Veterinary Anaesthesia and Analgesia, 2016, 43, 63–71
doi:10.1111/vaa.12262
RESEARCH PAPER
Cardiorespiratory parameters in the awake pigeon and during anaesthesia with isoflurane Julie Botman*, Alex Dugdale†, Fabien Gabriel* & Jean-Michel Vandeweerd* *Integrated Veterinary Research Unit (IVRU), Namur Research Institute for Life Sciences (NARILIS), Department of Veterinary Medicine, Faculty of Sciences, University of Namur, Namur, Belgium †Department of Anaesthesiology, Faculty of Health and Life Sciences, University of Liverpool, Liverpool, UK
Correspondence: Jean-Michel Vandeweerd, Integrated Veterinary Research Unit (IVRU), Namur Research Institute for Life Sciences (NARILIS), Department of Veterinary Medicine, Faculty of Sciences, University of Namur, Rue de Bruxelles 61, 5000 Namur, Belgium. E-mail: [email protected]
Abstract Objective To determine baseline cardiovascular and respiratory variables in the awake pigeon, and to assess those variables during anaesthesia at the individual minimal anaesthetic concentration (MAC) of isoflurane during spontaneous breathing. Study design Prospective, experimental trial. Animals Seven healthy adult pigeons weighing a mean standard deviation (SD) of 438 38 g. Methods Heart rate (HR), heart rhythm, respiratory rate (fR), end-expired carbon dioxide tension (PE′CO2), indirect systolic arterial pressure (SAP) and cloacal temperature (T) were measured in birds in the awake state (after acclimatization to handling). Two weeks later, the pigeons were anaesthetized with isoflurane in order to determine their MAC and evaluate the same cardiovascular and respiratory variables during a further 40 minutes of isoflurane anaesthesia. Results In the awake pigeon, mean SD HR, SAP, fR, PE′CO2 and T were, respectively, 155 28 beats minute 1, 155 21 mmHg, 34 6 breaths minute 1, 38 8 mmHg (5.1 1.1 kPa) and 41.8 0.5 °C. Mean isoflurane MAC was 1.8 0.4%. During maintenance of anaesthesia at MAC, although no significant decreases between values 63
obtained in the awake and anaesthetized states emerged in HR or respiratory rate, significant decreases in SAP and cloacal temperature and an increase in PE′CO2 were observed. No arrhythmia was identified in awake pigeons, whereas secondand third-degree atrioventricular blocks occurred under isoflurane. Conclusions and clinical relevance Isoflurane MAC in pigeons appeared to be higher than in other avian species. Isoflurane anaesthesia in pigeons resulted in hypercapnia, hypotension, mild hypothermia and second- and third-degree atrioventricular blocks. Keywords anaesthesia, bird, blood pressure, cardiorespiratory, heart rate, isoflurane, pigeon.
Introduction In birds, anaesthesia can be provided either by injectable agents or by inhalation agents. Inhalation anaesthesia is the preferred technique (Naganobu & Hagio 2000; Gunkel & Lafortune 2005) and isoflurane has been traditionally used for avian anaesthesia (Escobar et al. 2011). Isoflurane anaesthesia is characterized by minimal cardiovascular adverse effects, rapid induction and short recovery times, although short periods of excitement during induction and recovery, and apnoea or cardiac arrhythmias during maintenance, have been reported in bald eagles (Aguilar et al. 1995; Joyner et al. 2008).
Isoflurane in pigeons J Botman et al. In the pigeon, anaesthesia protocols for isoflurane in which the delivered concentrations (according to vaporizer dial setting) were 3.0–5.0% for induction and 1.5–3.0% for maintenance have been described (Korbel 1998; Touzot-Jourde et al. 2005). An isoflurane minimal anaesthetic concentration (MAC), defined as the end-expired concentration of anaesthetic agent at which 50% of anaesthetized individuals will not move in response to a supramaximal noxious stimulus (Eger et al. 1965), of a mean standard deviation (SD) of 1.51 0.15% has been reported in pigeons (Fitzgerald & Blais 1991). Heart rate (HR), respiratory rate (fR), arterial blood pressure [systolic (SAP), mean (MAP)], end-expired carbon dioxide tension (PE′CO2) and blood gas analysis have been documented in a study assessing the effects of intermittent positive pressure ventilation in pigeons undergoing coelioscopy anaesthetized with isoflurane (Touzot-Jourde et al. 2005). Temperature, reflexes and peripheral haemoglobin oxygen saturation (SpO2) have been described in a study comparing the uses of isoflurane and sevoflurane in healthy pigeons (Korbel 1998). The normal electrocardiogram (ECG) of the unanaesthetized competition pigeon has been described (Murcia et al. 2005). However, there is a lack of information on cardiovascular (HR, heart rhythm, SAP, MAP) and respiratory (fR, PE′CO2) parameters when pigeons are anaesthetized with isoflurane outwith the context of surgical or diagnostic procedures and during spontaneous breathing. In addition, respiratory parameters and blood pressure have not been documented in the awake pigeon. This study aimed to assess cardiovascular and respiratory variables in the awake pigeon and during anaesthesia at the individual’s MAC of isoflurane during spontaneous breathing. Materials and methods Birds Seven adult pigeons were used in this study. They were selected for good health based on a physical examination, and treated with fenbendazole (Panacur; MSD Animal Health Belgium NV, Belgium) and ronidazole (Trichocure; Oropharma NV, Belgium) against parasites (worms, coccidia and trichomonas) 2 months prior to the experiment. They were housed in an aviary measuring 3 9 2 9 2 m). All seven pigeons were acclimatized to handling during a
2 month period before the study commenced. All animals entered and completed all phases of the study. The experiment protocol (14/209) was approved by the Ethical Committee for Animal Welfare of the University of Namur. Based on a power calculation, this sample size was sufficient to demonstrate, should it occur, a 20% difference in HR, blood pressure and respiratory rate between awake and anaesthetized pigeons, and the occurrence of arrhythmias. The bracketing method (Escobar et al. 2012) used in this study in the determination of MAC can be performed in small samples. Baseline monitoring parameters in awake animals Several physiological variables were measured in each pigeon in the awake state without tranquillization. Measurements were performed in a quiet environment. The bird was covered with a light towel to reduce stress. After the measuring instrument (e.g. ECG) had been placed, the pigeon was gently restrained for 15 minutes before measurements were obtained. Birds were restrained in an upright position for ECG and gas measurements to reduce the effects of stress (Murcia et al. 2005). For technical reasons, indirect SAP and cloacal temperature (T) were measured in dorsal recumbency. Each measure was obtained separately. ECGs were recorded for periods of 10 minutes. An ECG (Cardiocap; Datex-Ohmeda Oy, Finland) was used to assess HR and rhythm. Blunted alligator clip electrodes were connected directly to the skin at the patagium of each wing and at the skin fold proximal to the left stifle joint. Topical alcohol was used sparingly to increase conductivity at the electrode sites, but efforts were made to avoid an evaporative cooling effect. A Doppler blood flow probe and occlusive cuff with sphygmomanometer (Doppler Vet BP; Mano Medical, France) was used to monitor indirect SAP. A blood pressure cuff (size: 2.5 cm) (Pedisphyg; CAS Medical Systems, Inc., CT, USA) was positioned between the tibiotarsal–tarsometatarsal joint and the stifle joint. The width of the blood pressure cuff was equivalent to 40–50% of the limb circumference. The Doppler probe was placed, using ultrasound coupling gel to ensure adequate contact, distal to the blood pressure cuff, over the metatarsal artery. For gas analysis (inspired CO2, PE′CO2, inspired isoflurane and end-expired isoflurane), the sectioned blind end of a latex glove finger (size: small) was fixed around the beak of the pigeon
© 2015 Association of Veterinary Anaesthetists and the American College of Veterinary Anesthesia and Analgesia, 43, 63–71
64
Isoflurane in pigeons J Botman et al.
