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A minimally invasive method for clinical trans-diaphragmatic pressure measurement in anaesthetized dogs
Veterinary Anaesthesia and Analgesia, 2014, 41, 278–283
doi:10.1111/vaa.12073
SHORT COMMUNICATION
A minimally invasive method for clinical trans-diaphragmatic pressure measurement in anaesthetized dogs Kiriaki Pavlidou*, Ioannis Savvas*, Yves Moens†, Dimitrios Vasilakos‡ & Dimitrios Raptopoulos* *Anaesthesiology and Intensive Care Unit, Companion Animal Clinic, Faculty of Veterinary Medicine, Aristotle University of Thessaloniki, Thessaloniki, Greece †Anaesthesiology and Perioperative Intensive Care, Veterinary University, Vienna, Austria ‡Anaesthesiology and ICU Department, AHEPA University Hospital, Thessaloniki, Greece Correspondence: Ioannis Savvas, Anaesthesiology and Intensive Care Unit, Companion Animal Clinic, Faculty of Veterinary Medicine, Aristotle University of Thessaloniki, St. Voutyra 11, GR-54627, Thessaloniki, Greece. E-mail: [email protected]
Abstract Objective To measure trans-diaphragmatic pressures, as an indication of diaphragmatic contractility, in anaesthetized dogs breathing normally, or during inspiratory obstruction (Mueller’s manoeuvre) in order to assess if the method is practicable for use in clinical circumstances. Study design Pilot study. Animals Twenty eight client-owned dogs, ASA I or II, 1–10 years old, 5–30 kg bodyweight, which required anaesthesia for surgery, and were to be positioned in lateral recumbency. Methods Following a standardized regimen of premedication and anaesthetic induction, anaesthesia was stabilized and maintained with isoflurane. Two commercially available balloon catheters were introduced orally, and advanced, one into the stomach and one into the mid-third of the oesophagus. Oesophageal and gastric pressures were measured from these catheters, and trans-diaphragmatic pressure (Pdi) calculated and recorded continuously. At three separate time points during anaesthesia, for one breath, inspiration was obstructed (Mueller’s manoeuvre) and Pdi was measured. Results Placement of the catheters in the stomach was not easy, and failed in three cases. In five dogs, 278
their size resulted in failure of correct placement of catheters. Good traces of all three pressures reflecting respiratory cycles were obtained from 20 dogs. During normal spontaneous breathing (mean SD [range]) Pdi was 5 2.1 (3–10) mmHg. During Mueller’s manoeuvre, Pdi was 14.6 4.5 (9–21) mmHg. Abnormal waveforms were seen included cardiac oscillations (five dogs), inadequate intragastric pressure tracing (one dog), deflections with a double peak (one dog), and multiple artifacts when there was increased heart rate and tachypnoea (two dogs in response to surgery). Conclusions and clinical relevance Measurement of trans-diaphragmatic pressure with balloon catheters was practicable in suitably sized dogs anaesthetized for clinical purposes and might be a useful tool in the assessment of diaphragmatic function. A range of catheters are required if the technique is to work in all dogs. Keywords balloon catheters, Dog, intra-gastric pressure, intra-oesophageal pressure, trans-diaphragmatic pressure.
Introduction Monitoring respiratory function is one of the cornerstones of medical and veterinary clinical practice in anaesthesia and intensive care. The diaphragm is the main inspiratory muscle and although it has
Trans-diaphragmatic pressure measurement in dogs K Pavlidou et al. received little attention, its normal function is of great importance for the anaesthetist. One of the main measurements used as an indicator of diaphragmatic contractility in humans is the trans-diaphragmatic pressure (Pdi), which is calculated as the difference between the intra-gastric (Pgast) and intra-oesophageal (Poes) pressures, the latter being taken as representative of intrapleural pressure (Green et al. 2002). Measurements are made through air-filled balloon ended catheters placed in the mid-third of the oesophagus and in the stomach (Benditt 2005). Abnormal Pdi is correlated well with respiratory muscle weakness and pathological conditions of diaphragm such as diaphragmatic fatigue. Respiratory muscle fatigue and/or diaphragmatic fatigue are defined as the inability of the relevant muscles to generate sufficient force and pressure in order to maintain alveolar ventilation. Fatigue may result from failure of the muscle and/or neuromuscular junction (peripheral fatigue) or from a decreased output of the central nervous system (central fatigue), and it is reversible during rest. In contrast, respiratory muscle weakness is a reduction in force generation that is fixed and not reversible by rest. Diaphragmatic fatigue has been associated with many respiratory diseases in humans and animals (Zakynthinos & Roussos 2005). To assess diaphragmatic muscle weakness, it is necessary to measure the Pdi when the maximal force that the patient can generate at inspiration is exerted (termed Pdi max). With co-operative human patients, a number of methods to produce inspiratory effort are used (Green et al. 2002), one of which is the Mueller’s manoeuvre, in which the patient is asked to make an inspiratory effort against a completely blocked airway (Benditt 2005). Variations include the pre-obstruction lung volume, and the number of consecutive obstructed breaths employed. Another method of obtaining Pdi max without positive co-operation from the patient is to use electrical stimuli of the phrenic nerves in order to cause a maximal diaphragmatic response. That method has been used in experimental animals for the measurement of Pdi (Hubmayr et al. 1990; Leduc et al. 2008). In most of the chronic respiratory problems seen in practice, fatigue has already been established in diaphragm. An experimental study in dogs measured Pdi in a fatigued-paralyzed diaphragm by the electrical stimulation of the phrenic nerves and without the application of modifications of Mueller’s
