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Identification of potential physiological and behavioral indicators of postoperative pain in horses after exploratory celiotomy for colic
Applied Animal Behaviour Science 80 (2003) 31–43
Identification of potential physiological and behavioral indicators of postoperative pain in horses after exploratory celiotomy for colic Lori C. Pritchetta, Catherine Ulibarrib, Malcolm C. Robertsc, Robert K. Schneidera, Debra C. Sellona,* a
Department of Veterinary Clinical Sciences, College of Veterinary Medicine, Washington State University, Pullman, WA 99164, USA b Department of Veterinary Comparative Anatomy, Pharmacology, and Physiology, Program in Neuroscience, College of Veterinary Medicine, Washington State University, Pullman, WA 99164, USA c Department of Animal Health and Resource Management, College of Veterinary Medicine, North Carolina State University, Raleigh, NC 27606, USA Accepted 10 September 2002
Abstract Physiological and behavioral parameters were determined in 27 horses to identify potential indicators of postoperative pain following exploratory celiotomy for colic. Experimental groups were 10 horses that received no treatment (Control), 10 horses anesthetized for a non-painful procedure (Anesthesia), and 7 horses that presented for emergency surgery for acute gastrointestinal disease (Surgery). Physiological and behavioral data were collected on the horses 0, 4, 8, 12, 16, 20, and 24– 30 h after entry into a stall in the equine intensive care unit of the Veterinary Teaching Hospital at Washington State University. Physiological data included: heart rate, respiratory rate, and plasma cortisol concentration. For the entire period of observation the surgery group had significantly higher plasma cortisol concentration and significantly elevated heart rate compared to the Control and Anesthesia groups, which did not differ for either variable. A numerical rating scale (NRS) of behavior was used to visually score the horses at the same time physiological data were collected. In addition, time budgets of behavior were calculated from 1 h segments of real-time video recording beginning at the 0, 4, 8 or 12 h, and 20 or 24–30 h time points. Time budgets for the Control and Anesthesia groups did not differ in the time spent in locomotor activities and both groups spent significantly more time in locomotion than the Surgery group. The Surgery group spent significantly more time displaying painful behavior compared to the Control and Anesthesia groups; however, the * Corresponding author. Tel.: þ1-509-335-0733; fax: þ1-509-335-3330. E-mail address: [email protected] (D.C. Sellon).
0168-1591/03/$ – see front matter # 2003 Elsevier Science B.V. All rights reserved. PII: S 0 1 6 8 - 1 5 9 1 ( 0 2 ) 0 0 2 0 5 - 8
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amount of time the Surgery group displayed painful behavior was small compared to the amount of time with no movement. The NRS scores substantiated the video taped behavioral data with significantly different scores for the Surgery group versus the Control and Anesthesia groups for multi-factor ratings of body posture and response to stimuli. We conclude that reduced locomotion, elevated plasma cortisol concentration, and elevated heart rate are potential indicators of postoperative pain in horses. # 2003 Elsevier Science B.V. All rights reserved. Keywords: Postoperative pain; Behavior; Horse
1. Introduction The stress response during the postoperative period involves a complex system of nociceptive signals transmitted from the surgical site that influence and are influenced by the physiologic state of the animal (Kehlet and Dahl, 1993). Not only is recognizing and treating this stress response desirable to alleviate suffering, but the systemic responses to pain can have deleterious effects on major organ systems (Bamberger et al., 1994). Postoperative analgesia in horses generally involves the use of nonsteroidal anti-inflammatory agents such as flunixin meglumine. These agents act locally to prevent nociceptor sensitization that accompanies inflammation, but in other species are not sufficient to relieve severe visceral pain associated with major abdominal surgery (Joris, 1996). Quantitative measures of physiology and behavior are useful to evaluate postoperative pain and the response to pain management in many species including humans (Schade et al., 1996), dogs (Hansen et al., 1997; Hardie et al., 1997), cats (Smith et al., 1996), and rats (Liles and Flecknell, 1993). However, to our knowledge, this work has not been done for the equine patient recovering from exploratory celiotomy. The objective of this study was to define physiological and behavioral parameters of normal stabled horses and horses recovering from exploratory celiotomy for colic. Our goal was to identify potential physiological and behavioral indicators of postoperative pain in horses that could be useful in measuring the response of horses to analgesic medications.
2. Materials and methods 2.1. Horses Three groups of horses were used. Group 1 (Control) included 10 horses from the teaching herd at the College of Veterinary Medicine, Washington State University (WSU) that were in good systemic health and sound at the walk. The average age of the Control group was 10.2 years (range 4–22 years); there were seven females and three geldings and the breeds represented were six Thoroughbreds and one each of Arabian, Hanoverian, Quarter Horse, and Warmblood. Group 2 (Anesthesia) included 10 client-owned horses that underwent general anesthesia for magnetic resonance imaging (MRI) of the distal limbs, a non-painful procedure.
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These horses were normal on physical examination and results of a complete blood count and serum biochemical profile were within normal limits. The Anesthesia horses were sound at the walk and had evidence of lameness in one or more legs at the trot. The average age of the Anesthesia group was 7.1 years (range 4–11 years); there were nine geldings and one female and the breeds represented were four Thoroughbreds, two Quarter Horses, two Paints, and one each of Arabian and Standardbred. Group 3 (Surgery) included seven client-owned horses that presented with acute gastrointestinal problems requiring surgical correction. The average age of the Surgery group was 13.4 years (range 6–19 years); there were five females, one gelding, and one stallion and the breeds represented were one each of Appaloosa, Arabian, Morgan, Paint, Quarter Horse, Tennessee Walking Horse, and Thoroughbred. The Surgery horses received flunixin meglumine at 1.1 mg kg1 IV prior to surgery or immediately following surgery and at approximately 12 and 24 h after entry into the stall. They also received intravenous potassium penicillin at 22,000 IU kg1 IVevery 6 h, gentamicin at 4.4–6.6 mg kg1 IVevery 24 h, and lactated Ringer’s solution at 1–2 l h1 during the observation period. No other analgesic medication was administered to the Surgery horses during the observation period. All procedures were approved by the Institutional Animal Care and Use Committee of WSU. All horses were housed indoors in one of two adjacent stalls in the equine intensive care unit of the Veterinary Teaching Hospital at WSU, a facility approved by the American Association of Laboratory Animal Care. The temperature and humidity in this environment is controlled year round. Control and Anesthesia horses were fed grass/alfalfa hay twice daily at 6.00–8.00 h and 16.00–18.00 h. The Surgery horses were not fed for the first 24 h after surgery. All horses had access to water available in a bucket suspended from the front of the stall. A catheter was placed in one jugular vein prior to anesthesia for the Surgery and Anesthesia horses and prior to entry into the stall for the Control horses. All horses except one Surgery and one Anesthesia horse (received no butorphanol) were premedicated with similar dosages of xylazine and butorphanol. Anesthesia was induced in all horses with similar dosages of glyceryl guiacolate, diazepam, and ketamine. Anesthesia was maintained in all horses by inhalation of isoflurane. 2.2. Sample collection Physiological and behavioral data were collected on the horses 0, 4, 8, 12, 16, 20, and 24–30 h after entry into the stall. For the Anesthesia and Surgery horses, the 0 h time point began when the horse was returned to the stall after recovery from anesthesia. For the Anesthesia horses, the 0 h was between 15.00 and 17.00 h; therefore, the 0 h for the Control horses was similarly defined. The 0 h for the Surgery horses varied depending on the time of presentation and surgery. Heart rate by auscultation and respiratory rate by observation within the stall were recorded for each time point. A venous blood sample was collected from the jugular catheter for plasma cortisol determination at the 0, 4, 8, and 24 h time points. The blood samples were placed in evacuated glass tubes with EDTA anticoagulant, centrifuged, and the harvested plasma was stored at 70 8C until assayed for cortisol concentration by radioimmunoassay (Animal Health Diagnostic Laboratory, College of Veterinary Medicine, Michigan State University, Lansing, MI).
