González‑Suárez et al. BMC Anesthesiology (2022) 22:186 https://doi.org/10.1186/s12871-022-01715-4 RESEARCH Open Access Detection of residual pulmonary alterations with lung ultrasound and effects on postoperative pulmonary complications for patients with asymptomatic SARS‑CoV‑2 infection undergoing surgeries Susana González‑Suárez1,2*, Antonio Barbara Ferreras1, Melissa Caicedo Toro1 and Macarena Aznar de Legarra1 Abstract Background: For patients with a clinical course of active SARS-CoV-2 (severe acute respiratory syndrome coronavirus 2) infection, there may be a higher risk of perioperative complications. Our main objective is to detect the residual pulmonary alterations in asymptomatic patients after SARS-CoV-2 infection undergoing surgery and determine their relationship with the clinical course of SARS-CoV-2 infection. The secondary aim is to investigate whether the pres‑ ence of residual pulmonary alterations have any affects on the severity of postoperative pulmonary complications. Methods: After approval by the Hospital’s Ethical Committee, this prospective observational study included consec‑ utive patients (n=103) undergoing various surgical procedures and anesthetic techniques with a history of past SARS- CoV-2 infection. On the day of surgery these patients remained asymptomatic and the polymerase chain reaction (PCR) test for SARS-CoV-2 was negative. The history, physical findings, and clinical course of SARS-CoV-2 infection were recorded. Lung ultrasound was performed before surgery to evaluate the possible residual pulmonary alterations (≥ 3 B-lines and pleural thickening), along with determitation of pulmonary static compliance values during surgery. Postoperative pulmonary complications were collected during hospital stay. Results: 24.27% (n=25) patients presented ≥ 3 B-lines, and 28% (n=29) patients presented pleural thickening. For 15 patients (21.7%) the pulmonary compliance was < 40 mL/cm ­H2O. Patients with pleural thickening had a higher incidence of pneumonia, acute respiratory syndrome distress, a need for vasoactive drugs and required more days of hospitalization during SARS-CoV-2 infection (p= 0.004, 0.001, 0.03, 0.00 respectively). Patients with ≥ 3 B-lines needed more days in an intensive care unit and vasoactive drugs during SARS-CoV2 infection (p= 0.04, 0.004 respectively). Postoperative pulmonary complications were observed in 5.8% (n=6) of the patients, and were more frequent in the presence of both, ≥ 3 B-lines and pleural thickening (p= 0.01). Conclusions: In asymptomatic post-COVID-19 patients, pathological findings detected by lung ultrasound before surgery are associated with the severity of the SARS-CoV2 infection and resulted in more postoperative pulmonary *Correspondence: susana.gonzalez@uab.cat 2 Universitat Autònoma de Barcelona, UAB, Barcelona, Spain Full list of author information is available at the end of the article © The Author(s) 2022. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://​creat​iveco​mmons.​org/​licen​ses/​by/4.​0/. The Creative Commons Public Domain Dedication waiver (http://​creat​iveco​ mmons.​org/​publi​cdoma​in/​zero/1.​0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. González‑Suárez et al. BMC Anesthesiology (2022) 22:186 Page 2 of 10 complications. In these patients, the incidence of postoperative pulmonary complications appears similar to that described in the surgical population before the pandemic. Trial registration: clini​caltr​ials.​gov (NCT04922931). June 21, 2021. “Retrospectively registered” Keywords: Post-COVID-19 patients, Lung ultrasound, Static compliance, Postoperative pulmonary complications Background (fever, dyspnea, cough, and digestive disorders) at time of The coronavirus disease 2019 (COVID-19), caused by surgery. a coronavirus SARS-CoV-2, infects a large part of our We included all consecutive post-COVID-19 patients population. In surgical patient’s COVID-19 can cause ≥ 18 years underwent various elective surgery (general a quick deterioration of lung function [1–3]. In addi- surgery, urology, neurology, otolaringology, gynecology, tion to a lung disorder, an alteration in other organs can cardiac, thoracic, and vascular surgery) and anesthetic occur and