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ORIGINAL ARTICLE
Heart, Lung and Circulation (2015) xx, 1–6 1443-9506/04/$36.00 http://dx.doi.org/10.1016/j.hlc.2015.11.004
Clinical Correlation of Early Atelectasis after Bilateral Internal Thoracic Artery Harvest for Coronary Artery Bypass Grafting
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a
Department of Medical Imaging, The Ottawa Hospital, University of Ottawa, Ottawa Hospital Research Institute, Ottawa, Ontario, Canada K1H 8L6 Department of Surgery – Cardiac Surgery Division, University of Ottawa Heart Institute, University of Ottawa, Ottawa, Ontario, Canada K1Y 4W7
b
Received 14 September 2015; received in revised form 13 November 2015; accepted 14 November 2015; online published-ahead-of-print xxx
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[TD$FIRSNAME]Carole[TD$FIRSNAME.] [TD$SURNAME]Dennie[,TD$SURNAME.] MD, FRCPC a*, [TD$FIRSNAME]Yen-Yen[TD$FIRSNAME.] [TD$SURNAME]Gee[TD$SURNAME.], BA b, [TD$FIRSNAME] Anastasia[TD$FIRSNAME.] [TD$SURNAME]Oikonomou[TD$SURNAME.], MD a, [TD$FIRSNAME]Rebecca[TD$FIRSNAME.] [TD$SURNAME]Thornhill[TD$SURNAME.], PhD a, [TD$FIRSNAME] Fraser[TD$FIRSNAME.] [TD$SURNAME]Rubens[TD$SURNAME.], MD, MSc, FACS, FRCSC b
Background
Atelectasis is a significant complication after cardiac surgery. The current study was designed to assess the significance of atelectasis after bilateral internal thoracic artery (BITA) harvest.
Methods
The ICU admission chest x-ray of 565 patients undergoing BITA was reviewed. Linear regression modelling was used to assess the relationship between atelectasis and oxygenation as well as patient variables to length of ventilation and length of stay in the Intensive Care Unit (ICU).
Results
Eighty-nine patients (15.8%) had Grade 2/3 atelectasis which was significantly more common on the left as compared to the right (left 0.149 95% CI [0.119-0.178], right 0.027 95% CI [0.013-0.040], p<0.001). Grade 2/3 atelectasis on the right was associated with a significant drop in the pO2 (p=0.001) and the per cent O2fractional O2 (PF) ratio (p=0.002). Factors associated with increased ventilation time included presence of Grade 2/3 atelectasis (p=0.001) and peripheral vascular disease (PVD) (p<0.001), both of which were predictors of prolonged ICU length of stay (p=0.002 and p<0.001 respectively).
Conclusions
Early atelectasis is related to impaired oxygenation, prolonged ventilation and prolonged ICU stay. Future research should focus on strategies to minimise atelectasis and to determine if these changes translate into better patient outcomes.
Keywords
Anaesthesia Lung-other Perioperative issues and risk analysis Cardiac-other Coronary disease Extracorporeal circulation
Introduction Q2
Respiratory insufficiency remains a significant complication after coronary bypass graft (CABG) surgery. The aetiology of respiratory dysfunction is multifactorial however postoperative atelectasis is recognised as a common contributor
resulting in decreased lung compliance, increased pulmonary vascular resistance, impaired oxygenation [1] and an increased risk of postoperative pneumonia [1]. The incidence of atelectasis after heart surgery has been previously reported, however this data reflects older surgical strategies for CABG that may not be currently relevant, such
*Corresponding author at: Department of Medical Imaging, The Ottawa Hospital, University of Ottawa, Ottawa Hospital Research Institute, 501 Smyth Road, Box 232, Ottawa, Ontario, Canada K1H 8L6. Tel.: +613 761-4164; fax: +613 761-4476, Email:
[email protected] © 2015 Published by Elsevier Inc on behalf of Australian and New Zealand Society of Cardiac and Thoracic Surgeons (ANZSCTS) and the Cardiac Society of Australia and New Zealand (CSANZ).
