Comparison of lidocaine and compression for velvet antler analgesia in wapiti

Abstract

This research compared ring block lidocaine anesthesia (L) and compression (C) for velvet antler removal in elk. Thirty-two wapiti were given 1 mg/kg body weight of zuclopenthixol acetate. The next day, they were restrained in a hydraulic chute and given either a compression device or a lidocaine ring block on the antler pedicle. Behavioral and physiological responses to treatment application and antler removal were recorded, and blood was collected for cortisol analysis. During application of L and C, increases in mean heart rate and systolic arterial blood pressure were greater in the C treatment group (P < 0.05, and P = 0.05, respectively). When antler was removed, more behavioral responses occurred in the C treatment group (P = 0.02) and its median behavior score was higher (P = 0.03). Mean heart rates increased for both treatment groups when antlers were removed (P < 0.01). It was concluded that application of C may be painful, and that C was not as effective as L for analgesia for velvet antler removal.

Introduction

Velvet antler is harvested in most countries where commercial farming of wapiti (North American elk) and deer species has become part of the agricultural economy (1). It is processed and exported to Asia for the practice of Traditional Chinese Medicine, or it is used in the rapidly expanding North American nutraceutical market, where it is marketed for its perceived benefits to human health and performance (2).

Antler is removed during the growth phase, known as velvet, when it consists of well vascularized and innervated cartilaginous tissue rather than the highly mineralized hard bone of mature antler (3). Animals respond to painful stimuli applied to velvet antler (4,5,6). Procedures for antler removal have been shown to be aversive (7), although Matthews and Cook (8) proposed that antler removal was no more stressful than handling alone, because no additional cortisol response was observed after antler removal. Controlled experiments on techniques for antler removal clearly indicate the need for analgesia (5,6,8,9,10).

Great Britain, Ireland, some European countries, and the state of California have banned the practice of removing velvet antler from deer on the basis of ethical and welfare considerations (1). Continuation of velvet antler removal internationally depends on developing techniques for removal that are scientifically proven to be safe and humane. Various techniques for achieving analgesia of the growing antler have been described (10,11,12,13). The most reliable is the ring block, which requires SC injections of lidocaine hydrochloride at the base of the antler pedicles (1,6,14). However, the potential for local anesthetic drug residues in antler intended for health conscious consumers, particularly in Western world markets, is of concern to velvet antler producers and marketers (15,16). Canadian regulations require a 5-day withdrawal period for meat after lidocaine use in food animals. Consequently, there has been increased international interest in developing drug-free means of inducing analgesia in the antler (12,13,15,17). A rubber ring stretched around the antler pedicle under very high tension is one such procedure. (10,14,17). A standard rubber ring was conditionally approved for use on red deer spikers (yearlings) in New Zealand pending a field audit of the technique (18). An alternative technique involving the use of electric current was evaluated, but the present technology was found to be ineffective in many animals (10,12,14).

Results from previous studies designed to investigate the relative effectiveness of analgesic methods for velvet antler removal were equivocal, due to problems in separating experimental effects from background physiological effects resulting from fear and stress (19,20). In those studies, responses to possible pain at antler removal could not be distinguished easily from the “flight or fight” reaction or, possibly, a “freeze” response to being restrained or handled. Conversely, the effect of the analgesic techniques used could not be separated from that of possible endorphin release or the dissociative effects seen with extreme fear resulting from physical restraint and handling. Indeed, Stookey et al (20) observed no difference among groups in which “electro-anesthesia,” lidocaine analgesia, or no analgesia was used. They postulated that this must be “due to psychological factors influencing the experience or expression of pain in the experimental animals” (20).

The objective of the present study was to compare and evaluate behavioral and physiological responses of North American elk during lidocaine ring block analgesia and compression with a high tension band, and subsequent velvet antler removal. The present study attempted to reduce potentially confounding effects of stress associated with experimental procedures per se, by the administration of zuclopenthixol acetate, a long-acting tranquilizer shown to be effective in elk for that purpose (21).

Materials and methods

Thirty-two, 3- and 4-year-old, male North American elk were used for this study in June 2001. They belonged to Manitoba Agriculture and were maintained on a farm in southern Manitoba. The study protocol was approved by the University of Saskatchewan Committee on Animal Care. Each animal was randomly assigned to a treatment group to receive either lidocaine (L) (n = 16) or compression (C) (n = 16).