manoeuvre (Hubmayr et al. 1990). However, the authors cannot find reports of clinical studies on the measurement of Pdi in a non-fatigued canine diaphragm. The aim of this study was to investigate the practicality of a technique for Pdi measurement in anaesthetized dogs, based on the measuring principles used in human medicine and which, as minimally invasive, could be adapted for clinical practice. Materials and methods Ethical approval for the study was obtained from the Ethics Committee of the Faculty of Veterinary Medicine, Aristotle University of Thessaloniki, Greece. Twenty eight client-owned dogs (1–10 years old, 5–30 kg of body weight) were enrolled into this pilot study. Each owner was informed in detail about the study protocol and written consent was obtained. The dogs were admitted to Companion Animal Clinic of the Faculty of Veterinary Medicine of Thessaloniki for surgical procedures, which required the dog to be in right or left lateral recumbency. Exclusion criteria were American Society of Anesthetists physical status III or higher, any active respiratory disease, a history of a chronic respiratory problem, abdominal and/or thoracic surgery, and anticipated necessity to apply intermittent positive pressure ventilation (IPPV) during surgery. A standard protocol for anaesthesia was used for all dogs. All the animals were premedicated with dexmedetomidine (Dexdomitor; Pfizer Hellas, Greece) at 175 lg m 2 and morphine (Morphine sulfate; Famar SA, Greece) at 0.1 mg kg 1 intramuscularly. Twenty minutes later, the cephalic vein was catheterized and the administration of Lactated Ringer’s solution (LR’s, Vioser, Greece) at 10 mL kg 1 hour 1 intravenously (IV) commenced. At this time, carprofen (Rimadyl, Pfizer Hellas, Greece) was also administered at 4 mg kg 1 IV. Anaesthesia was induced with propofol (Propofol MCT/LCT, Fresenius, Fresenius Kabi Hellas, Greece) IV to effect. An initial dose of 1–2 mg kg 1 was given, followed, if needed, by incremental doses of 0.5–1 mg kg 1 until endotracheal intubation could easily be performed. Anaesthesia was maintained with isoflurane (Isoflurane, Merial, Italy) in oxygen. The animals were breathing spontaneously through a circle rebreathing system. Throughout the whole procedure, haemodynamic and respiratory parameters were monitored constantly (Datex-Ohmeda S/5, GE Healthcare, Finland) and recorded every five
© 2013 Association of Veterinary Anaesthetists and the American College of Veterinary Anesthesia and Analgesia, 41, 278–283
279
Trans-diaphragmatic pressure measurement in dogs K Pavlidou et al.
minutes. In case of an end-tidal carbon dioxide partial pressure (PE′CO2) higher than 8.5 kPa, IPPV was applied and no further measurements of Pdi were made. The estimation of diaphragmatic contractility was based on Pdi measurement, using two commercially available 90 cm long oesophageal balloon catheters (Esophageal Balloon Catheter Set; CooperSurgical Company, CT, USA) with guide wires. The balloon was localized in the distal portion of the catheter and had a capacity of 3 mL of air. As the length of the balloon catheters was constant, but the body size of the animals varied, it proved helpful to mark the catheter prior to insertion to indicate at what point the balloon would reach the stomach or be in the mid-third of the oesophagus. These marks were made on the basis of the study of Waterman & Hashim (1991), who found that the place of the lower oesophageal sphincter can be determined by subtracting 5 cm from the pre-measured distance between the external length from lower jaw incisor tooth to the anterior border of the head of the 10th rib through the ankle of the mandible. When a surgical plane of anaesthesia was achieved, the two balloon catheters were introduced orally, and advanced into the pharynx, then oesophagus. Using the above anatomical landmarks, the first catheter was introduced into the stomach for the measurement of the Pgast, and the second one in the mid-third of the oesophagus for the measurement of the Poes. Following the insertion of the catheters, their proximal end was connected to a pressure transducer. The electrical connections from the transducers were attached to a pressure-monitoring device with the appropriate software (Pressure Monitoring system Buzzer-II; Michael Roehrich, Austria) and then to a computer. The analog signal of the transducers was digitized in the dedicated buzzer-device and the data were saved to a computer. The air-filled balloon catheters were secured in place by attaching to the endotracheal tube with an adhesive tape, and after removing the guide wires, they were re-connected to the transducer and the balloons were filled with 0.5– 1 mL of air. The pressure transducers were zeroed to the atmospheric pressure prior each measurement, with the transducers positioned level with the air-filled balloon catheters. In order to confirm the proper placement of the two catheters, the obtained graph on the computer screen was observed: if the balloon of the catheter was in the stomach, a positive deflection was observed during each inspi280