Please cite this article in press as: Dennie C, et al. Clinical Correlation of Early Atelectasis after Bilateral Internal Thoracic Artery Harvest for Coronary Artery Bypass Grafting. Heart, Lung and Circulation (2015), http://dx.doi.org/10.1016/j. hlc.2015.11.004
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as the use of systemic hypothermia, older generation oxygenators and limited use of the internal thoracic artery as a conduit. This latter aspect may particularly influence lung function due to the potential contribution of injury to the phrenic nerve from dissection and pleural breach. The aim of our study was to determine perioperative characteristics that predict atelectasis in patients who have undergone CABG and to determine the clinical outcomes related to the presence and/or severity of postoperative atelectasis. We hypothesised that atelectasis is more common with pleural breach and topical myocardial cooling with cold slush and that the degree of atelectasis on the initial x-ray on admission to the ICU is a predictor of respiratory dysfunction as determined by measures of oxygenation and length of ventilation.
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Materials and Methods
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Ethics
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Our tertiary care cardiac centre has approval from its institutional research ethics board to anonymously publish data that are prospectively collected before and after coronary artery bypass grafting. As such, individual patient consent was waived. We retrospectively analysed prospectively collected data from the Peri-Operative Database Unit to identify patients undergoing CABG with bilateral internal thoracic artery (BITA) harvest. Between May 2, 2006 and October 23, 2012, 9166 patients underwent CABG of which 2393 cases were performed with the BITA approach. Patients were excluded if they had undergone other procedures such as valve replacement or arrhythmia surgery. A final cohort of 565 cases was selected. The database captures detailed information on preoperative, peri-procedural and postoperative variables for all patients undergoing cardiac surgery and it is maintained by a team of full-time data abstractors who are responsible for data collection and an ongoing audit process. Follow-up until death or discharge was 100% for all patients included in the study. Peripheral vascular disease (PVD) was defined as the presence of claudication with confirmation of lower limb vascular stenosis on Doppler, a history of peripheral vascular intervention, a history of abdominal aortic aneurysm or documented renal or subclavian stenosis. Blood gases were sampled within one hour of arrival in the ICU and the FiO2 at the time of sampling was recorded. The PF ratio was calculated as the ratio of the pO2 and the FiO2.
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Chest Radiography
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Posteroanterior and lateral chest radiographs were obtained preoperatively and prior to discharge from hospital. Supine anteroposterior (AP) radiographs were obtained within six hours of arrival in the ICU. Radiographs were interpreted by one of four cardiothoracic radiologists with seven to 20 years of experience (SA, AAJ, AO, CD). All were blinded to patient characteristics. To verify the reproducibility of the atelectasis
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Figure 1 Post-operative chest radiograph in a 63-year old woman depicts grade 1 atelectasis in the left lower lung zone (arrows).
scoring system, inter-observer reliability between two radiologists (SA, AAJ) was tested in 100 patients. Atelectasis was graded using a modified rating scale based on that described by Wilcox et al. [2]: grade 0, no atelectasis, grade 1, plate-like atelectasis or a basal opacity occupying or obscuring one third or less of the width of the ipsilateral hemidiaphragm (Figure 1), grade 2, basal opacity occupying or obscuring between one and two-thirds of the width of the hemidiaphragm (Figure 2) and grade 3, basal opacity occupying or obscuring over two-thirds of the hemidiaphragm or complete lobar collapse (Figure 3). In evaluating atelectasis,
Figure 2 Supine AP chest radiograph in a 55-year old man demonstrates grade 2 bibasilar atelectasis (arrows).
Please cite this article in press as: Dennie C, et al. Clinical Correlation of Early Atelectasis after Bilateral Internal Thoracic Artery Harvest for Coronary Artery Bypass Grafting. Heart, Lung and Circulation (2015), http://dx.doi.org/10.1016/j. hlc.2015.11.004
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Figure 3 Early post-operative AP supine chest radiograph in a 70-year old male depicts Grade 3 atelectasis in the left lower lung zone (arrows).
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the position of the hemidiaphragm and ipsilateral hilum were also taken into consideration. Grade 2/3 atelectasis was defined as atelectasis > grade 1.
