Effects of reduction of inspired oxygen fraction or application of positive end-expiratory pressure after an alveolar recruitment maneuver on respiratory mechanics, gas exchange, and lung aeration in dogs during anesthesia and neuromuscular blockade

Valentina De Monte Dipartimento dell'Emergenza e dei Trapianti di Organi, Sezione di Chirurgia Veterinaria, Facoltà di Medicina Veterinaria, Università degli Studi di Bari, Aldo Moro, Valenzano, (Bari), Italy.

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Salvatore Grasso Dipartimento dell'Emergenza e dei Trapianti di Organi, Sezione di Anestesia e Terapia Intensiva, Facoltà di Medicina e Chirurgia, Università degli Studi di Bari, Aldo Moro, Bari, Italy.

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Carmelinda De Marzo Dipartimento dell'Emergenza e dei Trapianti di Organi, Sezione di Chirurgia Veterinaria, Facoltà di Medicina Veterinaria, Università degli Studi di Bari, Aldo Moro, Valenzano, (Bari), Italy.

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Antonio Crovace Dipartimento dell'Emergenza e dei Trapianti di Organi, Sezione di Chirurgia Veterinaria, Facoltà di Medicina Veterinaria, Università degli Studi di Bari, Aldo Moro, Valenzano, (Bari), Italy.

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Francesco Staffieri Dipartimento dell'Emergenza e dei Trapianti di Organi, Sezione di Chirurgia Veterinaria, Facoltà di Medicina Veterinaria, Università degli Studi di Bari, Aldo Moro, Valenzano, (Bari), Italy.

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Abstract

Objective—To evaluate the effectiveness of reduction of inspired oxygen fraction (Fio 2) or application of positive end-expiratory pressure (PEEP) after an alveolar recruitment maneuver (ARM) in minimizing anesthesia-induced atelectasis in dogs.

Animals—30 healthy female dogs.

Procedures—During anesthesia and neuromuscular blockade, dogs were mechanically ventilated under baseline conditions (tidal volume, 12 mL/kg; inspiratory-to-expiratory ratio, 1:2; Fio 2, 1; and zero end-expiratory pressure [ZEEP]). After 40 minutes, lungs were inflated (airway pressure, 40 cm H2O) for 20 seconds. Dogs were then exposed to baseline conditions (ZEEP100 group), baseline conditions with Fio 2 reduced to 0.4 (ZEEP40 group), or baseline conditions with PEEP at 5 cm H2O (PEEP100 group; 10 dogs/group). For each dog, arterial blood gas variables and respiratory system mechanics were evaluated and CT scans of the thorax were obtained before and at 5 (T5) and 30 (T30) minutes after the ARM.

Results—Compared with pre-ARM findings, atelectasis decreased and Pao 2:Fio 2 ratio increased at T5 in all groups. At T30, atelectasis and oxygenation returned to pre-ARM findings in the ZEEP100 group but remained similar to T5 findings in the other groups. At T5 and T30, lung static compliance in the PEEP100 group was higher than values in the other groups.

Conclusions and Clinical Relevance—Application of airway pressure of 40 cm H2O for 20 seconds followed by Fio 2 reduction to 0.4 or ventilation with PEEP (5 cm H2O) was effective in diminishing anesthesia-induced atelectasis and maintaining lung function in dogs, compared with the effects of mechanical ventilation providing an Fio 2 of 1.

Abstract

Objective—To evaluate the effectiveness of reduction of inspired oxygen fraction (Fio 2) or application of positive end-expiratory pressure (PEEP) after an alveolar recruitment maneuver (ARM) in minimizing anesthesia-induced atelectasis in dogs.

Animals—30 healthy female dogs.

Procedures—During anesthesia and neuromuscular blockade, dogs were mechanically ventilated under baseline conditions (tidal volume, 12 mL/kg; inspiratory-to-expiratory ratio, 1:2; Fio 2, 1; and zero end-expiratory pressure [ZEEP]). After 40 minutes, lungs were inflated (airway pressure, 40 cm H2O) for 20 seconds. Dogs were then exposed to baseline conditions (ZEEP100 group), baseline conditions with Fio 2 reduced to 0.4 (ZEEP40 group), or baseline conditions with PEEP at 5 cm H2O (PEEP100 group; 10 dogs/group). For each dog, arterial blood gas variables and respiratory system mechanics were evaluated and CT scans of the thorax were obtained before and at 5 (T5) and 30 (T30) minutes after the ARM.

Results—Compared with pre-ARM findings, atelectasis decreased and Pao 2:Fio 2 ratio increased at T5 in all groups. At T30, atelectasis and oxygenation returned to pre-ARM findings in the ZEEP100 group but remained similar to T5 findings in the other groups. At T5 and T30, lung static compliance in the PEEP100 group was higher than values in the other groups.

Conclusions and Clinical Relevance—Application of airway pressure of 40 cm H2O for 20 seconds followed by Fio 2 reduction to 0.4 or ventilation with PEEP (5 cm H2O) was effective in diminishing anesthesia-induced atelectasis and maintaining lung function in dogs, compared with the effects of mechanical ventilation providing an Fio 2 of 1.