proximal to the nares (Fig. 1). This technique has already been reported in the administration of anaesthetic gases (Colmar 2008). A 20 gauge nonblunted needle connected via a sampling line to the gas analyser (Capnomac Ultima; Datex-Ohmeda Oy) was inserted into the glove and maintained with care close to the beak to measure inspired and endexpired gas composition. The gas analyser measured isoflurane percentages to one decimal place and CO2 tensions to the nearest 1 mmHg. The sidestream sampling rate of the gas analyser was 200 mL minute 1. The fresh gas flow of oxygen was set at 2–49 minute ventilation (minute ventilation was estimated as 200 mL 1 kg minute 1) so that oxygen (100%) was delivered at 0.3 L minute 1 through the other end of the glove using a non-rebreathing Bain system. The gas analyser’s calibration was checked against room air prior to and after each anaesthetic (to check that no drift occurred) for each bird. Before and after the study, the machine’s calibration was checked with a standard gas mixture [Quick Cal calibration gas (5% CO2, 55% O2, 3% agent, 37% N2); GE Healthcare BVBA, Belgium] by the service engineers. To measure body temperature, an electronic thermometer (Digi-Vet SC 12; Jørgen Kruuse A/S, Denmark) was inserted into the cloaca. Induction and maintenance Two weeks later, birds were fasted for 6 hours. Prior to anaesthesia, birds were allowed to breathe 100% oxygen (1 L minute 1) via a facemask for 5 minutes. Anaesthesia was induced with isoflurane
Figure 1 End-expired gas composition was measured during isoflurane anaesthesia in seven pigeons using a needle inserted into the finger of a glove and connected to the capnograph. The needle tip was positioned as near as possible to the bird’s nares. 65
(Vetflurane; Virbac SA, France) delivered in 100% oxygen (1 L minute 1) using a Bain nonrebreathing system and an initial vaporizer setting of 4%. Once the bird was sufficiently relaxed and voluntary movement of the eyelids had ceased, the face mask was removed and the trachea was intubated with a 3 mm non-cuffed endotracheal tube. The bird was then positioned in dorsal recumbency on an insulated mattress under an infrared light. Oxygen delivery was adjusted to 0.3 L minute 1 for the remainder of the procedure. Birds were allowed to breathe spontaneously. Monitoring parameters during anaesthesia After induction, instruments for gas analysis, ECG and Doppler measurements were placed. Endexpired gas samples were collected via a 20 gauge needle, the tip of which was inserted to lie within the lumen of the endotracheal tube. The sampling line was connected to the gas analyser for continuous monitoring of the inspired and end-expired isoflurane percentages, and inspired and end-expired CO2 tensions. Inspired CO2, PE′CO2 and T were recorded at baseline (start of the period for MAC determination) and observed every 5 minutes during MAC determination. Temperature was maintained between 39.2 and 41.2 °C. After MAC had been determined and the end-expired isoflurane concentration had been maintained for 15 minutes at 1.0 MAC, monitored variables were recorded immediately and again after 5, 10, 15, 20, 25, 30, 35 and 40 minutes. HR (beats minute 1), fR (breaths minute 1), and PE′CO2 (mmHg and kPa) were recorded three times over 1 minute and mean values were calculated. Then SAP (mmHg) was measured, and T (°C) was recorded from the cloacal temperature probe. Approximately 3 minutes were necessary to obtain all measurements at every time-point. ECG was recorded for the entire anaesthetic period. For analysis, cardiac arrhythmias were assigned a score on a scale of 0–2 (0 = no arrhythmia, 1 = arrhythmias observed during less than half of the anaesthetic period, 2 = arrhythmias observed for more than half of the anaesthetic period). MAC determination After stabilization at a predetermined anaesthetic concentration, the jaws of a Rochester–Carmalt forceps were used to clamp (to the first ratchet lock)
© 2015 Association of Veterinary Anaesthetists and the American College of Veterinary Anesthesia and Analgesia, 43, 63–71
Isoflurane in pigeons J Botman et al. the proximal part of a digit either until a gross purposeful movement occurred, such as kicking of the limbs or moving of the wings, or for up to 60 seconds if no observable response occurred. The end-expired anaesthetic concentration was decreased by 10% if no movement occurred. The procedure was repeated until the bird reacted. From this point, end-expired anaesthetic concentration was increased by 10% until the reaction disappeared. The MAC was defined and calculated as ‘the median value between the maximal end-expired concentration that allowed movement and the minimal end-expired concentration that prevented movement’ (Naganobu & Hagio 2000). End-expired isoflurane concentration was determined as the average of four samples. Intervals of interest Time to induction was defined as the time from the start of inhalant anaesthetic administration to successful intubation (Mercado et al. 2008). The time between intubation and the first stimulation for MAC determination (stabilization period) and the mean time from the start of inhalant anaesthetic administration to successful MAC determination were measured. After the last monitoring parameter had been measured, the vaporizer was turned off and 100% oxygen was administrated until the endotracheal tube was removed. Time to extubation was defined as the time from stopping inhalation of isoflurane (vaporizer turned off) to the time of coughing, swallowing or shaking of the head, resulting in removal of the endotracheal tube (Granone et al. 2012). Recovery time was defined as the time from stopping anaesthetic administration (vaporizer turned off) until the bird was able to stand and walk unassisted. Total anaesthetic time was defined as the period from the start of anaesthetic inhalation to the time of ceasing anaesthetic inhalation (Phair et al. 2012). Data analysis Kolmogorov–Smirnov and Shapiro–Wilk tests were used to examine the normality of data. Because of normality, the paired Student’s t-test was used to compare variables. Scores for arrhythmias were analysed using the non-parametric Wilcoxon signed-rank test. Differences were considered to be significant at a p-value of < 0.05. IBM SPSS Statistics for Windows Version 20.3 (IBM Corp., NY, USA) was
used for all analyses. Results are presented as the mean SD. Results The mean SD weight of the pigeons was 438 38 g. The MAC of isoflurane in this series of pigeons was estimated at 1.8 0.4%. The time between intubation and the first stimulation for MAC determination (stabilization period) was 20 4 minutes and the time from the start of inhalant anaesthetic administration to successful MAC determination was 116 11 minutes (15 minutes after this time = T0). Inspired CO2 was measured during the procedure and confirmed as always zero in both awake and anaesthetized birds. Cloacal temperature progressively decreased throughout anaesthesia to reach a minimum value of 39.2 °C in one pigeon (mean: 39.8 °C) during the period of MAC determination. By the end of the recording period (T40), the temperature was 39.5 0.7 °C. Physiological parameters in both awake and anaesthetized pigeons are reported in Table 1. Intervals of interest are reported in Table 2. Changes in HR, SAP, fR and PE′CO2 during 40 minutes of anaesthesia are described in Figs 2 & 3. No arrhythmias were identified in awake pigeons. Under isoflurane, arrhythmias occurred frequently. The occurrence of arrhythmias is summarized in Table 3. Five pigeons developed seconddegree heart blocks. Arrhythmias resolved after the discontinuation of isoflurane. Discussion This study provides information about physiological variables in both the awake pigeon and the pigeon under isoflurane anaesthesia administered outwith the context of surgical or diagnostic procedures and during spontaneous breathing. Awake pigeons were found to have an HR of 155 28 beats minute 1, which is lower than the value of 273 83 beats minute 1 reported in the literature (Murcia et al. 2005); however, these earlier authors did not report a period of acclimatization to handling. The discrepancy between values may possibly be explained by the quietness of the pigeons in the current study, which had been accustomed to handling for a period of 2 months. Data from the present study show more similarity to those reported by R€ uther (1998), who recorded an HR of 121 beats minute 1 obtained from six
© 2015 Association of Veterinary Anaesthetists and the American College of Veterinary Anesthesia and Analgesia, 43, 63–71
66
Isoflurane in pigeons J Botman et al.
Table 1 Mean standard deviation heart rate (HR), systolic blood pressure (SAP), respiratory rate (fR), end-expired carbon dioxide tension (PE′CO2) and temperature (T) in seven pigeons in the awake state and under isoflurane anaesthesia at time 0 (15 minutes after stabilization at the individual minimal anaesthetic concentration value)
Variable
Awake state
HR (beats minute 1) SAP (mmHg) fR (breaths minute 1) PE′CO2 (mmHg) PE′CO2 (kPa) T (°C)
155 155 34 38 5.1 41.8
28 21* 6 8* 1.1 0.5*
Isoflurane anaesthesia 135 87 34 52 6.9 39.5
28 11* 8 7* 0.9 0.7*
*Significant difference between awake and anaesthetized pigeons (p < 0.05).
Table 2 Induction and recovery characteristics in seven pigeons anaesthetized with isoflurane. Results are reported as the mean standard deviation Time (minutes:seconds seconds)
Variable Time Time Time Total
to intubation to extubation to recovery anaesthetic time
4:18 8:42 17:36 159:54
60 108 204 630
pigeons over a period of several days using telemetry, which did not require concurrent handling. In this study, there was no significant decrease in HR from the awake to the anaesthetized state under isoflurane. This absence of a significant reduction in HR was also observed in a study conducted in crested caracaras (Escobar et al. 2011), whereas HR was found to be significantly lower in other studies carried out in anaesthetized common buzzards (Straub et al. 2003) and thick-billed parrots (Mercado et al. 2008). No arrhythmias were recorded in awake pigeons in the current study. Similar findings were observed in 64 awake pigeons also gently restrained in an upright position (Murcia et al. 2005). Conversely, in a study of awake and free-standing pigeons in which recordings were obtained by telemetry, nine of 10 awake pigeons were found to demonstrate seconddegree heart blocks (R€ uther 1998). This author reported that all atrioventricular (AV) blocks resolved with increasing HR. Second-degree AV heart blocks (in which at least one but less than the majority of P waves show no association with a QRS complex) occurred in five pigeons anaesthetized with isoflurane in this study, one of which also showed a third-degree AV heart 67
block. Arrhythmias under isoflurane anaesthesia were observed in two studies in bald eagles (Aguilar et al. 1995; Joyner et al. 2008). In those studies, second-degree heart block was the most frequently observed arrhythmia. Several hypotheses have been suggested to explain arrhythmias. Ocular pressure may be caused inadvertently during mask induction, increasing vagal tone and causing arrhythmias such as seconddegree heart block (Joyner et al. 2008). However, in the current study three pigeons had arrhythmias for more than half of the anaesthetic period. This suggests that an inadvertent oculocardiac reflex was not the cause of the second-degree heart block. Respiratory acidosis and hypoxaemia can also cause arrhythmias (Aguilar et al. 1995). In the current study, we did not measure partial pressure of oxygen and pH in arterial blood, but birds became mildly hypercapnic, which can lead to respiratory acidosis. As dorsal recumbency can reduce ventilation, possibly partly because abdominal viscera compress the abdominal air sacs (King & Payne 1964), it can predispose to CO2 retention and the resultant hypercapnia may then predispose to arrhythmias. Catecholamine release resulting from stress can also induce abnormalities of the heart rhythm, but tachycardic rhythms would tend to be more likely (Aguilar et al. 1995). In this study, the previous acclimatization of awake pigeons to handling may have prevented stress. In another study in unanaesthetized competition pigeons (Murcia et al. 2005), no prior training was performed and no arrhythmias occurred; however, competition pigeons are used to being hand-restrained. Arrhythmias were reported to occur spontaneously in free-standing pigeons at lower HRs and were reported to resolve when HR increased (R€ uther 1998). This might strengthen the
© 2015 Association of Veterinary Anaesthetists and the American College of Veterinary Anesthesia and Analgesia, 43, 63–71
Isoflurane in pigeons J Botman et al.