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Statistical Analysis
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Continuous variables were reported as mean SD or median interquartile range for non-normally distributed continuous variables. Categorical variables were reported as counts and percentages. Student’s t tests or Wilcoxon ranksum tests were used to compare continuous variables. For categorical variables, chi-square or Fisher’s exact tests were
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used. Linear regression was used to assess the relationship between atelectasis and oxygenation and the PF ratio. The impact of patient variables and operative strategy on the length of ventilation and Intensive Care Unit (ICU) length of stay were assessed as continuous variables and their association to perioperative characteristics were assessed using univariable and multivariable linear regression models. For the multivariable analysis, the independent effect on these continuous time variables was assessed by controlling for characteristics that had an association in the univariable analysis (p<0.1). A p value <0.05 was considered significant. All statistical analyses and plots were performed with Stata1 version 13.1 (College Station, Texas).
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Results
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A total of 565 patients were included in the study. Interobserver reliability for atelectasis grade was greater on the left (kappa=0.75) as compared to the right (kappa=0.51). Eightynine of 565 patients (15.8%) had Grade 2/3 atelectasis on the Day 0 chest radiograph. Patient and perioperative characteristics of those with and without Grade 2/3 atelectasis are listed in Table 1. Patients who developed Grade 2/3 atelectasis had a greater incidence of NYHA Class III or IV heart failure (p=0.002), diabetes (p=0.035) and longer cardiopulmonary bypass (CPB) times (p=0.028). The proportion of patients with Grade 2/3 atelectasis was significantly higher on the left as compared to the right (left 0.149 95% CI [0.119-0.178], right 0.027 95% CI [0.013-0.040], p<0.001). There was no relationship between the use of slush on the left
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Table 1 Patient characteristics Variable
Gr 0, 1 atelectasis (476)
Gr 2, 3 atelectasis (89)
p
Age (years)
61.0 9.1
60.0 10.4
0.363
Female
85 (17.9)
14 (15.7)
0.628
27.9 4.4 139 16
28.2 4.7 139 17
0.649 0.849 0.702
BMI (kg/m2) Preop Hb (g/dL) Preop creatinine (mmol/L)
94 70
97 58
LVEF (%)
55 13
52 13
0.147
4 (0.8)
0 (0)
1.00
Redo Urgent/Emergent
196 (41)
36 (40)
0.898
Class III/IV CHF
34 (7.3)
12 (13.5)
0.002
OPCAB
90 (19.2)
16 (18.0)
0.789
PVD Diabetes
55 (11.7) 118 (25.2)
10 (11.2) 32 (35.0)
0.895 0.035
COPD
37 (7.9)
8 (9.0)
0.727
Smoking (current)
98 (20.9)
18 (20.2)
0.315
Total CPB time (min)
78.9 28.5
86.9 25.7
Number of distals Use of slush
0.028
3 (2,3)
3 (3,3)
0.581
320 (67.2)
59 (66.3)
0.863
Legend: Values given mean (%), mean standard deviation or median (IQ). Abbreviations: BMI – body mass index, Hb – haemoglobin, LVEF – left ventricular ejection fraction, OPCAB – off-pump coronary artery bypass grafting, COPD – chronic obstructive pulmonary disease, CPB – cardiopulmonary bypass.
Please cite this article in press as: Dennie C, et al. Clinical Correlation of Early Atelectasis after Bilateral Internal Thoracic Artery Harvest for Coronary Artery Bypass Grafting. Heart, Lung and Circulation (2015), http://dx.doi.org/10.1016/j. hlc.2015.11.004
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Table 2 Patient outcomes Variable
Table 4 Univariable/Multivariable Model – Variables tested univariable model length of ventilation and ICU length of stay
Gr 0, 1
Gr 2, 3
atelectasis
atelectasis
574 266
614 360
0.213
Post op LOS (days)
6 (5, 7)
6 (5, 7)
0.744
LOS ICU (days)
1 (0.88, 1.88)
1 (0.88, 2)
0.300
Length of
6.1 (4.5, 9.8)
6.8 (4.7, 11.8) 0.206
3 (0.6)
4 (4.5)
CT drainage (mL)
p
Variable
ventilation (hours) Post op pneumonia
0.003
Legend: Values given mean (%), mean standard deviation or median (IQ).