In humans and other animals, general anesthesia is associated with development of pulmonary atelectasis in the dependent lung regions, despite mechanical ventilation.1–5 Atelectasis seriously affects the lungs’ mechanical properties (ie, reduction of lung compliance) and gas exchange (ie, increase in intrapulmonary shunt) during surgery and may cause postoperative pulmonary complications.1,6 The main mechanisms responsible for the development of atelectasis during anesthesia are absorption of the alveolar gas as a consequence of decreased functional residual capacity and closure of small airways (absorption atelectasis), increased pressure surrounding the alveoli (compression atelectasis), and impairment of surfactant function.6 Although the clinical impact of pulmonary atelectasis in dogs still needs to be fully determined, a recent study3 by our group revealed that, as in humans, healthy dogs develop pulmonary atelectasis when breathing high concentrations of oxygen in inspired gas during anesthesia. In particular, results of that study3 indicated that immediately after induction of anesthesia in dogs undergoing abdominal surgery, use of an Fio2 of 0.4 reduces the amount of atelectasis that develops in those patients, compared with use of a higher Fio2 (> 0.9). Oxygen is a highly diffusible gas that promotes partial (poor aeration) or complete (atelectasis) alveolar collapse in areas of the lungs affected by a partial or complete airway closure, respectively.6,7 The principal consequence of such an occurrence is an impairment of the alveolar ventilation-to-perfusion ratio that leads to an increase of venous admixture.1,7

The main strategies for preventing and treating anesthesia-related atelectasis are decreasing Fio2 and applying adequate positive pressure to reopen and allow gases into the collapsed alveoli (alveolar recruitment).8,9 Moreover, alveolar recruitment can also be achieved with a so-called ARM.8 An ARM is a temporary ventilation of the lungs at very high Paw intended to recruit the lung parenchyma.8 The effects of ARMs (eg, on gas exchange and lung mechanics) have been extensively investigated in humans with acute respiratory distress syndrome10,11 and in healthy people undergoing general anesthesia.12,13 Two main types of maneuvers that are applied are a vital-capacity ARM, which is characterized by a sustained inflation of the lungs at a Paw of 40 cm H2O for 10 to 40 seconds or a progressive increase in PEEP to gradually increase end-inspiratory Paw to 40 cm H2O.8 However, despite the efficacy of ARMs, the effects are transient, particularly in patients ventilated with pure oxygen.7 In humans undergoing anesthesia, the use of the lowest Fio2 compatible with arterial oxygenation and the application of adequate PEEP after the execution of an ARM are advocated by clinical guidelines.8

To our knowledge, there are few clinical protocols for preventing and treating anesthesia-related pulmonary atelectasis in veterinary patients. Recently, our group demonstrated that a vital-capacity ARM is safe and able to temporarily reduce atelectasis and improve gas exchange in healthy anesthetized dogs breathing pure oxygen.14 The aim of the study reported here was to evaluate the effectiveness of reduction of Fio2 to 0.4 or application of PEEP of 5 cm H2O after an ARM in minimizing anesthesia-induced atelectasis in dogs. To this end, gas exchange, respiratory mechanics, and lung aeration achieved via 3 ventilatory conditions applied after an ARM in dogs that were breathing pure oxygen since the induction of anesthesia were evaluated. Our hypothesis was that decreasing the Fio2 or applying low-level PEEP immediately after an ARM might prolong the improvement of lung function induced by such maneuver in anesthetized dogs.

Materials and Methods

Animals—Thirty client-owned healthy adult female mixed-breed dogs that were scheduled to undergo elective ovariohysterectomy were enrolled in the study. Written owner informed consent was obtained. For each dog, preoperative screening included a CBC, serum biochemical analyses, and thoracic radiography. Dogs with abnormal clinicopathologic findings or physical evidence of pulmonary disease were excluded from the study. The study was conducted in compliance with the Italian Animal Welfare and statutes of the University of Bari, relating to the use of client-owned animals in clinical investigations.

Anesthetic procedure and monitoring—Each dog was premedicated with acepromazine maleatea (0.03 mg/kg) and morphine sulphateb (0.3 mg/kg) administered IM. When an adequate level of sedation was achieved, a cephalic vein was catheterized and lactated Ringer's solution (5 mL/kg/h) was administered. Approximately 30 minutes after premedication, anesthesia was induced via administration of propofolc (4 to 6 mg/kg, IV) and maintained with a constant rate infusion of propofol (0.4 to 0.5 mg/kg/min, IV). When an adequate level of anesthesia was achieved (ie, absence of palpebral reflex and jaw tone), vecuronium bromided (0.1 mg/kg, IV) was administered. For each dog, the trachea was intubated and the lungs were mechanically ventilated.e An arterial catheter was placed in the left femoral artery for the invasive measurement of arterial blood pressure and for collection of arterial blood samples. A noncompliant extension line filled with heparinized saline (0.9% NaCl) solution was connected to the arterial catheter and to a calibrated electronic transducer (placed and zeroed at the level of the heart to obtain continuous arterial blood pressure readings).

Throughout the period of anesthesia, continuous lead II ECG was performed; heart rate (beats/min), respiratory rate (breaths/min), Petco2 (mm Hg), MAP and systolic and diastolic invasive arterial blood pressures (mm Hg), hemoglobin oxygen saturation (%), and Paw (cm H2O) were also continuously monitored.f The Fio2 was monitored continuously with an oxygen analyzerg positioned on the inspiratory limb of the breathing circuit. The oxygen analyzer was calibrated at room air and pure oxygen at the beginning of each experiment. Neuromuscular function was monitored with a peripheral nerve stimulatorh operating in a TOF stimulation mode. During each experiment, an intense neuromuscular block was maintained and additional doses of vecuronium (0.03 mg/kg IV) were administered to each dog when the first twitch of the TOF reappeared. Vecuronium administration was discontinued at the end of the experiment and during the following surgery. At the end of surgery, atropinei (0.02 mg/kg, IV) followed by neostigminej (0.05 mg/kg, IV) were administered to antagonize the neuromuscular block.

