Secondary Logo

Journal Logo

Technology, Computing, and Simulation: Original Clinical Research Report

Lung Ultrasonography for the Assessment of Perioperative Atelectasis: A Pilot Feasibility Study

Monastesse, Audrey MD*; Girard, Francois MD*; Massicotte, Nathalie MD*; Chartrand-Lefebvre, Carl MD; Girard, Martin MD*

Author Information
doi: 10.1213/ANE.0000000000001603

A recent retrospective analysis of 11,000 cases of general anesthesia (GA) for noncardiac and nonthoracic surgery concluded that approximately 50% of patients were hypoxemic during GA as defined by an arterial oxygen partial pressure (PaO2)/inspired oxygen fraction (FiO2) ratio of <300 with a subset of 4% of patients being severely hypoxemic.1

When hypoxemia leads to arterial desaturation, anesthesiologists are required to rapidly diagnose the underlying problem and to institute corrective measures. To do so, they are however confronted with the limited availability of diagnostic tests that can easily be used in the intraoperative period. This is in stark contrast to the plethora of diagnostic means available to a similar hypoxemic patient in an intensive care unit. Even then, clinicians are confronted to the poor quality of anteroposterior chest x-rays2 and the dangers3 associated with moving an unstable patient to the radiology department for advanced lung imaging. It is with these caveats in mind that lung ultrasonography was developed over the past 20 years. Lung ultrasonography is noninvasive, easy to use, portable, and devoid of the risks associated with repeated exposure to ionizing radiations. Evidence-based guidelines4 have recently been published with the aim of elaborating both a unified approach and vocabulary for the ultrasonographic evaluation of various lung pathologies. Over time, bedside lung ultrasonography has proved a valuable tool for the diagnosis and follow up of a number of pathologies such as pneumothorax (sensitivity 91%, specificity 98%),5 community-acquired pneumonia (sensitivity 94%, specificity 96%),6 and pulmonary edema (sensitivity 91%, specificity 94%).7

Pulmonary shunting of blood, the principal contributor to intraoperative hypoxemia, is principally caused by atelectasis.8 A very common phenomenon during GA, atelectasis is the consequence of a 20% reduction of the functional residual capacity. This reduction is caused by the loss of respiratory muscle tone, dorsal decubitus positioning, and denitrogenation during the preoxygenation period.9 It is estimated that up to 10% of patients undergoing GA for abdominal surgery will experience a postoperative pulmonary complication,10 yet despite a similar incidence, this has not raised the same concern as postoperative cardiac complications.11 Some authors have suggested that atelectasis might be an important culprit in the development of postoperative pulmonary complications.12–14

The aim of the present study was to investigate the feasibility of lung ultrasonography in the perioperative period. Given the relative scarcity of predictable, major respiratory events during GA, the study of atelectasis during laparoscopic surgery using the lung ultrasound (LUS) score,15 a semiquantitative echographic score of lung aeration, was chosen as a model for this pilot study. During laparoscopic surgery, the increase in intra-abdominal pressure pushes the diaphragm upward leading to further atelectasis formation in the dependent lung bases.16 In addition, pneumoperitoneum itself is associated with various complications that may worsen hypoxemia: capnothorax,17 endobronchial intubation,18 and gas embolism. We hypothesized that lung ultrasonography would be feasible in all patients, would correlate with changes in oxygenation by tracking changes in lung aeration, and would allow the diagnosis of pulmonary complications.

METHODS

Patients

This was an investigator-initiated, prospective, pilot observational study. The study protocol was approved by the Comité d’éthique de la recherche du Centre hospitalier de l’Université de Montréal (12.282) and registered at ClinicalTrials.gov (NCT01749436) before patient enrollment. Written informed consent was obtained from all patients. Between April 2013 and September 2013, consecutive patients ≥18 years old scheduled to undergo elective abdominal or gynecologic laparoscopic surgery in the dorsal or lithotomy position were screened for inclusion. Exclusion criteria were a body mass index (BMI) >40 kg/m2, American Society of Anesthesiologists physical status IV or V, a history of intrathoracic procedure including chest tubes, very severe pulmonary disease (forced expiratory volume in 1 second <30% of the predicted value), and any contraindication to radial artery cannulation.19

Anesthesia Protocol

Mechanical ventilation was standardized for all patients. GE Datex-Ohmeda Aestiva 3000 (GE Healthcare, Wauwatosa, WI) delivered volume-controlled ventilation with the following settings: tidal volume of 8 mL/kg of predicted body weight,20 FiO2 of 0.40, respiratory frequency of 12 breaths/min adjusted to obtain an end-tidal carbon dioxide between 30 and 35 mm Hg, inspiratory to expiratory ratio of 1:2, and no positive end-expiratory pressure (PEEP). After a 3-minute preoxygenation period using 100% oxygen, GA induction was performed using propofol and fentanyl or sufentanil. Tracheal intubation was facilitated with rocuronium. An arterial catheter was installed after the induction of GA. Adequate muscle relaxation (1 twitch or less on the train-of-four) was maintained with supplemental rocuronium administration as required. Neuromuscular blockade was reversed at the end of surgery with neostigmine and glycopyrrolate. Other aspects of anesthetic induction and maintenance were left at the discretion of the attending anesthesiologist. In case of arterial desaturation (defined as a peripheral oxygen saturation of <94%), FiO2 was increased to 1.00 and the attending anesthesiologist was free to alter ventilator settings at his or her discretion. Attempts were made to image the patient before and after any such interventions.