ration, whereas a negative deflection was an indication that the balloon of the catheter was in the oesophagus (Fig. 1a). All pressure measurements were sampled with a rate of 10 Hz. Pgast and Poes were measured and displayed and Pdi was calculated automatically from their difference by the software. In an attempt to obtain the maximum Poes, Pgast and Pdi, a modified Mueller’s manoeuvre was applied by disconnecting the endotracheal tube from the anaesthetic circuit and tightly closing the proximal end of the tube with a thumb during the respiratory pause after the end of expiration, and thus forcing the dog to attempt to breath against the obstructed airway (Fig 1a). Pgast and Poes were monitored continuously for 60 minutes independent of the duration of the surgery. In order to calculate Pdi, the Mueller’s manoeuvre of a single obstruction was performed three separate times on each animal, with a 30 minute interval between each measurement (one just after anaesthetic induction, one just after the start of the surgery and one at the end of the 60 minutes period). The air-filled balloon catheters were removed from the animal after the end of the 60-minute period. The anaesthesia and the Pdi measurement were performed by the same investigator throughout the study. Results Standard cardiorespiratory parameters were monitored as part of normal anaesthetic practice, and not as part of the study. During most surgical procedures, anaesthesia remained stable and the mean standard deviation (range) of the heart rate was 98 16 (76–121) beats minute 1, the respiratory rate was 9 3 (6–15) breaths minute 1, the mean arterial blood pressure was 74 13 (62–95) mmHg, the PE′CO2 was 6.3 0.9 kPa (47 7 [42–58] mmHg) and the end-tidal isoflurane concentration was 1.81 0.56 (1.25–2.11)%. In two cases, the plane of anaesthesia was lighter than ideal and the dog responded to the start of surgery with an increase in heart and respiratory rates. No attempt was made to carry out a Mueller’s manoeuvre until anaesthesia was restabilized. However, no change in cardiorespiratory parameters was noticed during the application of the Mueller’s manoeuvre in any animal. The mean value of Pdi under surgical anaesthesia was 5 2.1(3–10) mmHg during a spontaneous
© 2013 Association of Veterinary Anaesthetists and the American College of Veterinary Anesthesia and Analgesia, 41, 278–283
Trans-diaphragmatic pressure measurement in dogs K Pavlidou et al.
(a)
Figure 1 demonstrates three examples of traces illustrating measurements intra-gastric (Pgast), intra-oesophageal (Poes) and transdiaphragmatic (Pdi) pressures. x-axis represents time in seconds. y-axis Pdi in mmHg. (a) Pressure waves during spontaneous breathing and occluded airway (Mueller’s manoeuvre). (b) Pressure waves during increased respiratory rate (34 breaths minute 1). Fluctuations of the baseline did not allow for the accurate measurement of pressures. (c) Pressure waves during three normal breathing cycles with cardiac artifacts.
(b)
(c)
breath and 14.6 4.5 (9–21) mmHg during the application of the Mueller’s manoeuvre. During stable anaesthesia the application of the technique was performed easily, without difficulties. However, in three cases the balloon catheter could not pass the lower oesophageal sphincter and in five cases, the deflections were not accurate because of the size of the animal (small or large breeds of dogs). These eight animals were excluded from the study leaving 20 dogs in which the study was completed.
The following types of deflections were obtained: Normal deflections: Fig. 1(a) demonstrates two • clear deflections of the three pressure traces that were obtained during two respiratory cycle, one normal and one with the application of the modified Mueller’s manoeuvre, without any artifacts. • Deflections during increase heart rate and/or respiratory rate: It was impossible to apply the modified Mueller’s manoeuvre and to calculate Pdi when the heart and respiratory rates were very high in light planes of anaesthesia. This was observed in 2/20
© 2013 Association of Veterinary Anaesthetists and the American College of Veterinary Anesthesia and Analgesia, 41, 278–283
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Trans-diaphragmatic pressure measurement in dogs K Pavlidou et al.
cases and clear pressure tracings could not be obtained without artifacts (Fig. 1b). • Flat deflection of Pgast: The deflections of the pressures could change during surgical manipulation, despite the tight mounting of the catheters at the beginning of the measurement. In 1/20 cases, the tracing of Pgast became flat during Mueller’s manoeuvre. Nevertheless, Pgast value remained positive and therefore Pdi value could be calculated. • Cardiac oscillations between the deflections: Cardiac oscillations were also noticed on the recordings of Poes and Pgast between two breaths (Fig. 1c) in 5/20 cases. They could be reduced by adjusting the position of the balloon. • A double peak deflection: A deflection with a double peak was observed in 1/20 case throughout anaesthesia. This tended to be associated with cardiac oscillations and the double peak usually disappeared when the airway was occluded. Discussion In this study, a technique for the evaluation of diaphragmatic contractility in anaesthetised dogs via the Pdi measurement is presented. There were some practical difficulties. The introduction and proper placement of the balloon catheter into the stomach was difficult. The catheter could not be passed through the lower oesophageal sphincter and reach the stomach in three cases, probably because the sphincter was too tightly closed or the catheter had become soft from the body heat. For the small breeds of dogs the size of the balloon was too long (about 10 cm), and good traces and accurate measurements of Pgast and Poes could not be obtained. In contrast, in very large dogs the catheter length was too short and its balloon could not reach the oesophageal sphincter and pass into the stomach. Thus, these animals were excluded from the study. The catheters used were commercially available and designed for use in humans; a wider range of catheters is required if the method is to be applied to all dogs. A number of ‘aberrant’ traces were noted at times. Cardiac oscillations were seen when the balloon of the catheter was very close to the heart and originate from pressure changes within the pericardium and the aorta that are communicated to the oesophageal balloon. Cardiac oscillations did not appear to influence the Pdi measurement. No attempt was made to carry out the Mueller’s manoeuvre when the dog was tachypnoeic as there 282