Figure 2 Changes in mean heart rate (HR) and systolic arterial blood pressure (SAP) over time (T) during isoflurane anaesthesia in seven pigeons. The initial measurement (T0) was fixed at 15 minutes after stabilization at the individual minimal anaesthetic concentration value.
Figure 3 Changes in mean end-expired carbon dioxide tension (PE′CO2) and respiratory rate (fR) over time (T) during isoflurane anaesthesia in seven pigeons. T0 is fixed at 15 minutes after stabilization at the individual minimal anaesthetic concentration value.
hypothesis that arrhythmias can be linked to increased vagal tone (Aguilar et al. 1995), which occurs, for example, during anaesthesia. In this series, SAP in awake birds was 155 21 mmHg, which is similar to the values of 120–150 mmHg described in the literature (Boucher et al. 2009). During isoflurane anaesthesia, SAP was significantly lower (87 11 mmHg), as previously reported in pigeons undergoing coelioscopy (Touzot-Jourde et al. 2005). Isoflurane is known to be a vasodilator (Schnellbacher et al. 2012) and the consequent decrease in systemic vascular resistance may represent the main cause of hypotension; the degree of hypotension has been correlated with depth of isoflurane anaesthesia in other avian species (Ludders et al. 1989; Naganobu & Hagio 2000; Kim et al. 2011). In awake pigeons, a baseline respiratory rate of 30 breaths minute 1 has been reported (Villate 2001; Boussarie et al. 2002). A similar value was
observed in this study (34 6 breaths minute 1). The fR value did not differ significantly between awake and anaesthetized birds. Some short periods of apnoea occurred during induction or recovery, but resolved unaided or by slightly moving the endotracheal tube. Other studies have reported significant decreases in respiratory rate (Machin & Caulkett 2000; Joyner et al. 2008; Mercado et al. 2008; Escobar et al. 2011; Granone et al. 2012). However, birds in these studies were anaesthetized at isoflurane concentrations higher than MAC (Mercado et al. 2008; Granone et al. 2012), or at concentrations presumed to be higher (1.5–3.0%) in species for which MAC had not been determined (Machin & Caulkett 2000; Joyner et al. 2008; Escobar et al. 2011). As isoflurane is known to depress ventilation in a dose-dependent manner (Gleed & Ludders 2001), this could explain the absence of a decrease in respiratory rate in the present study.
© 2015 Association of Veterinary Anaesthetists and the American College of Veterinary Anesthesia and Analgesia, 43, 63–71
68
Isoflurane in pigeons J Botman et al.
Table 3 Occurrences of arrhythmia in seven pigeons during isoflurane anaesthesia
Pigeon
I
S
P1
P2
P3
P4
P5
P6
P7
P8
MAC
T0
T5
T10
T15
T20
T25
T30
T35
T40
1 2 3 4 5 6 7
0 0 0 0 0 0 0
2 0 0 2 0 0 0
2 2 0 0 0 0 0
2 2 0 0 0 2 0
2 3 2 2 0 2 0
2 3 2 2 0 2 0
2 2 0 2 0 2 0
2 2 2 0 / 0 0
2 / 0 / / 0 0
/ / / / / / 0
2 3 2 2 0 2 0
2 3 2 2 0 2 0
0 3 0 2 0 2 0
0 3 0 2 0 2 0
0 3 0 2 0 2 0
0 3 0 2 0 2 0
0 0 0 2 0 2 0
0 0 0 2 0 2 0
0 0 0 2 0 2 0
0 0 0 2 0 2 0
0 = no arrhythmia; 2 = second-degree atrioventricular block; 3 = third-degree atrioventricular block. I, intubation; MAC, minimal anaesthetic concentration; P, time period between two stimuli (= 15 minutes); S, period of stabilization (between intubation and first stimulus; 20 4 minutes). / indicates that MAC had been determined and no further stimulus was required. MAC corresponds to a period of 15 minutes at MAC before parameters were recorded.
Because of the difficulty of catheterizing an artery, blood gas analysis was not considered. Instead, PE′CO2 was used to assess ventilatory adequacy. A PE′CO2 of 38 8 mmHg (5.1 1.1 kPa) was measured in awake pigeons; this rose significantly under isoflurane anaesthesia to 52 7 mmHg (6.9 0.9 kPa). However, PE′CO2 has been found to overestimate PaCO2 by 5 mmHg (0.7 kPa) in pigeons and African grey parrots as a result of the cross-current mechanism of gas exchange in avian lungs (Touzot-Jourde et al. 2005; Longley 2008). Increases in PE′CO2 or PaCO2 have also been observed in other avian species anaesthetized with isoflurane during spontaneous ventilation (Ludders et al. 1989; Joyner et al. 2008; Escobar et al. 2011). Dorsal recumbency, muscle relaxation, the absence of a diaphragm, and the effects of isoflurane on the central nervous system and peripheral chemoreceptors may explain the ventilatory depression (Gleed & Ludders 2001). The MAC, determined for isoflurane using the ‘bracketing’ technique, was 1.8 0.4% in this series of seven pigeons. This value is higher than those reported for other avian species. MAC values for isoflurane were reported to be 1.07% in thickbilled parrots (Mercado et al. 2008), 1.34 0.14% in sandhill cranes (Ludders et al. 1989), 1.25 0.13% in chickens (Naganobu & Hagio 2000), 1.30 0.23% in Pekin ducks (Ludders et al. 1990), 1.45 0.07% in red-tailed hawks (Fitzgerald & Blais 1991) and 1.06 0.07% in cinereous vultures (Kim et al. 2011). Our findings also differ from the isoflurane MAC value of 1.51 0.15% measured in a study in 12 adult pigeons (Fitzgerald & Blais 1991). It is known that MAC values can vary by up to 10% within the same 69
animal and up to 20% within the same species (Quasha et al. 1980). In addition, different estimations of MAC can be obtained with different stimulation techniques (electric or mechanical) (Phair et al. 2012). A previous study in pigeons used an electrical stimulus (50 V, 50 Hz, 7.5 milliseconds) as a supramaximal stimulus (Fitzgerald & Blais 1991), whereas the present study used a mechanical stimulus (digit clamping). The difference between our findings and those of Fitzgerald & Blais (1991) may also be explained by subjectivity in the assessment of ‘a gross purposeful movement’ and the mode of application of the noxious stimulus. For example, the type of haemostat used (with or without plastic tubing on the jaws and applied at different ratchet locks) can influence the estimation of MAC (Valverde et al. 2003). Other physiological factors such as body temperature, metabolic rate, blood CO2 tension and large variations in blood pressure can influence the determination of MAC (Quasha et al. 1980). In laboratory mammals, MAC decreased by 4–5% per 1 °C decrease in temperature to result in the complete elimination of the requirement for anaesthesia at 20 °C (Eger 2001). In the current study, despite the use of an infrared light and insulated bed during anaesthesia, T values progressively decreased over time. Temperature was 39.7 °C at T0 and 39.5 0.7 °C during the 40 minutes of anaesthesia at MAC. However, this variation did not exceed 2 °C as temperature during the period of determination of MAC ranged from 41.2 °C to 39.2 °C. At a maximum temperature decrease of 2 °C, MAC may have been underestimated, although our values would still have been higher than those previously reported. This decrease in T during isoflurane anaesthesia was also
© 2015 Association of Veterinary Anaesthetists and the American College of Veterinary Anesthesia and Analgesia, 43, 63–71