Lung Ultrasonography

Figure 1.
Figure 1.:
Each hemithorax is separated into 6 quadrants: anterior, lateral, and posterior zones (separated by the anterior and posterior axillary lines) each divided in upper and lower portions. AAL indicates anterior axillary line; PAL, posterior axillary line.

Lung ultrasonography was performed by 2 trained echographists (AM and MG, respectively, with 6 months and 5 years of experience in lung ultrasonography) using a LOGIQ e echograph and a convex array 2- to 5-MHz transducer (GE Healthcare). Images were obtained at 5 predefined time points: before GA induction (time point A), 5 minutes after GA induction (time point B), 5 minutes after insufflation of the pneumoperitoneum (time point C), 15 minutes after the arrival of patients in the recovery room (time point D), and immediately before the discharge from the recovery room (time point E). Care was taken to set the focal zone on the pleural line. No second harmonic imaging was used. As previously described,15,21 the thorax was divided into 12 quadrants (Figure 1): anterior, lateral, and posterior zones (separated by the anterior and posterior axillary lines) each divided in upper and lower portions for the right and left lung. Intercostal spaces of each of these areas were scanned and a cine-loop of the most pathologic area of each quadrant was saved to digital format for offline analysis.

Aeration Loss Scores

Table 1.
Table 1.:
Original and Modified Lung Ultrasound Scores

Aeration loss was assessed by calculating the LUS score.15 Each of the 12 quadrants was assigned a score of 0 to 3 according to a simple grading system (Table 1). The LUS score (0–36) was then calculated by adding up the 12 individual quadrant scores with higher scores indicating more severe aeration loss. Based on previous personal observations and existing literature,22,23 we also defined from the onset a modified LUS score. This modified LUS score was hypothesized to be more sensitive than the original LUS score. It retains all of the elements of the original LUS score but reintroduces the evaluation of small subpleural consolidations as a part of the grading system (Table 1; Supplemental Digital Content, Supplemental Appendix, http://links.lww.com/AA/B518). Although the original LUS score was considered the main analysis tool, all analyses were performed using both LUS scores. Cine-loops were analyzed independently by 2 investigators (AM and MG). Discordant readings were reconciled by consensus. Ultrasound diagnoses of pneumothorax and endobronchial intubation were made according to the previously published criteria.24,25

Data Collection

Demographic and anthropometric data were collected for each patient. At each study point under GA, vital signs were collected including arterial blood gas analysis, mechanical ventilation parameters (tidal volume, respiratory frequency, PEEP, FiO2), peak inspiratory pressure, end-inspiratory plateau pressure, and operating table angulation. In the recovery room, results of arterial blood gas analysis, estimated delivered FiO2, and bed angulation were noted at each ultrasonographic examination. Presence and severity of pain were assessed preoperatively and before recovery room discharge and were evaluated using an 11-point (0–10) numeric rating scale. Duration of GA, duration of pneumoperitoneum, pneumoperitoneum insufflation pressure, and length of recovery room stay were also noted.

Statistical Analysis

Given the pilot nature of this study, we postulated that a mean 3-point difference in the original LUS score calculated at each time point would be observed. Sample size was calculated by simulating repeated-measure 1-way analysis of variance (ANOVA) using an AR(1) correlation matrix. A standard deviation (SD) of 3 was postulated for each time point except at time point A where a SD of 1 was postulated. Multiple correlation values were tried for the covariance matrix. Given a power of 80%, a P < .05, and an incomplete data set in 15% of patients, we calculated that 30 patients would need to be enrolled.

Results are expressed as mean ± SD or median and interquartile range (25%–75%), as appropriate. Spearman’s correlation was used to assess the relationship between changes in both LUS scores and changes in the PaO2/FiO2 ratio. Given the unavailability of the arterial line preinduction, no correlation coefficients involving time point A could be calculated. Furthermore, decreased pulmonary shunt from pneumoperitoneum insufflation (with stable oxygenation)26 despite worsening atelectasis27 has been reported. Because of this, no correlation involving time point C could be anticipated. We therefore planned to calculate only the correlation coefficients between time points B and D. Because of modifications to their ventilatory parameters, patients experiencing episodes of arterial desaturation were excluded from secondary analyses unless otherwise specified. Evolution of the original and modified LUS scores was analyzed using a repeated-measure 1-way ANOVA. Sphericity was not assumed, and the Geisser-Greenhouse correction was applied. Residuals were tested for normality using the D’Agostino-Pearson test (P = .49 for ANOVA using the original LUS score, P = .15 for ANOVA using the modified LUS score). Tukey’s multiple-comparison test was used for pairwise comparison of the various time points. A P value <.05 was considered significant.

Because of the small sample size, secondary analyses, whether pre hoc or post hoc, were reported as 95% confidence intervals along with unadjusted P values. A Bonferroni-corrected significance level of 0.05/62 = 0.0008 was used. Thus, P values <.0008 were considered significant and P values >.05 were considered nonsignificant. All intermediate P values were considered exploratory. Anatomic distribution of aeration loss per quadrant for both LUS scores was analyzed using a repeated-measure 1-way ANOVA with pairwise comparison of time point A with the other time points. Spearman’s correlations were used to assess the effect of BMI, pneumoperitoneum duration, postoperative pain, age, and operating table angulation on changes in both LUS scores at various time points. Statistical analyses were performed using SAS/STAT software, version 9.2 (SAS Institute Inc, Cary, NC).

