Journal of Clinical Monitoring and Computing (2020) 34:559–566 https://doi.org/10.1007/s10877-019-00350-8 ORIGINAL RESEARCH Early changes in diaphragmatic function evaluated using ultrasound in cardiac surgery patients: a cohort study António Tralhão1,5 · Pedro Cavaleiro1,6 · Mattia Arrigo1,7 · Jean‑Paul Lopes1 · Marion Lebrun1 · Mercedes Rivas‑Lasarte1,8 · Françoise Le Pimpec‑Barthes2,4 · Christian Latrémouille3,4 · Paul Achouh3,4 · Romain Pirracchio1,4 · Bernard Cholley1,4 Received: 25 March 2019 / Accepted: 1 July 2019 / Published online: 5 July 2019 © Springer Nature B.V. 2019 Abstract Little is known about the evolution of diaphragmatic function in the early post-cardiac surgery period. The main purpose of this work is to describe its evolution using ultrasound measurements of muscular excursion and thickening fraction (TF). Single-center prospective study of 79 consecutive uncomplicated elective cardiac surgery patients, using motion-mode during quiet unassisted breathing. Excursion and TF were measured sequentially for each patient [pre-operative (D1), 1 day (D2) and 5 days (D3) after surgery]. Pre-operative median for right and left hemidiaphragmatic excursions were 1.8 (IQR 1.6 to 2.1) cm and 1.7 (1.4 to 2.0) cm, respectively. Pre-operative median right and left thickening fractions were 28 (19 to 36) % and 33 (22 to 51) %, respectively. At D2, there was a reduction in both excursion (right: 1.5 (1.1 to 1.8) cm, p < 0.001, left: 1.5 (1.1 to 1.8), p = 0.003) and thickening fractions (right: 20 (15 to 34) %, p = 0.021, left: 24 (17 to 39) %, p = 0.002), fol- lowed by a return to pre-operative values at D3. A positive moderate correlation was found between excursion and thickening fraction (Spearman’s rho 0.518 for right and 0.548 for left hemidiaphragm, p < 0.001). Interobserver reliability yielded a bias below 0.1 cm with limits of agreement (LOA) of ± 0.3 cm for excursion and − 2% with LOA of ± 21% for thickening fractions. After cardiac surgery, the evolution of diaphragmatic function is characterized by a transient impairment followed by a quick recovery. Although ultrasound diaphragmatic excursion and thickening fraction are correlated, excursion seems to be a more feasible and reproducible method in this population. Keywords Diaphragm · Cardiac surgery · Ultrasound · Excursion, thickening List of abbreviations CABG Coronary artery bypass grafting COPD Chronic obstructive pulmonary disease António Tralhão and Pedro Cavaleiro have equally contributed to this work. cm Centimeter(s) DE Diaphragmatic excursion Electronic supplementary material The online version of this h Hours article (https​://doi.org/10.1007/s1087​7-019-00350​-8) contains supplementary material, which is available to authorized users. * António Tralhão Ocidental, Av. Professor Doutor Reinaldo dos Santos, atralhao@gmail.com 2790‑134 Carnaxide, Portugal 6 1 Present Address: Intensive Care Department, Centro Department of Anesthesia and Intensive Care, Hôpital Hospitalar Universitário do Algarve, Hospital de Faro, Faro, Européen Georges Pompidou, AP-HP, Paris, France Portugal 2 Department of Thoracic Surgery, Hôpital Européen Georges 7 Present Address: Department of Cardiology, University Heart Pompidou, AP-HP, Paris, France Center, University Hospital Zurich, Zurich, Switzerland 3 Department of Cardiac Surgery, Hôpital Européen Georges 8 Present Address: Cardiology Department, Hospital de Pompidou, AP-HP, Paris, France la Santa Creu i Sant Pau, Biomedical Research Institute 4 Université Sorbonne-Paris-Cité, Paris, France IIB‑Sant Pau, Universidad Autónoma de Barcelona, 5 Barcelona, Spain Present Address: Department of Cardiology, Hospital de Santa Cruz, Centro Hospitalar de Lisboa 13 Vol.:(0123456789) 560 Journal of Clinical Monitoring and Computing (2020) 34:559–566 LOA Limits of agreement study. Ethical approval for this study was provided by the M Motion local ethics committee (Comité d’éthique pour la recherche MHz Megahertz en Anesthésie—Réanimation, IRB 00010254). mm Millimeter(s) TF Thickening fraction 2.1 Patients and procedures