Isoflurane in pigeons J Botman et al. observed in other species despite the use of supplemental heat sources (Machin & Caulkett 2000; Joyner et al. 2008; Mercado et al. 2008; Escobar et al. 2011; Granone et al. 2012). A study in dogs demonstrated that profound hypocapnia [PaCO2 below 10–15 mmHg (1.3– 2.0 kPa)] and extreme hypercapnia [PaCO2 in excess of 90–95 mmHg (12.0–12.7 kPa)] can reduce MAC (Eisle et al. 1967). Another study in rats, however, demonstrated a linear relationship between MAC and PaCO2 (Brosnan et al. 2007). At this time, no information on the effects of changing PaCO2 on avian MAC, or indeed in pigeons, is available. It therefore remains to be determined whether the mild hypercapnia observed in this study had any influence on MAC values. Isoflurane resulted in the smooth and rapid induction of anaesthesia in pigeons. Time to induction was almost twice that reported in a previous study (Korbel 1998). One reason for the difference refers to discrepancies in definitions of the end point of anaesthetic induction: the present study defined induction as the time between the start of isoflurane administration and successful tracheal intubation, whereas Korbel (1998) used the start of isoflurane administration to the loss of reflexes to an ill-defined noxious stimulus. Secondly, anaesthesia was induced with 5% isoflurane by Korbel (1998), but with 4% isoflurane in the current study. Recovery time to standing/walking was longer in the present study than the time to return of the righting reflex (Korbel 1998), again demonstrating that careful description of the events that define these times is important. Return of the righting reflex occurs sooner than the ability to stand and walk unassisted. Furthermore, the whole process in this study (induction, MAC determination, 15 minutes of stabilization and 40 minutes for monitoring parameters) was longer than the 60 minutes of anaesthesia used by Korbel (1998) and may also have influenced recovery time. Conclusions The MAC of isoflurane determined in pigeons in the present study is higher than MAC values previously reported for pigeons and other birds. Isoflurane resulted in the smooth and rapid induction of anaesthesia in pigeons, similarly to other species, although recovery time in this study was longer than those reported elsewhere. Isoflurane resulted in mild hypothermia and hypotension. A salient find-
ing was the significant development of second- and third-degree cardiac blocks. Hypercapnia was also observed, which suggests that ventilatory assistance may be recommended. References Aguilar RF, Smith VE, Ogburn P et al. (1995) Arrhythmias associated with isoflurane anesthesia in bald eagles (Haliaeetus leucocephalus). J Zoo Wildl Med 26, 508–516. Boucher S, Bulliot C, Doumerc G et al. (2009) Examens Complementaires chez les NAC. Editions du Point Vet, France. Boussarie D, Schilliger L, Rival F (2002) Vade-Mecum d’Anesthesie des NAC. Editions Med’Com, France. Brosnan RJ, Eger EI II, Laster MJ et al. (2007) Anesthetic properties of carbon dioxide in the rat. Anesth Analg 105, 103–106. Colmar C (2008) Prise en charge chirurgicale de l’oiseau: l’attention du praticien. These de fin fichier technique a d’etude donnant acces a la pratique de la medecine veterinaire. Ecole Nationale Veterinaire de Toulouse. pp. 27–28. Eger EI II (2001) Age, minimum alveolar anesthetic concentration, and minimum alveolar anesthetic concentration-awake. Anesth Analg 93, 947–953. Eger EI II, Saidman LJ, Brandstater B (1965) Minimum alveolar anesthetic concentration: a standard of anesthetic potency. Anesthesiology 26, 756–763. Eisle JH, Eger EI II, Muallem M (1967) Narcotic properties of carbon dioxide in the dog. Anesthesiology 28, 856– 865. Escobar A, Thiesen R, Vitaliano S et al. (2011) Cardiorespiratory effects of isoflurane anesthesia in crested caracaras (Caracara plancus). J Zoo Wildl Med 42, 12–17. Escobar A, Valad~ ao CA, Brosnan RJ et al. (2012) Effects of butorphanol on the minimum anesthetic concentration for sevoflurane in guineafowl (Numida meleagris). Am J Vet Res 73, 183–188. Fitzgerald G, Blais D (1991) Effect of nitrous oxide on the minimal anaesthetic dose of isoflurane in pigeons and red-tailed hawks. Vet Anaesth Analg 18, 111–115. Gleed RD, Ludders JW (2001) Recent advances in veterinary anesthesia and analgesia: companion animals. International Veterinary Information Service, NY, USA. http://www.ivis.org/advances/Anesthesia_Gleed /ludders2/chapter.asp?LA=1 (Accessed 2 November 2013). Granone T, de Francisco O, Killos M et al. (2012) Comparison of three different inhalant anesthetic agents (isoflurane, sevoflurane, desflurane) in red-tailed hawks (Buteo jamaicensis). Vet Anaesth Analg 39, 29–37. Gunkel C, Lafortune M (2005) Current techniques in avian anesthesia. Semin Avian Exot Pet Med 14, 263– 276.
© 2015 Association of Veterinary Anaesthetists and the American College of Veterinary Anesthesia and Analgesia, 43, 63–71
70
Isoflurane in pigeons J Botman et al.
Joyner PH, Jones MP, Ward D et al. (2008) Induction and recovery characteristics and cardiopulmonary effects of sevoflurane and isoflurane in bald eagles. Am J Vet Res 69, 13–22. Kim Y, Lee SS, Suh E et al. (2011) Minimum anesthetic concentration and cardiovascular dose–response relationship of isoflurane in cinereous vultures (Aegypius monachus). J Zoo Wildl Med 42, 499–503. King AS, Payne DC (1964) Normal breathing and the effects of posture in Gallus domesticus. J Physiol (London) 174, 340–347. Korbel R (1998) Vergleichende Untersuchungen zur Inhalationsan€ asthesie mit Isofluran (Forene) und Sevofluran (SEVOrane) bei Haustauben (Columba livia Gmel., 1789, var. domestica) und Vorstellung eines Referenz-Narkoseprotokolls f€ ur V€ ogel. Tier€ arztl Prax 26 (K), 211–223. Longley LA (2008) Anaesthesia of Exotic Pets. Elsevier Saunders, USA. pp. 159–160. Ludders JW, Rode J, Mitchell GS (1989) Isoflurane anesthesia in sandhill cranes (Grus canadensis): minimal anesthetic concentration and cardiopulmonary doseresponse during spontaneous and controlled breathing. Anesth Analg 68, 511–516. Ludders JW, Mitchell GS, Rode J (1990) Minimal anesthetic concentration and cardiopulmonary dose response of isoflurane in ducks. Vet Surg 19, 304–307. Machin KL, Caulkett NA (2000) Evaluation of isoflurane and propofol anesthesia for intraabdominal transmitter placement in nesting female canvasback ducks. J Wildl Dis 36, 324–334. Mercado JA, Larsen RS, Wack RF et al. (2008) Minimum anesthetic concentration of isoflurane in captive thick-billed parrots (Rhynchopsitta pachyrhyncha). Am J Vet Res 69, 189–194. Murcia LMM, Bernal LJ, Montes AM et al. (2005) The normal electrocardiogram of the unanaesthetized
71
competition ‘Spanish Pouler’ pigeon (Columba livia gutturosa). J Vet Med A Physiol Pathol Clin Med 52, 347–349. Naganobu K, Hagio M (2000) Dose-related cardiovascular effects of isoflurane in chickens during controlled ventilation. J Vet Med Sci 62, 435–437. Phair K, Larsen S, Wack R et al. (2012) Determination of the minimum anesthetic concentration of sevoflurane in thick-billed parrots (Rhynchopsitta pachyrhyncha). Am J Vet Res 73, 1350–1355. Quasha AL, Eger EI II, Tinker JH (1980) Determination and applications of MAC. Anesthesiology 53, 315–334. R€ uther P (1998) Untersuchungen zur tageszeitabh€angigen Rhythmik der Ruheherzfrequenz und ausgew€ ahlter Arrhythmien bei der Brieftaube (Columba livia f. domestica). PhD thesis, Free University of Berlin. p. 103. Schnellbacher R, Cunha AF, Beaufrere H et al. (2012) Effects of dopamine and dobutamine on isofluraneinduced hypotension in Hispaniolan Amazon parrots (Amazona ventralis). Am J Vet Res 73, 952–958. Straub J, Forbes N, Thielebein J et al. (2003) The effects of isoflurane anaesthesia on some Doppler-derived cardiac parameters in the common buzzard (Buteo buteo). Vet J 166, 273–276. Touzot-Jourde G, Hernandez-Divers SJ, Trim CM (2005) Cardiopulmonary effects of controlled versus spontaneous ventilation in pigeons anesthetized for coelioscopy. J Am Vet Med Assoc 227, 1424–1428. Valverde A, Morey T, Hern andez J et al. (2003) Validation of several types of noxious stimuli for use in determining the minimum alveolar concentration for inhalation anesthetics in dogs and rabbits. Am J Vet Res 64, 957– 962. Villate D (2001) Maladies des Volailles (2nd edn). France Agricole, France. p. 45. Received 16 March 2014; accepted 4 December 2014.