increase mortality [4–6]. techniques (general, local, neuraxial and peripheral Based on clinical information and expert recommen- regional anesthesia) from June 30, 2020, to February 18, dations, it is suggested that for patients with a possi- 2021. Moreover, the included patients did not have base- ble COVID-19 infection, elective surgeries may be line pulmonary pathology prior to COVID-19. canceled or postponed with the focus to only maintain Exclusion criteria were as follows: patients under the emergency operations and elective cancer surgeries [4– age of 18 years old, pregnant, patients with hemody- 10]. Some authors obtained that the time of surgery for namic instability parameters (mean arterial pressure < 60 a patient who has suffered from SARS-CoV-2 should be mmHg and need for vasopressors), patients undergoing delayed up to at least 7 weeks after passing the infec- pulmonary surgery (lung neoplasms) or who previously tion [11]. had chest surgery, patients with pulmonary pathology To reduce the mortality rate and postoperative pulmo- before SARS-CoV-2 infection (obstructive or restrictive nary complications (PPC) we have included the patients pulmonary pathology), patients with a documented med- who underwent surgery on post-COVID-19 patients ical history of any degree of pulmonary arterial hyperten- when the infection had disappeared, there were no sion (both primary or secondary), heart failure or active symptoms, and the laboratory testing for SARS-CoV-2 respiratory infection. Figure 1 shows the flow diagram of infection was negative. In these circumstances, since the inclusion/exclusion process. the patients included in our study suffered from the dis- ease, residual lung lesions could be found despite being Pulmonary ultrasonography procedure and determination asymptomatic. Moreover, a lower incidence of PPC than of pulmonary static compliance that described in patients with active SARS-CoV-2 infec- The anesthesiologists used the Sonosite portable ultra- tion at the time of surgery could be expected. sound system and a 2- to 5 MHz convex transducer for lung ultrasound (LUS) procedure. During study research- ers utilized higher frequencies for evaluation of the pleu- Methods ral line to determine pleural thickening (defined as being Ethics statement and registration greater than 3 mm in width, with or without irregular The Ethics Committee approved this prospective obser- margins) [12] as well as a linear probe 6-15MHz if it was vational single-center study at the Vall d’Hebron Univer- deemed necessary. The scanning system included the sity Hospital, Barcelona, Spain (PR (AG)346/2020) and approach of 10 thoracic areas with 5 in each hemitho- retrospective registered at www.​clini​caltr​ials.​gov on June rax. Specifically, areas 1 and 2 denoted the upper anterior 11, 2021 (registration number: NCT04922931). All par- and lower anterior chest areas respectively; areas 3 and ticipants signed written informed consent forms before 4 denoted the upper lateral and basal lateral chest areas, enrolment in the study. All methods were carried out fol- respectively, and area 5 denoted posterior area located lowing relevant guidelines and regulations. posterior of the axillary line, at the point at which the diaphragm and adjacent lung segment were accessible in a supine position with slight lateralization of the patient. Study design and participants The anterolateral areas were delimited by three longitu- We defined post-COVID-19 patient as a patient who dinal lines: para-sternal line, anterior axillary line, and previously had a positive PCR test from oronasopharyn- posterior axillary line. A breast line delimited the upper geal swab, and then had one negative test performed at and lower areas resulting in five punctures of exploration least 4 days before surgery and the absence of symptoms (modified from Volpicelli et al. [13]. González‑Suárez et al. BMC Anesthesiology (2022) 22:186 Page 3 of 10 Fig. 1 Flow diagram of exclusion/inclusion criteria During the LUS procedure, the probe was placed verti- Other secondary outcome measures were the correla- cally perpendicular to the ribs at a depth of 9-12 cm in tion between static pulmonary compliance and B-lines