful input. We would also liketo thank all of the organizations involved, who allowed us into their facilities. Finally, we would like to thank allof the anonymous participants who made this study possible.Conflicts of Interest: The authors declare no conflict of interest.References1. ASPCA. Pet Statistics. 2016. Available online: https://www.aspca.org/animal-homelessness/shelter-intake-and-surrender/pet-statistics (accessed on 12 September 2017).2. Arluke, A. Managing Emotions in an Animal Shelter; Serpell, J., Ed.; Animals and Human Society: London, UK,1994; pp. 145–165.3. Andrukonis, A.; Protopopova, A. Occupational Health of Animal Shelter Employees by Live Release Rate,Shelter Type, and Euthanasia-Related Decision. Anthrozoös 2020, 33, 119–131. [CrossRef]4. 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The Impact of Caring and Killing on Physiological and Psychometric Measures of Stress in Animal Shelter Employees: A Pilot Study
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