© 2015 Association of Veterinary Anaesthetists and the American College of Veterinary Anesthesia and Analgesia, 43, 63–71
doi:10.1111/vaa.12262
RESEARCH PAPER
Cardiorespiratory parameters in the awake pigeon and during anaesthesia with isoflurane Julie Botman*, Alex Dugdale†, Fabien Gabriel* & Jean-Michel Vandeweerd* *Integrated Veterinary Research Unit (IVRU), Namur Research Institute for Life Sciences (NARILIS), Department of Veterinary Medicine, Faculty of Sciences, University of Namur, Namur, Belgium †Department of Anaesthesiology, Faculty of Health and Life Sciences, University of Liverpool, Liverpool, UK
Correspondence: Jean-Michel Vandeweerd, Integrated Veterinary Research Unit (IVRU), Namur Research Institute for Life Sciences (NARILIS), Department of Veterinary Medicine, Faculty of Sciences, University of Namur, Rue de Bruxelles 61, 5000 Namur, Belgium. E-mail: [email protected]
Abstract Objective To determine baseline cardiovascular and respiratory variables in the awake pigeon, and to assess those variables during anaesthesia at the individual minimal anaesthetic concentration (MAC) of isoflurane during spontaneous breathing. Study design Prospective, experimental trial. Animals Seven healthy adult pigeons weighing a mean standard deviation (SD) of 438 38 g. Methods Heart rate (HR), heart rhythm, respiratory rate (fR), end-expired carbon dioxide tension (PE′CO2), indirect systolic arterial pressure (SAP) and cloacal temperature (T) were measured in birds in the awake state (after acclimatization to handling). Two weeks later, the pigeons were anaesthetized with isoflurane in order to determine their MAC and evaluate the same cardiovascular and respiratory variables during a further 40 minutes of isoflurane anaesthesia. Results In the awake pigeon, mean SD HR, SAP, fR, PE′CO2 and T were, respectively, 155 28 beats minute 1, 155 21 mmHg, 34 6 breaths minute 1, 38 8 mmHg (5.1 1.1 kPa) and 41.8 0.5 °C. Mean isoflurane MAC was 1.8 0.4%. During maintenance of anaesthesia at MAC, although no significant decreases between values 63
obtained in the awake and anaesthetized states emerged in HR or respiratory rate, significant decreases in SAP and cloacal temperature and an increase in PE′CO2 were observed. No arrhythmia was identified in awake pigeons, whereas secondand third-degree atrioventricular blocks occurred under isoflurane. Conclusions and clinical relevance Isoflurane MAC in pigeons appeared to be higher than in other avian species. Isoflurane anaesthesia in pigeons resulted in hypercapnia, hypotension, mild hypothermia and second- and third-degree atrioventricular blocks. Keywords anaesthesia, bird, blood pressure, cardiorespiratory, heart rate, isoflurane, pigeon.
Introduction In birds, anaesthesia can be provided either by injectable agents or by inhalation agents. Inhalation anaesthesia is the preferred technique (Naganobu & Hagio 2000; Gunkel & Lafortune 2005) and isoflurane has been traditionally used for avian anaesthesia (Escobar et al. 2011). Isoflurane anaesthesia is characterized by minimal cardiovascular adverse effects, rapid induction and short recovery times, although short periods of excitement during induction and recovery, and apnoea or cardiac arrhythmias during maintenance, have been reported in bald eagles (Aguilar et al. 1995; Joyner et al. 2008).
Isoflurane in pigeons J Botman et al. In the pigeon, anaesthesia protocols for isoflurane in which the delivered concentrations (according to vaporizer dial setting) were 3.0–5.0% for induction and 1.5–3.0% for maintenance have been described (Korbel 1998; Touzot-Jourde et al. 2005). An isoflurane minimal anaesthetic concentration (MAC), defined as the end-expired concentration of anaesthetic agent at which 50% of anaesthetized individuals will not move in response to a supramaximal noxious stimulus (Eger et al. 1965), of a mean standard deviation (SD) of 1.51 0.15% has been reported in pigeons (Fitzgerald & Blais 1991). Heart rate (HR), respiratory rate (fR), arterial blood pressure [systolic (SAP), mean (MAP)], end-expired carbon dioxide tension (PE′CO2) and blood gas analysis have been documented in a study assessing the effects of intermittent positive pressure ventilation in pigeons undergoing coelioscopy anaesthetized with isoflurane (Touzot-Jourde et al. 2005). Temperature, reflexes and peripheral haemoglobin oxygen saturation (SpO2) have been described in a study comparing the uses of isoflurane and sevoflurane in healthy pigeons (Korbel 1998). The normal electrocardiogram (ECG) of the unanaesthetized competition pigeon has been described (Murcia et al. 2005). However, there is a lack of information on cardiovascular (HR, heart rhythm, SAP, MAP) and respiratory (fR, PE′CO2) parameters when pigeons are anaesthetized with isoflurane outwith the context of surgical or diagnostic procedures and during spontaneous breathing. In addition, respiratory parameters and blood pressure have not been documented in the awake pigeon. This study aimed to assess cardiovascular and respiratory variables in the awake pigeon and during anaesthesia at the individual’s MAC of isoflurane during spontaneous breathing. Materials and methods Birds Seven adult pigeons were used in this study. They were selected for good health based on a physical examination, and treated with fenbendazole (Panacur; MSD Animal Health Belgium NV, Belgium) and ronidazole (Trichocure; Oropharma NV, Belgium) against parasites (worms, coccidia and trichomonas) 2 months prior to the experiment. They were housed in an aviary measuring 3 9 2 9 2 m). All seven pigeons were acclimatized to handling during a
2 month period before the study commenced. All animals entered and completed all phases of the study. The experiment protocol (14/209) was approved by the Ethical Committee for Animal Welfare of the University of Namur. Based on a power calculation, this sample size was sufficient to demonstrate, should it occur, a 20% difference in HR, blood pressure and respiratory rate between awake and anaesthetized pigeons, and the occurrence of arrhythmias. The bracketing method (Escobar et al. 2012) used in this study in the determination of MAC can be performed in small samples. Baseline monitoring parameters in awake animals Several physiological variables were measured in each pigeon in the awake state without tranquillization. Measurements were performed in a quiet environment. The bird was covered with a light towel to reduce stress. After the measuring instrument (e.g. ECG) had been placed, the pigeon was gently restrained for 15 minutes before measurements were obtained. Birds were restrained in an upright position for ECG and gas measurements to reduce the effects of stress (Murcia et al. 2005). For technical reasons, indirect SAP and cloacal temperature (T) were measured in dorsal recumbency. Each measure was obtained separately. ECGs were recorded for periods of 10 minutes. An ECG (Cardiocap; Datex-Ohmeda Oy, Finland) was used to assess HR and rhythm. Blunted alligator clip electrodes were connected directly to the skin at the patagium of each wing and at the skin fold proximal to the left stifle joint. Topical alcohol was used sparingly to increase conductivity at the electrode sites, but efforts were made to avoid an evaporative cooling effect. A Doppler blood flow probe and occlusive cuff with sphygmomanometer (Doppler Vet BP; Mano Medical, France) was used to monitor indirect SAP. A blood pressure cuff (size: 2.5 cm) (Pedisphyg; CAS Medical Systems, Inc., CT, USA) was positioned between the tibiotarsal–tarsometatarsal joint and the stifle joint. The width of the blood pressure cuff was equivalent to 40–50% of the limb circumference. The Doppler probe was placed, using ultrasound coupling gel to ensure adequate contact, distal to the blood pressure cuff, over the metatarsal artery. For gas analysis (inspired CO2, PE′CO2, inspired isoflurane and end-expired isoflurane), the sectioned blind end of a latex glove finger (size: small) was fixed around the beak of the pigeon
© 2015 Association of Veterinary Anaesthetists and the American College of Veterinary Anesthesia and Analgesia, 43, 63–71
64
Isoflurane in pigeons J Botman et al.