RESULTS

Between April and September 2013, 42 patients were assessed for study eligibility. Twelve patients had 1 or more exclusion criteria leaving 30 patients for enrollment (Figure 2). Patient baseline characteristics are summarized in Table 2. All cases were performed laparoscopically throughout with the exception of 2 intestinal resection surgeries that required a brief open part for anastomosis creation. Hemodynamic and ventilatory parameters recorded at the different time points can be found in Table 3. During GA, 5 patients desaturated and had their ventilatory parameters altered by the attending anesthesiologist.

Table 2.
Table 2.:
Patients Characteristics (N = 30)
Table 3.
Table 3.:
Hemodynamics, Ventilatory Parameters, and Gas Exchange (N = 30)
Figure 2.
Figure 2.:
Study inclusion/exclusion flow diagram. SpO2 indicates peripheral oxygen saturation.

Each lung ultrasound examination required an average of 10 (8.1–12.9) minutes to complete per time point. All examinations were successfully completed. A total of 1860 cine-loops were acquired during the study. Fourteen cine-loops (0.9%) were deemed of insufficient quality for analysis. For statistical purposes, these missing values were replaced by the mean quotation of the other quadrants from the same examination. A sensitivity analysis was performed, which showed comparable results regardless of the value substituted.

As shown in Figure 3, changes in both the original and the modified LUS scores between time points B and D were moderately correlated with changes in the PaO2/FiO2 ratio.

Figure 3.
Figure 3.:
Relationship between changes in the original lung ultrasound (LUS) (A) and the modified LUS (B) scores and changes in the PaO2/FiO2 ratio using Spearman correlation coefficients. FiO2 indicates inspired oxygen fraction; PaO2, arterial partial pressure of oxygen.

Mean original LUS and modified LUS scores at baseline (time point A) were 1.41 ± 0.35 (range 0–7) and 2.11 ± 0.41 (range 0–7), respectively (n = 30). General anesthesia induction caused a significant increase in both the original (P = .0057) and the modified (P = .0002) LUS scores (Figure 4). This increase persisted throughout the study period. Pneumoperitoneum insufflation led to an additional increase in both LUS scores. However, this aeration loss was only statistically significant when assessed using the modified LUS score (P = .015). In a post hoc analysis, when analyzed per quadrant, the inferolateral and both posterior quadrants significantly deteriorated from baseline as reflected by increasing original and modified LUS scores (Figure 5). The appearance and evolution of small subpleural consolidations followed a similar trend (Supplemental Digital Content 1, Supplemental Appendix, http://links.lww.com/AA/B518). The temporal evolution of aeration in the left inferoposterior quadrant of a sample patient can be seen in Figure 6.

Figure 4.
Figure 4.:
Temporal evolution of the original lung ultrasound (LUS) and the modified LUS scores. Time points: A = before general anesthesia induction, B = 5 min after general anesthesia induction, C = 5 min after insufflation of the pneumoperitoneum, D = 15 min after the arrival of patients in the recovery room, and E = before discharge from the recovery room.
Figure 5.
Figure 5.:
Temporal evolution of the original LUS (A) and the modified LUS (B) scores per quadrant. For clarity, left and right sides were analyzed together. LUS, lung ultrasound; time points: A = before general anesthesia induction, B = 5 min after general anesthesia induction, C = 5 min after insufflation of the pneumoperitoneum, D = 15 min after the patient’s arrival in the recovery room, and E = before discharge from the recovery room.
Figure 6.
Figure 6.:
Lung ultrasonographic changes seen in the inferoposterior quadrant of a sample patient. After induction of general anesthesia, the preoperative normally aerated quadrant (A) underwent atelectasis formation leading to the appearance of subpleural consolidations (B). Pneumoperitoneum insufflation caused further deaeration and the development of a lung consolidation (C). Arrival in the recovery room led to partial reaeration with the reappearance of subpleural consolidations (D). Before discharge from the recovery room, the quadrant had returned to a normal state of aeration (E). White arrows, subpleural consolidations; white arrowheads, consolidation.

No significant correlation was found between changes in both LUS scores between time points D and E and pain scores at time point E (Table 4). Post hoc analyses of changes in aeration scores between time points A and B failed to reveal a significant correlation in both LUS scores with patients’ age or BMI. For changes in aeration scores between time points C and D, the analysis suggests a possible correlation between changes in both the original and modified LUS scores and pneumoperitoneum duration and patients’ age. No significant correlation was found between changes in both LUS scores and patients’ BMI or operating room table angulation.