was no clear respiratory pause at which to close the endotracheal tube. With tachycardia, there were many artifacts from the cardiac oscillations and therefore, the obtained traces are not clear. In this pilot study the obtained Pdi values are much lower than those reported in humans, which are reported to be in the region of 100 cm H2O (73 mmHg) (Benditt 2005). Body size and species differences may have contributed to these differences. Another important factor is the lung volume at which the maximal Pdi manoeuver is initiated as this affects the measurements (Benditt 2005). In dogs, Hubmayr et al. (1990) reported that the values of Pdi in a fatigued diaphragm after phrenic nerve stimulation increased from 5.8 cm H2O at total lung capacity to 37 cm H2O at functional residual capacity. In another study, the Pdi values were around 37 cm H2O after phrenic nerve stimulation of non-fatigued diaphragm and they increased from 44 cm H2O to 50 cm H2O with 50 and 100 mL kg 1 ascites in dogs (Leduc et al. 2008). However, both the above studies in dogs obtained Pdi by phrenic nerve stimulation which, whilst it does produce maximal diaphragmatic contraction, can only be an experimental technique and is inapplicable in normal clinical circumstances. The results of this current study in dogs, that the Pdi values are lower after the application of the Mueller’s manoeuvre than those after phrenic nerve stimulation in dogs is as anticipated and suggests that Mueller’s manoeuvre in anaesthetized animals does not always produce maximal effort of the diaphragm. In humans, normal Pdi tends to be lower in women than in men and to decrease with age. The influence of other factors (height, race, fitness) is not specified, although data suggest that Pdi in highly fit subjects is not different from normal subjects (Green et al. 2002). In our study obese animals were excluded as it has been shown that obesity may decrease diaphragmatic contractility in humans (Ora et al. 2011). The objective of our study was a pilot trial to see if it was practicable to measure Pdi in anaesthetized dogs in a clinical setting, and therefore potential side effects of the technique must be considered. A complication of the introduction of the catheters into the stomach could be gastro-oesophageal reflux; there was no obvious regurgitation in any animal during the whole procedure. Although that does not rule out the possibility of silent reflux, no clinical signs of oesophagitis were detected in any
© 2013 Association of Veterinary Anaesthetists and the American College of Veterinary Anesthesia and Analgesia, 41, 278–283
Trans-diaphragmatic pressure measurement in dogs K Pavlidou et al. animal post-operatively. A possible sequel to respiratory obstruction, such as was induced by the Mueller’s manoeuvre, is post-obstructive pulmonary oedema (POPE) (Udeshi et al. 2010). Prolonged inspiration against a fixed obstruction, which resulted in pulmonary oedema, was firstly noted in experimental anaesthetized dog models in 1927 (Moore & Binger 1927). In our study obstruction was not prolonged, was for one breath only at any one time, and no clinical signs of POPE were observed in any animal for up to 24 hours post-anaesthesia. In conclusion, the technique for Pdi measurement in anaesthetized dogs in a clinical setting was successfully applied in this pilot study. The modified Mueller’s manoeuvre was found to be feasible. The above findings suggest that Pdi measurement with balloon catheters may be a useful tool in the assessment of respiratory function in dogs in clinical conditions. Acknowledgements The authors thank the Referees for their very helpful advice which added to the quality of this paper.
This research has been co-financed by the European Union (European Social Fund – ESF) and Greek national funds through the Operational Program “Education and Lifelong Learning” of the National Strategic Reference Framework (NSRF) - Research
Funding Program: Heracleitus II. Investing in knowledge society through the European Social Fund. References Benditt JO (2005) Esophageal and gastric pressure measurements. Respir Care 50, 68–75. Green M, Road J, Sieck GC et al. (2002) Tests of respiratory muscle strength. ATS/ERS Statement on Respiratory Muscle Testing. Am J Respir Crit Care Med 166, 528– 547. Hubmayr RD, Sprung J, Nelson S (1990) Determinants of transdiaphragmatic pressure in dogs. J Appl Physiol 69, 2050–2056. Leduc D, Cappello M, Gevenois PA et al. (2008) Mechanics of the canine diaphragm in ascites: a CT study. J Appl Physiol 104, 423–428. Moore RL, Binger CA (1927) The response to respiratory resistance: a comparison of the effects produced by partial obstruction in the inspiratory and expiratory phases of respiration. J Exp Med 45, 1065–1080. Ora J, Laveneziana P, Wadell K et al. (2011) Effect of obesity on respiratory mechanics during rest and exercise in COPD. J Appl Physiol 111, 10–19. Udeshi A, Cantie SM, Pierre E (2010) Postobstructive pulmonary edema. J Crit Care 25, 508.e1–508.e5. Waterman AE, Hashim MA (1991) Measurement of the length and position of the lower oesophageal sphincter by correlation of external measurements and radiographic estimations in dogs. Vet Rec 129, 261– 264. Zakynthinos S, Roussos C (2005) Respiratory muscle fatigue. In: Physiologic Basis of Respiratory Disease. Hamid O, Shannon J, Martin J (eds). BC Decker, Hamilton. pp. 289–307. Received 18 May 2013; accepted 19 June 2013.