the anterior plane and 12-20 cm in the lateral plane, and and correlation between lung compliance values and the focus was placed at the pleural level. the time elapsed between COVID-19 diagnosis and sur- During operation, the static compliance was deter- gery. Other outcomes for the postoperative period were mined by respirators (Drager Perseus A500 and 30-day survival after surgery; hospital stay; need for IMV MAQUET ventilator) in patients with general anesthe- and NIMV; need for an emergent intubation [15]. Other sia. The controlled ventilation was performed with tidal outcomes for the postoperative complications were: the volumes of 7ml/kg adjusted for ideal body weight, with a influence of the ASA, surgical complexity and type of PEEP (Positive End-Expiratory Pressure) of 5 mm Hg and anesthesia on the incidence of PPC, occurrence of post- in a neuromuscular blocking state after orotracheal intu- operative non-pulmonary complications (PnPC) (need bation in a supine position. The static compliance value for vasoactive drugs, transfusion requirements, need for was calculated depending on the formula that is available a second surgery, thrombotic-associated complications in anesthesiology textbook [14] as follows: Cs = VT/P (upper or lower extremity ischemia, intestinal ischemia, plateau – PEEP where Cs denotes static compliance, acute myocardial infarction and stroke), non-pulmonary VT denotes tidal volume, and P plateau denotes plateau infections, acute kidney injury, arrhythmias and heart pressure. failure). Study outcomes Data collection We used as the main outcome the proportion of patients We collected demographic characteristics, baseline having the residual pulmonary alterations detected by comorbidities, American Society of Anesthesiologists lung ultrasound and static pulmonary compliance before (ASA) physical status classification, baseline character- operation, and the relationship between these inju- istics of the COVID-19 presentation and the number of ries with the clinical course of SARS-CoV-2 infection days from COVID-19 diagnosis to surgery. (cough, dyspnea, fever, digestive disorders, pneumonia, LUS data collection comprised the presence of atelec- thrombotic-associated complications (PTE, myocardial tasis, pleural effusion, B lines, pleural thickening, and the infarction, stroke, venous thrombosis), ARDS, need for presence of both, ≥ 3 B-lines and pleural thickening. mechanical ventilation, need for vasoactive drugs and The operative data collected included the static pulmo- days of hospitalization and admission to Intensive Care nary compliance values in patients who received general Unit). anesthesia, the type of anesthesia performed, the type of The secondary outcomes were the postoperative occur- surgery, and the risk of surgery according to the National rence of respiratory complications during hospital stay Institute for Clinical Excellence (NICE) classification of (ARDS, PTE, pneumonia, pneumothorax, atelectasis, the National Health Service UK. bronchospasm) and determine whether the incidence of Postoperative data collected included 30-day survival residual pulmonary injuries detected before surgery are after surgery, hospital stay, need for IMV and NIMV, associated with the appearance of PPC. emergent intubation, type of PnPC and type of PPC. González‑Suárez et al. BMC Anesthesiology (2022) 22:186 Page 4 of 10 All items that could be used to identify the patient of the following criteria: fever, new lung opacities, (clinical record ID number or name) were removed to leukocyte count >12.000/μ. protect personal data. – Atelectasis when the patient presented lung opaci- fication with a shift of the hilum, hemidiaphragm, or mediastinum toward the affected area on a chest Data measurement radiograph. For LUS, each region was scored according to four LUS – Bronchospasm, when the patient presented expira- aeration patterns inspired by Lichtenstein’s nomencla- tory wheezing, treated with bronchodilators. ture [16]: 0 points—presence of lung sliding with A-lines – Pneumothorax, when the patient presented air in the or one or two isolated B-lines; 1 point—moderate loss of pleural space on a chest radiograph. lung aeration with three or four