Table 4.
Table 4.:
Correlation Between the Evolution of the Original and Modified Lung Ultrasound Scores and Various Factors

Three complications were observed during lung ultrasonographic examinations. A right main-stem endobronchial intubation was detected after mobilizing a patient for positioning. This was associated with a brief episode of arterial desaturation that resolved shortly after the endotracheal tube was repositioned. The attending anesthesiologist then performed 4 recruitment maneuvers (30 cm H2O × 30 seconds) and applied a PEEP of 5 cm H2O. The following lung ultrasound examination showed moderate-to-severe loss of aeration of the patient’s left lower lobe that did not substantially improve until the patient left the recovery room (time point E). Small pneumothoraces were also discovered in the right inferoanterior quadrant of 2 patients at time point C, yielding an incidence in our population of 6.7%. In both cases, pneumothoraces had no discernible clinical repercussion and could not be imaged again 15 minutes after the arrival of patients in the recovery room (time point D). Finally, in 1 patient, lung ultrasonographic examination at time point D revealed a frank deterioration of both LUS scores. This patient’s lung ultrasonographic examination was characterized by the bilateral occurrence of regularly spaced B lines originating from a normal pleural line and worsening in a gravity-dependent fashion compatible with pulmonary edema. The patient, a 70-year-old woman, had no known cardiac history, normal renal function, had received 3 L of crystalloids intraoperatively, and no hypertensive events were documented. The patient remained asymptomatic and the lung ultrasound findings were unchanged at the time of recovery room discharge (time point E). The patient left the recovery room on room air but with the third worst PaO2/FiO2 ratio of the cohort. She was discharged to home on the first postoperative day.

Besides the patient with a right main-stem endobronchial intubation, 4 patients experienced an episode of desaturation: 2 postinduction of GA and 2 postpneumoperitoneum insufflation. These episodes prompted the attending anesthesiologists to perform recruitment maneuvers (2 patients), apply some PEEP (3 patients), and increase the tidal volume (3 patients). Because of the understandable uneasiness of attending anesthesiologists to delay treatment, we were unable to perform complete lung ultrasound examinations during these episodes. However, additional examinations performed posttreatment suggested a nonsignificant deterioration in the LUS scores compared with the preceding examination (original LUS score: 3.3 [0.5–7.5] to 5.0 [4.0–9.6], P = .19; modified LUS score: 5.5 [3.0–11.0] to 10.0 [7.0–13.7], P = .063).

DISCUSSION

Our pilot study demonstrates the feasibility of using lung ultrasonography during all phases of the perioperative period and its ability to both track perioperative atelectasis and detect respiratory complications. The evolution of perioperative aeration loss was moderately correlated with oxygenation changes.

Precise modeling of oxygenation during GA requires the simultaneous assessment of both pulmonary ventilation and perfusion, which likely explains the moderate correlation between changes in PaO2/FiO2 ratio and changes in both LUS scores observed in our study. Historically, the multiple inert gas elimination technique has been used in such studies.8,28 Compared to 2 studies performed in patients with acute respiratory distress syndrome (ARDS) and evaluating the effect of PEEP on ultrasonographically assessed lung aeration,21,29 our correlation was slightly weaker. This discrepancy is likely because of the very different states of pulmonary perfusion at time points B and D and comparatively stable pulmonary perfusion after PEEP increments in the 2 ARDS studies. Patients at time point B were in a head-down position under GA with the ensuing different hemodynamics and hypoxic pulmonary vasoconstriction states30 compared with patients at time point D who were awake and sitting at a 30° angle.

Computed tomography (CT)-measured lung aeration has been the gold standard for the study of perioperative atelectasis. However, cumulative radiation exposure31 and the need to transport the patient to or from the radiology department limit its use even in the research setting. Ideally suited to study perioperative aeration loss, lung ultrasonography allowed us to image our patients at multiple time points in the operating room even during ongoing surgery. The LUS score and its ancestor, the lung ultrasound reaeration score, have been shown to correlate both with changes in CT-measured lung aeration in patients with pneumonia32 and with changes in pressure–volume curve–assessed lung aeration in patients with ARDS.21,29 Intra- and interobserver agreement is good with reported κ coefficients of 0.75 and 0.70, respectively.32

As expected,13,33,34 induction of GA led to a marked decrease in lung aeration. We did not find any correlation between the degree of aeration loss and BMI. Previous studies have yielded conflicting results showing a strong,35 weak36, or absent correlation37 between CT-measured atelectasis area and BMI. We also observed reduced lung aeration after pneumoperitoneum insufflation. However, this result was only statistically significant when assessed using the modified LUS score suggesting better sensitivity. In support of this hypothesis, atelectasis resulting from pneumoperitoneum insufflation is less severe than the decrease in lung aeration associated with GA induction.16 At all times, aeration loss was predominant in the posterior and basal lung regions which is consistent with data from CT38 and from lung ultrasonography39 studies.

The present analysis suggests a possible correlation between age and changes in aeration between the postpneumoperitoneum period (time point C) and the arrival of patients in the recovery room (time point D). Advancing age has been shown to correlate with increasing perfusion to poorly ventilated lung units (low Va/Q).8 Airway closure, which also worsens with advancing age, is correlated to low Va/Q.40 When sufficient time is allowed, resorption atelectasis is thought to occur in lung units with a critically low Va/Q.41 When a 0.4 FiO2 is administered, more than 2 hours are necessary for susceptible poorly ventilated lung units to collapse.41 Mean duration of GA in our study was roughly 2.5 hours, suggesting resorption atelectasis as a possible etiologic factor to explain atelectasis. An association between atelectasis and anesthesia duration has been described in some42,43 but not in all38,44 studies. However, confounding the issue, our results also suggest that a longer duration of pneumoperitoneum was possibly associated with increased aeration loss. To our knowledge, the effect of the duration of pneumoperitoneum on the development of atelectasis has not been previously investigated. Whether our observed ongoing aeration loss is because of age-related resorption atelectasis or the influence of surgical factors is unclear and should be the subject of further research.