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doi:10.1111/vaa.12073
SHORT COMMUNICATION
A minimally invasive method for clinical trans-diaphragmatic pressure measurement in anaesthetized dogs Kiriaki Pavlidou*, Ioannis Savvas*, Yves Moens†, Dimitrios Vasilakos‡ & Dimitrios Raptopoulos* *Anaesthesiology and Intensive Care Unit, Companion Animal Clinic, Faculty of Veterinary Medicine, Aristotle University of Thessaloniki, Thessaloniki, Greece †Anaesthesiology and Perioperative Intensive Care, Veterinary University, Vienna, Austria ‡Anaesthesiology and ICU Department, AHEPA University Hospital, Thessaloniki, Greece Correspondence: Ioannis Savvas, Anaesthesiology and Intensive Care Unit, Companion Animal Clinic, Faculty of Veterinary Medicine, Aristotle University of Thessaloniki, St. Voutyra 11, GR-54627, Thessaloniki, Greece. E-mail: [email protected]
Abstract Objective To measure trans-diaphragmatic pressures, as an indication of diaphragmatic contractility, in anaesthetized dogs breathing normally, or during inspiratory obstruction (Mueller’s manoeuvre) in order to assess if the method is practicable for use in clinical circumstances. Study design Pilot study. Animals Twenty eight client-owned dogs, ASA I or II, 1–10 years old, 5–30 kg bodyweight, which required anaesthesia for surgery, and were to be positioned in lateral recumbency. Methods Following a standardized regimen of premedication and anaesthetic induction, anaesthesia was stabilized and maintained with isoflurane. Two commercially available balloon catheters were introduced orally, and advanced, one into the stomach and one into the mid-third of the oesophagus. Oesophageal and gastric pressures were measured from these catheters, and trans-diaphragmatic pressure (Pdi) calculated and recorded continuously. At three separate time points during anaesthesia, for one breath, inspiration was obstructed (Mueller’s manoeuvre) and Pdi was measured. Results Placement of the catheters in the stomach was not easy, and failed in three cases. In five dogs, 278
their size resulted in failure of correct placement of catheters. Good traces of all three pressures reflecting respiratory cycles were obtained from 20 dogs. During normal spontaneous breathing (mean SD [range]) Pdi was 5 2.1 (3–10) mmHg. During Mueller’s manoeuvre, Pdi was 14.6 4.5 (9–21) mmHg. Abnormal waveforms were seen included cardiac oscillations (five dogs), inadequate intragastric pressure tracing (one dog), deflections with a double peak (one dog), and multiple artifacts when there was increased heart rate and tachypnoea (two dogs in response to surgery). Conclusions and clinical relevance Measurement of trans-diaphragmatic pressure with balloon catheters was practicable in suitably sized dogs anaesthetized for clinical purposes and might be a useful tool in the assessment of diaphragmatic function. A range of catheters are required if the technique is to work in all dogs. Keywords balloon catheters, Dog, intra-gastric pressure, intra-oesophageal pressure, trans-diaphragmatic pressure.
Introduction Monitoring respiratory function is one of the cornerstones of medical and veterinary clinical practice in anaesthesia and intensive care. The diaphragm is the main inspiratory muscle and although it has
Trans-diaphragmatic pressure measurement in dogs K Pavlidou et al. received little attention, its normal function is of great importance for the anaesthetist. One of the main measurements used as an indicator of diaphragmatic contractility in humans is the trans-diaphragmatic pressure (Pdi), which is calculated as the difference between the intra-gastric (Pgast) and intra-oesophageal (Poes) pressures, the latter being taken as representative of intrapleural pressure (Green et al. 2002). Measurements are made through air-filled balloon ended catheters placed in the mid-third of the oesophagus and in the stomach (Benditt 2005). Abnormal Pdi is correlated well with respiratory muscle weakness and pathological conditions of diaphragm such as diaphragmatic fatigue. Respiratory muscle fatigue and/or diaphragmatic fatigue are defined as the inability of the relevant muscles to generate sufficient force and pressure in order to maintain alveolar ventilation. Fatigue may result from failure of the muscle and/or neuromuscular junction (peripheral fatigue) or from a decreased output of the central nervous system (central fatigue), and it is reversible during rest. In contrast, respiratory muscle weakness is a reduction in force generation that is fixed and not reversible by rest. Diaphragmatic fatigue has been associated with many respiratory diseases in humans and animals (Zakynthinos & Roussos 2005). To assess diaphragmatic muscle weakness, it is necessary to measure the Pdi when the maximal force that the patient can generate at inspiration is exerted (termed Pdi max). With co-operative human patients, a number of methods to produce inspiratory effort are used (Green et al. 2002), one of which is the Mueller’s manoeuvre, in which the patient is asked to make an inspiratory effort against a completely blocked airway (Benditt 2005). Variations include the pre-obstruction lung volume, and the number of consecutive obstructed breaths employed. Another method of obtaining Pdi max without positive co-operation from the patient is to use electrical stimuli of the phrenic nerves in order to cause a maximal diaphragmatic response. That method has been used in experimental animals for the measurement of Pdi (Hubmayr et al. 1990; Leduc et al. 2008). In most of the chronic respiratory problems seen in practice, fatigue has already been established in diaphragm. An experimental study in dogs measured Pdi in a fatigued-paralyzed diaphragm by the electrical stimulation of the phrenic nerves and without the application of modifications of Mueller’s