US Ultrasound Patients over 18 years of age undergoing elective cardiac surgery via sternotomy with normothermic cardiopulmo- 1 Introduction nary bypass were eligible for inclusion. Exclusion criteria were: (a) hemodynamic instability or respiratory distress Impaired diaphragmatic function following cardiac surgery precluding quiet spontaneous breathing during the first 48 due to mechanical or hypothermal damage to the phrenic postoperative hours (h) (b) thoracotomy and (c) absence of nerve has been well described [1–4]. Although moderate informed consent. All procedures were performed under in most cases, up to 6% of patients may suffer more severe general anesthesia and cardiopulmonary bypass. Clinical forms of diaphragmatic dysfunction leading to prolonged variables and surgical related details such as the optional mechanical ventilation and associated pulmonary complica- use of topical hypothermia (“slushed ice”) and whether one tions [5]. But apart from clinically relevant diaphragmatic or two internal thoracic arteries were employed during coro- dysfunctions, little is known about the natural course of nary bypass grafting were recorded. diaphragmatic function in the early post-operative period. Providing such description would help to better understand 2.2 Ultrasound measurements the impact of cardiac surgery on diaphragm function. Among the different tools to assess diaphragm perfor- Excursion and thickness of both hemidiaphragms were mance, ultrasound (US) techniques have gained an increas- measured sequentially in each patient at three different time ingly prominent role as a non-invasive bedside imaging points: (D1)—pre-operatively (the day before surgery), modality due to their simplicity, non-invasiveness, feasibil- (D2)—within the first 48 h after extubation and (D3)— ity and reproducibility [6–9]. US measurements have also between 96 and 174 h after extubation. The number of hours shown good correlation with the reference method, i.e., between extubation and each exam was recorded. transdiaphragmatic pressure measurement, whose semi-inva- All examinations were performed at bedside with the sive nature, complexity and expertise requirement compare patient in a 45° semi-recumbent position during quiet, unas- unfavorably against echography in daily clinical use [6]. sisted breathing. A commercially available US platform Currently, US evaluation of the diaphragm is based on (Philips CX50 CompactXtreme®) connected to a 2.5–3.5 regional excursion and thickening measurements, mainly Megahertz (MHz) phased-array transducer (excursion) or through a lateral thoracic or subcostal approach [6, 7]. a 3–12 MHz linear transducer (thickness) was used, with Although previous studies have established the range of nor- simultaneous display of electrocardiogram and thoracic mal values for these two indices, their feasibility and repro- impedance, to help in identifying each phase of the respira- ducibility was never compared in cardiac surgery patients tory cycle. [8, 10]. DE was evaluated using anatomical motion (M)-mode The primary aim of this study was to compare the excur- through a lateral approach from the mid-axillary line as sion and thickening of the diaphragm before and after car- previously described [6, 11]. Imaging was obtained and diac surgery, by analyzing bilateral diaphragmatic excur- recorded using a slow scrolling display speed [< 25 mm sion (DE) and thickening fraction (TF) during spontaneous (mm) per second], allowing the analysis (from end-expi- breathing. In addition, we compared the reproducibility and ration to end-inspiration), measurement and average of 3 feasibility of both measurements. consecutive respiratory cycles on the same screen (Fig. 1a). Imaging quality check included regularity in amplitude and frequency of the DE and visibility of the diaphragmatic line 2 Materials and methods throughout the respiratory cycle. In each patient, to ensure that all measurements were made from the same acoustic This was a single center study conducted prospectively at a window, the distance between