proximal to the nares (Fig. 1). This technique has already been reported in the administration of anaesthetic gases (Colmar 2008). A 20 gauge nonblunted needle connected via a sampling line to the gas analyser (Capnomac Ultima; Datex-Ohmeda Oy) was inserted into the glove and maintained with care close to the beak to measure inspired and endexpired gas composition. The gas analyser measured isoflurane percentages to one decimal place and CO2 tensions to the nearest 1 mmHg. The sidestream sampling rate of the gas analyser was 200 mL minute 1. The fresh gas flow of oxygen was set at 2–49 minute ventilation (minute ventilation was estimated as 200 mL 1 kg minute 1) so that oxygen (100%) was delivered at 0.3 L minute 1 through the other end of the glove using a non-rebreathing Bain system. The gas analyser’s calibration was checked against room air prior to and after each anaesthetic (to check that no drift occurred) for each bird. Before and after the study, the machine’s calibration was checked with a standard gas mixture [Quick Cal calibration gas (5% CO2, 55% O2, 3% agent, 37% N2); GE Healthcare BVBA, Belgium] by the service engineers. To measure body temperature, an electronic thermometer (Digi-Vet SC 12; Jørgen Kruuse A/S, Denmark) was inserted into the cloaca. Induction and maintenance Two weeks later, birds were fasted for 6 hours. Prior to anaesthesia, birds were allowed to breathe 100% oxygen (1 L minute 1) via a facemask for 5 minutes. Anaesthesia was induced with isoflurane
Figure 1 End-expired gas composition was measured during isoflurane anaesthesia in seven pigeons using a needle inserted into the finger of a glove and connected to the capnograph. The needle tip was positioned as near as possible to the bird’s nares. 65
(Vetflurane; Virbac SA, France) delivered in 100% oxygen (1 L minute 1) using a Bain nonrebreathing system and an initial vaporizer setting of 4%. Once the bird was sufficiently relaxed and voluntary movement of the eyelids had ceased, the face mask was removed and the trachea was intubated with a 3 mm non-cuffed endotracheal tube. The bird was then positioned in dorsal recumbency on an insulated mattress under an infrared light. Oxygen delivery was adjusted to 0.3 L minute 1 for the remainder of the procedure. Birds were allowed to breathe spontaneously. Monitoring parameters during anaesthesia After induction, instruments for gas analysis, ECG and Doppler measurements were placed. Endexpired gas samples were collected via a 20 gauge needle, the tip of which was inserted to lie within the lumen of the endotracheal tube. The sampling line was connected to the gas analyser for continuous monitoring of the inspired and end-expired isoflurane percentages, and inspired and end-expired CO2 tensions. Inspired CO2, PE′CO2 and T were recorded at baseline (start of the period for MAC determination) and observed every 5 minutes during MAC determination. Temperature was maintained between 39.2 and 41.2 °C. After MAC had been determined and the end-expired isoflurane concentration had been maintained for 15 minutes at 1.0 MAC, monitored variables were recorded immediately and again after 5, 10, 15, 20, 25, 30, 35 and 40 minutes. HR (beats minute 1), fR (breaths minute 1), and PE′CO2 (mmHg and kPa) were recorded three times over 1 minute and mean values were calculated. Then SAP (mmHg) was measured, and T (°C) was recorded from the cloacal temperature probe. Approximately 3 minutes were necessary to obtain all measurements at every time-point. ECG was recorded for the entire anaesthetic period. For analysis, cardiac arrhythmias were assigned a score on a scale of 0–2 (0 = no arrhythmia, 1 = arrhythmias observed during less than half of the anaesthetic period, 2 = arrhythmias observed for more than half of the anaesthetic period). MAC determination After stabilization at a predetermined anaesthetic concentration, the jaws of a Rochester–Carmalt forceps were used to clamp (to the first ratchet lock)
© 2015 Association of Veterinary Anaesthetists and the American College of Veterinary Anesthesia and Analgesia, 43, 63–71
Isoflurane in pigeons J Botman et al. the proximal part of a digit either until a gross purposeful movement occurred, such as kicking of the limbs or moving of the wings, or for up to 60 seconds if no observable response occurred. The end-expired anaesthetic concentration was decreased by 10% if no movement occurred. The procedure was repeated until the bird reacted. From this point, end-expired anaesthetic concentration was increased by 10% until the reaction disappeared. The MAC was defined and calculated as ‘the median value between the maximal end-expired concentration that allowed movement and the minimal end-expired concentration that prevented movement’ (Naganobu & Hagio 2000). End-expired isoflurane concentration was determined as the average of four samples. Intervals of interest Time to induction was defined as the time from the start of inhalant anaesthetic administration to successful intubation (Mercado et al. 2008). The time between intubation and the first stimulation for MAC determination (stabilization period) and the mean time from the start of inhalant anaesthetic administration to successful MAC determination were measured. After the last monitoring parameter had been measured, the vaporizer was turned off and 100% oxygen was administrated until the endotracheal tube was removed. Time to extubation was defined as the time from stopping inhalation of isoflurane (vaporizer turned off) to the time of coughing, swallowing or shaking of the head, resulting in removal of the endotracheal tube (Granone et al. 2012). Recovery time was defined as the time from stopping anaesthetic administration (vaporizer turned off) until the bird was able to stand and walk unassisted. Total anaesthetic time was defined as the period from the start of anaesthetic inhalation to the time of ceasing anaesthetic inhalation (Phair et al. 2012). Data analysis Kolmogorov–Smirnov and Shapiro–Wilk tests were used to examine the normality of data. Because of normality, the paired Student’s t-test was used to compare variables. Scores for arrhythmias were analysed using the non-parametric Wilcoxon signed-rank test. Differences were considered to be significant at a p-value of < 0.05. IBM SPSS Statistics for Windows Version 20.3 (IBM Corp., NY, USA) was
used for all analyses. Results are presented as the mean SD. Results The mean SD weight of the pigeons was 438 38 g. The MAC of isoflurane in this series of pigeons was estimated at 1.8 0.4%. The time between intubation and the first stimulation for MAC determination (stabilization period) was 20 4 minutes and the time from the start of inhalant anaesthetic administration to successful MAC determination was 116 11 minutes (15 minutes after this time = T0). Inspired CO2 was measured during the procedure and confirmed as always zero in both awake and anaesthetized birds. Cloacal temperature progressively decreased throughout anaesthesia to reach a minimum value of 39.2 °C in one pigeon (mean: 39.8 °C) during the period of MAC determination. By the end of the recording period (T40), the temperature was 39.5 0.7 °C. Physiological parameters in both awake and anaesthetized pigeons are reported in Table 1. Intervals of interest are reported in Table 2. Changes in HR, SAP, fR and PE′CO2 during 40 minutes of anaesthesia are described in Figs 2 & 3. No arrhythmias were identified in awake pigeons. Under isoflurane, arrhythmias occurred frequently. The occurrence of arrhythmias is summarized in Table 3. Five pigeons developed seconddegree heart blocks. Arrhythmias resolved after the discontinuation of isoflurane. Discussion This study provides information about physiological variables in both the awake pigeon and the pigeon under isoflurane anaesthesia administered outwith the context of surgical or diagnostic procedures and during spontaneous breathing. Awake pigeons were found to have an HR of 155 28 beats minute 1, which is lower than the value of 273 83 beats minute 1 reported in the literature (Murcia et al. 2005); however, these earlier authors did not report a period of acclimatization to handling. The discrepancy between values may possibly be explained by the quietness of the pigeons in the current study, which had been accustomed to handling for a period of 2 months. Data from the present study show more similarity to those reported by R€ uther (1998), who recorded an HR of 121 beats minute 1 obtained from six
© 2015 Association of Veterinary Anaesthetists and the American College of Veterinary Anesthesia and Analgesia, 43, 63–71
66
Isoflurane in pigeons J Botman et al.
Table 1 Mean standard deviation heart rate (HR), systolic blood pressure (SAP), respiratory rate (fR), end-expired carbon dioxide tension (PE′CO2) and temperature (T) in seven pigeons in the awake state and under isoflurane anaesthesia at time 0 (15 minutes after stabilization at the individual minimal anaesthetic concentration value)
Variable
Awake state
HR (beats minute 1) SAP (mmHg) fR (breaths minute 1) PE′CO2 (mmHg) PE′CO2 (kPa) T (°C)
155 155 34 38 5.1 41.8
28 21* 6 8* 1.1 0.5*
Isoflurane anaesthesia 135 87 34 52 6.9 39.5
28 11* 8 7* 0.9 0.7*
*Significant difference between awake and anaesthetized pigeons (p < 0.05).
Table 2 Induction and recovery characteristics in seven pigeons anaesthetized with isoflurane. Results are reported as the mean standard deviation Time (minutes:seconds seconds)
Variable Time Time Time Total
to intubation to extubation to recovery anaesthetic time
4:18 8:42 17:36 159:54
60 108 204 630
pigeons over a period of several days using telemetry, which did not require concurrent handling. In this study, there was no significant decrease in HR from the awake to the anaesthetized state under isoflurane. This absence of a significant reduction in HR was also observed in a study conducted in crested caracaras (Escobar et al. 2011), whereas HR was found to be significantly lower in other studies carried out in anaesthetized common buzzards (Straub et al. 2003) and thick-billed parrots (Mercado et al. 2008). No arrhythmias were recorded in awake pigeons in the current study. Similar findings were observed in 64 awake pigeons also gently restrained in an upright position (Murcia et al. 2005). Conversely, in a study of awake and free-standing pigeons in which recordings were obtained by telemetry, nine of 10 awake pigeons were found to demonstrate seconddegree heart blocks (R€ uther 1998). This author reported that all atrioventricular (AV) blocks resolved with increasing HR. Second-degree AV heart blocks (in which at least one but less than the majority of P waves show no association with a QRS complex) occurred in five pigeons anaesthetized with isoflurane in this study, one of which also showed a third-degree AV heart 67
block. Arrhythmias under isoflurane anaesthesia were observed in two studies in bald eagles (Aguilar et al. 1995; Joyner et al. 2008). In those studies, second-degree heart block was the most frequently observed arrhythmia. Several hypotheses have been suggested to explain arrhythmias. Ocular pressure may be caused inadvertently during mask induction, increasing vagal tone and causing arrhythmias such as seconddegree heart block (Joyner et al. 2008). However, in the current study three pigeons had arrhythmias for more than half of the anaesthetic period. This suggests that an inadvertent oculocardiac reflex was not the cause of the second-degree heart block. Respiratory acidosis and hypoxaemia can also cause arrhythmias (Aguilar et al. 1995). In the current study, we did not measure partial pressure of oxygen and pH in arterial blood, but birds became mildly hypercapnic, which can lead to respiratory acidosis. As dorsal recumbency can reduce ventilation, possibly partly because abdominal viscera compress the abdominal air sacs (King & Payne 1964), it can predispose to CO2 retention and the resultant hypercapnia may then predispose to arrhythmias. Catecholamine release resulting from stress can also induce abnormalities of the heart rhythm, but tachycardic rhythms would tend to be more likely (Aguilar et al. 1995). In this study, the previous acclimatization of awake pigeons to handling may have prevented stress. In another study in unanaesthetized competition pigeons (Murcia et al. 2005), no prior training was performed and no arrhythmias occurred; however, competition pigeons are used to being hand-restrained. Arrhythmias were reported to occur spontaneously in free-standing pigeons at lower HRs and were reported to resolve when HR increased (R€ uther 1998). This might strengthen the
© 2015 Association of Veterinary Anaesthetists and the American College of Veterinary Anesthesia and Analgesia, 43, 63–71
Isoflurane in pigeons J Botman et al.
