The risk of post-operative pulmonary complications in lung resection candidates with normal forced expiratory volume in 1 s and diffusing capacity of the lung for carbon monoxide: a prospective multicentre study

Ivan Cundrle Jr, Zdenek Merta, Monika Bratova, Pavel Homolka, Ladislav Mitas, Vladimir Sramek, Michal Svoboda, Zdenek Chovanec, Milos Chobola, Lyle J. Olson, Kristian Brat
ERJ Open Research 2023 9: 00421-2022; DOI: 10.1183/23120541.00421-2022

Abstract

Introduction According to the guidelines for preoperative assessment of lung resection candidates, patients with normal forced expiratory volume in 1 s (FEV1) and diffusing capacity of the lung for carbon monoxide (DLCO) are at low risk for post-operative pulmonary complications (PPC). However, PPC affect hospital length of stay and related healthcare costs. We aimed to assess risk of PPC for lung resection candidates with normal FEV1 and DLCO (>80% predicted) and identify factors associated with PPC.

Methods 398 patients were prospectively studied at two centres between 2017 and 2021. PPC were recorded from the first 30 post-operative days. Subgroups of patients with and without PPC were compared and factors with significant difference were analysed by uni- and multivariate logistic regression.

Results 188 subjects had normal FEV1 and DLCO. Of these, 17 patients (9%) developed PPC. Patients with PPC had significantly lower pressure of end-tidal carbon dioxide (PETCO2) at rest (27.7 versus 29.9; p=0.033) and higher ventilatory efficiency (V′E/V′CO2) slope (31.1 versus 28; p=0.016) compared to those without PPC. Multivariate models showed association between resting PETCO2 (OR 0.872; p=0.035) and V′E/V′CO2 slope (OR 1.116; p=0.03) and PPC. In both models, thoracotomy was strongly associated with PPC (OR 6.419; p=0.005 and OR 5.884; p=0.007, respectively). Peak oxygen consumption failed to predict PPC (p=0.917).

Conclusions Resting PETCO2 adds incremental information for risk prediction of PPC in patients with normal FEV1 and DLCO. We propose resting PETCO2 be an additional parameter to FEV1 and DLCO for preoperative risk stratification.

Abstract

In addition to FEV1 and DLCO, resting PETCO2 and V′E/V′CO2 slope deliver additional information on risk of post-operative pulmonary complication development in lung resection candidates https://bit.ly/3Erv0DB

Introduction

According to the most recent European Respiratory Society (ERS)/European Society of Thoracic Surgeons (ESTS) guidelines for preoperative assessment of lung resection candidates, spirometry and assessment of diffusing capacity of the lung for carbon monoxide (DLCO) should be part of routine diagnostic evaluation prior to thoracic surgery [1]. In cases where forced expiratory volume in 1 s (FEV1) or DLCO is lower than 80% of predicted, cardiopulmonary exercise testing (CPET) is also recommended [1].

Despite widespread use of less invasive surgical techniques (video-assisted and non-intubation thoracic surgery) over the last decade, peri-operative morbidity and mortality rates remain high compared to other elective surgical procedures. The reported 30-day post-operative mortality rates after pulmonary resection range from 2.1% to 3% [2–4] and as high as 6.6% [5] to 7.5% [6]. In contrast, reported 30-day mortality rates after cholecystectomy are 0.15% [7] and 0.08% for elective appendectomy [8]. Post-operative pulmonary complications (PPC) not only promote intensive care unit (ICU) readmission and prolonged hospital stay with adverse economic impact, but they also contribute to peri-operative mortality following lung resection [2].

Guided by current ERS/ESTS criteria for preoperative risk assessment, patients with FEV1 and DLCO >80% predicted are considered safely resectable up to the extent of pneumonectomy without further functional considerations [1]. However, it is unclear what proportion of patients with normal (>80% predicted) FEV1 and DLCO experience PPC after lung resection and which factors may be predictive of PPC in this patient subgroup.

Based on previous research demonstrating ventilatory efficiency (V′E/V′CO2) slope and resting pressure of end-tidal carbon dioxide (PETCO2) are independent predictors of PPC [5, 9–11], we hypothesised that these parameters may predict PPC in the subgroup of patients with normal preoperative lung function (FEV1 and DLCO ≥80% predicted). Therefore, the aims of this study were to: 1) assess frequency of PPC in patients with normal FEV1 and DLCO scheduled for elective lung resection; and 2) identify factors associated with increased risk of PPC in this subgroup.