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Table 1 Numerical rating scale (NRS) of behavior used to visually score horses Behavior category
1 a,b
Gross pain behaviors Head positionb Ear positionb
None Above withers Forward, frequent movement Location in stallb At door watching environment Spontaneous locomotionb Moves freely Response to open doorc Moves to door Response to approachc Move to observer, ears forward Lifting feetc Freely lift feet when asked Response to grainc
2
3
Occasional At withers Slightly back, little movement Standing in middle, Standing in middle, facing stall door facing sides of stall Occasional steps Looks at door Looks at observer, Moves away from ears forward observer Lift feet after mild encouragement
Moves to door and Looks at door reaches for grain
4 Continuous Below withers
Standing in middle, facing back of stall No movement No response Does not move, ears back Extremely unwilling to lift feet No response
a Gross pain behaviors include pawing, sweating, looking at the flank, flehmen, and lying down/standing up repeatedly. b Scores combined to yield Posture score. c Scores combined to yield Socialization score.
Two methods were used to assess behavior: a numerical rating scale (NRS) of behavior and time budgets calculated from real-time video recording. The numerical rating scale (NRS) of behavior (Table 1) was used to visually score the horses prior to collection of the physiological data. The NRS assigns a numeric score to each behavior category that is weighted based on a descriptive definition of the behavior in each column. The NRS yielded a total Behavior score for each time point that is the sum of the scores assigned for each behavior category in Table 1. The Behavior score was subdivided into two components: Posture score and Socialization score. The Posture score was the sum of the scores for the categories describing gross pain behaviors, head position, ear position, location in the stall and spontaneous locomotion. The Socialization score was the sum of the scores for categories to monitor the response of the horse to positive stimuli. The positive stimuli were: opening the door and saying the horse’s name (response to open door); slowly approaching the horse while talking (response to approach); attempting to lift one front foot (lifting feet); and offering the horse a bucket of grain from the open door (response to grain). Horses were not allowed to eat the grain. Time budgets of behavior were calculated from real-time video recordings of the horses. For real-time video recording, the stall was equipped with a video camera connected to a time-relay device, video monitor, and video recorder. Each horse was videotaped for 1 h beginning at times 0, 4, 8, 12, and 20 h and for 1 h beginning between 24 and 30 h. A sign was posted on the stall door at the start of each hour of videotaping to prevent feeding, cleaning, or other interruptions by the animal care personnel. The videotaped segments for the 0 h, 4 h, 8 or 12 h, and 20 or 24–30 h time points were used for behavior scoring. The 8 or 12 h and the 20 or 24 h time points were selected based upon the horse being present and alone in the stall during those times. One Control horse
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Table 2 Definitions of individual behaviors, grouped by category, used to score the real-time video recordings of horses Category
Behavior
Description
Active
Eat Defecate Drink Flick Lick Nose Paw
Toss Urinate
Eating hay placed in the stall. Lifting the tail and evacuating feces. Drinking water from the bucket. Rapid, repetitive flicking the tail while standing. Licking the salt block. Investigating the walls, floor, or water bucket while taking strides or standing. A repetitive action with forelimb extended forward and then drawn back with the ventral toe dragging. Lying down and rolling. Rubbing any part of the body against the side of the stall or the front leg or raising the hind leg to scratch the head. A shake that involves the whole body. Movement of the front or hind feet that moves the body direction. This is distinguished from walking because only 2 feet move. Tossing, shaking, or stretching the head while standing. A visible urinary stream.
Locomotion
Graze Walk
Strides taken with the head down and visibly eating the bedding. Strides taken forward or backward.
Pain
Flank gesture Flehmen Kick Stretch
Turning the head while standing to look at the side of the body. Extending the head forward and curling the upper lip. Lifting the hind leg to strike at the abdomen. A wide-based stance with the back ventroflexed.
Resting
Stand
No movement or activity while standing with attention to the environment or in a restful posture. Sternal or lateral recumbency.
Roll Scratch Shake Shift
Rest
was removed from the stall prior to the 24 h videotaping due to demand for the stall, therefore data from the 20 h time point were used. One Anesthesia horse was removed from the stall for clinical examination during the 8 h videotaping, therefore data from the 12 h time point were used. Each videotaped segment was assigned a unique random number that determined the order in which the segments were scored, independently, by two trained observers. One observer was involved in the initial data collection; the second observer had no prior knowledge of the horses or study objectives. Observations from videotaped behavior of normal horses and horses recovering from abdominal surgery were used to determine the behaviors amenable to definition and measurement (Table 2). These preliminary observations were made using horses not involved in this study and the behavior definitions were refined by the observers until the definitions were mutually exclusive. The observers then scored the type and duration in seconds of each defined behavior from the videotapes of the study horses. Entry into the stall at the half-hour point of each videotaped hour to evaluate the response to positive stimuli for the NRS and to collect physiological data were not included in the behavior scoring. The videotape observers ceased scoring behavior from the moment the stall door opened and resumed scoring behavior when the stall door closed again.
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For the final analysis, the individual behaviors were categorized as Active, Locomotion, Pain, or Resting and a time budget of these categories was computed for each videotaped hour. The time budget was calculated by dividing the total duration of each behavior category for a segment by the total time scored for that segment to yield the percent of time in each category for each videotaped hour. The average of the two observers’ time budgets for each videotaped segment was used in the statistical analysis. 2.3. Statistical analysis The physiological and behavioral data were analyzed by two-factor analysis of variance with repeated measures on one factor, time. The least squares means and standard errors were calculated from the model for the effects of group and time. Bonferroni’s t-test of differences between the means was performed for the effects of group and time. Significant ðP < 0:05Þ effects were confirmed by the nonparametric Kruskal–Wallis test (General Linear Models and NPAR1WAY procedures, SAS1, SAS Institute Inc., Box 8000, Cary, NC 27511). The possible confounding factors of age and sex were analyzed by the same procedures. For these analyses, age was categorized as young (<8 years) or old (8 years) and sex was categorized as male (geldings and stallion) or female. Age or sex was used as the classification variable in the place of group to determine the effects on the dependent variables. To determine the degree of agreement between the observers for the videotaped behavioral data, the duration of individual behaviors at each time point were compared with the Bland-Altman method (1986) as if the two observers were two different assessment methods. For this analysis, the differences between the observers’ scores were plotted versus the means of their scores, where a slope of 0 and intercept of 0 indicate no systematic disagreement. The correlation, P value, slope standard error (S.E.), intercept S:E:, mean difference (M.D.), standard deviation (S.D.) of the difference, and limits of agreement were determined (Regression and Means procedures, SAS1, SAS Institute Inc., Box 8000, Cary, NC 27511).