B- lines; 2 points—severe loss of lung aeration with five or more B-lines; and 3 The PnPC were recorded as reported by the attending points—presence of a hypoechoic poorly defined tissue physicians. characterized by complete loss of lung aeration. The LUS score ranging between 0 and 30 was calculated as the Data sources and management sum of points. Data was either collected prospectively by the research For surgical risk, we classified the surgical procedures team (ultrasound findings and pulmonary static compli- according to the following grades: ance) and retrospectively by the research team (clinical course of SARS-CoV-2 infection and postoperative data). I. I: Minor surgical procedures: poor surgical aggres- Retrospective data were obtained from the patient’s med- siveness, surgery with low probability of bleeding ical records. or easily detectable bleeding (excision of adenopa- thies, herniorrhaphys, amputation of fingers, litho- Statistical analysis tripsy, prostate biopsy). For categorical variables, frequencies and percent- II. II: Medium surgical procedures: greater probability ages were displayed for the total sample. Differences in of bleeding and/or if it occurs could go unnoticed parameters were calculated with Pearson’s Chi-squared by developing in a cavity (thyroidectomy, embolec- non-parametric test. The mean, standard deviation, and tomy, tonsillectomy, transurethral resection, tra- percentile descriptive were displayed for continuous vari- cheostomy, laparoscopy surgery for general, gine- ables. Differences in parameters were evaluated by Mann- cology and urology surgeries). Whitney (non-parametric) test or Student’s t tests for two III. III: Major surgical procedures: most important independent (parametric) samples based on the normal- degree of surgical aggressiveness with prolonged ity of the variables to be tested using the Shapiro-Wilks postoperative need (peripheral bypass-bypass, test. Spearman’s correlation coefficient was employed to spinal arthrodesis, laminectomy, open surgery measure the correlation between two variables. The level (for resection of the digestive tract, cystectomy, of significance used in the analyses was 5% (α-0.05) for nephrectomy). two- tailed tests. IV. IV: Very aggressive surgical procedures: prolonged surgeries with very specialized or critical care in Results the postoperative period, (open cardiac surgery, One hundred three post-COVID-19 patients were aortic surgery, intracranial surgery, aggressive neo- included in the study. The average number of days plastic surgery (pelviperitonectomy). between COVID-19 diagnosis and surgery was 108.56 ± 82.02. The mean age was 60.18 ± 14.95 years. During We used the following definitions for PCP: SARS-CoV-2 infection, the number of days of admis- sion to the ICU was 2.09 ± 8.82, IQR (0-1) and the total – ARDS detected by hypoxemia with a relationship days of hospitalization were 14.43 ± 44.69, IQR (2-8). between the arterial partial pressure of oxygen and The commorbidities of the patients and their relation- the fraction on inspired oxygen (PaO2/FiO2) less ship with the pathological ultrasonographic findings than 200, and bilateral pulmonary infiltrates in both and static compliance are shown in Table 1. Surgical and fields on a chest radiograph. anesthetic characteristics are shown in Table 2. – PTE was diagnosed by dyspnea clinic and chest com- At the time of surgery, 11.7% of the patients presented puted tomography angiography (CT angiography). atelectasis, and 7.8% presented pleural effusion. The – Pneumonia when the patient received antibiotics for presence of ≥ 3 B-lines were observed in 25 (24%) of the a suspected respiratory infection and met at least one patients. The global mean of B-lines score was 0.71 ± González‑Suárez et al. BMC Anesthesiology (2022) 22:186 Page 5 of 10 Table 1 Demographic characteristics, comorbidities, and their association with pulmonary pathological ultrasonographic findings and static compliance Total patients Pleural thickening, p-value B-lines ≥ 3, p-value Compliance <50, p-value n = 103 n = 29 n = 25 n = 35 (total n = 103) (total n = 103) (total n = 69) Age <50 23 (22.3) 1 (3.4) 0.005 3 (12) 0.33 6 (17.1) 0.93 50-69 43 (41.7) 12 (41.4) 11 (44) 18 (51.4) ≥70 37 (35.9) 16 (55.2) 11 (44) 11 (31.4) Sex Woman 45 (43.7) 8 (27.6) 0.04 8 (32) 0.33 20 (57.1) 0.18 Man 58 (56.3) 21 (72.4) 17 (68) 15 (42.9) ASA I 7 (6.8) 0 (0) 0.12 0 (0) 0.08 2 (5.7) 0.48 II 55 (53.4) 13 (44.8) 10 (40) 21 (60) III 38 (36.9) 15 (51.7) 14 (56) 10 (28.6) IV 3 (2.9) 1 (3.4) 1 (4) 2 (5.7) Cardiopathy 27 (26.2) 11 (37.9) 0.23 10 (40) 0.18 12 (34.3) 0.43 Vascular disease 14 (13.6) 5 (17.2) 0.49 3 (12) 0.79 7 (20) 0.08 Renal disease 14 (13.6) 4 (13.8) 0.97 3 (12) 0.79 2 (5.7) 0.57 Hypertension 61 (59.2) 20 (69) 0.21 15 (60) 0.93 21 (60) 0.68 Diabetes mellitus 32 (31.1) 10 (34.4) 0.89 8 (32) 0.90 8 (22.9) 0.72 Data are expressed as number (percentage Table 2 Anesthetic-surgical characteristics pulmonary compliance was < 40; for 20 patients (29%) Total patients, n =103 it was between 40-49, and for 34 patients (49.2%) it was ≥ 50 ml/cm H ­ 2O. The pulmonary compliance values Surgery General 42 (40.8) were higher as the time elapsed between COVID-19 Urology 21 (20.4) diagnosis and surgery increased (rho= 0.24, p=0.04) Vascular 9 (8.7) (Fig. 2). An inverse correlation was seen between pul- Neurology 7 (6.8) monary compliance and B lines (Fig. 3) (rho= -0.24, Cardiac 11 (10.7) p=0.04). Thoracic 5 (4.9) The patients with pleural thickening presented more Otolaryngology 4 (3.9) hospitalization days, a need for mechanical ventilation, Gynecology 4 (3.9) more incidence of dyspnea, fever, pneumonia, SDRA and Surgical complexity I 14 (13.6) a need for vasoactive drugs during SARS-CoV2 infection II 44 (42.7) (Table 3). III 32 (31.1) The patients with ≥ 3 B-lines had a higher incidence of IV 13 (12.6) ARDS, and they needed more days in intensive care unit Type of anesthesia General 69 (66.9) (ICU) and vasoactive drugs during SARS-CoV-2 infec- Spinal anesthesia 22 (21.3) tion (Table 3). Peripheral nerve block 3 (2.9) There was no association between compliance < 50 Local anesthesia 9 (8.7) ml/cmH2O and clinical course of COVID-19 infection Data are expressed as number (percentage) (Table 4). All patients survived 30 days after surgery. Hospital stay was 5.53 ± 15.67 days. The mean time for IMV was 1.56, IQR (0-0), and in patients with ≥ 3 B- lines was 2.84 1.29 ± 7.44, and for NIMV was 0.54 ± 2.13 days. Two ± 1.82, IQR (0-4). Sixteen patients (15.53%) presenting patients presented emergent orotracheal intubation due both, B-lines ≥ 3 and pleural thickening. to PPC. The global mean of pulmonary compliance obtained Six patients (5.8%) presented PPC. In these patients, in 69 patients who required general anesthesia, was the mean age was 56.50 ± 17.97, one woman and five 50.39 ± 13.89 ml/cm ­H2O. For 15 patients (21.7%) the men (p = 0.17)). One patient was ASA II, four patients González‑Suárez et al. BMC Anesthesiology (2022) 22:186 Page 6 of 10 Fig. 2 Correlation between pulmonary static compliance and time elapsed from COVID diagnostic to surgery Fig. 3 Correlation between pulmonary static compliance and B lines were ASA III, and one patient ASA IV (p = 0.05). Three pneumothorax, and bronchospasm, with the need for patients presented a degree of type 2 surgical complex- IMV for 30 days and NIMV for 4 days. Moreover, one ity, one patient presented type 3 and two patients pre- patient presented pneumonia, one patient presented sented type 4 (p = 0.32). Five patients with PPC received bronchospasm, and one patient presented ARDS with general anesthesia and one patient endovenous sedation the need for IMV for 7 days. Two patients presented (p= 0.64). atelectasis, one of which required NIMV for 4 days. The patients presented six different types of PPC. PPC and their relationship with pulmonary echo- Two of these patients required emergent orotracheal graphic findings and static compliance are shown in intubation; whilst only one patient presented sev- Table 5. Patients with both, ≥ 3 B-lines and pleural eral complications simultaneously: PTE, pneumonia, thickening, presented a higher occurrence of PPC. González‑Suárez et al. BMC Anesthesiology (2022) 22:186 Page 7 of 10 Table 3 Abnormal pulmonary ultrasonographic findings and clinical course of the SARS-CoV-2 infection Pleural thickening B-lines (≥ 3) No, 74 (71.84) Yes, 29 (28.15) p-value No, 