Methods

Study population

This was a prospective multicentre observational study including adult patients scheduled for lung resection surgery (mainly due to suspected or confirmed malignancy) at two tertiary-care (university type) centres in the Czech Republic (St. Anne's University Hospital in Brno and University Hospital Brno). Patient recruitment took place between May 2017 and September 2021. All patients scheduled for thoracic surgery were systematically screened for eligibility to participate in this observational study.

Inclusion criteria included written informed consent for participation, ability to undergo CPET, adult age (≥18 years) and lung resection surgery. Exclusion criteria included inability or patient refusal to undergo CPET, contraindication for lung resection due to predicted post-operative (ppo)-peak oxygen consumption (peak V′O2) <10 mL·kg−1·min−1 or <35% predicted, or ppo-FEV1 or DLCO <30% predicted (in accordance with the latest ERS/ESTS guidelines [1]). The study was conducted in accordance with the declaration of Helsinki and approvals were obtained from both institutional review boards including the Ethics Committee of the University Hospital Brno (reference code 150617/EK) and Ethics Committee of St. Anne's University Hospital in Brno (reference codes 19JS/2017 and 2G/2018). The study registration reference code (ClinicalTrials.gov) is NCT03498352.

Pulmonary function tests and cardiopulmonary exercise testing

The same CPET protocol was used as in our previous published studies [11, 12]. Briefly, each patient underwent preoperative spirometry, DLCO assessment and CPET. Spirometry (ZAN100 device; nSpire Health, Inc., Longmont, CO, USA) and DLCO assessments (PowerCube Diffusion+ device; Ganshorn Medizin Electronic GmbH, Niederlauer, Germany) were performed in agreement with current ERS standards and technical requirements [13].

Symptom-limited CPET to volitional fatigue to a rating of perceived exertion of 18 to 20 on the Borg scale was used in each patient on an electronically braked bicycle ergometer (Ergometrics 800®; Ergoline, Bitz, Germany) with an incorporated 12-channel electrocardiography unit (AT-104®; Schiller AG, Baar, Switzerland). The expired gases and volumes were analysed using the PowerCube-Ergo® system (Ganshorn Medizin Electronic GmbH, Niederlauer, Germany). The CPET protocol included a rest phase, warm-up phase and ramp protocol with linearly increasing resistance (15 W·min−1) with 3-min cool-down.

The following parameters were recorded: FEV1, forced vital capacity (FVC), FEV1/FVC (spirometry), DLCO, V′O2, carbon dioxide output (V′CO2), tidal volume (VT), breathing frequency (fb), minute ventilation (V′E), PETCO2, dead space ventilation to tidal volume ratio (VD/VT), respiratory exchange ratio (RER), V′E/V′CO2 ratio and V′E/V′CO2 slope (calculated up to peak exercise).

Post-operative pulmonary complications

PPC were recorded prospectively from the first 30 post-operative days or from the hospital stay. The PPC were defined similarly to previous studies [9, 11, 12, 14] and included: respiratory failure (requiring noninvasive ventilation or intubation plus invasive mechanical ventilation); acute respiratory distress syndrome (bilateral chest radiograph infiltrates not due to fluid overload or cardiac failure plus partial pressure of oxygen in arterial blood/inspiratory oxygen fraction (PaO2/FIO2) <300); tracheostomy; pneumonia (chest radiograph infiltrates plus at least two of the following signs: purulent sputum or fever or leukocytosis/leukopenia) and atelectasis (chest radiograph signs plus urgent bronchoscopy with removal of mucus plug). 30-day mortality and hospital and ICU length of stay (LOS) were also monitored.

Statistical analyses

Categorical parameters were described by absolute and relative frequencies. Continuous parameters were described by mean±sd and median supplemented by 5% quantile and 95% quantile. Statistically significant differences between two groups (with and without complications) were tested by Pearson chi-square test (Fisher exact test) for categorical and t-test (Mann–Whitney test) for continuous parameters.

Univariate logistic regression was used to identify risk factors of PPC in the subgroup of patients with FEV1 and DLCO ≥80%. Receiver operating characteristic (ROC) analysis was used to determine which parameters are useful to divide the patients into two groups according to presence of PPC. Cut-offs were chosen as the highest sum of sensitivity and specificity.