3. Results 3.1. Physiological data The Surgery group had a longer ðP < 0:001Þ duration of anesthesia than the Anesthesia group. Median duration of anesthesia was 150 and 85 min, respectively, for the Surgery group and Anesthesia groups. The Surgery group had a higher ðP < 0:001Þ heart rate than the Control and Anesthesia groups throughout the observation period (Fig. 1), however respiratory rate did not differ among the groups (data not shown). The heart rate did not differ between the Control and Anesthesia groups and did not vary with time, whereas the heart rate in the Surgery group declined with time. The average plasma cortisol concentrations for one Control and one Surgery horse were below the normal range of the reference laboratory (85–180 nmol l1), therefore these
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Fig. 1. Heart rate ðL:S:M: S:E:M:Þ of stabled horses measured by auscultation every 4 h for 24 h. The experimental groups were: Control ðn ¼ 10Þ, horses received no treatment; Anesthesia ðn ¼ 10Þ, horses anesthetized for magnetic resonance imaging, a non-painful procedure; and Surgery ðn ¼ 7Þ, horses that presented for emergency surgery for acute gastrointestinal disease. The elevation in heart rate for the Surgery group was significant ðP < 0:001Þ throughout the observation period.
horses were deleted from the analysis. The Surgery group had a higher ðP < 0:03Þ plasma cortisol concentration than the Control and Anesthesia groups at each time point sampled (Fig. 2). The plasma cortisol concentration did not differ between the Control and Anesthesia groups. There was a time effect due to the significant decline in the plasma cortisol concentration in the Anesthesia group for the 24 h sample. 3.2. Numerical rating score of behavior The Surgery group had a higher ðP < 0:001Þ Behavior score, Posture score, and Socialization score than the Control and Anesthesia groups. There was no difference between the Control and Anesthesia groups for any of the NRS scores. There was no effect of time on any of the NRS scores therefore the least squares means of the scores by group averaged over all time are presented in Table 3. 3.3. Videotaped behavior data The agreement between the observers’ scores for the duration of individual behaviors was such that the total of all differences for individual behaviors of any one horse could be expected (95% confidence interval) to be less than 4.8 min, or approximately 8%. The individual behavior scores were used to calculate hour time budgets for each videotaped segment. The good agreement between the observers for individual behaviors validated averaging the time budgets calculated for each segment of videotape. The hour time-budgets differed ðP < 0:001Þ between all three groups for Active, Resting, and Pain behavior (Fig. 3). The Anesthesia group was the most active and least restful for all time points, followed by the Control group. The Surgery group was the least active and the most
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Fig. 2. Plasma cortisol concentration ðL:S:M: S:E:M:Þ of stabled horses measured by radioimmunoassay at 0, 4, 8, and 24 h after entry into the stall. The experimental groups were: Control ðn ¼ 9Þ, horses that did not receive any treatment; Anesthesia ðn ¼ 10Þ, horses anesthetized for magnetic resonance imaging, a non-painful procedure; and Surgery ðn ¼ 6Þ, horses that presented for emergency surgery for acute gastrointestinal disease. The elevated plasma cortisol concentration for the Surgery group was significant ðP < 0:03Þ throughout the observation period.
restful for all time points. Active behavior differed significantly at each time point only for the Anesthesia group. There was not a significant time effect on Active behavior for the Control and Surgery groups. Surgery was the only group with significant time spent in Pain behavior, however, even for this group, the percent of time was small (0–9.7%) compared with the percent of time with no movement, Resting (78.6–85.9%). There was not a significant time effect for Locomotion or Resting behaviors, therefore, the least squares means of the 4 h time-budgets by group are presented in Table 4. The timebudget for Locomotion was not different between Control (13:6 2:1%) and Anesthesia Table 3 The Behavior, Posture, and Socialization scores ðL:S:M: S:E:M:Þ of stabled horses computed from a numerical rating scale of behavior as described for Table 1 Group
Behavior score
Posture score
Socialization score
Control Anesthesia Surgery
13.3 0.4a 12.4 0.4a 19.6 0.5b
7.9 0.3a 7.2 0.3a 11.5 0.3b
5.4 0.2a 5.1 0.2a 8.1 0.3b
Means with different letters within a column differ ðP < 0:05Þ by the Bonferroni’s t-test. The experimental groups were: Control ðn ¼ 10Þ, horses that did not receive any treatment; Anesthesia ðn ¼ 10Þ, horses anesthetized for magnetic resonance imaging, a non-painful procedure; and Surgery ðn ¼ 7Þ, horses that presented for emergency surgery for acute gastrointestinal disease.
Fig. 3. Time budgets ðL:S:M: S:E:M:Þ of behavior of stabled horses measured by real-time video recordings 0, 4, 8–12, and 20–30 h after entry into the stall. The experimental groups were: Control ðn ¼ 10Þ, horses received no treatment; Anesthesia ðn ¼ 10Þ, horses anesthetized for magnetic resonance imaging, a non-painful procedure; and Surgery ðn ¼ 7Þ, horses that presented for emergency surgery for acute gastrointestinal disease. The hour time-budgets differed ðP < 0:001Þ between all three groups for Active, Resting, and Pain behavior. The time-budget for Locomotion was not different between the Control and Anesthesia groups and was significantly greater for these two groups than the Surgery group ðP < 0:05Þ.
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Table 4 The average time budgets ðL:S:M: S:E:M:Þ of behavior of stabled horses measured by real-time video recording Group
Active
Locomotion
Pain
Resting
Control Anesthesia Surgery
22.6 3.2a 42.3 3.3b 11.1 4.0c
13.6 2.1a 14.0 2.2a 1.9 2.6b
0.0 0.5a 0.3 0.05a 3.9 0.6b
63.8 3.1a 43.3 3.2b 83.0 3.8c
Means with different letters within a column differ ðP < 0:05Þ by the Bonferroni’s t-test. The experimental groups were: Control ðn ¼ 10Þ, horses that did not receive any treatment; Anesthesia ðn ¼ 10Þ, horses anesthetized for magnetic resonance imaging, a non-painful procedure; and Surgery ðn ¼ 7Þ, horses that presented for emergency surgery for acute gastrointestinal disease.
(14:0 2:2%) and was greater ðP < 0:05Þ for these two groups than the Surgery group (1:9 2:6%). 3.4. Confounding variables: age and sex Age or sex did not have an effect on the physiological or behavioral variables analyzed in this data set.
4. Discussion In this study, both physiological and behavioral data were collected on three groups of horses in an attempt to identify indicators of postoperative pain in horses following abdominal surgery. The combination of physiological and behavioral data is considered more useful than physiological measures alone to assess individual animal differences in response to environmental change and challenge (Manteca and Deag, 1993). The three experimental groups were 10 horses that did not receive any treatment, 10 horses that were anesthetized for MRI, a non-painful procedure, and 7 horses that had emergency surgery for acute gastrointestinal disease. The horses undergoing anesthesia for MRI were included to account for the effects of recovery from anesthesia on physiological (Taylor, 1989) and behavioral parameters. The study period of 24 h was chosen because postoperative pain peaks within 6–24 h following abdominal surgery in dogs (Hansen, 1997). Auscultation of the heart rate in recovering animals is simple, objective, and noninvasive. Heart rate is frequently measured in the clinical setting to monitor animals in the postoperative period. In this study, the heart rate was significantly elevated in the Surgery group compared with the Control and Anesthesia groups. Unfortunately, the physiological response of heart rate in the postoperative period has not been a useful indicator for pain assessment in dogs (Hansen et al., 1997) or cats (Smith et al., 1996). Other factors such as temperament (McCann et al., 1988), drug administration, and hypovolemia (Carroll, 1996) can affect the heart rate, confounding any association between elevated heart rate and pain. The heart rate measure may be more useful if it is added as a physiological component of a behavioral measurement scale (Firth and Haldane, 1999).