manoeuvre (Hubmayr et al. 1990). However, the authors cannot find reports of clinical studies on the measurement of Pdi in a non-fatigued canine diaphragm. The aim of this study was to investigate the practicality of a technique for Pdi measurement in anaesthetized dogs, based on the measuring principles used in human medicine and which, as minimally invasive, could be adapted for clinical practice. Materials and methods Ethical approval for the study was obtained from the Ethics Committee of the Faculty of Veterinary Medicine, Aristotle University of Thessaloniki, Greece. Twenty eight client-owned dogs (1–10 years old, 5–30 kg of body weight) were enrolled into this pilot study. Each owner was informed in detail about the study protocol and written consent was obtained. The dogs were admitted to Companion Animal Clinic of the Faculty of Veterinary Medicine of Thessaloniki for surgical procedures, which required the dog to be in right or left lateral recumbency. Exclusion criteria were American Society of Anesthetists physical status III or higher, any active respiratory disease, a history of a chronic respiratory problem, abdominal and/or thoracic surgery, and anticipated necessity to apply intermittent positive pressure ventilation (IPPV) during surgery. A standard protocol for anaesthesia was used for all dogs. All the animals were premedicated with dexmedetomidine (Dexdomitor; Pfizer Hellas, Greece) at 175 lg m 2 and morphine (Morphine sulfate; Famar SA, Greece) at 0.1 mg kg 1 intramuscularly. Twenty minutes later, the cephalic vein was catheterized and the administration of Lactated Ringer’s solution (LR’s, Vioser, Greece) at 10 mL kg 1 hour 1 intravenously (IV) commenced. At this time, carprofen (Rimadyl, Pfizer Hellas, Greece) was also administered at 4 mg kg 1 IV. Anaesthesia was induced with propofol (Propofol MCT/LCT, Fresenius, Fresenius Kabi Hellas, Greece) IV to effect. An initial dose of 1–2 mg kg 1 was given, followed, if needed, by incremental doses of 0.5–1 mg kg 1 until endotracheal intubation could easily be performed. Anaesthesia was maintained with isoflurane (Isoflurane, Merial, Italy) in oxygen. The animals were breathing spontaneously through a circle rebreathing system. Throughout the whole procedure, haemodynamic and respiratory parameters were monitored constantly (Datex-Ohmeda S/5, GE Healthcare, Finland) and recorded every five
© 2013 Association of Veterinary Anaesthetists and the American College of Veterinary Anesthesia and Analgesia, 41, 278–283
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Trans-diaphragmatic pressure measurement in dogs K Pavlidou et al.
minutes. In case of an end-tidal carbon dioxide partial pressure (PE′CO2) higher than 8.5 kPa, IPPV was applied and no further measurements of Pdi were made. The estimation of diaphragmatic contractility was based on Pdi measurement, using two commercially available 90 cm long oesophageal balloon catheters (Esophageal Balloon Catheter Set; CooperSurgical Company, CT, USA) with guide wires. The balloon was localized in the distal portion of the catheter and had a capacity of 3 mL of air. As the length of the balloon catheters was constant, but the body size of the animals varied, it proved helpful to mark the catheter prior to insertion to indicate at what point the balloon would reach the stomach or be in the mid-third of the oesophagus. These marks were made on the basis of the study of Waterman & Hashim (1991), who found that the place of the lower oesophageal sphincter can be determined by subtracting 5 cm from the pre-measured distance between the external length from lower jaw incisor tooth to the anterior border of the head of the 10th rib through the ankle of the mandible. When a surgical plane of anaesthesia was achieved, the two balloon catheters were introduced orally, and advanced into the pharynx, then oesophagus. Using the above anatomical landmarks, the first catheter was introduced into the stomach for the measurement of the Pgast, and the second one in the mid-third of the oesophagus for the measurement of the Poes. Following the insertion of the catheters, their proximal end was connected to a pressure transducer. The electrical connections from the transducers were attached to a pressure-monitoring device with the appropriate software (Pressure Monitoring system Buzzer-II; Michael Roehrich, Austria) and then to a computer. The analog signal of the transducers was digitized in the dedicated buzzer-device and the data were saved to a computer. The air-filled balloon catheters were secured in place by attaching to the endotracheal tube with an adhesive tape, and after removing the guide wires, they were re-connected to the transducer and the balloons were filled with 0.5– 1 mL of air. The pressure transducers were zeroed to the atmospheric pressure prior each measurement, with the transducers positioned level with the air-filled balloon catheters. In order to confirm the proper placement of the two catheters, the obtained graph on the computer screen was observed: if the balloon of the catheter was in the stomach, a positive deflection was observed during each inspi280