To prevent collinearity of PETCO2 and V′E/V′CO2, we created two models for multivariate regression analysis separately for each parameter, and both models also contained thoracotomy as the strongest factor from the univariate analysis. Multivariate models adjusted by age, sex, thoracotomy, FEV1/FVC and DLCO were also calculated (see supplementary material). A forward stepwise method was used to obtain the final models. ROC analysis for comparison of both models was provided. Comparison of area under the curve (AUC) was performed by the DeLong test; p-values <0.05 were considered statistically significant. SPSS Statistics 25.0 (IBM Corp, Chicago, IL, USA) was used for analysis.

Results

The study cohort comprised 423 patients. Of these, 398 had complete data on lung function, DLCO and CPET and were further analysed (figure 1).

FIGURE 1
FIGURE 1

Flowchart of the study. DLCO: diffusing capacity of the lung for carbon monoxide; FEV1: forced expiratory volume in 1 s.

Of the 398 analysed subjects, 188 had values of FEV1 and DLCO ≥80% predicted. Subgroups of patients with normal FEV1 and DLCO (≥80% predicted) or FEV1 and/or DLCO <80% predicted had comparable age, body mass index and proportion of men. Differences between the subgroups were observed for CPET variables as the subgroup with normal FEV1 and DLCO had significantly lower V′E/V′CO2 slope, higher peak V′O2, higher PETCO2 and lower proportion of thoracotomy procedures. The subgroup with normal FEV1 and DLCO had about half the rate of PPC compared to the subgroup with decreased FEV1 and/or DLCO (9% versus 19%; p=0.004). A summary of patient characteristics for both subgroups is presented in table 1.

View this table:
TABLE 1

Comparison of patient groups according to FEV1 and DLCO

Of the 188 subjects with normal FEV1 and DLCO, 17 patients (9%) developed PPC. Patients in the subgroup with PPC had thoracotomy more frequently (82.4% versus 43.3%; p=0.004), had longer hospital and ICU LOS (12.35 versus 6.67 days and 7 versus 3.08 days; p<0.001 for both) and higher preoperative V′E/V′CO2 slope (31.1 versus 28; p=0.016) and lower resting PETCO2 (27.7 versus 29.9; p=0.033) compared to patients without PPC. The values of peak V′O2 were similar between the two subgroups (p=0.913) (table 2).

View this table:
TABLE 2

Characteristics of subgroups with and without post-operative pulmonary complications

Univariate logistic regression analysis demonstrated thoracotomy, resting PETCO2 and V′E/V′CO2 slope were associated with PPC (supplementary table S1). For model 1, multivariate analysis showed thoracotomy and resting PETCO2 (OR 6.419 and 0.872, respectively) were significant risk factors, while for model 2 thoracotomy and V′E/V′CO2 slope (OR 5.884 and 1.116, respectively) were independently associated with PPC (table 3). AUCs of these models were comparable (0.767 versus 0.781; p=0.617) (figure 2). Adjustment by age, sex, thoracotomy, FEV1/FVC and DLCO did not significantly change the result of the multivariate analysis (supplementary table S2). Ideal cut-off values for PPC prediction were ≤30.5 mmHg for resting PETCO2 and ≥28.1 for V′E/V′CO2 slope (table 2).

View this table:
TABLE 3

Multivariate logistic regression: post-operative pulmonary complications

FIGURE 2
FIGURE 2

Multivariate regression models for post-operative pulmonary complication prediction. AUC: area under the curve.

Discussion

The novel finding of our study was that 9% of patients with normal FEV1 and DLCO according to current preoperative assessment guidelines [1, 15] developed PPC. These patients exhibited preoperative signs of impaired ventilatory control (lower resting PETCO2 and increased V′E/V′CO2 slope) that may be used for risk stratification. Importantly, peak V′O2 failed to predict PPC in this specific subgroup.

The key functional measurements to assess preoperative fitness for radical thoracic surgery have been spirometry and DLCO examination. Predictive values of FEV1 and DLCO have been studied extensively and both are well established in preoperative functional assessment algorithms [1, 15]. The discriminative power of these parameters is stronger in patients with low values of FEV1 and/or DLCO but the test performance decreases with increasing values [1]. In our study, the rates of PPC were doubled in patients with decreased FEV1 and DLCO compared to those with normal values of both parameters. This finding confirms that the diagnostic utility of both parameters for basic risk assessment is high. On the other hand, even in the subgroup with normal FEV1 and DLCO, there were significant numbers of patients who developed PPC. Importantly, there were no differences in FEV1 and DLCO on comparison of patients with and without PPC, which suggests the need for additional predictors if improvements in patient management and outcomes are to be achieved.