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Plasma cortisol concentrations in cats (Smith et al., 1996) and dogs (Fox et al., 1994) have been shown to increase significantly in response to surgical stress. A similar response was seen in the horses in our study. The Surgery group had a higher plasma cortisol concentration than the Control and Anesthesia groups at each time point sampled. Although samples for cortisol analysis were obtained at similar times of day for Control and Anesthesia horses, this was not possible for Surgery horses. Therefore, any potential confounding influence of circadian rhythm on data analysis could not be addressed. Future studies are under way to address this possibility. It is possible the elevated plasma cortisol concentration observed in the Surgery group is related to the extent of surgical injury or underlying disease in addition to postoperative pain. However the purpose of this study was to identify potential indicators of postoperative pain in horses. The correlation, if any, between plasma cortisol levels and tissue injury is beyond the scope of this study. The average cortisol concentration for the Anesthesia group was higher than the Control group at each time point, however this difference was not significant. The significant decline in plasma cortisol concentration in the Anesthesia group at the 24 h time point suggests these horses did have a stress response to the MRI procedure. This is consistent with the significant adrenocortical response due to anesthesia alone that has been reported in ponies (Taylor, 1989). Two horses in our study, one in the Control group and one in the Surgery group, had abnormally low plasma cortisol concentrations. Assessing adrenal gland function may improve the value of cortisol measurements for pain assessment (Fox et al., 1994). However, adrenal function tests would not be practical for client-owned horses presenting with acute gastrointestinal disorders. We used the normal range of plasma cortisol concentrations from the laboratory that assayed the samples to exclude these two horses based upon the average of four plasma samples. Preliminary observations from videotaped behavior of normal horses and horses recovering from abdominal surgery were important first steps to define behaviors that were comprehensive and unambiguous (Martin and Bateson, 1993). Many of our definitions are similar to those used by others for assessing the well being of horses (Bagshaw et al., 1994; McDonnell et al., 1999). By randomizing the order in which the videotaped segments were viewed and scoring the behavior by two observers, one unfamiliar with the objectives of the study, we successfully obtained behavioral data that is both unbiased and reliable as determined by the excellent agreement between the observers’ scores. For any hour of videotape scoring of any horse, the total of the differences between the observers’ scores for the durations of individual behaviors would be less than 5 min. From the time budget data we conclude that recovery from anesthesia did not adversely affect behavior. In fact, the Anesthesia horses spent more time in Active behavior than the Controls, a difference that could not be attributed to the sex or age differences between these groups. A likely explanation is that the Control group was from the teaching herd and many were familiar with the hospital environment. Although time did not have a significant effect on Locomotion behavior by repeated measures analysis of variance, the Anesthesia horses spent more time during the first hour in Locomotion. This may be due to the fact that feed was withheld from these horses prior to anesthesia for MRI and they spent the first hour after recovery from anesthesia searching the stall for food.
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When time budgets for four observation hours are considered, the Control and Anesthesia groups did not differ in the time spent in Locomotion and both groups spent significantly more time in Locomotion than the Surgery group. We conclude that the presence or absence of voluntary walking is a potential indicator of postoperative pain. This is in contrast with the generally accepted signs of visceral pain in horses which include: restlessness, looking at the flank, pawing, stretching the body, crouching, stretching the neck and flehmen, vocalizing, lying down, getting up again, lying down and rolling. These are signs associated with colic where the pain is attributed to increased pressure in the gastrointestinal tract (Lowe, 1992). Pawing and rolling were categorized as Active behavior in this study because these behaviors were observed in normal horses during preliminary observations to develop the behavior definitions. Flehmen, flank gestures, kicking the abdomen, and stretching the body were seen in preliminary observations of horses recovering from abdominal surgery, therefore, these were categorized as Pain behavior for the hour time-budget. Although significant painful behaviors were observed in the Surgery group, as shown in Fig. 2, the amount of time spent displaying Pain behaviors was small compared to the amount of time with no movement (Resting). If we assume that horses experience pain after abdominal surgery, this suggests that postoperative pain behavior differs from preoperative pain behaviors associated with colic. Our observations of postoperative behavior in horses support the observation reported by Hansen (1997) that animals severely debilitated by major surgery may be the least able to act painfully. Pain measurement scales are used in human and animal medicine to assess postoperative pain and the response to analgesia (Schade et al., 1996; Firth and Haldane, 1999). In this study, our NRS of behavior resulted in a total Behavior score as well as component scores associated with body position (Posture) and response to positive stimuli (Socialization). Pain behavior and locomotion are two components of the Behavior and Posture scores wherein the presence of painful behavior and the lack of locomotion generate a higher score. These scores were significantly higher in the Surgery group and did not differ between the Control and Anesthesia groups. These results are consistent with those obtained from the hour time budgets. The Surgery group was less responsive to positive stimuli than the Control and Anesthesia groups as indicated by the significantly higher Socialization score for the Surgery group. Our finding that the response of horses to positive stimuli is altered in the postoperative period is consistent with the significant reduction in interactive behavior following ovariohysterectomy reported in dogs (Hardie et al., 1997).
5. Conclusion The purpose of this study was to identify potential physiological and behavioral indicators of postoperative pain in horses that undergo exploratory celiotomy for acute gastrointestinal disorders. We conclude that reduced locomotion, elevated plasma cortisol concentration and elevated heart rate are potential indicators of postoperative pain in horses that may be useful in future studies to evaluate the efficacy of analgesic treatments following abdominal surgery.
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Acknowledgements This study was funded by a grant from the Morris Animal Foundation and a National Institutes of Health Summer Research Fellowship for Students in Health Professional Schools. The authors thank the team of students who assisted with the sampling: Betsy Charles, Dawn Deming, Matt Dredge, GayLynn Goolsby, Beth Hayes, Carl Johnson, Kurt Johnson, Jodi Nicklas, Dana Reid, and Abby Snodgrass. We also thank Dr. Bryan Slinker and Mr. Robert Kirkpatrick for valuable assistance with the data.
