Veterinary Anaesthesia and Analgesia, 2014, 41, 592–601

doi:10.1111/vaa.12151

RESEARCH PAPER

Comparison of respiratory function during TIVA and isoflurane anaesthesia in ponies Part II: breathing patterns and transdiaphragmatic pressure Lidia Kowalczyk†,a & Barbara Steblaj*,a with Stijn Schauvliege*, Johannes Peter Schramel†, Kiriaki Pavlidou‡, Ioannis Savvas‡, Luc Duchateau§, Frank Gasthuys* & Yves Moens† *Department of Surgery and Anaesthesia of Domestic Animals, Faculty of Veterinary Medicine, University of Ghent, Merelbeke, Belgium †Anaesthesiology and Perioperative Intensive-Care, Vetmeduni Vienna, Vienna, Austria ‡Companion Animal Clinic, Department of Clinical Sciences, Faculty of Veterinary Medicine, Aristotle University of Thessaloniki, Thessaloniki, Greece §Department of Physiology and Biometrics, Faculty of Veterinary Medicine, University of Ghent, Merelbeke, Belgium

Correspondence: Lidia Kowalczyk, Anaesthesiology and Perioperative Intensive-Care, University of Veterinary Medicine, Veterinaerplatz 1, 1210 Vienna, Austria. E-mail: [email protected] a

Co-first authorship.

Abstract Objective To compare breathing patterns and transdiaphragmatic pressure during total intravenous (TIVA) and isoflurane anaesthesia in ponies. Study design Experimental, cross–over study. Animals Six healthy ponies weighing 286 (233– 388)  61 kg, age 13 (9–16)  3 years. Methods Following premedication with romifidine [80 lg kg1 intravenously (IV)], general anaesthesia was induced with midazolam (0.06 mg kg1 IV) and ketamine (2.5 mg kg1 IV) and maintained with either isoflurane (FE′Iso = 1.1%) (T-ISO) or an IV combination of romifidine (120 lg kg1 per hour), midazolam (0.09 mg kg1 hour1) and ketamine (3.3 mg kg1 hour1) (T-TIVA), while breathing 60% oxygen (FIO2). The circumference changes of the rib cage (RC) and abdominal compartment (ABD) were recorded using respiratory ultrasonic plethysmography (RUP). Balloon tipped catheters were placed in the distal oesophagus and the stomach and maximal transdiaphragmatic pressure (Pdi max) was calculated during Mueller’s manoeuvre. 592

Results The breathing pattern T-ISO was more regular and respiratory rate significantly lower compared with T-TIVA. Ponies in T-TIVA showed regularly appearing sighs, which were never observed in T-ISO. Different contribution of the RC and ABD compartments to the breathing pattern was observed with a smaller participation of the RC to the total volume change during T-ISO. Transdiaphragmatic pressures (mean 13.7  SD 8.61 versus 23.4  7.27 cmH2O, p < 0.0001) were higher in T-TIVA compared to T-ISO. The sum of the RC and ABD circumferential changes was lower during T-TIVA compared to T-ISO (6.32  4.42 versus 11.72  4.38 units, p < 0.0001). Conclusion and clinical relevance Marked differences in breathing pattern and transdiaphragmatic pressure exist during inhalation- and TIVA and these should be taken into account for clinical estimation of anaesthetic depth. Keywords breathing pattern, isoflurane, ponies, total intravenous anaesthesia, transdiaphragmatic pressure.

Respiratory function: part II L Kowalczyk & B Steblaj et al. Introduction Inhalational and total intravenous anaesthesia (TIVA) are well-established anaesthetic techniques in horses. While the cardiovascular effects of these drugs have been thoroughly described, the influence on respiratory muscles and breathing pattern received less attention. It is well known that numerous volatile and intravenous anaesthetics affect respiratory function in a drug specific and dose dependent manner, and that respiratory movements in humans are different during inhalational anaesthesia compared to TIVA (Jones et al. 1979; Brown 1998; Aliverti et al. 2011; Drummond et al. 2013). For assessment of the breathing pattern and influence of different anaesthetic protocols two novel techniques: respiratory ultrasonic plethysmography (RUP) and measurement of transdiaphragmatic pressure (Pdi) were used in the presented study. Recently, RUP has been used to record the circumference changes of the ribcage (RC) and the abdominal compartment (ABD) during intermittent positive pressure ventilation in anaesthetized horses. The amplitudes of these changes are a surrogate for volume changes of the RC and ABD (Russold et al. 2013). Changes in the baseline RC circumference are directly related to changes in end-expiratory lung volume (EELV) (Moens et al. 2013). Plotting RC circumference against ABD circumference in a Lissajous plot enables assessment of thoracoabdominal coupling and, indirectly, the contribution of different muscles to the work of breathing during different anaesthetic protocols (Sivan et al. 1990). Contraction and movement of the diaphragm with subsequent displacement of abdominal organs is an essential component of respiratory movement and can be evaluated by measuring the pressure that the diaphragm exerts, which is known as transdiaphragmatic pressure (Wolfe & Sorbello 2006). The latter is defined as the difference between intra-abdominal (Pabd) and intrapleural pressure (Ppl) and quantifies the pressure difference across the diaphragm (Kacmarek et al. 1990; Grippi 1995). Since Ppl correlates well with the distal oesophageal pressure (Poes) and Pabd with the gastric pressure (Pga), the transdiaphragmatic pressure (Pdi) is often calculated as Pdi = PgaPoes. It can be used to assess the diaphragmatic force rather independently from intercostal and accessory muscle activity and elastic recoil of the chest wall and lung (Benditt 2005).