Grade 2/3 atelectasis COPD Age Smoking Priority BMI OPCAB
Abbreviations: CT – chest tube, LOS – Length of stay, ICU – Intensive care
PVD
unit.
Preop Hb Gender Diabetes Skeletonised
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(p=0.735) or the right (p=0.972) to the development of Grade 2/3 atelectasis. There was also no relationship between preservation of the pleura (as reflected by no chest tube) and Grade 2/3 atelectasis on either the left (OR 0.806 95% CI [0.306-2.121] p=0.663) or the right (OR 0.471 95% CI [0.060-3.670] p=0.472). Patient outcomes are listed in Table 2. Patients who developed Grade 2/3 atelectasis had a significantly increased risk of pneumonia (p=0.003). Whereas Grade 2/3 atelectasis on the left was not associated with compromise in oxygenation, Grade 2/3 atelectasis on the right was associated with a significant drop in pO2 (p=0.001) and a drop in the PF ratio (p=0.007) (Table 3, Figure 4). Factors in the univariable model are listed in Table 4. Factors associated with an increased ventilation time in the multivariable analysis included presence of Grade 2/3 atelectasis on either side and PVD. Both remained strong predictors of a longer length of postoperative ventilation (p=0.001 and p<0.001 respectively). There was a highly significant interaction between PVD and atelectasis resulting in prolonged ventilation (p<0.001). Similarly, when assessed with regards to ICU stay, Grade 2/3 atelectasis and PVD remained predictors of prolonged ICU length of stay (p=0.002 and p<0.001 respectively). The interaction between PVD and atelectasis was highly predictive of both prolonged ventilation (p<0.001) and prolonged ICU stay (p<0.001). Patients with PVD and atelectasis had an expected ventilation time of 156 hours (95%CI[95.3, 216.8]) as compared to 66.3 hours (95%CI[26.4, 106.2]) in PVD
Abbreviations: BMI – body mass index, Hb – haemoglobin, COPD – chronic obstructive pulmonary disease, PVD – peripheral vascular disease.
patients without atelectasis. Patients with PVD and atelectasis had an expected ICU stay of 7.8 days (95%CI[4.9, 10.8]) as compared to 4.8 days (95%CI[2.6, 7.0]) in PVD patients without atelectasis.
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Discussion
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The radiologic finding of severe (Grade 2/3) atelectasis after BITA grafting is relatively common, occurring in up to 16% of all patients on admission after CABG surgery. Factors associated with the development of atelectasis included advanced NYHA class, diabetes and increased CPB time. There was no relationship between the use of slush for topical cooling and the development of atelectasis. Severe atelectasis on the right was associated with a significant decrease in the pO2 and the PF ratio. Finally, severe atelectasis and the presence of PVD were both significantly related to prolonged ventilation and ICU stay. There are numerous factors contributing to atelectasis after cardiac surgery including impaired clearance of secretions, decreased mobility, gastric distention, intraoperative lung contusion and lack of postoperative positive end-expiratory
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Table 3 Atelectasis, Oxygenation and Partial Pressure-Fractional Inspired Oxygen Ratio (PF Ratio) b coefficient
95% CI
p
pO2
Left Right
-8.005 -19.396
-17.211, 1.201 -30.483, -8.309
0.088 0.001
PF Ratio
Left
-11.041
-29.994, 7.911
0.252
Right
-35.984
-58.845, -13.128
0.002
Please cite this article in press as: Dennie C, et al. Clinical Correlation of Early Atelectasis after Bilateral Internal Thoracic Artery Harvest for Coronary Artery Bypass Grafting. Heart, Lung and Circulation (2015), http://dx.doi.org/10.1016/j. hlc.2015.11.004
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pressure (PEEP) while on CPB [2]. Investigators have reported a higher incidence of left-sided as compared to the right-sided atelectasis after cardiac surgery [3,4]. It has been suggested that left-sided prevalence relates to intraoperative injury to the left phrenic nerve due to the use of ‘‘slush’’ for topical hypothermia but analysis of phrenic nerve function postoperatively has not confirmed significant paresis [2]. The present study also did not find that the use of ‘‘slush’’ was associated with the development of severe atelectasis (as compared to 4 8C cold liquid saline poured over the heart). On the other hand, it was apparent in the current study that the clinical impact of atelectasis, as reflected by impairment of gas exchange, was greater on the right than the left. Although we can only speculate, we propose that this may relate to the larger relative volume of the right lung in the basal segments. The strong interaction between PVD and atelectasis in the outcomes of prolonged