Each animal was moved through a handling system (NV Elk Modular Handling System; Bateman, Saskatchewan) and weighed. Animals were held in a hydraulic squeeze chute (Kiwi Elk System; Wildwood, Alberta) for identification and administration of the long-acting tranquilizer zuclopenthixol acetate (Clopixol Acuphase, 50 mg/mL; Lundbeck Canada, Montreal, Quebec), 1 mg/kg body weight (BW), into a hind limb muscle. Antler pedicle circumference was measured and BW was recorded. The animals were returned to pasture overnight.

The following day, each animal was brought into the hydraulic chute and restrained for experimental procedures. A head halter was fitted and attached to the chute, preventing injury in the event of head tossing during the procedure. A 22-gauge Teflon catheter (Surflo IV Catheter; Terumo Medical, Elkton, Maryland, USA) was placed in the left or right medial auricular artery, secured with cyanoacrylate cement (Krazy Glue; Elmer's Products Canada, Brampton, Ontario) and tape, and connected to a pressure transducer via noncompliant plastic tubing filled with heparinized saline. The transducer was joined to a physiological monitor (Propaq 400; Protocol Systems, Beaverton, Oregon, USA) to measure direct arterial pressures and heart rate (HR).

The same treatment was applied to both antlers of each animal. Compression was applied by using a rubber band applicator marketed for bloodless closed castration of cattle (Callicrate Smart Bander; No-bull Enterprises, St Francis, Kansas, USA). The rubber loops supplied with the applicator for castrations could not be placed over the branched antlers. Instead, an open loop of generic rubber latex tubing, of similar dimension (8.34 mm OD × 1.71 mm ID) to that supplied by the manufacturer, was placed around the 1st antler pedicle. The ends were then threaded through a sliding aluminum locking clip (Callicrate Locktight Clip; No-bull Enterprises) and fastened tightly together with a clenched copper hog ring (Decker Manufacturing; Keokuk, Iowa, USA). This modified rubber loop closely resembled the factory closed loop designed for castration with the bander. The band applicator was attached to the loop and tension applied as per manufacturer's directions until the bander device (Callicrate Smart Bander) indicated maximum tension, factory precalibrated at 260 Newtons of force on each side of the loop, producing a band with an initial width of approximately 6.4 mm. The process was repeated immediately on the remaining antler. Compression was applied for a standard 4 min from completion of the 2nd band application prior to antler removal. Therefore, each antler was given this treatment for a minimum of 4 min.

Lidocaine hydrochloride (Xylocaine 2%, 20 mg/mL; Astra Pharma, Mississauga, Ontario) was administered as a SC ring block, using a minimum of 1.2 mL/cm of pedicle circumference, in an overlapping manner to encircle the base of the antler pedicle. Total volume used was recorded. A 4-minute waiting period elapsed between completion of the 2nd antler block and antler removal.

A tourniquet of rubber surgical tubing was placed tightly around each pedicle of the L treatment group immediately after the waiting period and before antler removal. Antlers were removed with a coarse steel saw (9 teeth/2.5 cm), approximately 3 cm distal to the coronet, or antler-pedicle junction. Tourniquets and compression bands remained in place for approximately 5 min thereafter to allow for hemostasis, after which they were removed before the animals were released into a paddock for postoperative observation.

Behavioral response scores according to Wilson et al (6), as agreed to between 2 observers, were used to quantify the reactions to the application of the treatments and antler removal (Table1). Scores were 0 = no movement; 1 = slight head movement, flinch; 2 = head movement or shake, moderate avoidance of either the treatment or the saw; 3 = whole body struggle, “flight response.” For statistical analysis of the numbers of animals responding to treatment, behavior scores 1–3 were combined to avoid bias in interpretation, since the obvious presence or absence of the C device during antler removal did not allow blinding to the analgesic method.

