Startseite Medizin Impact of combined diaphragm-lung ultrasound assessment on postoperative respiratory function in patients under general anesthesia recovery
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Impact of combined diaphragm-lung ultrasound assessment on postoperative respiratory function in patients under general anesthesia recovery

  • Ping Zhang , Wei-hong Huang , Long-cheng Fan , Zhong-yu Liu und Shan-liang Guo ORCID logo EMAIL logo
Veröffentlicht/Copyright: 22. Dezember 2025

Abstract

Objectives

The study aims to evaluate whether the ultrasonographic assessment of diaphragm and lung function in postanaesthesia care unit (PACU) can improve postoperative respiratory function recovery in patients under general anesthesia recovery.

Methods

This study enrolled 130 participants scheduled for elective abdominal surgery with planned postoperative transfer to PACU. Participants were randomized to either the diaphragm-lung ultrasound-guided group (group DL) or standard resuscitation group without ultrasound guidance (group N). The group DL received diaphragm and lung ultrasonography at four predefined intervals and intervention based on the ultrasound results was performed. The primary outcomes were the incidence of hypoxemia (PaO2/FiO2≤300  mmHg) at discharge of PACU and the extubation time. The postoperative pulmonary complications (PPCs) within the first 7 days was measured as a key secondary outcome.

Results

Compared with the group N, the incidence of hypoxemia (p<0.01) and the extubation time (p<0.01) were significantly reduced in the group DL. There was no significant difference in the incidence of PPCs between the two groups (p>0.1).

Conclusions

Dynamic assessment of pulmonary and diaphragm function by ultrasound improved the recovery of respiratory function in patients but did not reduce the incidence of PPCs.

Introduction

General anesthesia rapidly reduces functional residual capacity by approximately 20 % and impairs respiratory muscle function, particularly diaphragmatic activity [1]. The incidence of postoperative pulmonary complications (PPCs) in major surgery ranges from 1 to 23 % [2]. Abdominal surgery further compromises respiratory function through tissue trauma, phrenic nerve inhibition, and pneumoperitoneum effects [3]. Weingarten et al. [4] demonstrated that even a single episode of respiratory depression in postanaesthesia care unit (PACU) was strongly associated with subsequent respiratory complications. Inadequate recovery of respiratory physiology can lead to severe hypoxemia-induced end-organ damage and even death [4], 5]. Thus, effective respiratory monitoring and accelerated functional recovery during anesthesia emergence are critical. In recent years, with the continuous popularization and promotion of bedside ultrasound technology, bedside ultrasound has been proved to be of great value in evaluating patients’ real-time status [6], [7], [8].

Lung ultrasound (LUS) has been validated for the diagnosis of atelectasis, pneumonia, pleural effusion and pneumothorax [8], [9], [10], [11], [12]. Chen et al. [8] showed high accuracy of LUS in diagnosing different aetiologies of postoperative hypoxia in the PACU with a high degree of sensitivity and specificity. Both diaphragmatic excursion and diaphragm thickening fraction (DTF) showed good diagnostic performance in predicting extubation outcomes [13]. Previous publications on LUS and diaphragm ultrasound were mostly from emergency departments and ICUs. There are still few related studies on the application of the combination of the two in postoperative anesthesia recovery period.

Therefore, this study evaluates whether combined diaphragm-lung ultrasound assessment guiding targeted interventions in PACU enhances respiratory recovery after general anesthesia.

Methods

Trial design

This prospective, patient-blinded, single-center randomized controlled trial was approved by the Ethics Committee of Jiangxi Provincial People’s Hospital (2022-037, 2022/8/15) and was registered at the Chinese Clinical Trial Registry (trial number: ChiCTR2200064548; Date of registration: 11/10/2022). We enrolled 135 patients, aged 18–85 years, ASA I-III, who underwent elective abdominal surgery in our hospital from October 2022 to February 2023 and were transferred to the PACU with the endotracheal tube postoperatively. Exclusion criteria included preexisting respiratory conditions (diaphragmatic dysfunction, pleural effusion, pneumothorax, mediastinal emphysema, interstitial lung disease, moderate to severe chronic obstructive pulmonary disease), cardiac impairment (NYHA classe ≥III), neuromuscular disorders and thoracic surgery history. Withdrawal criteria included failure to transfer to PACU as planned or postoperative pain/sedation issues (VAS >3 or Ramsay score >2 after extubation).