78 (75.72) Yes, 25 (24.27) p-value Covid19-Surgery 109 ± 84.31 106.93 ± 77.37 0.33 115.23 ± 84.90 88 ± 70.03 0.15 Hospitalization days 2.65 ± 6.85 12.90 ±26.35 0.000 3.28 ± 7.19 12.56 ±28.46 0.11 ICU days 0.34 ±1.46 6.24 ±17.28 0.01 0.72 ±3.68 6.00 ±17.88 0.04 NIMV days 0.23 ± 1.58 1.34 ± 3.02 0.002 0.36 ± 1.84 1.12 ± 2.82 0.42 IMV days 0.09 ± 0.81 4.34 ± 13.65 0.03 0.41 ± 2.93 4.04 ± 14.04 0.06 Cough 22 (29.7) 10 (34.5) 0.64 24 (30.8) 8 (32.0) 0.91 Dyspnea 14 (18.9) 14 (48.3) 0.003 19 (24.4) 9 (36.0) 0.25 Fever 24 (32.4) 16 (55.2) 0.03 30 (38.5) 10 (40.0) 0.89 Digestive disorders 13 (17.6) 7 (24.1) 0.45 15 (19.2) 5 (20.0) 0.93 Pneumonia 19 (25.7) 16 (55.2) 0.004 24 (30.8) 11 (44.0) 0.22 Venous thrombosis 0 (0.0) 1 (3.4) 0.11 0 (0.0) 1 (4.0) 0.07 PTE 1 (1.4) 0 (13.8) 0.53 1 (1.3) 0 (0.0) 0.53 ARDS 0 (0.0) 4 (34.5) 0.001 2 (2.6) 2 (8.0) 0.01 Vasoactive drugs 1 (1.4) 3 (10.3) 0.02 1 (1.3) 3 (12.0) 0.01 COVID-19-Surgery: Days elapsed from diagnosis of SARS-CoV-2 infection to the day of surgery. ICU Intensive Care Unit. NIMV Non-invasive mechanical ventilation, IMV Invasive mechanical ventilation, PTE Pulmonary thromboembolism, ARDS Acute respiratory distress syndrome. Data are expressed as mean ± SD, and number (percentage) Table 4 Static compliance and clinical course of the SARS-CoV-2 Table 5 Postoperative pulmonary complications and their infection relationship with pulmonary compliance, B-lines, and pleural thickening Compliance Postoperative <50, n =35 ≥50, n =34 p-value pulmonary complications Covid19-Surgery 101.34 ± 73.16 135.03 ± 92.80 0.14 Hospitalization days 5.03 ± 14.87 5.82 ± 9.70 0.24 None Some p-value ICU days 2.52 ± 9.30 1.29 ± 5.39 0.32 Pulmonary compliance Total 69 (100) 64 (100) 5 (100) 0.66 NIMV days 0.94 ± 2.89 0.35 ± 1.25 0.64 <50 35 (50.7) 32 (50) 3 (60) IMV days 1.51 ± 7.83 0.74 ± 4.29 0.57 ≥50 34 (49.3) 32 (50) 2 (40) Cough 13 (37.1) 13 (38.2) 0.92 B-lines Total 103 (100) 97 (100) 6 (100) 0.13 Dyspnea 9 (25.7) 12 (35.3) 0.38 <3 78 (75.7) 75 (77.3) 3 (50) Fever 11 (31.4) 18 (52.9) 0.07 ≥3 25 (24.3) 22 (22.7) 3 (50) Digestive disorders 9 (25.7) 9 (26.5) 0.94 Pleural thickening Total 103 (100) 97 (100) 6 (100) 0.22 Pneumonia 12 (34.3) 15 (44.1) 0.40 No 74 (71.8) 71 (73.2) 3 (50) Venous thrombosis 1 (2.9) 0 (0) 0.32 Yes 29 (28.2) 26 (26.8) 3 (50) PTE 1 (2.9) 0 (0) 0.32 B-lines + Pleural thick- Total 103 (100) 97 (100) 6 (100) 0.01 ARDS 2 (5.7) 1 (2.9) 0.57 ening No 87 (84.5) 84 (86.6) 3 (50) Vasoactive drugs 3 (8.6) 0 (0) 0.08 Yes 16 (15.5) 13 (13.4) 3 (50) COVID-19-Surgery: Days elapsed from diagnosis of SARS-CoV-2 infection Data are expressed as number (percentage) to the day of surgery. ICU Intensive Care Unit. NIMV Non-invasive mechanical ventilation, IMV Invasive mechanical ventilation, PTE Pulmonary thromboembolism, ARDS Acute respiratory distress syndrome. Data are expressed as mean ± SD, and number (percentage) patients presented cardiac alteration and 1 (1%) patient The PnPC were gathered: 4 (3.9%) patients needed presented renal alterations. 15 patients (14.56%) required vasoactive drugs, 4 (3.9%) patients required a second red blood cell transfusion and 2 patients (1.94%) required surgery, 2 (1.9%) patients presented thrombosis, 3 (2.9%) fresh frozen plasma and platelets. patients presented surgical wound infection, 2 (1.9%) González‑Suárez et al. BMC Anesthesiology (2022) 22:186 Page 8 of 10 Discussion that ¨fibrosis¨ can be considered a potentially reversible In asymptomatic post-COVID-19 patients there are process, and the term ¨reversible pulmonary fibrosis¨ has residual lung lesions that are related to the clinical course been used in the current literature [28]. Truly, this term of SARS-CoV-2 infection. Patients with pleural thicken- encompasses a non-idiopathic form of pulmonary fibro- ing at the time of surgery had more symptoms of dysp- sis associated with COVID-19 infection, which is hetero- nea, more days of hospitalization and noninvasive/ geneous in many aspects and can present anytime from invasive mechanical ventilation during SARS-CoV-2 initial hospitalization to long term follow-up. However, infection comparted to patients who did not have pleu- there is still much uncertainty about many aspects of the ral thickening (p= 0.003, 0.000, 0.002, 0.03 respectively). COVID-19 condition. Also, patients with pleural thickening presented a clini- On the other hand, we demonstrated an inverse corre- cal course with a higher incidence of pneumonia, acute lation between pulmonary compliance and B-lines. Other respiratory syndrome distress, and a need for vasoactive authors also argue that the residual lung damage detected drugs during SARS-CoV2 infection (p= 0.004, 0.001, 0.03 by LUS could be responsible for a decrease in pulmonary respectively). Patients with ≥ 3 B-lines needed more days parenchyma distensibility or static compliance [29]. It is in intensive care unit and needed vasoactive drugs dur- possible that both, the low static compliance values, and ing SARS-CoV2 infection (p= 0.04. 0.004). No signs of most of the wounds observed by ultrasonography, indi- symptoms, days of hospitalization, or clinical course of cate residual pulmonary injuries that return to normal as COVID-19 were observed in patients with compliance < time passes. 50 ml/cmH2O the day of surgery. In our study, the use of LUS identifies certain pul- Other authors also demonstrated the presence of resid- monary alterations in asymptomatic post-COVID-19 ual lung wounds by SARS-CoV-2 infection. Lombardi F. patients undergoing surgery, and some of these pulmo- et al. [17] and Frija-Masson J. et al. [18] showed that the nary findings could be attributed to the SARS-CoV-2 residual respiratory impairment, including lower exercise since the patients did not present previous pulmonary tolerance, was correlated with the severity of respira- pathology; despite this, the incidence of PPC is low. tory failure during hospitalization. Abdulrahman et al. Most studies determine the PPC in patients with active [19] and Myall et al. [20] showed that although most SARS-CoV2 infection [30, 31]; in these cases, it is fore- cases of COVID-19 recover completely, a small propor- seeable that the complications will be greater than in tion of patients present pathological pulmonary findings those patients who have passed the infection or patients by LUS with the appearances of pleural line abnormali- who have been asymptomatic. Other studies found an ties and B line artifacts, which result from inflammation increase in PPC (51.2%) and mortality (23.8%) in patients and interstitial thickening that increase in number with who had SARS-CoV2 infection confirmed within 7 days severity. The persistence of LUS abnormalities was also before or 30 days after surgery [2]. However, the inci- seen in patients with dyspnea [21]; our study also found dence obtained of PPC in our study was much lower, that dyspnea is correlated with an increase in pulmonary probably because our patients had an average number of pathological findings by LUS. days from diagnosis of SARS-CoV2 infection to surgery However, we observed no correlation between the 108.56 ± 82.02 days, in the absence of symptoms and severity of the SARS-CoV-2 infection and a decrease in with negative PCR. These conditions would make surgery static pulmonary compliance. It is probable that the time feasible. So, as we observed PPC in 5.8% of our patients; between the diagnosis of the SARS-CoV-2 infection and this incidence corresponds to values obtained in the surgery had been sufficient time to cure the infection. pre-pandemic stage [32, 33], oscillating in some patients Thus, we observed that the pulmonary compliance val- between 2 to 19% [34]. Furthermore, some authors, also, ues were higher as the time elapsed between COVID-19 did not observe differences in their postoperative results diagnosis and surgery (Fig. 2). when comparing SARS-CoV-2 positive patients with Some patients in our study obtained low values of pul- patients who had tested negative for SARS-CoV- 2 [16]. monary compliance (< 40 ml/cm ­H2O in 21.7 % patients); These authors argue that the baseline characteristics of in some of these patients, this low compliance could be the patients have an important impact in the develop- associated with the presence of pulmonary “fibrosis” ment of PPC. Similarly, we observed that the baseline [22–24]. This fibrosis has been shown after isolated viral characteristics of the