References Bagshaw, C.S., Ralston, S.L., Fisher, H., 1994. Behavioral and physiological effect of orally administered tryptophan on horses subjected to acute isolation stress. Appl. Anim. Behav. Sci. 40, 1–12. Bamberger, A.H., Tanelin, D.L., Klein, K., 1994. Pain management for the postoperative patient. Tex. Med. 90, 54–56. Bland, J.M., Altman, D.G., 1986. Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1, 307–310. Carroll, G.L., 1996. How to manage perioperative pain. Vet. Med. 91, 353–357. Firth, A.M., Haldane, S.L., 1999. Development of a scale to evaluate postoperative pain in dogs. J. Am. Vet. Med. Assoc. 214, 651–659. Fox, S.M., Mellor, D.J., Firth, E.C., Hodge, H., 1994. Changes in plasma cortisol concentrations before, during and after analgesia, anaesthesia and anaesthesia plus ovariohysterectomy in bitches. Res. Vet. Sci. 57, 110– 118. Hansen, B., 1997. Through a glass darkly: using behavior to assess pain. Sem. Vet. Med. Surg. (Sm. An.) 12, 61– 74. Hansen, B.D., Hardie, E.M., Carroll, G.S., 1997. Physiological measurements after ovariohysterectomy in dogs: what’s normal? Appl. Anim. Behav. Sci. 51, 101–109. Hardie, E.M., Hansen, B.D., Carroll, G.S., 1997. Behavior after ovariohysterectomy in the dog: what’s normal? Appl. Anim. Behav. Sci. 51, 111–128. Joris, J., 1996. Efficacy of nonsteroidal antiinflammatory drugs in postoperative pain. Acta Anaesth. Belg. 47, 115–123. Kehlet, H., Dahl, J.B., 1993. Postoperative pain. World J. Surg. 17, 215–219. Liles, J.H., Flecknell, P.A., 1993. The effects of surgical stimulus on the rat and the influence of analgesis treatment. Br. Vet. J. 149, 515–525. Lowe, J.E., 1992. The balloon model for controlled abdominal pain in the horse. In: Short, C.E., Van Poznak, A. (Eds.), Animal Pain. Churchill Livingstone, New York, pp. 408–410. Manteca, X., Deag, J.M., 1993. Use of physiological measures to assess individual differences in reactivity. Appl. Anim. Behav. Sci. 37, 265–270. Martin, P., Bateson, P., 1993. Measuring Behavior: An Introductory Guide. Cambridge University Press, Cambridge, pp. 56–61. McCann, J.S., Heird, J.C., Bell, R.W., Lutherer, L.O., 1988. Normal and more highly reactive horses. I. Heart rate, respiration rate and behavioral observations. Appl. Anim. Behav. Sci. 19, 201–214. McDonnell, S.M., Freeman, D.A., Cymbaluk, N.F., Schott, H.C., Hinchcliff, K., Kyle, B., 1999. Behavior of stabled horses provided continuous or intermittent access to drinking water. Am. J. Vet. Res. 60, 1451–1456. Schade, J.G., Joyce, B.A., Gerkensmeyer, J., Keck, J.F., 1996. Comparison of three preverbal scales for postoperative pain assessment in a diverse pediatric sample. J. Pain Symptom Manage. 12, 348–359. Smith, J.D., Allen, S.W., Quandt, J.E., Tackett, R.L., 1996. Indicators of postoperative pain in cats and correlation with clinical criteria. Am. J. Vet. Res. 57, 1674–1678. Taylor, P.M., 1989. Equine stress responses to anesthesia. Br. J. Anaesth. 63, 702–709.
Identification of potential physiological and behavioral indicators of postoperative pain in horses after exploratory celiotomy for colic Lori C. Pritchetta, Catherine Ulibarrib, Malcolm C. Robertsc, Robert K. Schneidera, Debra C. Sellona,* a
Department of Veterinary Clinical Sciences, College of Veterinary Medicine, Washington State University, Pullman, WA 99164, USA b Department of Veterinary Comparative Anatomy, Pharmacology, and Physiology, Program in Neuroscience, College of Veterinary Medicine, Washington State University, Pullman, WA 99164, USA c Department of Animal Health and Resource Management, College of Veterinary Medicine, North Carolina State University, Raleigh, NC 27606, USA Accepted 10 September 2002
Abstract Physiological and behavioral parameters were determined in 27 horses to identify potential indicators of postoperative pain following exploratory celiotomy for colic. Experimental groups were 10 horses that received no treatment (Control), 10 horses anesthetized for a non-painful procedure (Anesthesia), and 7 horses that presented for emergency surgery for acute gastrointestinal disease (Surgery). Physiological and behavioral data were collected on the horses 0, 4, 8, 12, 16, 20, and 24– 30 h after entry into a stall in the equine intensive care unit of the Veterinary Teaching Hospital at Washington State University. Physiological data included: heart rate, respiratory rate, and plasma cortisol concentration. For the entire period of observation the surgery group had significantly higher plasma cortisol concentration and significantly elevated heart rate compared to the Control and Anesthesia groups, which did not differ for either variable. A numerical rating scale (NRS) of behavior was used to visually score the horses at the same time physiological data were collected. In addition, time budgets of behavior were calculated from 1 h segments of real-time video recording beginning at the 0, 4, 8 or 12 h, and 20 or 24–30 h time points. Time budgets for the Control and Anesthesia groups did not differ in the time spent in locomotor activities and both groups spent significantly more time in locomotion than the Surgery group. The Surgery group spent significantly more time displaying painful behavior compared to the Control and Anesthesia groups; however, the * Corresponding author. Tel.: þ1-509-335-0733; fax: þ1-509-335-3330. E-mail address: [email protected] (D.C. Sellon).
0168-1591/03/$ – see front matter # 2003 Elsevier Science B.V. All rights reserved. PII: S 0 1 6 8 - 1 5 9 1 ( 0 2 ) 0 0 2 0 5 - 8
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amount of time the Surgery group displayed painful behavior was small compared to the amount of time with no movement. The NRS scores substantiated the video taped behavioral data with significantly different scores for the Surgery group versus the Control and Anesthesia groups for multi-factor ratings of body posture and response to stimuli. We conclude that reduced locomotion, elevated plasma cortisol concentration, and elevated heart rate are potential indicators of postoperative pain in horses. # 2003 Elsevier Science B.V. All rights reserved. Keywords: Postoperative pain; Behavior; Horse
1. Introduction The stress response during the postoperative period involves a complex system of nociceptive signals transmitted from the surgical site that influence and are influenced by the physiologic state of the animal (Kehlet and Dahl, 1993). Not only is recognizing and treating this stress response desirable to alleviate suffering, but the systemic responses to pain can have deleterious effects on major organ systems (Bamberger et al., 1994). Postoperative analgesia in horses generally involves the use of nonsteroidal anti-inflammatory agents such as flunixin meglumine. These agents act locally to prevent nociceptor sensitization that accompanies inflammation, but in other species are not sufficient to relieve severe visceral pain associated with major abdominal surgery (Joris, 1996). Quantitative measures of physiology and behavior are useful to evaluate postoperative pain and the response to pain management in many species including humans (Schade et al., 1996), dogs (Hansen et al., 1997; Hardie et al., 1997), cats (Smith et al., 1996), and rats (Liles and Flecknell, 1993). However, to our knowledge, this work has not been done for the equine patient recovering from exploratory celiotomy. The objective of this study was to define physiological and behavioral parameters of normal stabled horses and horses recovering from exploratory celiotomy for colic. Our goal was to identify potential physiological and behavioral indicators of postoperative pain in horses that could be useful in measuring the response of horses to analgesic medications.
2. Materials and methods 2.1. Horses Three groups of horses were used. Group 1 (Control) included 10 horses from the teaching herd at the College of Veterinary Medicine, Washington State University (WSU) that were in good systemic health and sound at the walk. The average age of the Control group was 10.2 years (range 4–22 years); there were seven females and three geldings and the breeds represented were six Thoroughbreds and one each of Arabian, Hanoverian, Quarter Horse, and Warmblood. Group 2 (Anesthesia) included 10 client-owned horses that underwent general anesthesia for magnetic resonance imaging (MRI) of the distal limbs, a non-painful procedure.