A proposed strategy to improve outcomes in the post-operative period might be more precise identification of patients at risk of PPC development. The potential role of another possible strategy – prehabilitation prior to thoracic surgery – remains controversial and unresolved to this date and should be further investigated in the future [16]. Our data show that in patients with normal FEV1 and DLCO scheduled for thoracotomy, V′E/V′CO2 slope and resting PETCO2 are strong predictors of PPC. The diagnostic utility of V′E/V′CO2 slope in patients with decreased FEV1 and DLCO has been demonstrated over the last decade by several research groups, as they independently predict PPC [5, 9, 10], prolonged airleak [12] and 30-day mortality [14, 17]. Our research group also recently demonstrated excellent performance of PETCO2 at rest for PPC prediction [5, 11].

The main determinants of low PETCO2 are hyperventilation and increased dead space ventilation (ventilation/perfusion mismatch). In our patients, PaCO2 was not significantly different between both groups, suggesting ventilation/perfusion mismatch may be the reason for low PETCO2 in the PPC group and may also explain its superiority compared to PaCO2 in the PPC prediction. Indeed, V′E/V′CO2 is also related to hyperventilation (PaCO2) and dead space ventilation (VD/VT ratio) [18]. As there were no differences in the PaCO2, the observed difference in the V′E/V′CO2 slope must have been caused by changes in the ventilation/perfusion mismatch, i.e. VD/VT. However, we must acknowledge that no differences were observed also in the VD/VT ratio in our study. This may be explained by direct measurement of PaCO2 versus underestimation of VD/VT [19].

In the subgroup of patients with normal FEV1 and DLCO (≥80% predicted), the predictive properties of V′E/V′CO2 slope and resting PETCO2 were comparable (AUCs 0.767 and 0.781). This is in agreement with previous research of our work group in an unselected lung surgery patient population [11], as both parameters are determined by similar physiology [5, 11, 18, 20, 21]. Indeed, the two parameters showed a strong inverse correlation and can be used as mutual surrogates [5, 11].

Our results showed different optimal cut-off values for V′E/V′CO2 slope (28.1) and PETCO2 at rest (30.5 mmHg) compared to previous reports [5, 9–11]. For V′E/V′CO2 slope, values of 35 were reported most frequently as optimal cut-offs [5, 9–11], while for resting PETCO2, the reported cut-offs were 30 mmHg [5] and, more recently, 28.4 mmHg [11]. The observed variability of cut-offs (more pronounced in the case of V′E/V′CO2 slope) may be explained by different composition of our study cohort, as this subgroup analysis contained only data of healthier subjects with normal lung functions (FEV1 and DLCO). We suggest that the observed cut-offs be limited to this specific subgroup of healthier patients.

Importantly, peak V′O2 failed to predict PPC. This finding is in agreement with our previous study in unselected lung surgery candidates [11] and extends the series of previous reports where the predictive value of peak V′O2 has been questioned [5, 9–11, 14, 17]. It is known that peak V′O2 is determined by a wider range of factors (including cardiac output, vascular resistance, muscle capillary density and mitochondrial function), while V′E/V′CO2 and PETCO2 are more directly related to ventilation [22]. However, in this selected population of healthy subjects, predictive value of peak V′O2 might have also been influenced by a subject's normal fitness.

Clinical implementation of our findings relates mostly to the utility of resting PETCO2. Though V′E/V′CO2 slope showed excellent predictive value for PPC, the overall cost-effectiveness of performing CPET in this otherwise healthy population with normal lung function seems very low. Instead, we propose routine use of PETCO2 in patients with normal lung functions scheduled for thoracotomy since this surgical procedure was the second strongest risk factor of PPC as shown by our data. Video-assisted thoracic surgery is a safer alternative to conventional thoracotomy [23]. However, in some patients, thoracotomy cannot be avoided due to known adhesions or unfavourable anatomical conditions. In these patients, resting PETCO2 might be beneficial with regard to identifying patients at risk of PPC development and requiring more intensive preoperative management (e.g. pulmonary prehabilitation) as PPC are associated with longer hospital LOS and costs [16, 24].