ration, whereas a negative deflection was an indication that the balloon of the catheter was in the oesophagus (Fig. 1a). All pressure measurements were sampled with a rate of 10 Hz. Pgast and Poes were measured and displayed and Pdi was calculated automatically from their difference by the software. In an attempt to obtain the maximum Poes, Pgast and Pdi, a modified Mueller’s manoeuvre was applied by disconnecting the endotracheal tube from the anaesthetic circuit and tightly closing the proximal end of the tube with a thumb during the respiratory pause after the end of expiration, and thus forcing the dog to attempt to breath against the obstructed airway (Fig 1a). Pgast and Poes were monitored continuously for 60 minutes independent of the duration of the surgery. In order to calculate Pdi, the Mueller’s manoeuvre of a single obstruction was performed three separate times on each animal, with a 30 minute interval between each measurement (one just after anaesthetic induction, one just after the start of the surgery and one at the end of the 60 minutes period). The air-filled balloon catheters were removed from the animal after the end of the 60-minute period. The anaesthesia and the Pdi measurement were performed by the same investigator throughout the study. Results Standard cardiorespiratory parameters were monitored as part of normal anaesthetic practice, and not as part of the study. During most surgical procedures, anaesthesia remained stable and the mean standard deviation (range) of the heart rate was 98 16 (76–121) beats minute 1, the respiratory rate was 9 3 (6–15) breaths minute 1, the mean arterial blood pressure was 74 13 (62–95) mmHg, the PE′CO2 was 6.3 0.9 kPa (47 7 [42–58] mmHg) and the end-tidal isoflurane concentration was 1.81 0.56 (1.25–2.11)%. In two cases, the plane of anaesthesia was lighter than ideal and the dog responded to the start of surgery with an increase in heart and respiratory rates. No attempt was made to carry out a Mueller’s manoeuvre until anaesthesia was restabilized. However, no change in cardiorespiratory parameters was noticed during the application of the Mueller’s manoeuvre in any animal. The mean value of Pdi under surgical anaesthesia was 5 2.1(3–10) mmHg during a spontaneous
© 2013 Association of Veterinary Anaesthetists and the American College of Veterinary Anesthesia and Analgesia, 41, 278–283
Trans-diaphragmatic pressure measurement in dogs K Pavlidou et al.
(a)
Figure 1 demonstrates three examples of traces illustrating measurements intra-gastric (Pgast), intra-oesophageal (Poes) and transdiaphragmatic (Pdi) pressures. x-axis represents time in seconds. y-axis Pdi in mmHg. (a) Pressure waves during spontaneous breathing and occluded airway (Mueller’s manoeuvre). (b) Pressure waves during increased respiratory rate (34 breaths minute 1). Fluctuations of the baseline did not allow for the accurate measurement of pressures. (c) Pressure waves during three normal breathing cycles with cardiac artifacts.
(b)
(c)
breath and 14.6 4.5 (9–21) mmHg during the application of the Mueller’s manoeuvre. During stable anaesthesia the application of the technique was performed easily, without difficulties. However, in three cases the balloon catheter could not pass the lower oesophageal sphincter and in five cases, the deflections were not accurate because of the size of the animal (small or large breeds of dogs). These eight animals were excluded from the study leaving 20 dogs in which the study was completed.
The following types of deflections were obtained: Normal deflections: Fig. 1(a) demonstrates two • clear deflections of the three pressure traces that were obtained during two respiratory cycle, one normal and one with the application of the modified Mueller’s manoeuvre, without any artifacts. • Deflections during increase heart rate and/or respiratory rate: It was impossible to apply the modified Mueller’s manoeuvre and to calculate Pdi when the heart and respiratory rates were very high in light planes of anaesthesia. This was observed in 2/20
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Trans-diaphragmatic pressure measurement in dogs K Pavlidou et al.
cases and clear pressure tracings could not be obtained without artifacts (Fig. 1b). • Flat deflection of Pgast: The deflections of the pressures could change during surgical manipulation, despite the tight mounting of the catheters at the beginning of the measurement. In 1/20 cases, the tracing of Pgast became flat during Mueller’s manoeuvre. Nevertheless, Pgast value remained positive and therefore Pdi value could be calculated. • Cardiac oscillations between the deflections: Cardiac oscillations were also noticed on the recordings of Poes and Pgast between two breaths (Fig. 1c) in 5/20 cases. They could be reduced by adjusting the position of the balloon. • A double peak deflection: A deflection with a double peak was observed in 1/20 case throughout anaesthesia. This tended to be associated with cardiac oscillations and the double peak usually disappeared when the airway was occluded. Discussion In this study, a technique for the evaluation of diaphragmatic contractility in anaesthetised dogs via the Pdi measurement is presented. There were some practical difficulties. The introduction and proper placement of the balloon catheter into the stomach was difficult. The catheter could not be passed through the lower oesophageal sphincter and reach the stomach in three cases, probably because the sphincter was too tightly closed or the catheter had become soft from the body heat. For the small breeds of dogs the size of the balloon was too long (about 10 cm), and good traces and accurate measurements of Pgast and Poes could not be obtained. In contrast, in very large dogs the catheter length was too short and its balloon could not reach the oesophageal sphincter and pass into the stomach. Thus, these animals were excluded from the study. The catheters used were commercially available and designed for use in humans; a wider range of catheters is required if the method is to be applied to all dogs. A number of ‘aberrant’ traces were noted at times. Cardiac oscillations were seen when the balloon of the catheter was very close to the heart and originate from pressure changes within the pericardium and the aorta that are communicated to the oesophageal balloon. Cardiac oscillations did not appear to influence the Pdi measurement. No attempt was made to carry out the Mueller’s manoeuvre when the dog was tachypnoeic as there 282