probe placement and the tertiary university-affiliated hospital, between October and lower extremity of the ribcage on the mid-axillary line was December 2015. All consecutive patients admitted to the measured and used as the reference site for the subsequent Cardiac Surgical Department prior to elective cardiac sur- exams. Under normal quiet breathing conditions, hemidi- gery were screened for enrollment. Informed consent was aphragm dysfunction was defined as an excursion < 1 cm obtained from all individual participants included in the (cm) downwards during inspiration, and diaphragmatic 13 Journal of Clinical Monitoring and Computing (2020) 34:559–566 561 thickness values, measured in mm. We further calculated TF as: Inspiratory thickness −expiratory thickness TF = × 100 Expiratory thickness Exams were performed individually by experienced operators (AT, PC, MA, JPL, ML, MRL). In order to meas- ure interoperator reliability, the first 20 patients had their examinations at D1, D2 and D3 performed twice, by two different operators (AT, PC, MA). The first operator selected the best acoustic window and registered the measurement site as described above. The order of the operators and of each hemidiaphragm evaluation was randomized using a computer-generated sequence. 2.3 Statistical analysis Results are reported as mean ± standard deviation, median (IQR 25th to 75th percentiles) or number (proportion). Continuous variables were compared using Wilcoxon’s signed-rank test. Comparison between repeated measures was performed using Friedman’s test. Spearman correla- tion coefficient (rho) was used to evaluate the correlation between variations in diaphragmatic excursion and TF. The Chi square test, Mann–Whitney’s U or t test were used for univariate analysis of diaphragmatic dysfunction occurrence, Fig. 1  a Diaphragmatic excursion obtained using anatomical as appropriate. The Bland and Altman method for repeated M-Mode with a 2.5–3.5 MHz transducer. Measurements (dotted lines measurements was performed to describe the interoperator between cursors) were obtained over 3 consecutive respiratory cycles. reliability for both excursion and thickness measurements The yellow line corresponds to variations in thoracic impedance with [12]. A p-value smaller than 0.05 was used to define statisti- respiration. b Diaphragmatic thicknesses (distance between vertically placed cursors) measured using regular M-Mode with a 3–12 MHz cal significance. All analyses were performed using SPSS transducer at end-expiration and end-inspiration. Measurements were 22.0 (IBM, Chicago, IL) and Stata (Release 14. College Sta- obtained at end-expiration (minimal thickness) and end-inspiration tion, TX: StataCorp LP). (maximal thickness) over 3 consecutive respiratory cycles. The yel- low line corresponds to variations in thoracic impedance with respira- tion 3 Results paralysis corresponded to an absence of motion (0 cm) or a paradoxical motion (diaphragmatic ascension during inspi- The study flowchart is presented in Fig. 2. Patient charac- ration) [8]. teristics are presented in Table 1. Median time to diaphragm Hemidiaphragm thickness imaging was performed at evaluation was 19 (13 to 29) h after extubation for D2 and the point where the muscle fibers make contact with the 120 (114 to 136) h after extubation for D3. rib cage, between the 8th and 10th intercostal spaces on the mid-axillary line, the so-called zone of apposition, angling 3.1 Diaphragmatic excursion the ultrasound beam close to 90° [10].Correct measurement requires proper recognition of both pleural and peritoneal DE measurements were obtained in all 79 patients for D1, 67 leaflets as continuous hyperechoic lines surrounding the patients for D2 and 70 patients for D3. 