Assessment of changes in lung aeration and diaphragmatic function using ultrasonography in laparoscopic abdominal surgery: a prospective observational study
Article information
Abstract
Background
A few studies investigating the perioperative use of lung ultrasound (LUS) have shown loss of lung aeration with decline in diaphragmatic function after general anesthesia. We aimed to measure changes in lung aeration and diaphragmatic functions using LUS in patients undergoing elective laparoscopic cholecystectomy.
Methods
Forty patients of American Society of Anesthesiologists I/II undergoing elective laparoscopic cholecystectomy under general anesthesia were enrolled. For all patients, LUS examination was performed at 5 time points: preoperative room, after intubation, after deflation of pneumoperitoneum, 30 min after extubation, and 24 h post-extubation. The aeration loss was assessed using the modified LUS score. The diaphragmatic excursion was also evaluated preoperatively, and at 30 min and 24 h post-extubation.
Results
A progressive increase in modified LUS score was seen after intubation, after deflation of pneumoperitoneum, 30 min postoperative, after extubation and 24 h post-extubation at postoperative anesthesia care unit (PACU) as compared to preoperative room (P < 0.0001). The maximum modified LUS score was observed postoperatively after 30 min: 8 (5, 10) and 24 h post-extubation in PACU: 8 (4.25, 11.0). No significant change in the diaphragmatic excursion or respiratory complications was observed.
Conclusions
Our study found a progressive loss of lung aeration after the induction of general anesthesia in laparoscopic cholecystectomy, extending up to the 24-h perioperative period. However, diaphragmatic excursion remained unchanged. The study also suggests that LUS is a valuable tool for detecting perioperative atelectasis and quantifying the aeration loss.
INTRODUCTION
During laparoscopic surgery, the creation of a pneumoperitoneum causes a cephalic displacement of the diaphragm, which can lead to decreased pulmonary compliance and functional residual capacity [1,2]. Maintaining a steep Trendelenburg position for extended periods while the pneumoperitoneum is in place may further limit diaphragmatic movement. Some studies have reported a significant decline in postoperative diaphragmatic inspiratory amplitude compared to preoperative values [3]. In anesthetized patients, micro-atelectasis frequently develops in the dependent lung zones, resulting in pulmonary shunting of blood, reduced lung compliance, and intraoperative hypoxemia [4]. The negative effects of atelectasis can persist into the postoperative period, potentially delaying patient recovery [5].
Recent studies have investigated the impact of pneumoperitoneum during laparoscopic surgery on lung aeration and diaphragmatic function [6,7]. These studies reported a significant decrease in lung aeration and diaphragmatic movement in the postoperative period [8]. Additionally, they found lung ultrasound (LUS) to be a valuable tool for diagnosing respiratory complications, such as pleural effusion, pneumonia, atelectasis, and endobronchial intubation during the perioperative period [9]. In light of these findings, we aimed to measure changes in lung aeration and diaphragmatic function using LUS in patients undergoing elective laparoscopic cholecystectomy under general anesthesia.
MATERIALS AND METHODS
This prospective observational study was conducted at a tertiary care teaching institute after obtaining approval from the Institutional Ethics Committee of Employees’ State Insurance Corporation Postgraduate Institute of Medical Sciences and Research (Reg No. ESIPGIMSR-IEC/2023003). All procedures involving human participants were performed in accordance with the ethical standards of the institutional and/or national research committee and with the Helsinki Declaration and its later amendments or comparable ethical standards. Trial registered at Clinical Trial Registry India (CTRI/2023/08/056843). A total of 40 adult patients, classified as American Society of Anesthesiologists (ASA) grade I/II and aged 18 to 65 years, were enrolled in the study from April 2023 to December 2023, all undergoing elective laparoscopic cholecystectomy under general anesthesia. Patients with obesity (body mass index > 35 kg/m2), pregnant patients, and those with a history of intrathoracic procedures, including the placement of chest tubes, were excluded from the study.
All participants were enrolled by the principal investigator (DS) following a thorough pre-anesthetic evaluation and obtaining their written informed consent. To minimize inter-observer variability, the assessment was done by one of the two designated anesthesiology residents (SP and GG). For each patient, the clip recordings were recorded and reassessed for modified LUS scoring, verified by a professor of anesthesiology (DS) having formal training and certification in lung and cardiac ultrasonography (USG).