Figure 2 Changes in mean heart rate (HR) and systolic arterial blood pressure (SAP) over time (T) during isoflurane anaesthesia in seven pigeons. The initial measurement (T0) was fixed at 15 minutes after stabilization at the individual minimal anaesthetic concentration value.
Figure 3 Changes in mean end-expired carbon dioxide tension (PE′CO2) and respiratory rate (fR) over time (T) during isoflurane anaesthesia in seven pigeons. T0 is fixed at 15 minutes after stabilization at the individual minimal anaesthetic concentration value.
hypothesis that arrhythmias can be linked to increased vagal tone (Aguilar et al. 1995), which occurs, for example, during anaesthesia. In this series, SAP in awake birds was 155 21 mmHg, which is similar to the values of 120–150 mmHg described in the literature (Boucher et al. 2009). During isoflurane anaesthesia, SAP was significantly lower (87 11 mmHg), as previously reported in pigeons undergoing coelioscopy (Touzot-Jourde et al. 2005). Isoflurane is known to be a vasodilator (Schnellbacher et al. 2012) and the consequent decrease in systemic vascular resistance may represent the main cause of hypotension; the degree of hypotension has been correlated with depth of isoflurane anaesthesia in other avian species (Ludders et al. 1989; Naganobu & Hagio 2000; Kim et al. 2011). In awake pigeons, a baseline respiratory rate of 30 breaths minute 1 has been reported (Villate 2001; Boussarie et al. 2002). A similar value was
observed in this study (34 6 breaths minute 1). The fR value did not differ significantly between awake and anaesthetized birds. Some short periods of apnoea occurred during induction or recovery, but resolved unaided or by slightly moving the endotracheal tube. Other studies have reported significant decreases in respiratory rate (Machin & Caulkett 2000; Joyner et al. 2008; Mercado et al. 2008; Escobar et al. 2011; Granone et al. 2012). However, birds in these studies were anaesthetized at isoflurane concentrations higher than MAC (Mercado et al. 2008; Granone et al. 2012), or at concentrations presumed to be higher (1.5–3.0%) in species for which MAC had not been determined (Machin & Caulkett 2000; Joyner et al. 2008; Escobar et al. 2011). As isoflurane is known to depress ventilation in a dose-dependent manner (Gleed & Ludders 2001), this could explain the absence of a decrease in respiratory rate in the present study.
© 2015 Association of Veterinary Anaesthetists and the American College of Veterinary Anesthesia and Analgesia, 43, 63–71
68
Isoflurane in pigeons J Botman et al.
Table 3 Occurrences of arrhythmia in seven pigeons during isoflurane anaesthesia
Pigeon
I
S
P1
P2
P3
P4
P5
P6
P7
P8
MAC
T0
T5
T10
T15
T20
T25
T30
T35
T40
1 2 3 4 5 6 7
0 0 0 0 0 0 0
2 0 0 2 0 0 0
2 2 0 0 0 0 0
2 2 0 0 0 2 0
2 3 2 2 0 2 0
2 3 2 2 0 2 0
2 2 0 2 0 2 0
2 2 2 0 / 0 0
2 / 0 / / 0 0
/ / / / / / 0
2 3 2 2 0 2 0
2 3 2 2 0 2 0
0 3 0 2 0 2 0
0 3 0 2 0 2 0
0 3 0 2 0 2 0
0 3 0 2 0 2 0
0 0 0 2 0 2 0
0 0 0 2 0 2 0
0 0 0 2 0 2 0
0 0 0 2 0 2 0
0 = no arrhythmia; 2 = second-degree atrioventricular block; 3 = third-degree atrioventricular block. I, intubation; MAC, minimal anaesthetic concentration; P, time period between two stimuli (= 15 minutes); S, period of stabilization (between intubation and first stimulus; 20 4 minutes). / indicates that MAC had been determined and no further stimulus was required. MAC corresponds to a period of 15 minutes at MAC before parameters were recorded.
Because of the difficulty of catheterizing an artery, blood gas analysis was not considered. Instead, PE′CO2 was used to assess ventilatory adequacy. A PE′CO2 of 38 8 mmHg (5.1 1.1 kPa) was measured in awake pigeons; this rose significantly under isoflurane anaesthesia to 52 7 mmHg (6.9 0.9 kPa). However, PE′CO2 has been found to overestimate PaCO2 by 5 mmHg (0.7 kPa) in pigeons and African grey parrots as a result of the cross-current mechanism of gas exchange in avian lungs (Touzot-Jourde et al. 2005; Longley 2008). Increases in PE′CO2 or PaCO2 have also been observed in other avian species anaesthetized with isoflurane during spontaneous ventilation (Ludders et al. 1989; Joyner et al. 2008; Escobar et al. 2011). Dorsal recumbency, muscle relaxation, the absence of a diaphragm, and the effects of isoflurane on the central nervous system and peripheral chemoreceptors may explain the ventilatory depression (Gleed & Ludders 2001). The MAC, determined for isoflurane using the ‘bracketing’ technique, was 1.8 0.4% in this series of seven pigeons. This value is higher than those reported for other avian species. MAC values for isoflurane were reported to be 1.07% in thickbilled parrots (Mercado et al. 2008), 1.34 0.14% in sandhill cranes (Ludders et al. 1989), 1.25 0.13% in chickens (Naganobu & Hagio 2000), 1.30 0.23% in Pekin ducks (Ludders et al. 1990), 1.45 0.07% in red-tailed hawks (Fitzgerald & Blais 1991) and 1.06 0.07% in cinereous vultures (Kim et al. 2011). Our findings also differ from the isoflurane MAC value of 1.51 0.15% measured in a study in 12 adult pigeons (Fitzgerald & Blais 1991). It is known that MAC values can vary by up to 10% within the same 69
animal and up to 20% within the same species (Quasha et al. 1980). In addition, different estimations of MAC can be obtained with different stimulation techniques (electric or mechanical) (Phair et al. 2012). A previous study in pigeons used an electrical stimulus (50 V, 50 Hz, 7.5 milliseconds) as a supramaximal stimulus (Fitzgerald & Blais 1991), whereas the present study used a mechanical stimulus (digit clamping). The difference between our findings and those of Fitzgerald & Blais (1991) may also be explained by subjectivity in the assessment of ‘a gross purposeful movement’ and the mode of application of the noxious stimulus. For example, the type of haemostat used (with or without plastic tubing on the jaws and applied at different ratchet locks) can influence the estimation of MAC (Valverde et al. 2003). Other physiological factors such as body temperature, metabolic rate, blood CO2 tension and large variations in blood pressure can influence the determination of MAC (Quasha et al. 1980). In laboratory mammals, MAC decreased by 4–5% per 1 °C decrease in temperature to result in the complete elimination of the requirement for anaesthesia at 20 °C (Eger 2001). In the current study, despite the use of an infrared light and insulated bed during anaesthesia, T values progressively decreased over time. Temperature was 39.7 °C at T0 and 39.5 0.7 °C during the 40 minutes of anaesthesia at MAC. However, this variation did not exceed 2 °C as temperature during the period of determination of MAC ranged from 41.2 °C to 39.2 °C. At a maximum temperature decrease of 2 °C, MAC may have been underestimated, although our values would still have been higher than those previously reported. This decrease in T during isoflurane anaesthesia was also
© 2015 Association of Veterinary Anaesthetists and the American College of Veterinary Anesthesia and Analgesia, 43, 63–71