To ensure adequate analgesia during surgery for each dog, cardiovascular variables were evaluated; if the heart rate or MAP increased by more than 30% of the presurgical values, an additional bolus of morphine (0.2 mg/kg, IV) was to be administered. All dogs were continuously monitored in the recovery room for the first 4 hours after discontinuation of anesthesia; thereafter, a complete physical examination was performed every 8 hours for the next 2 days.

Study protocol—Each dog was positioned in dorsal recumbency immediately after intubation (performed in sternal recumbency) and maintained in this position until the end of the experiment. Each dog was initially ventilated (baseline ventilation) in a volume-controlled mode with a VT of 12 mL/kg, an inspiratory-to-expiratory time ratio of 1:2, an end-inspiratory pause of 33% of the inspiratory time, an Fio2 of 1, and PEEP of 0 cm H2O (ie, ZEEP); respiratory rate was regulated to maintain the Petco2 at 35 to 40 mm Hg. Forty minutes after the induction of anesthesia, a vital-capacity ARM was performed; lungs were inflated to a Paw of 40 cm H2O for 20 seconds. To perform this recruitment maneuver, the ventilator was temporarily switched to a continuous positive Paw mode that applied a pressure of 40 cm H2O for 20 seconds to the dog's respiratory system.

After the ARM, each dog was randomly assigned to 1 of 3 groups in which baseline mechanical ventilation was applied with an Fio2 of 1 (ZEEP100 group [n = 10]), baseline mechanical ventilation was applied with an Fio2 of 0.4 (ZEEP40 group [10]), or baseline mechanical ventilation was applied with an Fio2 of 1 and the addition of PEEP at 5 cm H2O (PEEP100 group [10]). Cardiovascular function (heart rate and MAP), gas exchange, respiratory mechanics, and pulmonary aeration were evaluated 10 minutes before (baseline) and 5 (T5) and 30 (T30) minutes after the ARM. The MAP and heart rate during the ARM were also recorded as the values displayed on the screen of the monitor at the end of the ARM immediately before discontinuation of the continuous positive Paw mode. At the end of the experiment, each dog underwent ovariohysterectomy.

Gas exchange assessment—For gas exchange assessment, an arterial blood sample (1 mL) was collected at baseline, T5, and T30. Blood samples were collected before CT was performed, and respiratory mechanics were evaluated; each sample was immediately analyzed.k Arterial blood pH (pH), Pao2 (mm Hg), and Paco2 (mm Hg) were measured and corrected for the body temperature of the dog at the time of sample collection. Arterial blood O2 saturation was calculated by the analyzer. The Pao2:Fio2 ratio was calculated as an index to describe pulmonary arterial blood oxygenation. Alveolar dead space was estimated as a percentage of the VT by use of the following equation15:

article image

where Petco2 corresponds to the value measured at the moment of arterial blood sample collection.

Evaluation of respiratory system mechanics—For each dog, gas flow was measured with a heated pneumotachographl connected to a differential pressure transducerm placed between the Y-piece of the ventilator circuit and the endotracheal tube. The pneumotachogram was linear over the experimental range of gas flows. Volume was obtained by numerical integration of the flow signal. Values of Paw were measured proximally to the endotracheal tube with a pressure transducer.n Changes in intrathoracic pressure were evaluated by assessment of Pes. The Pes was measured with a thin latex balloon-tipped catheter system, which was connected to a pressure transducer. An esophageal balloon (volume, 10 mL) was introduced through the dog's mouth and advanced in the distal third of the esophagus. The balloon was then filled with 1 mL of air, and its correct position was confirmed by the observation of the cardiac oscillations and the changes in Pes during tidal ventilation.16 The position of the catheter was further confirmed via CT.

To estimate the static mechanical properties of the respiratory system, an end-inspiration and a end-expiration automatic airway occlusion (each of 4 seconds’ duration) were performed at each measurement time point via operation of the appropriate control of the ventilatore that closes both the inspiratory and the expiratory branches of the circuit system at the end of an inspiration and expiration, respectively.17 The total PEEP of the respiratory system (PEEPtotRS) was measured as the plateau pressure in Paw during the end-expiratory occlusion. The total PEEP of the thoracic wall (PEEPtotTW) was measured as the plateau pressure of Pes during the end-expiratory occlusion. The total PEEP applied to the lung (PEEPtotL) was determined as follows: PEEPtotL (cm H2O) = PEEPtotRS - PEEPtotTW. Static compliance of the respiratory system (adjusted for the dog's body weight) was calculated as follows:

article image

where Pawplat is the value of Paw during the 4-second-long end-inspiratory occlusion.

Static compliance of the thoracic wall (adjusted for the dog's body weight) was calculated as follows:

article image

where Pesplat is the value of Pes during the end-inspiratory occlusion, with its value at the elastic equilibrium point of the respiratory system used as a reference value. Static compliance of the lung (adjusted for the dog's body weight) was calculated as follows:

article image

For each dog, measurements of respiratory mechanics were performed after confirming intense neuromuscular blockade (absence of any twitch response during TOF stimulation). For further data analysis, values of the aforementioned variables were displayed and collected on a personal computero through a 12-bit analog-to-digital converter boardp at a sample rate of 200 Hz.o The pneumotachograph and the transducers used to measure flow and pressures (airway and esophageal) underwent 2-point calibration before the beginning of each experiment.