On the morning of surgery, after wheeling the patient into the preoperative patient holding area, LUS was performed using the curvilinear (2–5 MHz) transducer probe of (SonoSite M-Turbo, FUJIFILM Sonosite) ultrasound machine. For the scan, each hemithorax was divided into 6 quadrants (Fig. 1), and a 6-second clip of each quadrant was recorded. The aeration loss was assessed using the modified LUS score (Table 1) [10], and the total modified LUS score (0–36) was calculated by adding up 12 individual quadrant scores.
Hemithorax is divided by two horizontal lines and one vertical line. AAL: anterior axillary line, PAL: posterior axillary line.
For each patient, the modified LUS score was calculated at the 5 time points: preoperative room, after intubation, after deflation of pneumoperitoneum, at 30 min after extubation, and 24 h post-extubation in postoperative anesthesia care unit (PACU). The diaphragmatic excursion was assessed at the preoperative room, at 30 min after extubation, and 24 h post-extubation in PACU in spontaneously breathing patients using M-mode ultrasound with the curvilinear probe placed on the right costal margin between the anterior and posterior axillary line [11]. The excursion was recorded as the maximum height of inspiration from the baseline of the graph, and the mean of three consecutive measurements was taken as the final value (Fig. 2).
General anesthesia was induced with propofol 2 mg/kg, fentanyl 2 mcg/kg, and vecuronium 0.1 mg/kg IV, and the trachea was intubated with an appropriate-size endotracheal tube. Each patient was ventilated using volume-controlled mode with a tidal volume of 6–8 ml/kg/min, a respiratory rate of 12–16/min, and to maintain end-tidal CO2 between 35 to 45 mmHg and without application of positive end-expiratory pressure (PEEP). Anesthesia was maintained with inhalation agents 50% O2/N2O, sevoflurane 1–2% and additional top-ups of fentanyl and vecuronium bromide as per train of four (TOF) ratio monitoring using a neuromuscular monitor (Dräger Atlan A350, Dräger). The TOF monitoring was set at a 10-min interval and the neuromuscular blockade was maintained at a TOF count of < 2 twitches. The top-up dose of vecuronium bromide (1 mg) was given on the appearance of the third twitch of TOF. In case of any desaturation (SpO2 < 92%) or respiratory complication, the attending anesthesiologist was free to alter ventilator settings at his discretion.
Attempts were made to image the patient before and after any such interventions. Each patient underwent laparoscopic surgery in a 20–30° Trendelenburg position. The pneumoperitoneum was established and maintained at a pressure of 12 mmHg with an insufflation flow rate of 3–4 L/min, in accordance with institutional protocols. During surgery, peak pressure, plateau pressure, dynamic compliance, and total duration of pneumoperitoneum were recorded. After completion of surgery, the neuromuscular blockage was reversed when the TOF count was > 2, and the trachea was extubated after the TOF ratio was > 0.9. The patient was shifted to PACU, where they were monitored for the next 24 h before being shifted to the ward.
Statistical analysis
The sample size has been calculated based on a previous study by Xie et al. [12] on the assessment of atelectasis and diaphragmatic excursion during video-assisted thoracic surgery. After induction of general anesthesia, the LUS score in ventilated non-operated lungs changed significantly from 0.15 ± 0.58 to 0.78 ± 1.02, with a maximum score of 6.73 ± 2.67 at the end of surgery. The sample size of 28 patients was calculated to detect a statistically significant change in LUS score with an effect size of 0.4 at an alpha error of 0.05 and a power of 90%. To compensate for any dropouts, we recruited 40 patients for the study.
The IBM SPSS Statistics ver. 25.0 software, was used for the statistical analysis (IBM Co.). Numbers and percentages were used to represent the categorical variables, while mean ± SD and median (1Q, 3Q) were used to represent the quantitative data. Data was assessed for normality using the Shapiro–Wilk test. In non-normally distributed data, we employed the Mann–Whitney test. Comparisons across temporal follow-up were made using the Wilcoxon signed rank test and the paired t-test. P values below 0.05 were considered statistically significant.
RESULTS
Out of 40 patients enrolled in the study, 2 patients were excluded due to the conversion of laparoscopic surgery to open surgery. During the study, modified LUS score and diaphragm excursion were successfully measured at all the specified time points for the 38 patients, and their clips were recorded. The demographic data of the patients enrolled in the study are shown in Table 2. Table 3 shows the ventilator parameters for the patient enrolled in the study; a statistically significant increase in peak airway pressure and decline in dynamic compliance were seen after deflation of pneumoperitoneum compared to the values after intubation.