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These horses were normal on physical examination and results of a complete blood count and serum biochemical profile were within normal limits. The Anesthesia horses were sound at the walk and had evidence of lameness in one or more legs at the trot. The average age of the Anesthesia group was 7.1 years (range 4–11 years); there were nine geldings and one female and the breeds represented were four Thoroughbreds, two Quarter Horses, two Paints, and one each of Arabian and Standardbred. Group 3 (Surgery) included seven client-owned horses that presented with acute gastrointestinal problems requiring surgical correction. The average age of the Surgery group was 13.4 years (range 6–19 years); there were five females, one gelding, and one stallion and the breeds represented were one each of Appaloosa, Arabian, Morgan, Paint, Quarter Horse, Tennessee Walking Horse, and Thoroughbred. The Surgery horses received flunixin meglumine at 1.1 mg kg1 IV prior to surgery or immediately following surgery and at approximately 12 and 24 h after entry into the stall. They also received intravenous potassium penicillin at 22,000 IU kg1 IVevery 6 h, gentamicin at 4.4–6.6 mg kg1 IVevery 24 h, and lactated Ringer’s solution at 1–2 l h1 during the observation period. No other analgesic medication was administered to the Surgery horses during the observation period. All procedures were approved by the Institutional Animal Care and Use Committee of WSU. All horses were housed indoors in one of two adjacent stalls in the equine intensive care unit of the Veterinary Teaching Hospital at WSU, a facility approved by the American Association of Laboratory Animal Care. The temperature and humidity in this environment is controlled year round. Control and Anesthesia horses were fed grass/alfalfa hay twice daily at 6.00–8.00 h and 16.00–18.00 h. The Surgery horses were not fed for the first 24 h after surgery. All horses had access to water available in a bucket suspended from the front of the stall. A catheter was placed in one jugular vein prior to anesthesia for the Surgery and Anesthesia horses and prior to entry into the stall for the Control horses. All horses except one Surgery and one Anesthesia horse (received no butorphanol) were premedicated with similar dosages of xylazine and butorphanol. Anesthesia was induced in all horses with similar dosages of glyceryl guiacolate, diazepam, and ketamine. Anesthesia was maintained in all horses by inhalation of isoflurane. 2.2. Sample collection Physiological and behavioral data were collected on the horses 0, 4, 8, 12, 16, 20, and 24–30 h after entry into the stall. For the Anesthesia and Surgery horses, the 0 h time point began when the horse was returned to the stall after recovery from anesthesia. For the Anesthesia horses, the 0 h was between 15.00 and 17.00 h; therefore, the 0 h for the Control horses was similarly defined. The 0 h for the Surgery horses varied depending on the time of presentation and surgery. Heart rate by auscultation and respiratory rate by observation within the stall were recorded for each time point. A venous blood sample was collected from the jugular catheter for plasma cortisol determination at the 0, 4, 8, and 24 h time points. The blood samples were placed in evacuated glass tubes with EDTA anticoagulant, centrifuged, and the harvested plasma was stored at 70 8C until assayed for cortisol concentration by radioimmunoassay (Animal Health Diagnostic Laboratory, College of Veterinary Medicine, Michigan State University, Lansing, MI).
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Table 1 Numerical rating scale (NRS) of behavior used to visually score horses Behavior category
1 a,b
Gross pain behaviors Head positionb Ear positionb
None Above withers Forward, frequent movement Location in stallb At door watching environment Spontaneous locomotionb Moves freely Response to open doorc Moves to door Response to approachc Move to observer, ears forward Lifting feetc Freely lift feet when asked Response to grainc
2
3
Occasional At withers Slightly back, little movement Standing in middle, Standing in middle, facing stall door facing sides of stall Occasional steps Looks at door Looks at observer, Moves away from ears forward observer Lift feet after mild encouragement
Moves to door and Looks at door reaches for grain
4 Continuous Below withers
Standing in middle, facing back of stall No movement No response Does not move, ears back Extremely unwilling to lift feet No response
a Gross pain behaviors include pawing, sweating, looking at the flank, flehmen, and lying down/standing up repeatedly. b Scores combined to yield Posture score. c Scores combined to yield Socialization score.
Two methods were used to assess behavior: a numerical rating scale (NRS) of behavior and time budgets calculated from real-time video recording. The numerical rating scale (NRS) of behavior (Table 1) was used to visually score the horses prior to collection of the physiological data. The NRS assigns a numeric score to each behavior category that is weighted based on a descriptive definition of the behavior in each column. The NRS yielded a total Behavior score for each time point that is the sum of the scores assigned for each behavior category in Table 1. The Behavior score was subdivided into two components: Posture score and Socialization score. The Posture score was the sum of the scores for the categories describing gross pain behaviors, head position, ear position, location in the stall and spontaneous locomotion. The Socialization score was the sum of the scores for categories to monitor the response of the horse to positive stimuli. The positive stimuli were: opening the door and saying the horse’s name (response to open door); slowly approaching the horse while talking (response to approach); attempting to lift one front foot (lifting feet); and offering the horse a bucket of grain from the open door (response to grain). Horses were not allowed to eat the grain. Time budgets of behavior were calculated from real-time video recordings of the horses. For real-time video recording, the stall was equipped with a video camera connected to a time-relay device, video monitor, and video recorder. Each horse was videotaped for 1 h beginning at times 0, 4, 8, 12, and 20 h and for 1 h beginning between 24 and 30 h. A sign was posted on the stall door at the start of each hour of videotaping to prevent feeding, cleaning, or other interruptions by the animal care personnel. The videotaped segments for the 0 h, 4 h, 8 or 12 h, and 20 or 24–30 h time points were used for behavior scoring. The 8 or 12 h and the 20 or 24 h time points were selected based upon the horse being present and alone in the stall during those times. One Control horse
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Table 2 Definitions of individual behaviors, grouped by category, used to score the real-time video recordings of horses Category
Behavior
Description
Active
Eat Defecate Drink Flick Lick Nose Paw
Toss Urinate
Eating hay placed in the stall. Lifting the tail and evacuating feces. Drinking water from the bucket. Rapid, repetitive flicking the tail while standing. Licking the salt block. Investigating the walls, floor, or water bucket while taking strides or standing. A repetitive action with forelimb extended forward and then drawn back with the ventral toe dragging. Lying down and rolling. Rubbing any part of the body against the side of the stall or the front leg or raising the hind leg to scratch the head. A shake that involves the whole body. Movement of the front or hind feet that moves the body direction. This is distinguished from walking because only 2 feet move. Tossing, shaking, or stretching the head while standing. A visible urinary stream.
Locomotion
Graze Walk
Strides taken with the head down and visibly eating the bedding. Strides taken forward or backward.
Pain
Flank gesture Flehmen Kick Stretch
Turning the head while standing to look at the side of the body. Extending the head forward and curling the upper lip. Lifting the hind leg to strike at the abdomen. A wide-based stance with the back ventroflexed.
Resting
Stand
No movement or activity while standing with attention to the environment or in a restful posture. Sternal or lateral recumbency.
Roll Scratch Shake Shift
Rest
was removed from the stall prior to the 24 h videotaping due to demand for the stall, therefore data from the 20 h time point were used. One Anesthesia horse was removed from the stall for clinical examination during the 8 h videotaping, therefore data from the 12 h time point were used. Each videotaped segment was assigned a unique random number that determined the order in which the segments were scored, independently, by two trained observers. One observer was involved in the initial data collection; the second observer had no prior knowledge of the horses or study objectives. Observations from videotaped behavior of normal horses and horses recovering from abdominal surgery were used to determine the behaviors amenable to definition and measurement (Table 2). These preliminary observations were made using horses not involved in this study and the behavior definitions were refined by the observers until the definitions were mutually exclusive. The observers then scored the type and duration in seconds of each defined behavior from the videotapes of the study horses. Entry into the stall at the half-hour point of each videotaped hour to evaluate the response to positive stimuli for the NRS and to collect physiological data were not included in the behavior scoring. The videotape observers ceased scoring behavior from the moment the stall door opened and resumed scoring behavior when the stall door closed again.