Figure 1—
Figure 1—

Distribution of CT image-derived radiographic attenuations (HUs; left column) and representative transverse CT images of the thorax (right column) obtained from 3 anesthetized and mechanically ventilated dogs at 30 minutes after performance of an ARM and exposure to 1 of 3 post-ARM ventilatory conditions. Initially, each dog was mechanically ventilated under baseline conditions (VT, 12 mL/kg; inspiratory-to-expiratory ratio, 1:2; Fio2, 1; and ZEEP). After 40 minutes, the dog's lungs were inflated (Paw, 40 cm H2O) for 20 seconds (the ARM). Each dog was then exposed to baseline conditions (ZEEP100 treatment), baseline conditions with Fio2 reduced to 0.4 (ZEEP40 treatment), or baseline conditions with PEEP at 5 cm H2O (PEEP100 treatment). The y-axis numbers in the left column panels represent the number of pixels.

Citation: American Journal of Veterinary Research 74, 1; 10.2460/ajvr.74.1.25

CT scanning and analysis of lung aeration—For each dog, frontal topograms and helical CT images of the thorax were obtained with a third-generation spiral CTq at baseline, T5, and T30 during end-expiration apnea, with the dog positioned in the scanner in dorsal recumbency. To maintain a constant volume of gas during the CT scan, the endotracheal tube was clamped during the end-expiratory phase immediately before the scan was commenced. Mechanical ventilation was resumed immediately after the CT images were obtained. All images were obtained at a setting of 120 kVp and 160 mA by use of a lung algorithm; matrix size was 512 × 512, field of view was 35, and pitch was 1.5. Images (slice thickness, 10 mm) were reconstructed. The CT images were analyzed by means of a computer programr by an operator (CD) who was unaware of the dog's treatment allocation, as previously described.3–5 Briefly, both right and left lungs were chosen as regions of interest for analysis; in the CT images, the outer boundary of each region of interest was traced along the inner aspect of the ribs and the inner boundary of each region of interest was traced along the mediastinal organs. The part of the pulmonary hilum containing the trachea, main bronchi, and hilar blood vessels was excluded from each region of interest. In accordance with previous studies,3,4 aeration status of regions (or compartments) within the lung was classified as hyperinflated (ie, composed of pixels with CT numbers of −1,000 to −901 HUs), normo-aerated (ie, composed of pixels with CT numbers of −900 to −501 HUs), poorly aerated (ie, composed of pixels with CT numbers of −500 to −101 HUs), and nonaerated (ie, composed of pixels with CT numbers of −100 to 100 HUs, indicative of complete atelectasis). The area (mm2) of each compartment in each CT image was calculated. For each dog, the data acquired in each CT image were then added together to yield the total area that each type of compartment (ie, hyperinflated, normo-aerated, poorly aerated, or nonaerated) occupied within both lungs. Numeric surface area values of each type of compartment were expressed as a percentage of the total lung surface. The EELV was computed by including pixels with density values of −1,000 to 100 HUs according to the following formula18:

article image

where each voxel is a pixel with a square base of 0.59 mm on each side and a height corresponding to the CT slice thickness (10 mm). The EELV was then normalized for the dog's body weight and expressed as milliliters per kilogram.

Statistical analysis—For all recorded numeric variables, the mean ± SD are reported. Data were tested for normal distribution with the Shapiro-Wilk test. Groups were compareds with regard to dogs’ age, weight, and duration of CT scanning by use of a 1-way ANOVA. Data regarding gas exchange, respiratory mechanics, lung aeration, and cardiovascular function, all obtained at baseline, T5, and T30, were compareds within and between groups with a 2-way ANOVA for repeated measures (time and treatment), followed by a Student-Newman-Keuls test. A value of P < 0.05 was considered significant.

Results

All experiments were completed without development of intra- or postoperative complications in any dog. The mean ± SD scanning time for the helical CT was 49 ± 11 seconds. There were no significant differences among the dogs in the ZEEP100, ZEEP40, and PEEP100 groups with respect to mean age (32.4 ± 11.1 months, 31.2 ± 21.3 months, and 29.4 ± 24.4 months, respectively) and mean body weight (21.7 ± 6.5 kg, 21.5 ± 10.0 kg, and 22.0 ± 9.8 kg, respectively). No pathologically altered lung parenchyma was detected in any dog via CT. Within each study group, the ARM resulted in a decrease in heart rate and MAP, compared with baseline values. However, at baseline, T5, and T30, there were no differences in heart rate and MAP among the 3 groups (Table 1).

Table 1—

Mean ± SD heart rate and MAP in 30 anesthetized and mechanically ventilated dogs before (baseline), during, and 5 (T5) and 30 (T30) minutes after performance of an ARM and exposure to 1 of 3 post-ARM ventilatory conditions (10 dogs/group) that included an Fio2 of 1 and ZEEP (ZEEP100 group), an Fio2 of 0.4 and ZEEP (ZEEP40 group), or an Fio2 of 1 and PEEP at 5 cm H2O (PEEP100 group).

VariableGroupBaselineDuring ARM*T5T30
Heart rate (beats/min)ZEEP100108.1 ± 14.383.3 ± 10.5a108.6 ± 20.4107.5 ± 21.4
 ZEEP40105.6 ± 22.678.5 ± 9.3a107.7 ± 20.4106.8 ± 18.3
 PEEP100107.2 ± 19.680.2 ± 11.5a107.6 ± 26.8106.7 ± 28.0
MAP(mm Hg)ZEEP10087.2 ± 13.455.5 ± 7.2a87.4 ± 12.186.6 ± 12.7
 ZEEP4087.3 ± 13.158.3 ± 5.6a87.5 ± 20.786.3 ± 17.6
 PEEP10087.2 ± 11.257.5 ± 6.2a87.4 ± 15.986.5 ± 11.1

Initially, each dog was mechanically ventilated under baseline conditions (VT, 12 mL/kg; inspiratory-to-expiratory ratio, 1:2; Fio2, 1; and ZEEP); after 40 minutes, the dog's lungs were inflated (Paw, 40 cm H2O) for 20 seconds (the ARM). Each dog was then exposed to the assigned post-ARM ventilatory conditions.