After induction of general anesthesia and creation of pneumoperitoneum, a progressive increase in modified LUS score was seen after intubation, after deflation of pneumoperitoneum, 30 min after extubation and 24 h post-extubation compared to the baseline Preoperatively; the difference is statistically highly significant, P < 0.0001 (Fig. 3). The maximum modified LUS score was observed postoperatively at 30 min after extubation: 8 (5, 10) and 24 h post-extubation: 8 (4.25, 11.0). Also, the comparison of modified LUS scores between the two consecutive time points showed a statistically significant increase in the modified LUS (P < 0.05) (Fig. 3).
Temporal evolution of modified lung ultrasound score. Pre-Op, Af-Int, Def-Pneumo, 30 min Post-Op, and 24 h Post-Op. Af-Int vs. Pre-Op (P < 0.0001), Def-Pneumo vs. Pre-Op (P < 0.0001), 30 min Post-Op vs. Pre-Op (P < 0.0001), 24 h Post-Op vs. Pre-Op (P < 0.0001), Def-Pneumo vs. Af-Int (P < 0.0001), 30 min Post-Op vs. Def-Pneumo (P = 0.008). All P values < 0.05 were considered statistically significant. Pre-Op: preoperative, Af-Int: after intubation, Def-Pneumo: after deflation of pneumoperitoneum, Post-Op: postoperative.
The baseline preoperative modified LUS score for all the lung quadrants in the preoperative room was 0 (0, 1). Statistically significant increases in lung scores were observed in quadrants L2 to L6 and R2 to R6 at 24 h postoperative as compared to preoperative room (P < 0.05), which shows postoperative lung aeration loss. The highest distribution of aeration loss was seen in the quadrant 6 (left: 2 [0, 3], right: 1 [1, 3]; P<0.0001), followed by quadrant 5 (left: 1 [0, 3], right: 1 [0, 3]; P < 0.0001) and 4 (left: 1 [0, 3]; P < 0.0001, right: 0 [0, 2]; P < 0.005). No significant change was seen in the diaphragmatic excursion at 30 min postoperatively in PACU (1.28 + 0.38 cm) and 24 h postoperatively (1.33 + 0.43 cm) as compared to the preoperative room (1.39 + 0.49 cm). Also, we did not observe any respiratory compromise or complications in any patient during surgery or 24 h before discharge from PACU.
DISCUSSION
Our study aimed to measure the changes in lung aeration and diaphragmatic excursion after laparoscopic cholecystectomy abdominal surgery. The findings of our study show that there is a progressive loss of lung aeration after general anesthesia and pneumoperitoneum in laparoscopic abdominal surgery. The maximum modified LUS was observed postoperatively at 30 min after extubation: 8 (5, 10) and at 24 h after extubation in PACU: 8 (4.25, 11.0). The decline in lung aeration persisted for 24 h in the postoperative period.
Quadrant-wise distribution of modified LUS showed that maximum lung aeration loss was in the posterior and lateral quadrants, i.e., 6, 5, and 4, whereas the anterior quadrants 1, 2, and 3 were relatively spared of the aeration loss. The highest modified LUS score was seen in the left side quadrant 6, which remains the most dependent region of the lung after positioning in laparoscopic cholecystectomy surgery. However, aeration loss did not result in any clinical respiratory complications, desaturation, or prolonged postoperative oxygen requirements. Furthermore, we saw no reduction in diaphragmatic excursion following surgery.
In 2017, Monastesse et al. [13] described the modified LUS in a pilot feasibility study they conducted on the use of LUS for the assessment of perioperative lung atelectasis. The modified LUS score incorporated the LUS finding of subpleural consolidations in the original LUS score. Their study found the evolution of aeration loss to be moderately correlated with the changes in arterial oxygenation. The researchers designated lung USG as a “monitor of the lung” that aided in the early detection of perioperative clinical complications such as pneumothorax, endobronchial intubation, and sub-clinical pulmonary edema in anesthetized patients. The present study also supports the feasibility of LUS in the perioperative period to assess atelectasis and diaphragmatic movement. Later, in 2020, Xie et al. [12] studied the feasibility of perioperative LUS in patients undergoing video-assisted thoracic surgery. They noted a significant aeration loss throughout the surgery, starting from induction of general anesthesia with a 15% incidence of postoperative atelectasis. Also, they found a negative correlation of aeration loss with diaphragmatic excursion. In contrast, Kim et al. [14] found that diaphragmatic excursion and lung compliance significantly decreased after major laparoscopic pelvic surgery.