ventilation and ICU stay point to the clinical relevance of this patient factor in cardiac surgery. Vascular disease is often strongly correlated to other organ dysfunction and we have also demonstrated that PVD is strongly correlated to sternal wound infections in this patient cohort [5]. This suggests that tests designed to assess interventions to prevent atelectasis should be targeted at this subpopulation to demonstrate maximal clinical impact. Other technical factors unique to cardiac surgery that have been suggested to predispose to atelectasis include direct mechanical phrenic nerve injury and pleural breach related to internal thoracic artery (ITA) harvest [6]. In the present study the degree of atelectasis was evaluated in patients on admission to the ICU when they were still on positive pressure ventilation and thus phrenic function or dysfunction would not be contributory. Further, it would be anticipated that the incidence of phrenic nerve damage after BITA harvest should be the same on both sides. As there was a left predominance, this suggests that phrenic nerve involvement is unlikely to be causative. There was also no difference in the incidence of severe atelectasis if pleural breach had occurred as determined by the need for a pleural tube. Both of these factors could play a role in atelectasis at later stages due to decreased lung volumes in the former and inhibited inspiration due to pain in the latter, however they would not contribute to early atelectasis in the fully ventilated patient. Finally, we did not demonstrate that an off-pump approach impacted on the degree of atelectasis. This finding is consistent with other reports [7] in which only minimal differences in plate-like atelectasis were seen. Based on this, it is not apparent that conventional ventilation strategies during coronary surgery prevent collapse. The predictable relationship between severe atelectasis and impaired gas exchange, prolonged ventilation and prolonged ICU stay supports atelectasis as an important target for interventions designed to improve perioperative care. For example, the open lung approach refers to a strategy to utilise recruitment manoeuvers with sufficient PEEP to increase transpulmonary pressure to maintain open the maximum possible number of alveoli with the minimum delta pressure (Pplateau – PEEP) while preventing over distension [8,9].
Authors have also recommended continued ventilation during CPB as apnoea results in microatelectasis, pulmonary oedema and poor compliance. This latter approach has been supported by the demonstration of improved outcomes in one randomised controlled trial [10] however these findings have been challenged in a systematic review [11]. Finally early extubation has been proposed as an effective strategy [12] that may also minimise respiratory insufficiency by rapid patient mobilisation and minimised sedation. An important limitation of the current study is that it cannot delineate if unreported protective strategies utilised intraoperatively by individual anaesthetists (such as forceful bagging prior to weaning) may play a role in the incidence of this problem. Also, although the study showed an association between atelectasis and ventilator and ICU outcomes, it could not prove if this was causative, nor could it determine if preventing the atelectasis would result in improved outcomes.
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Conclusions
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This study has demonstrated that severe atelectasis after BITA harvest has a left-sided predominance, however right-sided atelectasis, when present, is associated with greater changes in oxygenation. Topical slush, pleural breach and direct phrenic damage were not determined to be factors in the development of early atelectasis after cardiac surgery. Clinical trials are warranted to test strategies that may prevent perioperative atelectasis and to determine if this improvement is associated with changes in the length of required ventilation and ICU stay in this population.
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Acknowledgements
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We would like to acknowledge Subhapradha Anand MD (SA) and Abdullah Al Jebreen MD (AAJ) for their contribution to chest radiographic interpretation. This original research has received no external financial support.
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Please cite this article in press as: Dennie C, et al. Clinical Correlation of Early Atelectasis after Bilateral Internal Thoracic Artery Harvest for Coronary Artery Bypass Grafting. Heart, Lung and Circulation (2015), http://dx.doi.org/10.1016/j. hlc.2015.11.004
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