Baseline direct arterial pressures and HR measurements were taken prior to application of the analgesic treatment (Time 1, (T₁)); during the administration of L or C treatment (T₂); 4 min after application of treatment to the 2nd antler and immediately prior to antler removal (T₃); immediately after antler removal (T₄); and at 1 (T₅), 2 (T₆), and 3 min after antler removal (T₇), as described in Figure 1. Blood was drawn from the arterial catheter prior to application of treatment and 3 min after antler removal, allowed to clot at room temperature, and then placed on ice for transport to a veterinary laboratory, where cortisol was analyzed by using a chemiluminesence immunoassay technique.

Figure 1. Time-line drawing showing antler removal events with behavior, heart rate, and blood pressure data points (T).

Data were analyzed and graphs generated using software (Prism, Version 3.0; GraphPad Software, San Diego, California and SPSS for Windows, Version 10.0; Analytical Software, Chicago, Illinois, USA). The statistical significance level was set at P < 0.05. Behavior scores for left and right antlers were pooled within treatment groups and the median response scores compared with a Mann Whitney test. The number of responders (scores 1–3 on one or both antlers) and nonresponders (score 0 on both antlers) were grouped by treatment and compared with a Fisher's exact test. Relative risk was calculated from the ratios of responders and nonresponders in each treatment group. Changes in HR, systolic arterial pressures (SAPs), mean arterial pressures (MAPs), and diastolic arterial pressures (DAPs) were determined by subtracting the baseline value (that was immediately preceding application of treatment) from each subsequent measurement. A positive value indicated an increase in HR or arterial pressure at that time. Repeated measures ANOVA (SPSS) was used to determine within-treatment group changes over time and to compare HR and arterial pressures over time between treatment groups. A Bonferroni multiple comparison test was used to determine where significant differences occurred (22). The changes in HR and arterial pressure from baseline at specific times were compared between treatments with a t-test. Mean pre- and post-antler removal serum cortisol values were compared by using t-tests.

Results

The clinical result on the day of experimental observations after having zuclopenthixol acetate administered the day before, was similar to that reported by Read et al (21). All animals were reasonably alert and sensitive to handling pressure at the time of experimentation but visibly lacking in the alarm or sympathetic response observed the previous day during the preliminary procedures.

The mean pedicle circumference in the L group was 17.1, s =1.6 cm. The total volume of lidocaine for both antlers combined averaged 50.4 , s = 9.27 mL.

Behavioral response scores for each antler during application of L and C, and during antler removal, are shown in Table 1. No response was observed when C was applied to either antler in 9 of 16 animals, and 6 of 16 when L was applied. The difference was not statistically significant. No response was observed on removal of either antler from 3 of 16 animals treated with C, and 10 of 16 animals treated with L (P = 0.03). Antler removal was 2.2 times more likely to evoke a behavioral response after compression than after lidocaine (95% CI, 1.2 to 4.3). While there was no significant difference in median behavioral scores between treatment groups during treatment application (P = 0.35), the median behavioral score was significantly higher in the C-treated group during antler removal (P = 0.03).

Table 1.

Mean and standard error of the mean (s_¯x) of HRs at each observation time are presented in Figure 2. Heart rates changed significantly from baseline over the experimental period (T₁ - T₇) within both treatment groups (Figure 2). In the C-treated group, the increases in HR during application of treatment (T₁ vs. T₂) and immediately after antler removal (T₁ vs. T₄) were significant (P < 0.01 and P < 0.05, respectively). In the L-treated group, there was a significant increase in HR immediately after antler removal (T₁ vs T₄) (P < 0.01), but not during application of treatment. Analysis showed a significantly larger increase in HR during application of C than of L (T₁ vs T₂) (P = 0.03), but no difference in magnitude of HR increase between C- and L-treated groups as a result of antler removal (T₁ vs. T₄).

Figure 2. Mean (± standard error of the mean) heart rates (bpm) in wapiti with compression (n = 16) and lidocaine (n = 16) pretreatment (T₁), during treatment administration (T₂), 4 min posttreatment (T₃), immediately and 1 to 3 min after antler removal (T_{4 - 7}). (^a) denotes significant difference from T₁ between treatments.

Systolic (SAPs), DAPs, and MAPs did not change significantly over the experimental period (T₁ - T₇) within either group (Figure 3). There was also no overall difference in arterial pressures between L and C treatment groups. However, comparisons of arterial pressures at specific events, for example, T₂, showed a significantly larger increase in SAPs during application of C than of L (T₂, P = 0.05).