Values of heart rate and MAP displayed on the screen of the patient monitor at the end of the ARM immediately before discontinuation of the continuous positive Paw mode were recorded as the values during the ARM.

Within a group, value at this time point was significantly (P < 0.05) different from the baseline value.

Gas exchange—Baseline gas exchange variables did not differ among the ZEEP100, ZEEP40, and PEEP100 groups (Table 2). The Pao2:Fio2 ratio was significantly increased from baseline at T5 in all 3 groups; however, at T30, the improvement in oxygenation persisted only in the ZEEP40 and PEEP100 groups. In each of the 3 groups, Paco2 did not change from baseline values at T5 or T30; values did not differ among groups at any time point. In the PEEP100 group, the percentage of VT delivered to the dead space (ie, VDalv/VT) was significantly decreased at T5 and T30, compared with the baseline value; at T5 and T30, the values of VDalv/VT in that group were significantly less than the corresponding values in the ZEEP100 and ZEEP40 groups.

Table 2—

Mean ± SD values of gas exchange variables in 30 anesthetized and mechanically ventilated dogs before (baseline) and at 5 (T5) and 30 (T30) minutes after performance of an ARM and exposure to 1 of 3 post-ARM ventilatory conditions (10 dogs/group) that included an Fio2 of 1 and ZEEP (ZEEP100 group), an Fio2 of 0.4 and ZEEP (ZEEP40 group), or an Fio2 of 1 and PEEP at 5 cm H2O (PEEP100 group).

VariableGroupBaselineT5T30
Pao2 (mm Hg)ZEEP100448.3 ± 100.9568.4 ± 69.2a475.0 ± 54.8b
 ZEEP40452.12 ± 71.5223.8 ± 8.1a,c214.1 ± 12.3a,c
 PEEP100453.0 ± 110.4581.33 ± 19.6a,d569.0 ± 30.2a,c,d
Pao2:Fio2 ratioZEEP100448.3 ± 100.9568.4 ± 69.2a475.0 ± 54.8b
 ZEEP40452.1 ± 71.5559.6 ± 20.2a535.3 ± 30.9a,c
 PEEP100453.0 ± 110.4581.3 ± 19.6a569.0 ± 30.2a,c
Paco2 (mm Hg)ZEEP10038.6 ± 4.240.3 ± 6.140.6 ± 7.0
 ZEEP4038.1 ± 4.839.8 ± 5.940.3 ± 5.0
 PEEP10038.3 ± 3.538.9 ± 4.840.7 ± 7.3
VDalv/VT (%)ZEEP10012.7 ± 5.47.7 ± 4.4a11.5 ± 3.8
 ZEEP4011.7 ± 5.89.8 ± 3.68.3 ± 3.4
 PEEP10010.9 ± 5.45.7 ± 3.5a,c,d4.2 ± 2.5a,c,d

Within a group, value at this time point was significantly (P < 0.05) different from the value at T5.

Within a variable for a given time point, value was significantly (P < 0.05) different from the value for the ZEEP100 group.

Within a variable for a given time point, value was significantly (P < 0.05) different from the value for the ZEEP40 group.

VDalv/VT = Percentage of dead space of the VT.

See Table 1 for remainder of key.

Respiratory mechanics—At baseline, CstatRS, CstatL, and CstatTW were similar among the ZEEP100, ZEEP40, and PEEP100 groups (Table 3). Compared with baseline values, the application of PEEP after the ARM significantly improved CstatL and CstatRS both at T5 and T30. Both CstatL and CstatRS were significantly greater at T5 and T30 in the PEEP100 group, compared with values in the ZEEP100 and ZEEP40 groups. At T5 and T30, a similar pattern of change was evident for both plateau pressure of the airways and EELV; these variables were significantly increased at those time points in the PEEP100 group, compared with baseline values and with the corresponding values in the other 2 groups. The CstatTW and minute volume remained stable in all groups despite the different experimental conditions.

Table 3—

Mean ± SD values of respiratory mechanics variables in 30 anesthetized and mechanically ventilated dogs before (baseline) and at 5 (T5) and 30 (T30) minutes after performance of an ARM and exposure to 1 of 3 post-ARM ventilatory conditions (10 dogs/group) that included an Fio2 of 1 and ZEEP (ZEEP100 group), an Fio2 of 0.4 and ZEEP (ZEEP40 group), or an Fio2 of 1 and PEEP at 5 cm H2O (PEEP100 group).