Patients were randomized to diaphragm-lung ultrasound-guided group (group DL) or standard resuscitation group without ultrasound guidance (group N) using a computer-generated sequence of random numbers. Allocation details were sealed in numbered envelopes. The group DL underwent pulmonary and diaphragmatic ultrasound assessments at four timepoints: admission in operating room (T0), admission in PACU (T1), 15 min after extubation (T2), and discharge of PACU (T3). The enrollment and allocation of participants are compiled in Figure 1.

Figure 1: 
Consort flow diagram.
Figure 1:

Consort flow diagram.

Anesthesia method

Standardized monitoring included three-lead electrocardiography, SpO2, blood pressure, and BIS was performed after patients entered the room. After a FiO2 60 % pre-oxygenation, general anesthesia was induced with standard doses of propofol, vecuronium bromide and sufentanil. Tracheal intubation was performed, followed by an anesthesia machine (Drager, Germany) for mechanical ventilation, using volume-controlled ventilation, tidal volume of 8 mL/kg, respiratory rate of 12–18 times/min, FiO2 40 %, positive end-expiratory pressure (PEEP) of 5–8 cmH2O and end-tidal CO2 (Philips IntelliVue MP, Philips Medizin Systeme, Germany) controlled between 35 and 45 mmHg. Maintenance of anesthesia used 1.0 MAC sevoflurane, remifentanil 0.1–0.5 ug⋅kg−1⋅h−1, propofol 4–6 mg⋅kg−1⋅h−1, intermittently gave vecuronium bromide 0.03 mg/kg, adjusting the dosage of drugs according to the depth of anesthesia, and the BIS was maintained at 40–60. During the operation, the fluctuation range of a mean arterial pressure (MAP) should not exceed 20 % of the base value. Vecuronium bromide was stopped about 40 min before the end of the operation. Sevoflurane was stopped about 10 min before the end of the operation. Remifentanil was stopped after the operation. In both group, recruitment maneuver was carried out by manual infation with 30 cmH2O airway pressure with FiO2 of 0.4 for 30s at the end of the operation [14].

All the patients were admitted to the PACU with tracheal intubation, and were placed at a head height of 30°. Patients in PACU were given neostigmine 0.02 mg/kg and atropine 10 μg/kg after spontaneous breathing occurs. Extubation was determined by the anesthesiologist in PACU when patients met the following criteria: responsive to verbal commands, return of spontaneous breathing with a tidal volume  ≥5 mL/kg, respiratory rate of 10–20 breaths/min, end-tidal CO2 <45 mmHg with a regular waveform, and SpO2 >95 %. After extubation, the VAS score and Ramsay sedation score were assessed, and oxygen was inhaled through a nasal oxygen tube at an oxygen flow rate of 5 L/min. When the patient’s Steward score is ≥6 points, the patient can be sent out of the PACU and transferred to the ward. At T3 (PACU discharge), arterial blood samples were obtained from all patients. The PaO2/FiO2 ratio was calculated from these analyses, with values ≤300 mmHg defining hypoxemia [15].

LUS assessment and intervention

The patient was examined for LUS by 12-zone approach. Each half of the chest is divided into front, outside, and rear areas by the anterior axillary line and the posterior axillary line, and divided into upper and lower areas through the nipple level. There are 6 areas in total and 12 areas in bilateral lungs [16]. A fixed lung sonographer scans and scores each area (0–3 points), and adopts the modified scoring standard of Monastesse et al. [17]: a (0 point): normal aeration-lung sliding sign with A lines or ≤2 separate B-lines; b (1 point): Mild aeration defect – multiple distinct B lines (fused B lines less than 50 % of intercostal space on vertical scan), one or more small pleura inferior consolidation is separated by normal pleural line; c (2 points): Moderate lung aeration defect-multiple merged B-lines (fused B lines are more than 50 % of the intercostal space on vertical scan), multiple small subpleural consolidations are separated by thickened or irregular pleural lines; d (3 points): white lung or lung consolidation-atelectasis: air bronchus sign, debris sign, tissue-like sign. The LUS scores of the 12 zones were pooled and analyzed to calculate LUS score (0–36 points).

The higher the score, the more severe the ventilation loss, except for pneumothorax. At T1 (PACU admission) – T2 (15 min post-extubation), lung ultrasound showed more than 15 B-lines in the anterior chest region, suggesting that extravascular lung water increased and furosemide 20 mg was given [12]. At T1, LUS score >2 points in a single area or >10 points in total, ultrasound-guided lung recruitment was performed.