No correlation was detected between pain severity and changes in lung aeration during the patient’s stay in the recovery room. Although a trend toward improvement was observed, no significant change in aeration was noticed during this period. Few studies have quantified atelectasis in the immediate postoperative period,37,45–47 and none have studied its evolution in the immediate postextubation period. Our results are compatible with those of Lindberg et al46 that describe worsened atelectasis 2 hours postextubation compared with postinduction measurements.

The lack of diagnostic tools available to anesthesiologists in the operating room leads them to mostly treat hypoxemic episodes by increasing the FiO2.1 With 4% of patients receiving GA for noncardiac and nonthoracic surgery experiencing an episode of severe hypoxemia (PaO2/FiO2 <100 mm Hg), the ability of lung ultrasonography to diagnose various types of complications is another key finding of our study. In 2 patients, a clinically insignificant self-resolving capnothorax was detected at the most anterior portion of their right chest shortly after pneumoperitoneum insufflation. Although this 6% incidence is superior to the 1.6% reported in the literature,17 we believe this could be explained by our systematic search for this complication during its likely peak incidence using a more sensitive tool than a chest x-ray.48 Interestingly, a similar incidence of hepatic hydrothorax49 is found in cirrhotic patients possibly reflecting a similar mechanism, that is, right-sided diaphragmatic defects.50 A pneumothorax in a mechanically ventilated patient could result in a tension pneumothorax, a potentially life-threatening emergency. During ongoing surgery, ultrasonography may be the only reliable way of detecting a pneumothorax51,52 ensuring prompt treatment. By following the lateral position of the lung point, it is also possible to estimate the size and progression of a pneumothorax.53,54

Although a relatively rare occurrence, endobronchial intubation is responsible for one-fifth of episodes of desaturation during general anesthesia.55 Lung auscultation, the mainstay of endobronchial intubation diagnosis in the operating room, performs rather poorly,56 especially in the hands of less-experienced clinicians.57 Although never compared head-to-head, lung ultrasonography is an extremely sensitive and specific tool to detect endobronchial intubation58 that could prove superior to auscultation.

Finally, 1 of our patients developed pulmonary edema with rapid clinical improvement despite no specific treatment. The precise etiology could not be determined although unrecognized upper airway obstruction was suspected.

We present the results of a pilot study. As such, the small number of patients enrolled results in insufficient statistical power for some of our outcomes. Second, the lack of an ultrasound examination before GA emergence precludes a definitive assessment of intraoperative aeration loss because tracheal extubation may cause further atelectasis.47 Such a time point should be included in future studies of perioperative aeration loss. Third, because all our patients were receiving supplemental oxygen via nasal prongs in the recovery room, true inspired oxygen fraction could only be estimated and may have decreased the strength of the observed correlations. Fourth, despite its theoretical advantages over the original LUS score and the improved discrimination observed in our study, the modified LUS score will require validation before its use can be generalized (see Supplemental Digital Content 1, Supplemental Appendix, http://links.lww.com/AA/B518). Fifth, although our reported examination time (10 minutes) might seem long, others have reported similar durations.59,60 Unfortunately, because of this, we could not perform complete examinations of patients acutely desaturating. However, most authors report times of <3 to 5 minutes for a screening 8 zone examination,61–63 thus making it more practical in a “real-world” situation. This is different from our approach, because we meticulously scanned each intercostal space before recording a cine-loop of the most pathologic area. Finally, because anesthesiologists usually have access to patients’ chest, lung ultrasonography may be used in a variety of surgical settings. However, cardiothoracic surgeries and surgeries requiring the arms to be tucked alongside the body could be problematic. We circumvented this issue by using gutters to position the arms allowing room to maneuver the probe to the lateral and posterior aspects of our patients’ chests. In emergency situations, most diagnostic protocols for the evaluation of respiratory failure or hypoxemia rely on a simple anterior approach64 or a combined anterior and lateral one.65 When access to the chest is impossible, a transesophageal approach to lung ultrasonography has also been suggested.66

In conclusion, in a model of laparoscopic surgery-induced atelectasis, this pilot study demonstrates the feasibility of lung ultrasonography during the perioperative period. Lung ultrasonography also allows the tracking of perioperative atelectasis and facilitates the diagnosis of respiratory complications. The evolution of aeration loss correlates moderately with changes in oxygenation. Given the limited diagnostic means available to anesthesiologists during the intraoperative period, further research on the role of lung ultrasonography in the operating room should be encouraged. The ability of lung ultrasonography to “monitor the lung” of ventilated patient67 could allow better interpretation of 2 recently published randomized controlled trials exploring the effect of intraoperative mechanical ventilation parameters on postoperative pulmonary complications.68,69

ACKNOWLEDGMENTS

The authors thank Ms. Monique Ruel, RN, for her valuable assistance and dedication, M. Martin Ladouceur, PhD, for statistical advice, and Jean-François Hardy, MD, for his help in reviewing this manuscript.

DISCLOSURES

Name: Audrey Monastesse, MD.

Contribution: This author helped design the study, conduct the study, analyze the data, and write the manuscript.