VariableGroupBaselineT5T30
VM (L/min)ZEEP1004.7 ± 1.84.8 ± 1.94.8 ± 1.8
 ZEEP404.7 ± 2.44.6 ± 2.24.6 ± 2.1
 PEEP1004.8 ± 2.04.7 ± 2.14.7 ± 2.1
Respiratory rate (breaths/min)ZEEP10018.1 ± 2.518.1 ± 2.518.7 ± 2.3
 ZEEP4016.2 ± 2.316.8 ± 2.516.8 ± 2.5
 PEEP10016.8 ± 3.318.8 ± 4.116.8 ± 4.1
EELV (mL/kg)ZEEP10030.6 ± 6.232.7 ± 7.933.1 ± 7.4
 ZEEP4030.2 ± 10.131.6 ± 9.832.0 ± 9.0
 PEEP10031.1 ± 9.455.9 ± 12.9a,c,d56.1 ± 13.1a,c,d
Pplataw (cm H2O)ZEEP1008.1 ± 1.76.0 ± 1.16.4 ± 1.3
 ZEEP409.0 ± 1.56.4 ± 1.16.6 ± 1.2
 PEEP1008.8 ± 2.211.3 ± 1.2a,c,d11.5 ± 1.3a,c,d
CstatRS (mL/cm H2O/kg)ZEEP1001.6 ± 0.41.9 ± 0.31.8 ± 0.3
 ZEEP401.6 ± 0.42.0 ± 0.22.0 ± 0.2
 PEEP1001.5 ± 0.5a2.9 ± 0.8a,c,d2.8 ± 0.8a,c,d
CstatL (mL/cm H2O/kg)ZEEP1002.8 ± 0.93.6 ± 1.43.1 ± 1.1
 ZEEP402.8 ± 1.43.9 ± 0.93.8 ± 0.9
 PEEP1002.4 ± 1.3a7.9 ± 3.9a,c,d7.7 ± 3.8a,c,d
CstatTW (mL/cm H2O/kg)ZEEP1004.2 ± 0.94.8 ± 1.04.5 ± 1.3
 ZEEP404.1 ± 0.34.4 ± 1.04.3 ± 0.9
 PEEP1004.0 ± 1.35.2 ± 1.85.2 ± 1.5

Pplataw = Plateau pressure of the airways.

See Tables 1 and 2 for key.

Lung aeration—The 4 aeration compartments (classified as hyperinflated, normo-aerated, poorly aerated, or nonaerated) were similar at baseline in the ZEEP100, ZEEP40, and PEEP100 groups (Table 4). In the ZEEP100 group, the nonaerated compartment (indicative of atelectasis) at T5 was smaller than that at baseline, but returned to the baseline value at T30. In the ZEEP40 and PEEP100 groups, the nonaerated lung compartment at both T5 and T30 was smaller than that at baseline. The overall mean baseline value of atelectasis (nonaerated compartment) for all 30 study dogs was 4.2 ± 1.1%.

Table 4—

Mean ± SD relative percentages of hyperinflated, normo-aerated, poorly aerated, and nonaerated lung compartments (expressed as percentage of the entire lung surface) in 30 anesthetized and mechanically ventilated dogs before (baseline) and at 5 (T5) and 30 (T30) minutes after performance of an ARM and exposure to 1 of 3 post-ARM ventilatory conditions (10 dogs/group) that included an Fio2 of 1 and ZEEP (ZEEP100 group), an Fio2 of 0.4 and ZEEP (ZEEP40 group), or an Fio2 of 1 and PEEP at 5 cm H2O (PEEP100 group).

Lung classificationGroupBaselineT5T30
HyperinflatedZEEP1001.2 ± 0.81.3 ± 1.51.0 ± 1.3
 ZEEP401.1 ± 0.91.3 ± 1.31.3 ± 1.3
 PEEP1001.1 ± 0.11.2 ± 1.01.2 ± 0.9
Normo-aeratedZEEP10074.8 ± 8.976.9 ± 7.374.7 ± 7.1
 ZEEP4073.9 ± 4.677.2 ± 4.479.3 ± 3.3a
 PEEP10073.6 ± 6.984.5 ± 2.5a,c,d84.3 ± 2.2a,c,d
Poorly aeratedZEEP10019.5 ± 8.019.0 ± 6.918.8 ± 7.0
 ZEEP4021.3 ± 4.819.2 ± 5.217.2 ± 3.9a
 PEEP10020.0 ± 5.111.9 ± 2.9a,c,d12.2 ± 2.6a,c,d
Nonaerated (atelectasis)ZEEP1004.3 ± 1.43.2 ± 1.2a4.5 ± 1.2b
 ZEEP404.4 ± 0.62.1 ± 0.5a,c2.0 ± 0.2a,c
 PEEP1004.7 ± 0.32.0 ± 0.3a,c2.1 ± 0.2a,c

In CT images of each dog's thorax, aeration status of compartments within the lung was classified as hyperinflated (ie, composed of pixels with CT numbers of −1,000 to −901 HUs), normo-aerated (ie, composed of pixels with CT numbers of −900 to −501 HUs), poorly aerated (ie, composed of pixels with CT numbers of −500 to −101 HUs), and nonaerated (ie, composed of pixels with CT numbers of −100 to 100 HUs, indicative of complete atelectasis). The area (mm2) of each compartment in each CT image was calculated. For each dog, the data acquired in each CT image were then added together to yield the total area that each type of compartment (ie, hyperinflated, normo-aerated, poorly aerated, or nonaerated) occupied within both lungs; these values were expressed as a percentage of the total lung surface.

See Tables 1 and 2 for key.

The poorly aerated lung compartment remained similar to the baseline value at T5 and T30 in the ZEEP100 group; however, at T5 and T30, this compartment in the ZEEP100 group was significantly larger than that in the PEEP100 group. In the ZEEP40 group at T5, the poorly aerated lung compartment remained similar to the baseline value; at T30, this component was significantly smaller than the baseline value. Compared with the baseline value, the normo-aerated lung compartment remained stable at T5 and T30 in the ZEEP100 group, whereas it was significantly larger at T5 and T30 in the PEEP100 group and significantly larger at T30 in the ZEEP40 group. The normo-aerated lung compartment in the PEEP100 group at T5 and T30 was significantly larger than the corresponding values in the ZEEP100 or ZEEP40 group. The hyperinflated lung compartment remained stable in all groups at T5 and T30, compared with baseline values.