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For the final analysis, the individual behaviors were categorized as Active, Locomotion, Pain, or Resting and a time budget of these categories was computed for each videotaped hour. The time budget was calculated by dividing the total duration of each behavior category for a segment by the total time scored for that segment to yield the percent of time in each category for each videotaped hour. The average of the two observers’ time budgets for each videotaped segment was used in the statistical analysis. 2.3. Statistical analysis The physiological and behavioral data were analyzed by two-factor analysis of variance with repeated measures on one factor, time. The least squares means and standard errors were calculated from the model for the effects of group and time. Bonferroni’s t-test of differences between the means was performed for the effects of group and time. Significant ðP < 0:05Þ effects were confirmed by the nonparametric Kruskal–Wallis test (General Linear Models and NPAR1WAY procedures, SAS1, SAS Institute Inc., Box 8000, Cary, NC 27511). The possible confounding factors of age and sex were analyzed by the same procedures. For these analyses, age was categorized as young (<8 years) or old (8 years) and sex was categorized as male (geldings and stallion) or female. Age or sex was used as the classification variable in the place of group to determine the effects on the dependent variables. To determine the degree of agreement between the observers for the videotaped behavioral data, the duration of individual behaviors at each time point were compared with the Bland-Altman method (1986) as if the two observers were two different assessment methods. For this analysis, the differences between the observers’ scores were plotted versus the means of their scores, where a slope of 0 and intercept of 0 indicate no systematic disagreement. The correlation, P value, slope standard error (S.E.), intercept S:E:, mean difference (M.D.), standard deviation (S.D.) of the difference, and limits of agreement were determined (Regression and Means procedures, SAS1, SAS Institute Inc., Box 8000, Cary, NC 27511).
3. Results 3.1. Physiological data The Surgery group had a longer ðP < 0:001Þ duration of anesthesia than the Anesthesia group. Median duration of anesthesia was 150 and 85 min, respectively, for the Surgery group and Anesthesia groups. The Surgery group had a higher ðP < 0:001Þ heart rate than the Control and Anesthesia groups throughout the observation period (Fig. 1), however respiratory rate did not differ among the groups (data not shown). The heart rate did not differ between the Control and Anesthesia groups and did not vary with time, whereas the heart rate in the Surgery group declined with time. The average plasma cortisol concentrations for one Control and one Surgery horse were below the normal range of the reference laboratory (85–180 nmol l1), therefore these
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Fig. 1. Heart rate ðL:S:M: S:E:M:Þ of stabled horses measured by auscultation every 4 h for 24 h. The experimental groups were: Control ðn ¼ 10Þ, horses received no treatment; Anesthesia ðn ¼ 10Þ, horses anesthetized for magnetic resonance imaging, a non-painful procedure; and Surgery ðn ¼ 7Þ, horses that presented for emergency surgery for acute gastrointestinal disease. The elevation in heart rate for the Surgery group was significant ðP < 0:001Þ throughout the observation period.
horses were deleted from the analysis. The Surgery group had a higher ðP < 0:03Þ plasma cortisol concentration than the Control and Anesthesia groups at each time point sampled (Fig. 2). The plasma cortisol concentration did not differ between the Control and Anesthesia groups. There was a time effect due to the significant decline in the plasma cortisol concentration in the Anesthesia group for the 24 h sample. 3.2. Numerical rating score of behavior The Surgery group had a higher ðP < 0:001Þ Behavior score, Posture score, and Socialization score than the Control and Anesthesia groups. There was no difference between the Control and Anesthesia groups for any of the NRS scores. There was no effect of time on any of the NRS scores therefore the least squares means of the scores by group averaged over all time are presented in Table 3. 3.3. Videotaped behavior data The agreement between the observers’ scores for the duration of individual behaviors was such that the total of all differences for individual behaviors of any one horse could be expected (95% confidence interval) to be less than 4.8 min, or approximately 8%. The individual behavior scores were used to calculate hour time budgets for each videotaped segment. The good agreement between the observers for individual behaviors validated averaging the time budgets calculated for each segment of videotape. The hour time-budgets differed ðP < 0:001Þ between all three groups for Active, Resting, and Pain behavior (Fig. 3). The Anesthesia group was the most active and least restful for all time points, followed by the Control group. The Surgery group was the least active and the most
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Fig. 2. Plasma cortisol concentration ðL:S:M: S:E:M:Þ of stabled horses measured by radioimmunoassay at 0, 4, 8, and 24 h after entry into the stall. The experimental groups were: Control ðn ¼ 9Þ, horses that did not receive any treatment; Anesthesia ðn ¼ 10Þ, horses anesthetized for magnetic resonance imaging, a non-painful procedure; and Surgery ðn ¼ 6Þ, horses that presented for emergency surgery for acute gastrointestinal disease. The elevated plasma cortisol concentration for the Surgery group was significant ðP < 0:03Þ throughout the observation period.
restful for all time points. Active behavior differed significantly at each time point only for the Anesthesia group. There was not a significant time effect on Active behavior for the Control and Surgery groups. Surgery was the only group with significant time spent in Pain behavior, however, even for this group, the percent of time was small (0–9.7%) compared with the percent of time with no movement, Resting (78.6–85.9%). There was not a significant time effect for Locomotion or Resting behaviors, therefore, the least squares means of the 4 h time-budgets by group are presented in Table 4. The timebudget for Locomotion was not different between Control (13:6 2:1%) and Anesthesia Table 3 The Behavior, Posture, and Socialization scores ðL:S:M: S:E:M:Þ of stabled horses computed from a numerical rating scale of behavior as described for Table 1 Group
Behavior score
Posture score
Socialization score
Control Anesthesia Surgery
13.3 0.4a 12.4 0.4a 19.6 0.5b
7.9 0.3a 7.2 0.3a 11.5 0.3b
5.4 0.2a 5.1 0.2a 8.1 0.3b
Means with different letters within a column differ ðP < 0:05Þ by the Bonferroni’s t-test. The experimental groups were: Control ðn ¼ 10Þ, horses that did not receive any treatment; Anesthesia ðn ¼ 10Þ, horses anesthetized for magnetic resonance imaging, a non-painful procedure; and Surgery ðn ¼ 7Þ, horses that presented for emergency surgery for acute gastrointestinal disease.
Fig. 3. Time budgets ðL:S:M: S:E:M:Þ of behavior of stabled horses measured by real-time video recordings 0, 4, 8–12, and 20–30 h after entry into the stall. The experimental groups were: Control ðn ¼ 10Þ, horses received no treatment; Anesthesia ðn ¼ 10Þ, horses anesthetized for magnetic resonance imaging, a non-painful procedure; and Surgery ðn ¼ 7Þ, horses that presented for emergency surgery for acute gastrointestinal disease. The hour time-budgets differed ðP < 0:001Þ between all three groups for Active, Resting, and Pain behavior. The time-budget for Locomotion was not different between the Control and Anesthesia groups and was significantly greater for these two groups than the Surgery group ðP < 0:05Þ.
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Table 4 The average time budgets ðL:S:M: S:E:M:Þ of behavior of stabled horses measured by real-time video recording Group
Active
Locomotion
Pain
Resting
Control Anesthesia Surgery
22.6 3.2a 42.3 3.3b 11.1 4.0c
13.6 2.1a 14.0 2.2a 1.9 2.6b
0.0 0.5a 0.3 0.05a 3.9 0.6b
63.8 3.1a 43.3 3.2b 83.0 3.8c
Means with different letters within a column differ ðP < 0:05Þ by the Bonferroni’s t-test. The experimental groups were: Control ðn ¼ 10Þ, horses that did not receive any treatment; Anesthesia ðn ¼ 10Þ, horses anesthetized for magnetic resonance imaging, a non-painful procedure; and Surgery ðn ¼ 7Þ, horses that presented for emergency surgery for acute gastrointestinal disease.
(14:0 2:2%) and was greater ðP < 0:05Þ for these two groups than the Surgery group (1:9 2:6%). 3.4. Confounding variables: age and sex Age or sex did not have an effect on the physiological or behavioral variables analyzed in this data set.