Limitations of this study include: 1) small numbers of patients with PPC in the subgroup of subjects with normal lung functions; however, this is consistent with a low risk population; 2) patients were recruited based on values of ppo-peak V′O2 ≥10 mL·kg−1·min−1 (thus meeting the valid ERS criteria for resectability), and so preselection bias might be introduced; and 3) this subgroup analysis contained only data from healthier subjects with normal lung function (FEV1 and DLCO ≥80%), suggesting the findings and observed cut-offs of resting PETCO2 and V′E/V′CO2 slope are not generalisable to non-selected populations and remain limited solely to this subgroup of healthier patients.

We conclude that V′E/V′CO2 slope and resting PETCO2 bring incremental information regarding risk of PPC development in patients with normal values of FEV1 and DLCO prior to thoracic surgery. We propose that routine resting capnography (PETCO2 measurement) be performed in addition to spirometry and DLCO assessment for patients scheduled for lung resection via thoracotomy.

Supplementary material

Supplementary Material

Please note: supplementary material is not edited by the Editorial Office, and is uploaded as it has been supplied by the author.

Supplementary material 00421-2022.supplement

Footnotes

  • Provenance: Submitted article, peer reviewed.

  • Acknowledgements: The authors would like to thank all the patients participating in this study for sharing their data with the scientific community.

  • The study was registered at www.ClinicalTrials.gov with identifier number NCT03498352. The datasets generated and/or analysed during the current study are available from the corresponding author on reasonable request.

  • Ethics: The study was conducted in accordance with the declaration of Helsinki and approved by the local Ethics Committee of St Anne's University Hospital in Brno (reference number 19JS/2017, date of approval 12 April 2017; reference number 2G/2018, date of approval 21 March 2018) and by the local Ethics Committee of the University Hospital Brno (reference number 150617/EK, date of approval 19 June 2017). All participants signed written informed consent. The manuscript adheres to the applicable STROBE guidelines for observational studies.

  • Consent for publication: Not applicable.

  • Author contributions: All authors contributed to the data collection, analysis and interpretation, and writing of the manuscript. I. Cundrle Jr, K. Brat and L.J. Olson designed the study. I. Cundrle Jr registered the CMRD project at ClinicalTrials.gov. I. Cundrle Jr and K. Brat secured funding for the research project. I. Cundrle Jr, K. Brat, M. Bratova, Z. Merta, P. Homolka, L. Mitas, V. Sramek and Z. Chovanec collected the data within both centres. K. Brat and I. Cundrle Jr designed the analyses for this particular study. M. Svoboda performed the statistical analysis. K. Brat, M. Svoboda and I. Cundrle Jr drafted the manuscript. All authors critically revised the manuscript for intellectual content and approved the final submitted version.

  • Conflict of interests: M. Bratova received lecture and fees from Roche CZ, Bristol-Myers Squibb CZ and MSD CZ outside the submitted work. K. Brat received lecture and consulting fees from Chiesi CZ, Boehringer Ingelheim CZ, Novartis CZ, AstraZeneca CZ and Angelini CZ outside the submitted work. The other authors (I. Cundrle Jr, P. Homolka, M. Chobola, V. Sramek, Z. Merta, L. Mitas, M. Svoboda, Z. Chovanec and L.J. Olson) have nothing to disclose.

  • Support statement: The study has been funded by Ministry of Health of the Czech Republic research grant number NU21-06-00086. Further support received from Ministry of Health of the Czech Republic – conceptual development of research organisations (MH CZ-DRO FNBr 65269705). The sponsors had no role in the study design, data collection or analysis and preparation of the manuscript. Funding information for this article has been deposited with the Crossref Funder Registry.

  • Received August 29, 2022.
  • Accepted November 2, 2022.
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The risk of post-operative pulmonary complications in lung resection candidates with normal forced expiratory volume in 1 s and diffusing capacity of the lung for carbon monoxide: a prospective multicentre study
Ivan Cundrle, Zdenek Merta, Monika Bratova, Pavel Homolka, Ladislav Mitas, Vladimir Sramek, Michal Svoboda, Zdenek Chovanec, Milos Chobola, Lyle J. Olson, Kristian Brat
ERJ Open Research Mar 2023, 9 (2) 00421-2022; DOI: 10.1183/23120541.00421-2022
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