Discussion

Vital-capacity ARMs have been shown to effectively but transiently improve lung aeration and arterial oxygenation in healthy anesthetized dogs that are ventilated with pure oxygen.14 Results of the study reported here have indicated that either reducing Fio2 to 0.4 without applying PEEP or maintaining ventilation with pure oxygen while applying PEEP at 5 cm H2O is an effective strategy for prolonging the positive effects of an ARM for up to 30 minutes.

Dogs included in the present study developed pulmonary atelectasis after induction of anesthesia when they were mechanically ventilated with an Fio2 > 0.9. However, the amount of atelectasis that developed in these study dogs was less than that which developed in dogs of a previous study3 (overall mean baseline value of atelectasis [nonaerated compartment] in all dogs in the present study was 4.2 ± 1.1%, compared with a value of 12.8 ± 3.7% in the previous study). Because the only relevant difference between the 2 studies was the CT scan timing (before surgery in the present study and after surgery in the previous study3), we speculate that the greater amount of atelectasis that developed in the dogs of the previous study could have been related to surgical factors (ie, ovariohysterectomy).

In dogs of the ZEEP100, ZEEP40, and PEEP100 groups in the present study, gas exchange and lung aeration significantly improved 5 minutes after the ARM, compared with pre-ARM baseline values. The data obtained in the ZEEP100 group confirmed the short-term nature of ARM-induced atelectasis clearance,14 suggesting the need for adequate post-ARM strategies to prevent alveolar derecruitment.

When the ARM was followed by a reduction of the Fio2 (from 1 to 0.4) in the ZEEP40 group, the improvement in gas exchange and lung aeration in those dogs was maintained for up to 30 minutes. These data confirmed that absorption atelectasis has an important role in dogs that are undergoing general anesthesia and ventilated with pure oxygen. We speculate that after the ARM, the reduction in Fio2 prevented the development of absorption atelectasis in lung areas affected by partial airway closure, as occurs in human patients.7,19 Interestingly, the Pao2 in the ZEEP40 group did not decrease to < 200 mm Hg at T5 and T30. Therefore, in the ZEEP40 group, adequate oxygenation was maintained despite the use of a lower Fio2 after the ARM. This fact may support revision of the use of pure oxygen during general anesthesia in veterinary patients, as traditionally applied in many countries.

In agreement with human data, the application of 5 cm H2O of PEEP was able to prolong the positive effects of the ARM in terms of gas exchange, lung mechanics, and lung aeration for up to 30 minutes, despite the use of high Fio2.20–22 Results of a study8 of acute respiratory distress syndrome in humans and experimental animal models indicate that the critical opening pressure required to recruit collapsed alveoli (atelectasis) is significantly higher than the PEEP that must be applied to keep recruited alveoli open at end-expiration. Of note, despite the fact that the improvement in oxygenation was similar in the ZEEP40 and PEEP100 groups in the study reported here, the improvement in respiratory mechanics (CstatL) was significantly more pronounced in the PEEP100 group. We speculate that although the use of low Fio2 prevented development of absorption atelectasis in the ZEEP40 group, the application of PEEP in the PEEP100 group increased the EELV, thereby improving lung mechanical properties and counteracting development of compression atelectasis.20 On the other hand, the reduction in VDalv/VT, absence of hyperinflation detectable via CT, improvement in lung mechanics, and stable cardiovascular variables all strongly indicated that the moderate PEEP (5 cm H2O) applied was sufficient to keep the alveoli open without inducing alveolar overdistension and hemodynamic impairment. In our opinion, the ARM-PEEP strategy represents the most logical approach to optimizing lung recruitment during general anesthesia in dogs.

Although Pes is considered the best estimation of pleural pressure, several factors can influence the accuracy of this measurement.23 The gold-standard technique to confirm the correct positioning of the esophageal balloon is considered the occlusion test: the change in Paw equals the change in Pes during a spontaneous inspiratory effort against an occluded airway.24 In the study reported here, the dogs were administered a neuromuscular blocking agent; thus, performance of an occlusion test was not possible, and the adequacy of Pes measurement was estimated simply by analyzing the synchronous change in Pes and Paw during a normal mechanical inspiration, as previously reported.16 This technical limitation could have influenced the lung mechanics data obtained in the study reported here.

The pneumotachograph and the pressure transducers used to measure flow and pressures (airways and esophageal) underwent 2-point calibration before the beginning of each experiment as suggested by the manufacturers. Although this recommendation is considered adequate for a clinical setting, we concede that a more precise calibration (ie, > 2 points) should perhaps have been performed in our study.