Lung Recruitment Method: The ultrasound probe was placed in the most severe area of atelectasis, maintaining the airway pressure at 15 cmH2O, increasing PEEP by 5 cmH2O each time and maintaining it for 5 s after each increase, with a maximum of 40 cmH2O with FiO2 of 0.4 until the lung consolidation disappears under ultrasound. Besides, the pressure at that time was maintained for 30 s, and then decreased to maintain the previous ventilator setting [14], 18]. If MAP or heart rate changes >15 %, stop the recruitment maneuver.

Diaphragm ultrasound assessment and intervention

The patient was placed in a supine position with a head height of 30°, and a 10–15 MHz high-frequency linear array probe was placed perpendicular to the long axis of the ribs in the 8–10 intercostal space between the anterior axillary line and the midaxillary line, and 0.5–2 cm above the costophrenic sinus. Diaphragm thickness was assessed by the same sonographer. In B mode, find the diaphragm. In M mode, measure the end-inspiration and end-expiration diaphragm thickness, and calculate the DTF=(end-inspiration thickness – end-expiration thickness)/end-expiration thickness × 100 %, DTF is the average of 3 breaths. To ensure the reproducibility of the ultrasound examination, the position of the probe was carefully marked and the ultrasound examination of the diaphragm was performed at the same location in the PACU. Diaphragm ultrasonic images of one representative patient at different time points are displayed in Figure 2. DTF less than 30 % is a measure of ultrasonographic diaphragmatic dysfunction [19]. When the ultrasound evaluation of the diaphragm at T2 (15 min post-extubation) indicates diaphragmatic dysfunction, the patient will be given additional neostigmine 30 μg/kg plus atropine 10 μg/kg, and the maximum dose of neostigmine is 5 mg/d [20].

Figure 2: 
The left figure shows the end-inspiratory and end-expiration diaphragm thickening at T0 with the DTF reaching 50 %. The right figure shows the end-inspiratory and end-expiration diaphragm thickening of the same patient at T2, and the DTF is 23.5 %, suggesting that the patient’s diaphragm function is incompetent at this time point.
Figure 2:

The left figure shows the end-inspiratory and end-expiration diaphragm thickening at T0 with the DTF reaching 50 %. The right figure shows the end-inspiratory and end-expiration diaphragm thickening of the same patient at T2, and the DTF is 23.5 %, suggesting that the patient’s diaphragm function is incompetent at this time point.

Outcomes

The primary outcomes were the incidence of hypoxemia (PaO2/FiO2≤300  mmHg) at T3 (PACU discharge) and the extubation time(time from admission to PACU to extubation). The PPCs within the first 7 postoperative days was measured as a key secondary outcome. The PPCs were defined according to the ARISCAT study (the criteria of respiratory infection, respiratory failure, bronchospasm, atelectasis, pleural effusion, pneumothorax, and aspiration pneumonitis.) [2], 21], 22]. Complications that do not need to be treated or have no clinical significance, such as a small amount of pneumothorax or pleural effusion, localized subcutaneous emphysema and so forth will not be recorded if they do not adversely affect the patient’s postoperative recovery and discharge.

The other secondary outcomes were defined as follows:(1) the DTF and LUS score at four time points, (2) the PACU length-of-stay and the interventions during PACU length-of-stay, (3) the SpO2 at four time points and the lowest SpO2 in each group after extubation, Details of the protocol are provided in Figure 3.

Figure 3: 
Schematic diagram of the study protocol.
Figure 3:

Schematic diagram of the study protocol.

Statistical analysis

According to the results of the pre-test, the incidence of hypoxemia in the two groups after extubation was taken as the main result (the incidence of hypoxemia in the two groups was 0.35 and 0.10 respectively). Setting α=0.05, 1-β=0.9, and loss-to-follow-up rate of 10 %, the sample size of at least 60 cases in each group was calculated by PASS 15 software (NCSS, Canada).The measurement data conforming to the normal distribution were expressed as mean±standard deviation (x±s), and the independent sample t-test was used for comparison between groups. The measurement data that were not normally distributed were expressed as the median (interquartile range) [M(IQR)], and the non-parametric Mann-Whitney U test was used for comparison between groups. The enumeration data was expressed as the number of cases (percentage), and the chi-square test or continuous corrected chi-square test was used for comparison between groups. One-way repeated measures analysis of variance (ANOVA) was used to analyze changes in SpO2, lung ventilation and diaphragm thickness at different time points. For all analyses, a two-sided p<0.05 was considered statistically significant. SPSS 26.0 statistical software (IBM, USA) was used when analyzing the data.