Figure 3. Mean (± standard error of the mean) systolic blood pressure (mmHg) in wapiti given compression (n = 16) and lidocaine (n = 16) pretreatment (T₁), during treatment administration (T₂), 4 min posttreatment (T₃), immediately and 1 to 3 min after antler removal (T_{4 - 7}). (^a) denotes significant difference from T₁ between treatments.

Mean pretreatment serum cortisol concentrations for C and L groups were 167, s = 41 nmol/L and 162, s = 32 nmol/L, respectively. Mean posttreatment cortisol concentrations for C and L groups were 186, s = 32 and 179, s = 36 nmol/L, respectively. Serum cortisol concentrations increased in both groups after antler removal, but these changes were not significant either within or between treatment groups.

Discussion

This is the first published report evaluating the potential of a high tension rubber band as an alternative to local anesthetic for inducing analgesia of the antler of adult stags. This research was prompted by the need for elk and deer industries marketing velvet antler to pursue methods for analgesia that do not involve the risk of chemical residues (15,23)

A report of a previous study claimed that 1 h after the application of a rubber ring, analgesia was sufficient for antler removal in yearling (spiker) red deer (14). No reference to the pressure or tension of the ring was provided. The ring described is unlikely to have produced the pressure delivered by the technique described in this paper, so direct comparisons cannot be made. The report gave anecdotal evidence that a high-tension band produced effective analgesia more rapidly. While no difference in various behaviors after ring application compared with lidocaine analgesia was reported in the previous study (14), physiological responses, such as HR and blood pressures, that might be used as complementary measures of pain (24) were not investigated. Such measures should be used in conjunction with behavioral observations, because a paradoxical response of no physical movement to pain can occur, either because of a “freeze” response to the overall restraint and treatment circumstance or because the procedure is so painful that movement is inhibited. These effects may be detected by physiological measurements. Thus, behavioral observations alone, as employed in the previous study, may not be adequate for distinguishing whether or not application of the technique for analgesia of the antler per se is painful.

Heart rate, blood pressure, and serum cortisol measurements were used concurrently with behavioural scores in a previous study in elk to evaluate both whether “electro-analgesia” (EA), claimed to produce velvet antler analgesia (25), was effective and whether the technique itself was a painful or noxious stimulus (12). In that study, behavioral scores were not assessed during application of analgesic treatment (T₂), but 4 min after (T₃), there were significant increases in both HR and SAPs in the EA group, but not the lidocaine group. Based on this information, the study concluded that EA was inadequate for analgesia and that its application was painful (12). Thus, investigation of any novel method for analgesia should include not only whether analgesia is produced, but whether the technique per se is a noxious painful stimulus. This confirms that observations additional to behavior are required for such studies.

Previous authors evaluating the effectiveness of techniques for analgesia of velvet antlers reported difficulty in separating the stress response, resulting from animal handling and restraint from that resulting from pain associated with antler removal (5,8,20,26), from nonspecific movements by the deer, associated with activity about the head (6). Read et al (21) demonstrated the usefulness of zuclopenthixol acetate, a tranquilizer without intrinsic analgesic properties, for reducing the effect of stress of handling on physiological measurements, while likely not interfering with physical responses to pain. In an experiment similar to the present study, but investigating EA (25), Woodbury et al (12) showed that this drug effectively minimized the influence of the background stress of handling, restraint, and experimental manipulation on the main parameters measured. In the present experiment, this drug clearly tranquilized the animals, although some did struggle during physical restraint in the chute. Thus, while it is unlikely that all “background” influences were eliminated, we are confident that our data largely reflect the effects of application of the treatments and antler removal and not fear or distress associated with handling and restraint.

Compression was chosen for this study, because Matthews and Suttie (14) had suggested that pressure around the antler pedicle is effective in inducing analgesia in young stags and had shown promise in adult stags. Induction of analgesia after the application of compression bands has been reported in other species. A rat hind limb model has been studied extensively (27), and compression and ischemia may contribute to the local anesthetic effect of IV regional anesthesia in humans (28). Such studies were conducted largely on soft tissue. The anatomy of the antler pedicle and its supporting structures is such that there is limited depth of soft tissue containing nerves between skin and bone (11). A band applying very high pressure about the pedicle may induce analgesia more rapidly than 1 h, the time needed when the rubber ring technique of Matthews and Suttie (14) is applied. The bander marketed for castration of bulls (Callicrate Smart Bander; No-bull Enterprises) applies a very high pressure by tension upon a rubber band. In the present study, the mean tension applied to each side of the loop, despite being influenced by physical differences in antler pedicles between animals, would have been substantial in all cases. However, results of this study must be interpreted in the context of the specifications of the band used, since variations to these specifications may produce different results.