Most TIVA protocols for clinical equine anaesthesia are based on ketamine. In contrast to inhalant anaesthetics, ketamine preserves the activity of intercostal muscles in humans (Mankikian et al. 1986; Tokics et al. 1987; Warner et al. 1996). A comparison of the breathing pattern between inhalation anaesthesia and ketamine based TIVA has not been reported in ponies or horses. In addition, the technique of transdiaphragmatic pressure measurement has not yet been described for anaesthetized equidae. In the present study the combination of measurement of circumference changes with RUP and measurement of Pdi was chosen to compare the breathing pattern and to assess the diaphragmatic activity during isoflurane anaesthesia and a ketamine-based TIVA. The results of the comparison of cardiorespiratory variables are reported separately (Steblaj et al. 2013). Materials and methods Six ponies (one mare and five geldings) weighing mean 286 (range 233–388)  SD 61 kg, aged 13 (9–16)  3 years with a body score condition of 4–5 of five, and classified as ASA (American Society of Anaesthesiologists) I (normal, healthy patient), were included in the present study which was approved by the local Ethical Committee (EC2010/159). Preparation of the ponies, details of induction and maintenance of anaesthesia, plus instrumentation to measure cardiorespiratory parameters are reported in the companion paper (Steblaj et al. 2013). Anaesthesia was maintained either with isoflurane (FE0 Iso = 1.1%) (Isoflurane, UK) (T-ISO) or with IV romifidine (120 lg kg1 per hour), midazolam (0.09 mg kg1 per hour) and ketamine (3.3 mg kg1 per hour) in total intravenous anaesthesia (T-TIVA). Measurements of transdiaphragmatic pressure and breathing pattern Instrumentation for transdiaphragmatic pressure and breathing pattern measurements was carried out during the 30 minute stabilization period following induction of anaesthesia. The RUP sensor consisted of a compliant ethanol filled rubber tube with an inner diameter of 7 mm that act as a waveguide for ultrasound. The distance between tube endings is calculated from the time delay of ultrasonic pulses propagating between

© 2014 Association of Veterinary Anaesthetists and the American College of Veterinary Anesthesia and Analgesia, 41, 592–601

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transducers at the ends of the tube and has resolution of 0.3 mm. For the measurement of circumferential changes, the rib cage sensor (RC) was placed at the level of the 11th intercostal space and the abdominal sensor (ABD) caudally to the last rib, over the exposed and freely moving part of the body. Not compliant metal chains close the perimeter below the body. Signals evoked by breathing movements were transmitted via Bluetooth to a personal computer at a sampling rate of 10 Hz. Circumference changes of the RC and the ABD are closely related to lung volume changes during spontaneous breathing (Schramel et al. 2012). Therefore, compartmental circumference changes are denoted as volume changes in the manuscript. Two balloon-tipped catheters were placed for Pga and Poes measurements. Through the lumen of the nasogastric tube, one balloon catheter (CRE Wire guided Balloon Dilatation Catheter Oesophageal/ Colonic, 240 cm, balloon size 5.5 cm; Boston Scientific, Natick, MA, USA) was introduced into the stomach to measure Pga. The balloon was inflated with 5 mL of room air and connected to a pressure transducer (Pressure Monitoring system Buzzer-II; Michael Roehrich, Austria), in turn connected to a laptop computer for data storage. Correct positioning of the catheter was confirmed by an increase in pressure during inspiration. The nasogastric tube was withdrawn to the level of the distal oesophagus and a second balloon catheter was introduced. This balloon was also inflated with 5 mL of room air and connected to the second pressure transducer to measure Poes. Correct positioning of the second catheter in the distal third of the oesophagus was confirmed by a decrease of the pressure during inspiration. The distance between the two balloons was maintained at 40 cm to standardize the procedure between the ponies and both treatments. Finally, the nasogastric tube was withdrawn to the level of the pharynx and correct positioning of both catheters was again confirmed. All these pressure measurements were in cmH2O. Transdiaphragmatic pressure was calculated as Pdi = PgaPoes and displayed and stored on the computer at a sample rate of 10 Hz. From T0 (30 minutes after the induction) onwards, Pdi was measured during Mueller’s manoeuvre (inspiration with occluded airway) every 5 minutes, during three consecutive breaths, over a period of 60 minutes. Mueller’s manoeuvres were performed by disconnecting the endotracheal tube from the Y piece of the anaesthetic circuit and 594