67 patients (85%) had structure of interest. The diaphragmatic muscle layer was measurements obtained at all the 3 pre-specified time points. then measured between the pleura and peritoneum at both Median baseline excursion at D1 was not significantly differ- end-inspiration and end-expiration using regular M-mode, ent between the right and the left hemidiaphragms (1.8 (1.6 and the values averaged over 3 consecutive respiratory to 2.1) cm versus 1.7 (1.4 to 2.0) cm, p = 0.06). A significant cycles (Fig. 1b). Hemidiaphragm thickening was defined as time-variation of DE (Fig. 3) was found for both right and the difference between end-inspiratory and end-expiratory left hemidiaphragms (p < 0.001 for right, p = 0.032 for left 13 562 Journal of Clinical Monitoring and Computing (2020) 34:559–566 unilateral diaphragmatic paralysis was noted in 4 (5.8%) patients at D2 (all persistent) and in 1 (1%) additional patient at D3. 3.3 Diaphragmatic thickening fraction Diaphragmatic thickness measurements were obtained in 57 patients at D1 and 42 patients at D2 and D3 (no measure in 10 patients due to US machine unavailability and in 27 patients due to poor acoustic window). 42 patients (53%) had measurements obtained at all 3 pre-specified time points. Median right and left hemidiaphragm thickness was 1.8 (1.6 to 2.0) mm and 1.8 (1.5 to 2.1) mm at D1, respectively. Median TF at baseline was significantly different between the right and left hemidiaphragms (28 (19 to 36) % versus. 33 (22 to 51) %, p = 0.015). Similarly to excursion, we found a significant time-var- iation of TF after surgery (p = 0.039 for right, p = 0.046 for left hemidiaphragm, Fig. 4). Using D1 as the reference, a smaller TF was observed at D2 (20 (15 to 34) %, p = 0.021 for the right, and 24 (17 to 39) %, p = 0.002 for the left hemidiaphragm). This was again followed by an increase to near pre-operative levels at D3 (29 (18 to 37) %, p = 0.84 for the right, and 29 (19 to 50) %, p = 0.20 for the left hemidi- aphragm) vs. D1.Correlation between excursion and TF Considering D1 values as the reference, a positive moder- ate monotonic correlation was found between measurements in both hemidiaphragms (Spearman’s rho 0.518 for the right; Spearman’s rho 0.548 for the left hemidiaphragm, both p values < 0.001, Supplementary Figs. S1 and S2). When D2 values were used as a reference, a similar result was found Fig. 2  Study flowchart from D2 to D3, but with a weaker correlation (Spearman’s rho 0.293, p = 0.046 for the right; Spearman’s rho 0.384, p value = 0.036 for the left hemidiaphragm, Supplementary hemidiaphragm, Friedman’s test). Using D1 as the reference, Figs. S3 and S4). a shorter excursion was observed on D2, for right (1.5 (1.1 to 1.8) cm, p < 0.001) and left hemidiaphragms (1.5 (1.1 to 3.4 Interobserver reliability 1.8), p = 0.003), followed by a return to near-baseline values on D3 (1.8 (1.4 to 2.0) cm, p = 0.204 for the right; 1.6 (1.4 Interobserver reliability was analyzed using a Bland and Alt- to 2.1) cm, p = 0.323 for the left hemidiaphragm) vs. D1. man representation on 54 pairs of measurements for excur- Median reduction in DE measured at D2 was 0.5 (0.0 to sion (Fig. 5), which yielded a bias below 0.1 cm with limits 0.8) cm and 0.2 (− 0.2 to 0.8) cm for right and left hemidi- of agreement (LOA) of ± 0.3 cm. For TF (37 pairs of meas- aphragms, respectively. urements), we obtained a bias of -2% with LOA of ± 21% (Fig. 6). 3.2 Hemidiaphragmatic dysfunction or paralysis 3.5 Subgroup analysis Considering the threshold value of 1.0 cm, diaphragmatic dysfunction was present in 25 (36%) patients at D2—4 We analyzed the incidence of diaphragmatic dysfunction patients with bilateral dysfunction and 21 patients with according to different variables such as age, gender, coro- unilateral dysfunction (12 right-sided, 9 left-sided), which nary artery bypass grafting (CABG) versus other types of persisted on D3 in 8 (12%) patients—all unilateral (1 right- surgery, use of two internal thoracic arteries versus one in sided, 8 left-sided). New onset of diaphragmatic dysfunc- CABG patients and use of topical hypothermia versus no tion after D2 was observed in 1 (1%) patient. New onset hypothermia. None of these variables had a statistically 13 Journal of Clinical Monitoring and Computing (2020) 34:559–566 563 Table 1  Patient characteristics (n = 79) Age (years) [mean (SD)] 