Results

Patient enrollment and characteristics

A total of 135 patients undergoing elective abdominal surgery at Jiangxi Provincial People’s Hospital (October 2022–February 2023) were assessed for eligibility. Five patients were excluded because they met any of the withdrawal criteria and 130 patients were finally enrolled. There were 65 cases in each group, including 61 males and 69 females. There was no significant difference between the two groups in gender, age, BMI, ASA class, smoking rate, operation time, operation type, operation method, intraoperative fluid intake and output, and muscle relaxant usage (Table 1). There were no reintubation events in both groups.

Table 1:

Patient characteristics (N=130).

Category Group DL Group N p-Value
Age, years 56.45 ± 14.13

59.35 ± 13.10 0.226
Male gender 32 (49.2 %) 29 (44.6 %) 0.598
BMI, kg/m2 23.07 ± 3.46 22.33 ± 3.04 0.197
ASA Class/Case, % 0.103
II 36 (55.4 %) 45 (69.2 %)
III 29 (44.6 %) 20 (30.8 %)
Perioperative smoking 8 (12.3 %) 14 (21.15 %) 0.16
SpO2–T0,% 98.51 ± 1.59 98.35 ± 1.54 0.451
Operation time, min 199.11 ± 87.67 214.72 ± 96.02 0.335
Inpatient days, d 10.00 (6.50, 14.00) 9.00 (6.00, 13.00) 0.823
Operation type 0.625
Gastrectomy and pancreatectomy 15 (23.1 %) 17 (26.2 %)
Hepatectomy 8 (12.3 %) 12 (18.5 %)
Enterectomy 18 (27.7 %) 13 (20.0 %)
Others 24 (36.9 %) 23 (35.4 %)
Laparoscopy 57 (87.7 %) 59 (90.8 %) 0.571
Intraoperative fluid Intake, mL 1600.00 (1200.0, 2000.0) 1500.00 (1235.0, 2200.0) 0.450
Intraoperative fluid Output, mL 450.00 (275.00, 775.00) 450.00 (380.00) 0.307
Muscle relaxant usage, mg 14.00 (12.00, 17.00) 16.00 (12.00, 20.00) 0.095

Perioperative ultrasound findings

Compared with T0 (operating room admission), the end-inspiratory diaphragm thickening of patients in the group DL was significantly reduced at T1 (PACU admission) and T2 (15 min post-extubation) (p<0.01). The thickness of the diaphragm at the end of inspiration was minimum at T1, which was statistically different from other time points (p<0.01). There was still a statistically significant difference in end-inspiratory diaphragm thickening between T3 (PACU discharge) and T0 (p<0.01). Compared with T0, the DTF of patients at T1, T2, and T3 decreased significantly (p<0.01). The DTF of patients at T1 was the lowest, and began to increase at T1–T3, but T3 was still lower than T0 (p<0.01). Compared with T0, the LUS score of patients at T1, T2, and T3 was significantly increased (p<0.01) (Table 2).

Table 2:

LUS Score, Diaphragm thickening and DTF at different time points.

T0 T1 T2 T3
LUS Score 0.23 ± 0.52 5.22 ± 2.89a 4.31 ± 2.05a 3.89 ± 1.96a
End-inspiration, mm 0.29 ± 0.07 0.24 ± 0.07a 0.27 ± 0.06a 0.29 ± 0.07
End-exspiration, mm 0.20 ± 0.04 0.19 ± 0.05 0.19 ± 0.04 0.20 ± 0.04
DTF, % 49.06 ± 14.75 28.51 ± 12.62a 38.87 ± 9.36a 43.83 ± 8.26a
  1. Compared with T0, ap<0.05.

Primary outcomes

Post-extubation hypoxemia occurred in 20 patients in the group N vs. 5 patients in the group DL. The incidence of hypoxemia in the group DL was significantly lower than group N (7.7 VS 30.8 %, p<0.01). Time to extubation was significantly shorter in the group DL compared with the group N (p<0.01). The detailed results were presented in Table 3.