manually occluding the lumen of the endotracheal tube at end – expiration, while the pressure data were stored on the computer. The RC and the ABD circumference changes were measured with RUP continuously throughout anaesthesia. Cardiovascular and respiratory parameters were recorded every 5 minutes, while arterial blood gases were taken for analysis every 10 minutes (such sampling being before the Mueller’s manoeuvre) (Steblaj et al. 2013). Data analysis and statistics Data for Pdi were analysed with signal analysis software (Qtiplot, MicroCal, Northampton, MA, USA). For each series of three consecutive breaths at a specific timepoint, three peak values for Pga and Poes were determined, while taking the respective baseline values at that time point into account. Three resulting Pdi values (difference between Pga and Poes) were then averaged to obtain a single value of maximum transdiaphragmatic pressure (Pdi max) at each time point. For analysis of RUP data, shortly after T0, and before performing Mueller’s manoeuvres a period of 3 minutes of artefact free waveforms was selected for descriptive analysis. For both treatments the amplitudes of the RC and the ABD circumference changes were calculated by the root mean square (RMS) value of the waveform amplitudes during all Mueller0 s manoeuvres. The root mean square of the waveform amplitude is considered an equivalent for the area under the curve (Hoffman et al. 2001). Values are presented in units, as they are not calibrated to volumes. For every Mueller’s manoeuvre the RMS value of the sum of the RC and the ABD samples was also calculated. Finally, the RC circumference was plotted against the ABD circumference (Lissajous plot) to visualize the relative contribution and occurrence of potential thoraco-abdominal asynchrony. The effects of T-ISO and T-TIVA on Pdi max and RUP values were compared using a mixed model analysis of variance with pony as random effect and treatment, time and their interaction as categorical fixed effects. Based on this model, an overall comparison was made between both treatments, using all data from all ponies, to analyse whether there was a ‘global’ treatment effect (at a = 0.05). Additionally, a comparison between treatments was made at two specific timepoints (T30 and T60, using Bonferroni correction

© 2014 Association of Veterinary Anaesthetists and the American College of Veterinary Anesthesia and Analgesia, 41, 592–601

Respiratory function: part II L Kowalczyk & B Steblaj et al. a = 0.025). Separate analyses at other timepoints were not performed, because correction for multiple comparisons would have overly reduced the power of the study. Finally, the same model was used to detect changes over time in the measured variables and to examine whether this evolution over time was different between the two treatments (interaction treatment-time). Results Maximum transdiaphragmatic pressure (Pdi max) was lower during T-TIVA compared to T-ISO (mean  SD was 13.7  8.61 versus 23.4  7.27 cmH2O, p < 0.0001). The corresponding sum of RC and ABD volume changes was also lower during T-TIVA compared to T-ISO (6.32  4.42 versus 11.72  4.38 units, p < 0.0001). Both time courses are depicted in Fig. 1. Typical respiratory patterns for T-TIVA and T-ISO and corresponding Lissajous plots are depicted in Figs 2 and 3 respectively. During T-ISO, typically a low respiratory rate (fR), a quite regular breathing pattern and large amplitude of the movements of the ABD compartment compared to the RC were noted. Additionally, active abdominal contractions during expiration, characterized by a marked decrease of the ABD volume appeared at regular intervals. Ponies in T-TIVA had a higher fR and RUP tracings showed a periodically rising and falling amplitude with regularly appearing sighs (about once every 2 minutes; 0.62  0.54 sighs minute1). The latter are characterised by one deep breath of at least three-fold amplitude of the RC and the ABD waveform compared to normal breaths. To the contrary, sighs were never observed in T-ISO.