Conflicts of Interest: Audrey Monastesse reported no conflicts of interest.

Name: Francois Girard, MD.

Contribution: This author helped design the study and write the manuscript.

Conflicts of Interest: Francois Girard reported no conflicts of interest.

Name: Nathalie Massicotte, MD.

Contribution: This author helped design the study and write the manuscript.

Conflicts of Interest: Nathalie Massicotte reported no conflicts of interest.

Name: Carl Chartrand-Lefebvre, MD.

Contribution: This author helped design the study and write the manuscript.

Conflicts of Interest: Carl Chartrand-Lefebvre reported no conflicts of interest.

Name: Martin Girard, MD.

Contribution: This author helped design the study, conduct the study, analyze the data, and write the manuscript.

Conflicts of Interest: Martin Girard consulted for GE Healthcare and was awarded an equipment grant from GE Healthcare in July 2015.

This manuscript was handled by: Maxime Cannesson, MD, PhD.

REFERENCES

1. Blum JM, Fetterman DM, Park PK, Morris M, Rosenberg AL. A description of intraoperative ventilator management and ventilation strategies in hypoxic patients. Anesth Analg. 2010;110:16161622.
2. Hayden GE, Wrenn KW. Chest radiograph vs. computed tomography scan in the evaluation for pneumonia. J Emerg Med. 2009;36:266270.
3. Schwebel C, Clec’h C, Magne S, et al.; OUTCOMEREA Study Group. Safety of intrahospital transport in ventilated critically ill patients: a multicenter cohort study*. Crit Care Med. 2013;41:19191928.
4. Volpicelli G, Elbarbary M, Blaivas M, et al.; International Liaison Committee on Lung Ultrasound (ILC-LUS) for International Consensus Conference on Lung Ultrasound (ICC-LUS). International evidence-based recommendations for point-of-care lung ultrasound. Intensive Care Med. 2012;38:577591.
5. Alrajhi K, Woo MY, Vaillancourt C. Test characteristics of ultrasonography for the detection of pneumothorax: a systematic review and meta-analysis. Chest. 2012;141:703708.
6. Chavez MA, Shams N, Ellington LE, et al. Lung ultrasound for the diagnosis of pneumonia in adults: a systematic review and meta-analysis. Respir Res. 2014;15:50.
7. Pivetta E, Goffi A, Lupia E, et al.; SIMEU Group for Lung Ultrasound in the Emergency Department in Piedmont. Lung ultrasound-implemented diagnosis of acute decompensated heart failure in the ED: a SIMEU multicenter study. Chest. 2015;148:202210.
8. Gunnarsson L, Tokics L, Gustavsson H, Hedenstierna G. Influence of age on atelectasis formation and gas exchange impairment during general anaesthesia. Br J Anaesth. 1991;66:423432.
9. Hedenstierna G, Edmark L. The effects of anesthesia and muscle paralysis on the respiratory system. Intensive Care Med. 2005;31:13271335.
10. Lawrence VA, Hilsenbeck SG, Mulrow CD, Dhanda R, Sapp J, Page CP. Incidence and hospital stay for cardiac and pulmonary complications after abdominal surgery. J Gen Intern Med. 1995;10:671678.
11. Smetana GW, Lawrence VA, Cornell JE; American College of Physicians. Preoperative pulmonary risk stratification for noncardiothoracic surgery: systematic review for the American College of Physicians. Ann Intern Med. 2006;144:581595.
12. van Kaam AH, Lachmann RA, Herting E, et al. Reducing atelectasis attenuates bacterial growth and translocation in experimental pneumonia. Am J Respir Crit Care Med. 2004;169:10461053.
13. Duggan M, Kavanagh BP. Pulmonary atelectasis: a pathogenic perioperative entity. Anesthesiology. 2005;102:838854.
14. Futier E, Marret E, Jaber S. Perioperative positive pressure ventilation: an integrated approach to improve pulmonary care. Anesthesiology. 2014;121:400408.
15. Soummer A, Perbet S, Brisson H, et al.; Lung Ultrasound Study Group. Ultrasound assessment of lung aeration loss during a successful weaning trial predicts postextubation distress*. Crit Care Med. 2012;40:20642072.
16. Andersson LE, Bååth M, Thörne A, Aspelin P, Odeberg-Wernerman S. Effect of carbon dioxide pneumoperitoneum on development of atelectasis during anesthesia, examined by spiral computed tomography. Anesthesiology. 2005;102:293299.
17. Murdock CM, Wolff AJ, Van Geem T. Risk factors for hypercarbia, subcutaneous emphysema, pneumothorax, and pneumomediastinum during laparoscopy. Obstet Gynecol. 2000;95:704709.
18. Inada T, Uesugi F, Kawachi S, Takubo K. Changes in tracheal tube position during laparoscopic cholecystectomy. Anaesthesia. 1996;51:823826.
19. Scheer B, Perel A, Pfeiffer UJ. Clinical review: complications and risk factors of peripheral arterial catheters used for haemodynamic monitoring in anaesthesia and intensive care medicine. Crit Care. 2002;6:199204.