Szabó et al. [15] investigated the diagnostic utility of modified LUS in predicting postoperative pulmonary complications (PPCs) in patients undergoing elective major abdominal surgery under general anesthesia. They found that the postoperative LUS at 1 h did not correlate with PPC, whereas the modified LUS at 24 h was a significant predictor of PPCs with an odds ratio of 2.641. The study indicated that a modified LUS score value of 5 or more at postoperative 24 h has high sensitivity (0.944) and reasonable specificity (0.776).
However, in Zieleskiewicz et al. [16]’s study on patients undergoing major abdominal surgery, the cut-off value for LUS score was higher; patients with a LUS score of 12 or more were at greater risk of developing PPC (12 [7, 18] vs. 8 [4, 12]; P < 0.001). A recent multi-centric study concluded that the LUS score on postoperative Day 1 is a predictor of PPC after major abdominal surgery. A cut- off value of LUS score of 12 had a sensitivity of 0.54, specificity of 0.77, and negative predictive value of 0.74 [17]. In our study, the postoperative median modified LUS score was 8; however, no PPC was observed.
Our study provides evidence of the occurrence of micro-atelectatic changes and aeration loss, notably in the dependent lung quadrants, even after short-duration laparoscopic procedures such as laparoscopic cholecystectomy, and confirms the findings of earlier studies on using modified LUS for assessment of aeration loss. However, we did not observe any significant change in diaphragmatic functions, which is contrary to the findings of an earlier study by Ayoub et al. [18] on the assessment of diaphragmatic movement after cholecystectomy surgery. This study included subjects undergoing either open or laparoscopic cholecystectomy and had a modest sample size of 14 patients. The preservation of diaphragmatic function in our study could be due to the minimally invasive laparoscopic procedure, short duration of surgery (< 2 h), use of intermediate-acting neuromuscular relaxant, adequate ostoperative use of neuromuscular reversal, and adequate pain relief postoperatively.
Our study has a few limitations. Firstly, we could not conduct follow-up assessments with ultrasound after 24 postoperative h to look for the resolution of micro-atelectasis due to the discharge of most of the patients from the hospital on the first postoperative day. Secondly, we did not confirm the presence of micro-atelectasis with computed tomography imaging, as the patients were clinically asymptomatic and had no respiratory compromise. Also, we did not perform arterial blood gas analysis and spirometry for the patients, which could have provided a more comprehensive physiological correlation with LUS findings. However, these were not included in the study protocol due to ethical committee concerns regarding patient comfort and the invasiveness of additional non-routine investigations in ASA I and II patients undergoing laparoscopic surgery. We excluded sick patients, including ASA III/IV and patients undergoing any other prolonged laparoscopic procedure, which could explain the finding of a modified LUS score lower than 12 without any PPC. An earlier study marked modified LUS > 12 as a cut-off value for developing PPC [18].
To conclude, our study shows that during laparoscopic cholecystectomy surgery, there is a progressive loss of lung aeration after induction of general anesthesia to a 24-h postoperative period. However, diaphragmatic excursion remained unchanged. The study also indicates that LUS with a modified LUS score is a valuable tool for detecting perioperative atelectasis and quantifying the aeration loss, underscoring its application in perioperative periods.
Notes
FUNDING
None.
CONFLICTS OF INTEREST
No potential conflict of interest relevant to this article was reported.
DATA AVAILABILITY STATEMENT
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
AUTHOR CONTRIBUTIONS
Conceptualization: Divya Sethi. Data curation: Stuti Prajapati. Formal analysis: Garima Garg. Methodology: Divya Sethi, Stuti Prajapati, Garima Garg. Visualization: Divya Sethi, Stuti Prajapati, Garima Garg. Writing - original draft: Divya Sethi, Garima Garg. Writing - review & editing: Stuti Prajapati, Garima Garg. Investigation: Stuti Prajapati, Garima Garg. Resources: Stuti Prajapati, Garima Garg. Software: Garima Garg. Supervision: Divya Sethi. Validation: Divya Sethi.