The slope and shape of the Lissajous plots were different in both treatment groups, as shown in Fig. 2 and 3. In T-TIVA, narrow elliptical loops were observed, with a slope of about 45 degrees (Fig. 3, right), whereas during T-ISO the slope was flat and the shape more irregular with phases of paradoxical movements. Typical pressure waveforms of Poes, Pga and Pdi and corresponding RC and ABD volume changes during Mueller’s manoeuvre are shown in Fig. 4. In both treatments, Pga is much smaller than Pdi. The change in the ABD circumference is relatively large compared to the RC, in particular in T-ISO, but surprisingly not accompanied by an increase in Pga. Results for the RC and the ABD RMS values and selected respiratory parameters during normal breathing are presented in Table 1. Other cardiorespiratory parameters are reported separately (Steblaj et al. 2013). Discussion In this study clear differences in breathing pattern between the two anaesthesia protocols were demonstrated with regard to fR, the volume changes and relative contribution of the RC and ABD during normal breathing and during airway occlusion, the presence of sighs and biphasic respiratory patterns. The values for Pdi max, recorded during Mueller0 s manoeuvres, were significantly different between the protocols. The fact that different anaesthetic protocols caused different breathing patterns is not unexpected, as also in humans various anaesthetic agents have been shown to influence the breathing pattern differently (Mankikian et al. 1986; Aliverti et al. 2011; Drummond et al. 2013). However, the results from those

Figure 1 Maximum transdiaphragmatic pressure (Pdi max) and sum (SUM) of the rib cage and abdominal circumference changes in T-TIVA and T-ISO during Mueller maneuvers (mean values). Amplitude is given as RMS value of units (see text). Standard deviations not included for clarity. T0 represents time 30 minutes after the induction of anaesthesia.

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Figure 2 Compartment circumference changes during T-TIVA in a laterally recumbent, spontaneously breathing pony. Left: Rib cage (RC) (upper curve) and abdominal (ABD) (lower curve). Both waveforms and amplitudes are similar. Spontaneous deep breaths (a) characterized by an about three times increased tidal volume are present. Note the varying respiratory rate and baseline (see text). Right: Lissajous plot (RC versus ABD). Arrows indicate the direction of rotation.

Figure 3 Compartment circumference changes during T-ISO in a laterally recumbent, spontaneously breathing pony. Left: Rib cage (RC) (upper curve) and abdominal (ABD) (lower curve). RC amplitude is smaller than ABD amplitude. Set of multiple breaths (a) is followed by a biphasic prolonged abdominal expiration (b). Right: Lissajous plot (RC versus ABD). Arrows indicate the direction of rotation.

studies are not necessarily applicable in equidae. Standing adult horses have a unique biphasic character of respiratory movements (Koterba et al. 1988). At rest, both inspiration and expiration have an active and passive phase (Art & Leukeux 1988). This biphasic breathing pattern in standing horses is caused by a period of active contraction of the abdominal muscles at the end of expiration that displaces the diaphragm into the rib cage. This augmented active exhalation is followed by passive lung inflation towards the relaxed volume of the respiratory system (passive phase of inspiration) (Art 596

& Leukeux 1988; Koterba et al. 1988; Hall et al. 1991). It is not clear whether such a pattern is maintained during anaesthesia or influenced by the anaesthetic protocol used. Hall et al. (1991), using stethography, recorded irregular breathing patterns during halothane anaesthesia, whether or not guaifenesin was used. Spillman (2004) used spirometry to demonstrate specific, apneustic breathing patterns in horses anaesthetized with TIVA (ketamineclimazolam), ISO and ISO-medetomidine. However, neither of these studies examined the contribution of ribcage and abdominal compartments to the

© 2014 Association of Veterinary Anaesthetists and the American College of Veterinary Anesthesia and Analgesia, 41, 592–601

Respiratory function: part II L Kowalczyk & B Steblaj et al.

Figure 4 Selected pressure waveforms for Pdi (upper panels) and the rib cage and abdominal circumference changes (lower panels) during a Mueller manoeuvre in T-ISO (right panels) and T-TIVA (left panels). Arrows indicate positive oesophageal pressure considered as artifacts from oesophageal contraction.

Table 1 Blood gas parameters of six ponies anaesthetized with isoflurane (T-ISO) and total intravenous anaesthesia (TTIVA) Parameter

T-ISO

pH PaCO2 (mmHg) PaCO2 (kPa) PaO2 (mmHg) PaO2 (kPa) P(A-a) O2 (mmHg) P(A-a) O2 (kPa) TV (L) fR (breaths minute1) MV (L minute1) Sighs (minute1) RC amplitude (RMS) ABD amplitude (RMS)

7.37 53 94 267 3.8 9.0 33.8 0 3.8 6.6

      

T-TIVA 0.02 2 7.1  0.3 26 12.5  3.5 28 35.6  3.7 1.8 3.2 14.3

 2.9  8.7

7.40 48 67 314 2.8 19.2 47.7 0.6 3.4 5.0

         

p-Value 0.02 2 6.4  0.3 26 8.9  3.5 28 41.9  3.7 1.8 7.6 19.6 0.5 0.7 3.7

Comparison of respiratory function during TIVA and isoflurane anaesthesia in ponies Part II: breathing patterns and transdiaphragmatic pressure.

To compare breathing patterns and transdiaphragmatic pressure during total intravenous (TIVA) and isoflurane anaesthesia in ponies...
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