20. Ventilation with lower tidal volumes as compared with traditional tidal volumes for acute lung injury and the acute respiratory distress syndrome. The Acute Respiratory Distress Syndrome Network. N Engl J Med. 2000;342:13011308.
21. Bouhemad B, Brisson H, Le-Guen M, Arbelot C, Lu Q, Rouby JJ. Bedside ultrasound assessment of positive end-expiratory pressure-induced lung recruitment. Am J Respir Crit Care Med. 2011;183:341347.
22. Rode B, Vučić M, Siranović M, et al. Positive end-expiratory pressure lung recruitment: comparison between lower inflection point and ultrasound assessment. Wien Klin Wochenschr. 2012;124:842847.
23. Soldati G, Inchingolo R, Smargiassi A, et al. Ex vivo lung sonography: morphologic-ultrasound relationship. Ultrasound Med Biol. 2012;38:11691179.
24. Turner JP, Dankoff J. Thoracic ultrasound. Emerg Med Clin North Am. 2012;30:451473ix.
25. Sim SS, Lien WC, Chou HC, et al. Ultrasonographic lung sliding sign in confirming proper endotracheal intubation during emergency intubation. Resuscitation. 2012;83:307312.
26. Andersson L, Lagerstrand L, Thörne A, Sollevi A, Brodin LA, Odeberg-Wernerman S. Effect of CO(2) pneumoperitoneum on ventilation-perfusion relationships during laparoscopic cholecystectomy. Acta Anaesthesiol Scand. 2002;46:552560.
27. Futier E, Constantin JM, Pelosi P, et al. Intraoperative recruitment maneuver reverses detrimental pneumoperitoneum-induced respiratory effects in healthy weight and obese patients undergoing laparoscopy. Anesthesiology. 2010;113:13101319.
28. Dueck R, Young I, Clausen J, Wagner PD. Altered distribution of pulmonary ventilation and blood flow following induction of inhalation anesthesia. Anesthesiology. 1980;52:113125.
29. Shen P, Luo R, Gao Y, Wang J, Zhang M. Assessment of positive end-expiratory pressure induced lung volume change by ultrasound in mechanically ventilated patients. Zhonghua Jie He He Hu Xi Za Zhi. 2014;37:332336.
30. Lumb AB, Slinger P. Hypoxic pulmonary vasoconstriction: physiology and anesthetic implications. Anesthesiology. 2015;122:932946.
31. Brenner DJ, Hall EJ. Computed tomography—an increasing source of radiation exposure. N Engl J Med. 2007;357:22772284.
32. Bouhemad B, Liu ZH, Arbelot C, et al. Ultrasound assessment of antibiotic-induced pulmonary reaeration in ventilator-associated pneumonia. Crit Care Med. 2010;38:8492.
33. Brismar B, Hedenstierna G, Lundquist H, Strandberg A, Svensson L, Tokics L. Pulmonary densities during anesthesia with muscular relaxation—a proposal of atelectasis. Anesthesiology. 1985;62:422428.
34. Tokics L, Hedenstierna G, Strandberg A, Brismar B, Lundquist H. Lung collapse and gas exchange during general anesthesia: effects of spontaneous breathing, muscle paralysis, and positive end-expiratory pressure. Anesthesiology. 1987;66:157167.
35. Rothen HU, Sporre B, Engberg G, Wegenius G, Hedenstierna G. Re-expansion of atelectasis during general anaesthesia: a computed tomography study. Br J Anaesth. 1993;71:788795.
36. Strandberg A, Tokics L, Brismar B, Lundquist H, Hedenstierna G. Constitutional factors promoting development of atelectasis during anaesthesia. Acta Anaesthesiol Scand. 1987;31:2124.
37. Eichenberger A, Proietti S, Wicky S, et al. Morbid obesity and postoperative pulmonary atelectasis: an underestimated problem. Anesth Analg. 2002;95:17881792.
38. Reber A, Engberg G, Sporre B, et al. Volumetric analysis of aeration in the lungs during general anaesthesia. Br J Anaesth. 1996;76:760766.
39. Acosta CM, Maidana GA, Jacovitti D, et al. Accuracy of transthoracic lung ultrasound for diagnosing anesthesia-induced atelectasis in children. Anesthesiology. 2014;120:13701379.
40. Rothen HU, Sporre B, Engberg G, Wegenius G, Hedenstierna G. Airway closure, atelectasis and gas exchange during general anaesthesia. Br J Anaesth. 1998;81:681686.
41. Dantzker DR, Wagner PD, West JB. Instability of lung units with low Va/Q ratios during O2 breathing. J Appl Physiol. 1975;38:886895.
42. Gunnarsson L, Strandberg A, Brismar B, Tokics L, Lundquist H, Hedenstierna G. Atelectasis and gas exchange impairment during enflurane/nitrous oxide anaesthesia. Acta Anaesthesiol Scand. 1989;33:629637.
43. Rothen HU, Sporre B, Engberg G, Wegenius G, Reber A, Hedenstierna G. Prevention of atelectasis during general anaesthesia. Lancet. 1995;345:13871391.
44. Cai H, Gong H, Zhang L, Wang Y, Tian Y. Effect of low tidal volume ventilation on atelectasis in patients during general anesthesia: a computed tomographic scan. J Clin Anesth. 2007;19:125129.
45. Strandberg A, Tokics L, Brismar B, Lundquist H, Hedenstierna G. Atelectasis during anaesthesia and in the postoperative period. Acta Anaesthesiol Scand. 1986;30:154158.