patients, evaluated according to the infections [25] and especially after persistent viral infec- ASA classification, are associated with the appearance tions [26]. Nevertheless, Wallace et al. [27] argues that of PPC. Therefore, most of patients with PPC presented ¨fibrosis¨ should not apply to the abnormalities seen high ASA scores. Other factors, such as a severe evolu- in cases of post-viral pulmonary fibrosis, since these tion of the SARS-CoV-2 infection (in terms of pneumo- changes could be reversed over time. Some authors argue nia, PTE, the need for vasoactive drugs, hospital stay) González‑Suárez et al. BMC Anesthesiology (2022) 22:186 Page 9 of 10 and both, pleural thickening, and B lines ≥ 3, were also design, patient recruitment, data collection, interpretation of results and writ‑ ing the manuscript. All authors read and approved the final manuscript. observed in our patients with PPC. Our study has some limitations. Given the low num- Funding ber of complications, we only studied whether the This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. influence of the pulmonary pathological findings and the severe course of the SARS-CoV-2 infection affect Availability of data and materials the appearance of any of the PPC, and not of each of All data that support the findings of this study will be available from the cor‑ responding author. the PPC separately. Also, regarding the LUS technique, as with many areas of ultrasound imaging and inter- pretation, the identification and quantification of the Declarations nature of B-lines and pleural line can be somewhat sub- Ethics approval and consent to participate jective and subject to interpretation [35]. To resolve This project PR (AG) 346/2020, was approved by the Research Ethics Commit‑ tee of the Vall d’Hebron University Hospital, Barcelona, Spain (June 26, 2020), this possible misinterpretation of LUS findings, these and was registered at clini​caltr​ials.​gov (NCT04922931). Patients were enrolled examinations could be performed by more than one in the study after written informed consent. All methods were carried out in expert anesthesiologist. Even by taking this limitation accordance with relevant guidelines and regulations. into account, it’s known that the LUS constitutes a use- Consent for publication ful predictive tool of clinical respiratory deterioration No individual person’s data was included or revealed in this study. course and outcome, with the advantage that it can be Competing interests easily performed bedside [36–40]. Moreover, the inci- The authors declare that they have no competing interest dence of residual lung alterations that we observed in our study cannot be attributed completely to SARS- Author details 1 Department of Anesthesiology, Hospital Universitari Vall d’Hebron, Passeig CoV-2 infection, since it is possible that these lesions de la Vall d’Hebron 119, 08035, Barcelona, Spain. 2 Universitat Autònoma de are observed in patients without SARS-CoV-2 and Barcelona, UAB, Barcelona, Spain. without previous lung pathology. Received: 9 January 2022 Accepted: 27 May 2022 Conclusion In asymptomatic post-COVID-19 patients undergoing References surgery, the severity of SARS-CoV-2 infection in terms 1. Nahshon C, Bitterman A, Haddad R, Hazzan D, Lavie O. Hazardous post‑ of hospitalization, need for mechanical ventilation, the operative outcomes of unexpected COVID-19 infected patients: a call for global consideration of sampling all asymptomatic patients before clinical course of pneumonia, and the need for vasoac- surgical treatment. World J Surg. 2020;44(8):2477–81. https://​doi.​org/​10.​ tive drugs, is associated with an increase of pulmonary 1007/​s00268-​020-​05575-2. pathological findings determined by LUS. Nevertheless, 2. Collaborative CS. Mortality and pulmonary complications in patients undergoing surgery with perioperative SARS-CoV-2 infection: an inter‑ the incidence of PPC could correspond to that described national cohort study. Lancet. 2020;396:27–38. https://​doi.​org/​10.​1016/​ in the pre-pandemic stage. S0140-​6736(20)​31182-X. 3. Garatti A, Castelvecchio S, Daprati A, Molfetta R, Volpe M, De Vincentiis C, et al. 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