62 (14) Male gender 54 (68) Weight (kg) (median [25th–75th percentiles]) 74 [62−83] Height (m) [mean (SD)] 1.7 (0.1) Body mass index (kg/m2) [mean (SD)] 26 (4.7) Body surface area ­(m2) [mean (SD)] 1.9 (0.3) COPD Type of surgery 4 (5) Valvular 36 (42) Coronary 25 (32) Aortic 2 (3) Combined 13 (17) Other 3 (2) Internal thoracic artery use in CABG (isolated or combined) One 31 (63) Two 18 (37) Cardiopulmonary bypass time (min) [mean (SD)] 107 (53) Aortic cross clamp time (min) [mean (SD)] 74 (43) Logistic EUROSCORE I (%) (median [25th–75th percentiles]) 3.5 [2.0−6.2] ASA score 2 16 (20) 3 57 (72) 4 6 (8) Ventilation duration (h) (median [25th–75th percentiles]) 11 [8−18] Use of catecholamines 22 (28) Extra-corporeal life support 1 (1) Renal replacement therapy 2 (3) NIPV after extubation 4 (5) Values are presented as number (percentage), unless otherwise indicated ASA American Society of Anesthesiologists; NIPV non-invasive positive-pressure ventilation, SD standard deviation, COPD chronic obstructive pulmonary disease significant association with the occurrence of post-operative on time to ventilator weaning, extubation success and inten- diaphragmatic dysfunction (Supplementary Table S1). sive care unit length of stay [1–3]. Hitherto, there have been several studies analyzing the incidence and predictors of dia- phragmatic dysfunction in this population using a variety of 4 Discussion methods, but only a few have used US techniques [4–6]. As for any variable of interest, it is crucial to define normality, In a population of consecutive, elective cardiac surgery as this forms the basis for a correct diagnosis and prognosis. patients undergoing planned sternotomy, we have been able Boussuges et al. have previously set the DE threshold to to describe the time course of diaphragmatic function during define diaphragmatic dysfunction [8]. However, the dynamic spontaneous breathing by comparing it with the preoperative characterization of diaphragm mechanics after cardiac sur- state. In this regard, our results can be summarized as fol- gery has not been described yet. lows: (1) immediate post-operative diaphragmatic function We observed a consistent pattern of global diaphragm is almost always reduced, (2) the nature of diaphragmatic excursion reduction [median − 0.4 (− 0.8 to 0.1) cm] 48 h dysfunction is transient in the majority of cases and shows after surgery. After this apparent diaphragm “stunning”, a a recovery by the 5th post-operative day, (3) diaphragmatic rapid normalization to pre-operative values for right and US assessment is both feasible and reproducible but (4) dia- left excursion ensued. In 36% of these patients, the reduc- phragm excursion seems to be superior to thickening for tion in DE was seemingly severe enough to be graded as bedside assessment. “dysfunction” according to current criteria [8]. Neverthe- Diaphragmatic dysfunction is clinically relevant in car- less, this greater reduction in excursion was also transient diac surgery patients owing to a potentially negative impact and showed rapid recovery by D3. Based on a clinical 13 564 Journal of Clinical Monitoring and Computing (2020) 34:559–566 Fig. 3  Time variation of diaphragmatic excursion for right and left Fig. 4  Time variation of diaphragmatic thickening fraction for right hemidiaphragms and left hemidiaphragms uneventful course for our patient population, such dysfunc- obtain our values by averaging 3 consecutive respiratory tion is probably benign in nature. Moreover, this altera- cycles, thereby avoiding selection bias. tion in diaphragmatic function, even in case of unilateral In our analysis, we found a similar dynamic profile diaphragmatic paralysis, was not associated with clinical between muscular excursion and thickening. Diaphrag- signs of respiratory impairment. matic thickening during inspiration has the theoretical Studies on diaphragmatic function focusing on cardiac advantage of better reflecting the active contraction of mus- surgery patients with an uneventful course are scarce. cle bundles [13]. While this may