46. Lindberg P, Gunnarsson L, Tokics L, et al. Atelectasis and lung function in the postoperative period. Acta Anaesthesiol Scand. 1992;36:546553.
47. Benoît Z, Wicky S, Fischer JF, et al. The effect of increased FIO(2) before tracheal extubation on postoperative atelectasis. Anesth Analg. 2002;95:17771781.
48. Soldati G, Testa A, Sher S, Pignataro G, La Sala M, Silveri NG. Occult traumatic pneumothorax: diagnostic accuracy of lung ultrasonography in the emergency department. Chest. 2008;133:204211.
49. Singh A, Bajwa A, Shujaat A. Evidence-based review of the management of hepatic hydrothorax. Respiration. 2013;86:155173.
50. Huang PM, Chang YL, Yang CY, Lee YC. The morphology of diaphragmatic defects in hepatic hydrothorax: thoracoscopic finding. J Thorac Cardiovasc Surg. 2005;130:141145.
51. Ueda K, Ahmed W, Ross AF. Intraoperative pneumothorax identified with transthoracic ultrasound. Anesthesiology. 2011;115:653655.
52. Jang DM, Seo HS, Park JH, Lee B, Song JG, Hwang GS. Rapid identification of spontaneously resolving capnothorax using bedside M-mode ultrasonography during laparoscopic surgery: the ‘lung point’ sign—two case reports. Korean J Anesthesiol. 2013;65:578582.
53. Volpicelli G, Boero E, Sverzellati N, et al. Semi-quantification of pneumothorax volume by lung ultrasound. Intensive Care Med. 2014;40:14601467.
54. Oveland NP, Lossius HM, Wemmelund K, Stokkeland PJ, Knudsen L, Sloth E. Using thoracic ultrasonography to accurately assess pneumothorax progression during positive pressure ventilation: a comparison with CT scanning. Chest. 2013;143:415422.
55. Szekely SM, Runciman WB, Webb RK, Ludbrook GL. Crisis management during anaesthesia: desaturation. Qual Saf Health Care. 2005;14:e6.
56. Brunel W, Coleman DL, Schwartz DE, Peper E, Cohen NH. Assessment of routine chest roentgenograms and the physical examination to confirm endotracheal tube position. Chest. 1989;96:10431045.
57. Sitzwohl C, Langheinrich A, Schober A, et al. Endobronchial intubation detected by insertion depth of endotracheal tube, bilateral auscultation, or observation of chest movements: randomised trial. BMJ. 2010;341:c5943.
58. Lichtenstein DA, Lascols N, Prin S, Mezière G. The ‘lung pulse’: an early ultrasound sign of complete atelectasis. Intensive Care Med. 2003;29:21872192.
59. Unluer EE, Karagoz A, Senturk, GO, Karaman M, Olow K, Bayata S. Bedside lung ultrasonography for diagnosis of pneumonia. Hong Kong J Emerg Med. 2013;21:98104.
60. Testa A, Soldati G, Copetti R, Giannuzzi R, Portale G, Gentiloni-Silveri N. Early recognition of the 2009 pandemic influenza A (H1N1) pneumonia by chest ultrasound. Crit Care. 2012;16:R30.
61. Cibinel GA, Casoli G, Elia F, et al. Diagnostic accuracy and reproducibility of pleural and lung ultrasound in discriminating cardiogenic causes of acute dyspnea in the emergency department. Intern Emerg Med. 2012;7:6570.
62. Volpicelli G, Mussa A, Garofalo G, et al. Bedside lung ultrasound in the assessment of alveolar-interstitial syndrome. Am J Emerg Med. 2006;24:689696.
63. Liteplo AS, Marill KA, Villen T, et al. Emergency thoracic ultrasound in the differentiation of the etiology of shortness of breath (ETUDES): sonographic B-lines and N-terminal pro-brain-type natriuretic peptide in diagnosing congestive heart failure. Acad Emerg Med. 2009;16:201210.
64. Lichtenstein DA, Mezière GA. Relevance of lung ultrasound in the diagnosis of acute respiratory failure: the BLUE protocol. Chest. 2008;134:117125.
65. Silva S, Biendel C, Ruiz J, et al. Usefulness of cardiothoracic chest ultrasound in the management of acute respiratory failure in critical care practice. Chest. 2013;144:859865.
66. Rehfeldt KH, Bruggink SM, Pulido JN. Transesophageal echocardiographic imaging of ultrasound lung rockets. Anesthesiology. 2014;121:1335.
67. Bouhemad B, Mongodi S, Via G, Rouquette I. Ultrasound for ‘lung monitoring’ of ventilated patients. Anesthesiology. 2015;122:437447.
68. Futier E, Constantin JM, Paugam-Burtz C, et al.; IMPROVE Study Group. A trial of intraoperative low-tidal-volume ventilation in abdominal surgery. N Engl J Med. 2013;369:428437.
69. PROVE Network Investigators for the Clinical Trial Network of the European Society of AnaesthesiologyHemmes SN, Gama de Abreu M, Pelosi P, Schultz MJ. PROVE Network Investigators for the Clinical Trial Network of the European Society of Anaesthesiology, High versus low positive end-expiratory pressure during general anaesthesia for open abdominal surgery (PROVHILO trial): a multicentre randomised controlled trial. Lancet. 2014;384:495503.

Supplemental Digital Content

Copyright © 2016 International Anesthesia Research Society