Table 3:

Comparison of extubation time, incidence rate of hypoxemia at T3 and pulmonary complications and PACU length-of-stay(two groups).

Group DL Group N p-Value
Extubation time 24.00 (12.50, 45.00)a 35.00 (20.50, 50.50) 0.009
Incidence rate of hypoxemia after extubation 7.7 %a 30.8 % 0.001
Incidence rate of pulmonary complications 3.1 % 6.2 % 0.680
PACU length-of-stay 62.00 (50.50, 83.00)a 83.00 (67.50, 100.50) 0.000
  1. Compared with the Group N, ap<0.05.

Secondary outcomes

There was no significant difference in the incidence of postoperative pulmonary complications between the two groups (3.1 VS. 6.2 %, p>0.1), including 2 cases in the group DL (1 case of pulmonary infection, 1 case of pulmonary infection combined with pleural effusion) and 4 cases in Group N (2 cases of pulmonary infection, 2 cases of pulmonary infection combined with pleural effusion). PACU length of stay was significantly shorter in the group DL vs. group N (p<0.01). The detailed results were summarized in Table 3.

There was no significant difference in SpO2 and the lowest SpO2 after extubation between the two groups at different time points (Table 4).

Table 4:

Comparison of SpO2 and lowest SpO2 at each time point (two groups).

SpO2–T0 SpO2–T1 SpO2–T2 SpO2–T3 Lowest SpO2
Group DL 98.51 ± 1.59 99.66 ± 0.67 99.06 ± 1.39 99.43 ± 0.88 98.17 ± 1.69
Group N 98.35 ± 1.54 99.75 ± 0.56 98.86 ± 1.57 99.38 ± 1.07 97.43 ± 2.90
P 0.451 0.471 0.330 0.906 0.078

In the group N, furosemide was used in 2 patients at T1, and 3 patients needed to use masks or oropharyngeal airway after extubation at T2. In the group DL, 5 patients received furosemide at T1, 9 patients underwent ultrasound-guided lung recruitment maneuvers, and 8 patients received neostigmine and atropine at T2. Total interventions were significantly higher in the group DL vs. group N (p<0.05). Compared with the group N, the number of intervention cases required at T1 in the group DL was significantly increased (p<0.05), referring to Table 5 for detailed data.

Table 5:

The number of cases requiring intervention at different time points after extubation (two groups).

Total number of cases T0 T1 T2 T3
Group N 5 0 2 3 0
Group DL 22a 0 14a 8 0
P 0.000 0.003 0.207
  1. Compared with the group N, ap<0.05.

Discussion

Respiratory insufficiency is common in patients recovering from anesthesia with delayed recognition risking hypoxic organ damage and mortality [23]. This underscores the critical need for enhanced respiratory monitoring during anesthesia recovery. Our study demonstrates that combined diaphragm-lung ultrasound assessment significantly reduced extubation time and post-extubation hypoxemia compared to conventional resuscitation.

Auscultation as one of the essential components of the clinical examination might be challenging as dorsal lung fields are difficult to reach in supine positioned patients, and the environment in PACU is often noisy. Cox’s [9] study suggested that the agreement between lung ultrasound and auscultation is poor where 33 % of patients showed ultrasound evidence of pulmonary edema, yet 51 % of these had normal auscultation findings. Meanwhile the diagnostic accuracy of auscultation was better in non-ventilated than in ventilated patients. In our study, more patients with increased extravascular lung water were screened in the ultrasound group than those who relied on auscultation and SpO2 solely, and diuretics were used before the patients developed obvious symptoms of pulmonary edema which is related to that ultrasound is highly sensitive, specific, and reproducible for diagnosing the increase of extravascular lung water and pulmonary edema in patients at the bedside [12], 24]. Studies by other scholars also showed that Ultrasound-guided alveolar recruitment, regardless of the technique, could be more effective because it facilitates real-time monitoring of the expansion of collapsed alveoli [17], 25]. An ultrasound-guided recruitment manoeuvre was performed in the ultrasound group which can be conducive to confirming the effects of lung recruitment manoeuvres [17] and 9 patients received it with immediate efficacy confirmation in the group DL.