was no clear respiratory pause at which to close the endotracheal tube. With tachycardia, there were many artifacts from the cardiac oscillations and therefore, the obtained traces are not clear. In this pilot study the obtained Pdi values are much lower than those reported in humans, which are reported to be in the region of 100 cm H2O (73 mmHg) (Benditt 2005). Body size and species differences may have contributed to these differences. Another important factor is the lung volume at which the maximal Pdi manoeuver is initiated as this affects the measurements (Benditt 2005). In dogs, Hubmayr et al. (1990) reported that the values of Pdi in a fatigued diaphragm after phrenic nerve stimulation increased from 5.8 cm H2O at total lung capacity to 37 cm H2O at functional residual capacity. In another study, the Pdi values were around 37 cm H2O after phrenic nerve stimulation of non-fatigued diaphragm and they increased from 44 cm H2O to 50 cm H2O with 50 and 100 mL kg 1 ascites in dogs (Leduc et al. 2008). However, both the above studies in dogs obtained Pdi by phrenic nerve stimulation which, whilst it does produce maximal diaphragmatic contraction, can only be an experimental technique and is inapplicable in normal clinical circumstances. The results of this current study in dogs, that the Pdi values are lower after the application of the Mueller’s manoeuvre than those after phrenic nerve stimulation in dogs is as anticipated and suggests that Mueller’s manoeuvre in anaesthetized animals does not always produce maximal effort of the diaphragm. In humans, normal Pdi tends to be lower in women than in men and to decrease with age. The influence of other factors (height, race, fitness) is not specified, although data suggest that Pdi in highly fit subjects is not different from normal subjects (Green et al. 2002). In our study obese animals were excluded as it has been shown that obesity may decrease diaphragmatic contractility in humans (Ora et al. 2011). The objective of our study was a pilot trial to see if it was practicable to measure Pdi in anaesthetized dogs in a clinical setting, and therefore potential side effects of the technique must be considered. A complication of the introduction of the catheters into the stomach could be gastro-oesophageal reflux; there was no obvious regurgitation in any animal during the whole procedure. Although that does not rule out the possibility of silent reflux, no clinical signs of oesophagitis were detected in any
© 2013 Association of Veterinary Anaesthetists and the American College of Veterinary Anesthesia and Analgesia, 41, 278–283
Trans-diaphragmatic pressure measurement in dogs K Pavlidou et al. animal post-operatively. A possible sequel to respiratory obstruction, such as was induced by the Mueller’s manoeuvre, is post-obstructive pulmonary oedema (POPE) (Udeshi et al. 2010). Prolonged inspiration against a fixed obstruction, which resulted in pulmonary oedema, was firstly noted in experimental anaesthetized dog models in 1927 (Moore & Binger 1927). In our study obstruction was not prolonged, was for one breath only at any one time, and no clinical signs of POPE were observed in any animal for up to 24 hours post-anaesthesia. In conclusion, the technique for Pdi measurement in anaesthetized dogs in a clinical setting was successfully applied in this pilot study. The modified Mueller’s manoeuvre was found to be feasible. The above findings suggest that Pdi measurement with balloon catheters may be a useful tool in the assessment of respiratory function in dogs in clinical conditions. Acknowledgements The authors thank the Referees for their very helpful advice which added to the quality of this paper.
This research has been co-financed by the European Union (European Social Fund – ESF) and Greek national funds through the Operational Program “Education and Lifelong Learning” of the National Strategic Reference Framework (NSRF) - Research
Funding Program: Heracleitus II. Investing in knowledge society through the European Social Fund. References Benditt JO (2005) Esophageal and gastric pressure measurements. Respir Care 50, 68–75. Green M, Road J, Sieck GC et al. (2002) Tests of respiratory muscle strength. ATS/ERS Statement on Respiratory Muscle Testing. Am J Respir Crit Care Med 166, 528– 547. Hubmayr RD, Sprung J, Nelson S (1990) Determinants of transdiaphragmatic pressure in dogs. J Appl Physiol 69, 2050–2056. Leduc D, Cappello M, Gevenois PA et al. (2008) Mechanics of the canine diaphragm in ascites: a CT study. J Appl Physiol 104, 423–428. Moore RL, Binger CA (1927) The response to respiratory resistance: a comparison of the effects produced by partial obstruction in the inspiratory and expiratory phases of respiration. J Exp Med 45, 1065–1080. Ora J, Laveneziana P, Wadell K et al. (2011) Effect of obesity on respiratory mechanics during rest and exercise in COPD. J Appl Physiol 111, 10–19. Udeshi A, Cantie SM, Pierre E (2010) Postobstructive pulmonary edema. J Crit Care 25, 508.e1–508.e5. Waterman AE, Hashim MA (1991) Measurement of the length and position of the lower oesophageal sphincter by correlation of external measurements and radiographic estimations in dogs. Vet Rec 129, 261– 264. Zakynthinos S, Roussos C (2005) Respiratory muscle fatigue. In: Physiologic Basis of Respiratory Disease. Hamid O, Shannon J, Martin J (eds). BC Decker, Hamilton. pp. 289–307. Received 18 May 2013; accepted 19 June 2013.
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