hold true in mechanically Lerolle et al. studied the diaphragm of patients with dif- ventilated patients [13], such difference was not apparent ficult weaning from mechanical ventilation and a com- from our study. Moreover, since obtaining appropriate parator group of patients extubated within 12 h post- acoustic windows for thickening imaging can be quite dif- operatively [6]. Among patients from the latter group, ficult and sometimes even impossible (34% failure rate in a reduction in DE was also encountered on the 2nd or our cohort), excursion appears as an easier measurement 3rd post-operative day [6]. However, some differences to assess the function of the diaphragm in spontaneously with respect to the present study should be noted. Excur- breathing patients. To further compare both methodologies, sion measurements were made between forced expiration we undertook a reproducibility sub-study, evaluating excur- and maximal inspiration requiring patient’s cooperation, sion and thickening measured twice in the same patients by whereas we studied patients breathing normally, without two different operators. Visual analysis and numerical com- effort. This accounts for the difference between a − 40% parison show that both methods are reproducible, although reduction in diaphragmatic excursion decrease observed they seem to suggest that excursion is a more reproducible in the study by Lerolle et al. [6] and the one found in metric of diaphragm function than thickening. Previous this study (− 17%). We chose to avoid forced inspiration authors found a good reproducibility for each parameter because the ability to mobilize a vital capacity in the post- when measured individually [8, 10].The small disparity we operative period is impaired by postoperative pain and is encountered may be a reflection of the difference between highly variable among patients. This also allowed us to the magnitude of excursion (centimeters) and thickening 13 Journal of Clinical Monitoring and Computing (2020) 34:559–566 565 Fig. 5  Bland-Altman plot: representation of the agreement between paired diaphragmatic excursion measurements obtained by two different opera- tors Fig. 6  Bland-Altman plot: representation of the agreement between paired diaphragmatic thickening fraction measure- ments obtained by two different operators (millimeters) measurements. Due to the very small values in the percentage of thickening. Finally, the correlation of of diaphragm thicknesses, any inaccuracy in the placement diaphragmatic thickness and excursion was moderate. This of the cursors can result in proportionately greater errors finding may be interpreted as another reason to use excursion 13 566 Journal of Clinical Monitoring and Computing (2020) 34:559–566 instead of thickening to assess diaphragmatic function due to Research involving human participants and/or animals All procedures the inherent measurement errors with the latter. performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research Our study has a number of strengths. First, and to the best committee (Comité d’éthique pour la recherche en Anesthésie—Réani- of our knowledge, this is the first study to describe the natu- mation, IRB 00010254) and with the 1964 Helsinki declaration and its ral course of diaphragmatic function in consecutive elective later amendments or comparable ethical standards. cardiac surgery patients using US as the assessment tool. Informed consent Informed consent was obtained from all individual Second, we have described how the diaphragm behaves after participants included in the study. planned sternotomy using serial measurements, demonstrat- ing a transient postoperative dysfunction of the main respira- tory muscle, even in asymptomatic patients. Third, we have also added to the work of previous authors by demonstrating References that such evaluation is both feasible and reproducible in this 1. McCool FD, Tzelepis GE. Dysfunction of the diaphragm. N Eng particular subset of patients. J Med. 2012;366:932–42. 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