Isoflurane in pigeons J Botman et al. observed in other species despite the use of supplemental heat sources (Machin & Caulkett 2000; Joyner et al. 2008; Mercado et al. 2008; Escobar et al. 2011; Granone et al. 2012). A study in dogs demonstrated that profound hypocapnia [PaCO2 below 10–15 mmHg (1.3– 2.0 kPa)] and extreme hypercapnia [PaCO2 in excess of 90–95 mmHg (12.0–12.7 kPa)] can reduce MAC (Eisle et al. 1967). Another study in rats, however, demonstrated a linear relationship between MAC and PaCO2 (Brosnan et al. 2007). At this time, no information on the effects of changing PaCO2 on avian MAC, or indeed in pigeons, is available. It therefore remains to be determined whether the mild hypercapnia observed in this study had any influence on MAC values. Isoflurane resulted in the smooth and rapid induction of anaesthesia in pigeons. Time to induction was almost twice that reported in a previous study (Korbel 1998). One reason for the difference refers to discrepancies in definitions of the end point of anaesthetic induction: the present study defined induction as the time between the start of isoflurane administration and successful tracheal intubation, whereas Korbel (1998) used the start of isoflurane administration to the loss of reflexes to an ill-defined noxious stimulus. Secondly, anaesthesia was induced with 5% isoflurane by Korbel (1998), but with 4% isoflurane in the current study. Recovery time to standing/walking was longer in the present study than the time to return of the righting reflex (Korbel 1998), again demonstrating that careful description of the events that define these times is important. Return of the righting reflex occurs sooner than the ability to stand and walk unassisted. Furthermore, the whole process in this study (induction, MAC determination, 15 minutes of stabilization and 40 minutes for monitoring parameters) was longer than the 60 minutes of anaesthesia used by Korbel (1998) and may also have influenced recovery time. Conclusions The MAC of isoflurane determined in pigeons in the present study is higher than MAC values previously reported for pigeons and other birds. Isoflurane resulted in the smooth and rapid induction of anaesthesia in pigeons, similarly to other species, although recovery time in this study was longer than those reported elsewhere. Isoflurane resulted in mild hypothermia and hypotension. A salient find-
ing was the significant development of second- and third-degree cardiac blocks. Hypercapnia was also observed, which suggests that ventilatory assistance may be recommended. References Aguilar RF, Smith VE, Ogburn P et al. (1995) Arrhythmias associated with isoflurane anesthesia in bald eagles (Haliaeetus leucocephalus). J Zoo Wildl Med 26, 508–516. Boucher S, Bulliot C, Doumerc G et al. (2009) Examens Complementaires chez les NAC. Editions du Point Vet, France. Boussarie D, Schilliger L, Rival F (2002) Vade-Mecum d’Anesthesie des NAC. Editions Med’Com, France. Brosnan RJ, Eger EI II, Laster MJ et al. (2007) Anesthetic properties of carbon dioxide in the rat. Anesth Analg 105, 103–106. Colmar C (2008) Prise en charge chirurgicale de l’oiseau: l’attention du praticien. These de fin fichier technique a d’etude donnant acces a la pratique de la medecine veterinaire. Ecole Nationale Veterinaire de Toulouse. pp. 27–28. Eger EI II (2001) Age, minimum alveolar anesthetic concentration, and minimum alveolar anesthetic concentration-awake. Anesth Analg 93, 947–953. Eger EI II, Saidman LJ, Brandstater B (1965) Minimum alveolar anesthetic concentration: a standard of anesthetic potency. Anesthesiology 26, 756–763. Eisle JH, Eger EI II, Muallem M (1967) Narcotic properties of carbon dioxide in the dog. Anesthesiology 28, 856– 865. Escobar A, Thiesen R, Vitaliano S et al. (2011) Cardiorespiratory effects of isoflurane anesthesia in crested caracaras (Caracara plancus). J Zoo Wildl Med 42, 12–17. Escobar A, Valad~ ao CA, Brosnan RJ et al. (2012) Effects of butorphanol on the minimum anesthetic concentration for sevoflurane in guineafowl (Numida meleagris). Am J Vet Res 73, 183–188. Fitzgerald G, Blais D (1991) Effect of nitrous oxide on the minimal anaesthetic dose of isoflurane in pigeons and red-tailed hawks. Vet Anaesth Analg 18, 111–115. Gleed RD, Ludders JW (2001) Recent advances in veterinary anesthesia and analgesia: companion animals. International Veterinary Information Service, NY, USA. http://www.ivis.org/advances/Anesthesia_Gleed /ludders2/chapter.asp?LA=1 (Accessed 2 November 2013). Granone T, de Francisco O, Killos M et al. (2012) Comparison of three different inhalant anesthetic agents (isoflurane, sevoflurane, desflurane) in red-tailed hawks (Buteo jamaicensis). Vet Anaesth Analg 39, 29–37. Gunkel C, Lafortune M (2005) Current techniques in avian anesthesia. Semin Avian Exot Pet Med 14, 263– 276.
© 2015 Association of Veterinary Anaesthetists and the American College of Veterinary Anesthesia and Analgesia, 43, 63–71
70
Isoflurane in pigeons J Botman et al.
Joyner PH, Jones MP, Ward D et al. (2008) Induction and recovery characteristics and cardiopulmonary effects of sevoflurane and isoflurane in bald eagles. Am J Vet Res 69, 13–22. Kim Y, Lee SS, Suh E et al. (2011) Minimum anesthetic concentration and cardiovascular dose–response relationship of isoflurane in cinereous vultures (Aegypius monachus). J Zoo Wildl Med 42, 499–503. King AS, Payne DC (1964) Normal breathing and the effects of posture in Gallus domesticus. J Physiol (London) 174, 340–347. Korbel R (1998) Vergleichende Untersuchungen zur Inhalationsan€ asthesie mit Isofluran (Forene) und Sevofluran (SEVOrane) bei Haustauben (Columba livia Gmel., 1789, var. domestica) und Vorstellung eines Referenz-Narkoseprotokolls f€ ur V€ ogel. Tier€ arztl Prax 26 (K), 211–223. Longley LA (2008) Anaesthesia of Exotic Pets. Elsevier Saunders, USA. pp. 159–160. Ludders JW, Rode J, Mitchell GS (1989) Isoflurane anesthesia in sandhill cranes (Grus canadensis): minimal anesthetic concentration and cardiopulmonary doseresponse during spontaneous and controlled breathing. Anesth Analg 68, 511–516. Ludders JW, Mitchell GS, Rode J (1990) Minimal anesthetic concentration and cardiopulmonary dose response of isoflurane in ducks. Vet Surg 19, 304–307. Machin KL, Caulkett NA (2000) Evaluation of isoflurane and propofol anesthesia for intraabdominal transmitter placement in nesting female canvasback ducks. J Wildl Dis 36, 324–334. Mercado JA, Larsen RS, Wack RF et al. (2008) Minimum anesthetic concentration of isoflurane in captive thick-billed parrots (Rhynchopsitta pachyrhyncha). Am J Vet Res 69, 189–194. Murcia LMM, Bernal LJ, Montes AM et al. (2005) The normal electrocardiogram of the unanaesthetized
71
competition ‘Spanish Pouler’ pigeon (Columba livia gutturosa). J Vet Med A Physiol Pathol Clin Med 52, 347–349. Naganobu K, Hagio M (2000) Dose-related cardiovascular effects of isoflurane in chickens during controlled ventilation. J Vet Med Sci 62, 435–437. Phair K, Larsen S, Wack R et al. (2012) Determination of the minimum anesthetic concentration of sevoflurane in thick-billed parrots (Rhynchopsitta pachyrhyncha). Am J Vet Res 73, 1350–1355. Quasha AL, Eger EI II, Tinker JH (1980) Determination and applications of MAC. Anesthesiology 53, 315–334. R€ uther P (1998) Untersuchungen zur tageszeitabh€angigen Rhythmik der Ruheherzfrequenz und ausgew€ ahlter Arrhythmien bei der Brieftaube (Columba livia f. domestica). PhD thesis, Free University of Berlin. p. 103. Schnellbacher R, Cunha AF, Beaufrere H et al. (2012) Effects of dopamine and dobutamine on isofluraneinduced hypotension in Hispaniolan Amazon parrots (Amazona ventralis). Am J Vet Res 73, 952–958. Straub J, Forbes N, Thielebein J et al. (2003) The effects of isoflurane anaesthesia on some Doppler-derived cardiac parameters in the common buzzard (Buteo buteo). Vet J 166, 273–276. Touzot-Jourde G, Hernandez-Divers SJ, Trim CM (2005) Cardiopulmonary effects of controlled versus spontaneous ventilation in pigeons anesthetized for coelioscopy. J Am Vet Med Assoc 227, 1424–1428. Valverde A, Morey T, Hern andez J et al. (2003) Validation of several types of noxious stimuli for use in determining the minimum alveolar concentration for inhalation anesthetics in dogs and rabbits. Am J Vet Res 64, 957– 962. Villate D (2001) Maladies des Volailles (2nd edn). France Agricole, France. p. 45. Received 16 March 2014; accepted 4 December 2014.
© 2015 Association of Veterinary Anaesthetists and the American College of Veterinary Anesthesia and Analgesia, 43, 63–71