4. Discussion In this study, both physiological and behavioral data were collected on three groups of horses in an attempt to identify indicators of postoperative pain in horses following abdominal surgery. The combination of physiological and behavioral data is considered more useful than physiological measures alone to assess individual animal differences in response to environmental change and challenge (Manteca and Deag, 1993). The three experimental groups were 10 horses that did not receive any treatment, 10 horses that were anesthetized for MRI, a non-painful procedure, and 7 horses that had emergency surgery for acute gastrointestinal disease. The horses undergoing anesthesia for MRI were included to account for the effects of recovery from anesthesia on physiological (Taylor, 1989) and behavioral parameters. The study period of 24 h was chosen because postoperative pain peaks within 6–24 h following abdominal surgery in dogs (Hansen, 1997). Auscultation of the heart rate in recovering animals is simple, objective, and noninvasive. Heart rate is frequently measured in the clinical setting to monitor animals in the postoperative period. In this study, the heart rate was significantly elevated in the Surgery group compared with the Control and Anesthesia groups. Unfortunately, the physiological response of heart rate in the postoperative period has not been a useful indicator for pain assessment in dogs (Hansen et al., 1997) or cats (Smith et al., 1996). Other factors such as temperament (McCann et al., 1988), drug administration, and hypovolemia (Carroll, 1996) can affect the heart rate, confounding any association between elevated heart rate and pain. The heart rate measure may be more useful if it is added as a physiological component of a behavioral measurement scale (Firth and Haldane, 1999).
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Plasma cortisol concentrations in cats (Smith et al., 1996) and dogs (Fox et al., 1994) have been shown to increase significantly in response to surgical stress. A similar response was seen in the horses in our study. The Surgery group had a higher plasma cortisol concentration than the Control and Anesthesia groups at each time point sampled. Although samples for cortisol analysis were obtained at similar times of day for Control and Anesthesia horses, this was not possible for Surgery horses. Therefore, any potential confounding influence of circadian rhythm on data analysis could not be addressed. Future studies are under way to address this possibility. It is possible the elevated plasma cortisol concentration observed in the Surgery group is related to the extent of surgical injury or underlying disease in addition to postoperative pain. However the purpose of this study was to identify potential indicators of postoperative pain in horses. The correlation, if any, between plasma cortisol levels and tissue injury is beyond the scope of this study. The average cortisol concentration for the Anesthesia group was higher than the Control group at each time point, however this difference was not significant. The significant decline in plasma cortisol concentration in the Anesthesia group at the 24 h time point suggests these horses did have a stress response to the MRI procedure. This is consistent with the significant adrenocortical response due to anesthesia alone that has been reported in ponies (Taylor, 1989). Two horses in our study, one in the Control group and one in the Surgery group, had abnormally low plasma cortisol concentrations. Assessing adrenal gland function may improve the value of cortisol measurements for pain assessment (Fox et al., 1994). However, adrenal function tests would not be practical for client-owned horses presenting with acute gastrointestinal disorders. We used the normal range of plasma cortisol concentrations from the laboratory that assayed the samples to exclude these two horses based upon the average of four plasma samples. Preliminary observations from videotaped behavior of normal horses and horses recovering from abdominal surgery were important first steps to define behaviors that were comprehensive and unambiguous (Martin and Bateson, 1993). Many of our definitions are similar to those used by others for assessing the well being of horses (Bagshaw et al., 1994; McDonnell et al., 1999). By randomizing the order in which the videotaped segments were viewed and scoring the behavior by two observers, one unfamiliar with the objectives of the study, we successfully obtained behavioral data that is both unbiased and reliable as determined by the excellent agreement between the observers’ scores. For any hour of videotape scoring of any horse, the total of the differences between the observers’ scores for the durations of individual behaviors would be less than 5 min. From the time budget data we conclude that recovery from anesthesia did not adversely affect behavior. In fact, the Anesthesia horses spent more time in Active behavior than the Controls, a difference that could not be attributed to the sex or age differences between these groups. A likely explanation is that the Control group was from the teaching herd and many were familiar with the hospital environment. Although time did not have a significant effect on Locomotion behavior by repeated measures analysis of variance, the Anesthesia horses spent more time during the first hour in Locomotion. This may be due to the fact that feed was withheld from these horses prior to anesthesia for MRI and they spent the first hour after recovery from anesthesia searching the stall for food.
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When time budgets for four observation hours are considered, the Control and Anesthesia groups did not differ in the time spent in Locomotion and both groups spent significantly more time in Locomotion than the Surgery group. We conclude that the presence or absence of voluntary walking is a potential indicator of postoperative pain. This is in contrast with the generally accepted signs of visceral pain in horses which include: restlessness, looking at the flank, pawing, stretching the body, crouching, stretching the neck and flehmen, vocalizing, lying down, getting up again, lying down and rolling. These are signs associated with colic where the pain is attributed to increased pressure in the gastrointestinal tract (Lowe, 1992). Pawing and rolling were categorized as Active behavior in this study because these behaviors were observed in normal horses during preliminary observations to develop the behavior definitions. Flehmen, flank gestures, kicking the abdomen, and stretching the body were seen in preliminary observations of horses recovering from abdominal surgery, therefore, these were categorized as Pain behavior for the hour time-budget. Although significant painful behaviors were observed in the Surgery group, as shown in Fig. 2, the amount of time spent displaying Pain behaviors was small compared to the amount of time with no movement (Resting). If we assume that horses experience pain after abdominal surgery, this suggests that postoperative pain behavior differs from preoperative pain behaviors associated with colic. Our observations of postoperative behavior in horses support the observation reported by Hansen (1997) that animals severely debilitated by major surgery may be the least able to act painfully. Pain measurement scales are used in human and animal medicine to assess postoperative pain and the response to analgesia (Schade et al., 1996; Firth and Haldane, 1999). In this study, our NRS of behavior resulted in a total Behavior score as well as component scores associated with body position (Posture) and response to positive stimuli (Socialization). Pain behavior and locomotion are two components of the Behavior and Posture scores wherein the presence of painful behavior and the lack of locomotion generate a higher score. These scores were significantly higher in the Surgery group and did not differ between the Control and Anesthesia groups. These results are consistent with those obtained from the hour time budgets. The Surgery group was less responsive to positive stimuli than the Control and Anesthesia groups as indicated by the significantly higher Socialization score for the Surgery group. Our finding that the response of horses to positive stimuli is altered in the postoperative period is consistent with the significant reduction in interactive behavior following ovariohysterectomy reported in dogs (Hardie et al., 1997).
5. Conclusion The purpose of this study was to identify potential physiological and behavioral indicators of postoperative pain in horses that undergo exploratory celiotomy for acute gastrointestinal disorders. We conclude that reduced locomotion, elevated plasma cortisol concentration and elevated heart rate are potential indicators of postoperative pain in horses that may be useful in future studies to evaluate the efficacy of analgesic treatments following abdominal surgery.
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Acknowledgements This study was funded by a grant from the Morris Animal Foundation and a National Institutes of Health Summer Research Fellowship for Students in Health Professional Schools. The authors thank the team of students who assisted with the sampling: Betsy Charles, Dawn Deming, Matt Dredge, GayLynn Goolsby, Beth Hayes, Carl Johnson, Kurt Johnson, Jodi Nicklas, Dana Reid, and Abby Snodgrass. We also thank Dr. Bryan Slinker and Mr. Robert Kirkpatrick for valuable assistance with the data.
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