The hemodynamic impact of a vital-capacity ARM may limit its application in some clinical conditions.8 In the study reported here, a reduction in heart rate (24.5%) and MAP (35.5%) was evident during the ARM, compared with the pre-ARM baseline values, and these reductions were strictly related to the duration of the ARM. These findings are in agreement with those of an investigation of the effect of an ARM on hemodynamics in 10 anesthetized pigs by Nunes et al.25 One should also consider that in the study reported here, contrary to common practice, the ARM was not preceded by fluid loading, which may have an important role in preventing or reducing the hemodynamic impact of such a maneuver in the study dogs.8 Studies in pediatric human patients26 and in pigs27 have revealed that a vital-capacity ARM is safe in terms of integrity of the alveolar-capillary barrier even when repeatedly applied during the same anesthetic episode. The target Paw applied in the study reported here (40 cm H2O) was chosen on the basis of a recommendation for humans undergoing general anesthesia.12 However, specific studies in dogs are lacking and it is questionable whether the same results could have been obtained with Paws < 40 cm H2O. The same considerations apply for the duration of the ARM in the study reported here. In the human medical literature, ARM durations of 10 to 40 seconds have been reported,12 and it appears that the minimum time required to completely resolve atelectasis is 10 to 13 seconds.12 The dog-specific ARM target pressure and duration of application have yet to be established. Cycling ARMs have been also applied in anesthetized humans.13 Even though cycling ARMs may have less negative effects on the hemodynamic profile, compared with the effects of noncycling ARMs, they are more complicated to perform and require more sophisticated equipment.8,13 For this reason, we decided to test a vital-capacity ARM, which can be easily performed by simply inflating the reservoir bag of the breathing circuit, in the present study.

With regard to the clinical interpretation of the data obtained in the present study, one should also consider the potential impact that the anesthetic protocol could have had on the study results. The dogs were evaluated during neuromuscular blockade, and that paralysis could have enhanced the mechanisms responsible for the development of atelectasis (reduction in functional residual capacity and compression of the pulmonary parenchyma), compared with the effects in nonparalyzed dogs in which, to a certain extent, diaphragmatic tone is preserved. For the same reason, it would be interesting to assess the impact that a ketamine-based anesthetic protocol could have on atelectasis development in dogs that are not administered a neuromuscular blocking agent, as previously investigated in humans.28 Moreover, the use of inhalant anesthetic agents in the study reported here could have further impeded gas exchange because of the effects such drugs have on the pulmonary circulation (impairment of the hypoxic pulmonary vasoconstriction), compared with the effects of propofol.29 Without doubt, all of these speculations need further investigation in dogs.

A recruitment strategy is successful only if it is able both to reopen a collapsed area of the lungs and to keep that area open.8 According to this definition, in the study reported here, reduction of Fio2 and application of PEEP at 5 cm H2O were both successful in preventing alveolar derecruitment for up to 30 minutes after an ARM and can therefore be proposed for clinical application in dogs. Moreover, PEEP was associated with better lung compliance, most likely because of a recruiting and stabilizing effect on the alveoli. The decision regarding which of the 2 strategies to apply to a patient must be made on the basis of the clinical situation. Except for very short procedures (< 30 minutes), the data obtained in the present study do not support the use of a single ARM without reduction in Fio2 or addition of PEEP after its execution. Although results of the present study indicated that the ventilatory setting might have an important influence on the development of pulmonary atelectasis, one should also consider that other factors, such as a change in recumbency, body condition score, abdominal and thoracic cavity conformation, or surgical factors, might also have a relevant role in pulmonary aeration. In human patients, the major adverse effects of atelectasis (eg, impairment of oxygenation, pulmonary infection, and alteration of lung mechanics) became clinically relevant in the postoperative period.1 At this time, data regarding the impact of atelectasis during the postoperative period in dogs are lacking; thus, we can only speculate that adequate intraoperative treatment of atelectasis may improve lung function during recovery from surgery and anesthesia.

ABBREVIATIONS

ARM

Alveolar recruitment maneuver

CstatL

Static compliance of the lungs

CstatRS

Static compliance of the respiratory system

CstatTW

Static compliance of the thoracic wall

EELV

End-expiratory lung volume

Fio2

Inspired oxygen fraction

HU

Hounsfield unit

MAP

Mean invasive arterial blood pressure

Paw

Airway pressure

PEEP

Positive end-expiratory pressure

Petco2

End-tidal partial pressure of carbon dioxide

Pes

Esophageal pressure

TOF

Train of four

VDalv

Alveolar dead space

VT

Tidal volume

ZEEP

Zero end-expiratory pressure

a.

Prequillant 1%, Fatro SpA, Bologna, Italy.

b.

Morfina Cloridrato 1%, Molteni SpA, Firenze, Italy.

c.

PropVet 1%, Esteve Hospira Inc, Lake Forest, Ill.

d.

Norcuron 10 mg, NV Organon, Oss, Holland.

e.

Servo 300, Siemens-Elema, Solna, Sweden.

f.

SC 6002XL, Siemens, Danvers, Mass.

g.

MiniOX 3000, MSA, Gurnee, Ill.

h.

MiniStim, model MS-II, Life-Tech Inc, Houston, Tex.

i.

Atropina Solfato 0.01%, Fatro, Ozzano Emilia, Italy.

j.

Intrastigmina 0.5 mg, ILFI, Milano, Italy.

k.

VetStat, IDEXX Laboratories Inc, Westbrook, Me.

l.

Fleisch No. 2, Fleisch, Lausanne, Switzerland.

m.

Diff-Cap, Special Instruments GmbH, Nordlingen, Germany.

n.

Digima-Clic ± 100 cm H2O, Special Instruments GmbH, Nordlingen, Germany.

o.

ICU Lab, KleisTEK Engineering, Bari, Italy.

p.

DAQCard 700, National Instrument Corp, Austin, Tex.

q.

GE ProSpeed sx, General Electric, New York, NY.

r.

DicomWorks, version 1.3.5, Inviweb, Cité Internationale, Lyon, France.

s.

MedCalc, version 9.2.0.1, MedCalc Software bvba, Mariakerke, Belgium.

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