Clinical implementation of quantitative neuromuscular monitoring remains limited by practicality constraints resulting in persistently high rates of postoperative residual curarization (PORC) [26], 27]. In addition, there is some uncertainty in the metabolism of neuromuscular blocking drugs, and PORC may occur when the antagonistic drug effect disappears. An observational study revealed that 18 % of patients maintained a train-of-four ratio (TOFr) <0.9 20 minutes after neostigmine administration [28]. In the absence of muscle monitoring, DTF measured by ultrasound can be used to evaluate the recovery of the diaphragm after operation, and for conscious patients, it is more comfortable than train-of-four (TOF) and can help anesthesiologists to detect PORC patients in PACU. In the group DL, we identified 8 patients (12.3 %) with DTF <30 % at T2 (15 min post-extubation), which was consistent with previous research results [29]. The results of this study showed that the DTF of the patient was the lowest at T1 (PACU admission), and began to increase at T1–T3 (PACU discharge), suggesting that the patient’s spontaneous breathing recovered after the operation, and the diaphragm and other respiratory muscle groups gradually recovered their contraction function. In the meantime, DTF at T3 was still lower than T0 (p<0.01), indicating that the contractile function of the diaphragm had not recovered to the preoperative awake state before the patient returned to the ward after spontaneous breathing, suggesting that the deep breathing function was impaired after the operation, which was consistent with the research results of Kim et al. [30].

While individual applications of lung or diaphragmatic ultrasound are established, their combined impact on respiratory recovery remained unverified. Integrating diaphragm-lung ultrasound with standard monitoring enables precision-guided interventions that significantly accelerate extubation and reduce hypoxemia incidence.

Hypoxemia represents a potentially life-threatening yet frequent perioperative complication. In our study, hypoxaemia was defined as PaO2/FiO2≤300 mmHg [15] rather than the indicator of SpO2. Studies have shown that when the inhaled oxygen concentration is 25–30 %, even if the patient has trespiratory depression and hypoventilation, the SpO2 remains above 95 % [31]. PaO2/FiO2 can better reflect the pulmonary oxygenation function of patients and the accuracy was greater than SpO2 under the condition of auxiliary oxygen supply [32]. Interestingly, inconsistent with the results of the incidence of hypoxemia in our study, there was no significant difference in SpO2 at each time point and the lowest SpO2 after extubation between the two groups of patients (Table 4), which may be related to the ability of auxiliary oxygen supply to cover up the abnormal respiratory function of patients after SpO2 detection. We expected that ultrasound assessment and intervention would reduce the incidence of postoperative pulmonary complications in patients. Although PPCs were numerically lower in the group DL (3.1 vs. 6.2 %), this difference lacked statistical significance (p>0.1). It may be related to limited sample size and absence of routine postoperative imaging.

This study still has the following limitations. Firstly, the feasibility of ultrasound assessment of diaphragm function has been confirmed, but it is easily interfered by factors such as BMI and sedation level. This experiment was not compared with other methods for assessing diaphragmatic function. Secondly, diaphragm and lung examination has high repeatability and feasibility, but its accuracy and effectiveness depend on the experience of the operator. Lastly, exclusion of patients with preexisting respiratory conditions limits generalizability to high-risk populations.

In summary, this study demonstrates that real-time assessment of pulmonary aeration and diaphragmatic function during anesthesia recovery facilitates rapid diagnosis of impairment etiology, early detection of PORC and targeted interventions accelerating respiratory recovery.


Corresponding author: Shan-liang Guo, Department of Anesthesiology, Jiangxi Provincial People’s Hospital, The First Affiliated Hospital of Nanchang Medical College, NO.152 Aiguo Road, Nanchang, Jiangxi 330006, China, E-mail:
Ping Zhang and Wei-hong Huang contributed equally to this work.

Acknowledgments

The authors appreciate the efforts of all those involved in the study and the members of the research team for their dedicated efforts in conducting the clinical trial and completing the follow-up.

  1. Funding information: This work was supported by the Health Commission of Jiangxi Province, 202310125.

  2. Author contribution: Shan-liang Guo: study design, methodology, Writing-Reviewing and Editing. Ping Zhang: Study design, Data analysis, study implementation. Wei-hong Huang: Data collection, writing – original draf. Long-cheng Fan: Data collection, Study design. Zhong-yu Liu: Data analysis, Software.

  3. Conflict of interest: The authors have no conflict of interest to declare.

  4. Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Received: 2025-02-10
Accepted: 2025-09-17
Published Online: 2025-12-22

© 2025 the author(s), published by De Gruyter, Berlin/Boston

This work is licensed under the Creative Commons Attribution 4.0 International License.

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