A behavioral response to antler removal was interpreted to mean that the animal was experiencing pain associated with surgical incision, incorporating the proposition that the higher the response score, the more painful the experience. Statistical analysis of numbers of animals responding combined all positive scores to remove potential observational bias, since the observations could not be blinded and because some animals respond to nonspecific stimuli during this procedure (1,6). Behaviors during application of treatment and antler removal could be interpreted as either pain or discomfort, or nonspecific response to manipulations about the head, although it is likely that the latter would be random between treatments. Thus, behavioral responses alone must be interpreted with caution. Behavioral observations during application of C and L in this study suggested no difference in aversiveness of either treatment.

Increase in HR and blood pressure was interpreted as evidence of a sympathetic nervous system response to pain experienced due to treatment application and antler removal (24). Concurrent observation of significantly elevated HR and SAP suggested that the application of C was a more aversive, possibly painful, stimulus than the application of L. It should be noted that the difference in HR recorded here may underestimate the real magnitude of the stimulus during the application of C, since more deer moved during application of L than C, and movement alone could have increased HR.

Removal of antlers from animals in both treatment groups elicited behavioral responses. This suggests that the lidocaine blocks were not fully effective on 6 of 16 animals. Wilson et al (6) observed behavioral responses to nonpainful stimuli and concluded that approximately 3% to 5% of deer responded to nonspecific stimuli during antler removal. The apparently higher nonachievement of analgesia following lidocaine in this study may be due to differences in technique, animal species, environment, handling system, and, possibly, drug potency. Similar apparent failure of ring blocks was observed in an observational survey referred to by Bartels et al (29). These observations suggest that the repeatability and reproducibility of ring block lidocaine analgesia for velvet antler removal requires further study. This is important, not just because only repeatable and reproducible forms of analgesia should be used for velvet antler removal (29), but because injectable local anesthetic is the current “gold standard” against which other techniques can be compared. If this standard is variable, interpretation of results of different studies is confounded.

The present study showed that more animals responded behaviorally to the acute pain stimulus of sawing the antler in the C-treatment group than in the L group, although no difference in physiological responses, including HR, were observed despite the fact that more animals in the C group moved. This could suggest that the 4-minute wait time was not adequate in all cases. It is notable that Matthews and Suttie (14) reported a wait time of 1 h for effective analgesia with their, probably lower pressure, compression ring. In that length of time, it is likely that nerves would have become ischemic and that conduction would have ceased. In this study, 4 min after compression was applied, there was apparent analgesia of 13 of 32 antlers, but this resulted in only 3 nonresponders out of 16 animals. This suggests that rapid onset of analgesia may be achievable if the technique used could be modified to improve repeatability. The mechanism of such analgesia is unknown. However, before this is investigated, it will be necessary to confirm that application of the technique is not painful, and there will need to be greater repeatability of analgesia (29). Science has a special responsibility in this regard (1).

While this study has shown that application of compression about the pedicle is simple, it has also shown that its application appears more aversive than the application of a lidocaine ring block, and that 4 min after application, analgesia is not as effective after compression as after lidocaine. However, the number and magnitude of differences with compression observed in this study are less than those observed when the same model was used in previous research to test EA (12). This could suggest that application of compression may not be as painful or aversive as EA. This seemingly more subtle difference in analgesia and aversiveness between C and L, combined with the complexity of behavioral and physiological observations and their interpretation in the conscious animal, suggests the need to employ more refined models, such as those used elsewhere for the study of pain associated with surgical procedures. It is essential that thorough investigations are undertaken before any new technique for antler analgesia is adopted by veterinarians, deer industries, and regulatory authorities, since there is an ethical and moral responsibility to ensure that there is no additional cost to animal welfare in doing so (1). CVJ