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The Effect of Deep Versus Moderate Neuromuscular Block on Surgical Conditions and Postoperative Respiratory Function in Bariatric Laparoscopic Surgery: A Randomized, Double Blind Clinical Trial

Baete, Sam MD*; Vercruysse, Gerd MD*; Vander Laenen, Margot MD*; De Vooght, Pieter MD*; Van Melkebeek, Jeroen MD*; Dylst, Dimitri MD*; Beran, Maud MD*; Van Zundert, Jan MD, PhD*; Heylen, René MD, PhD*; Boer, Willem MD*; Van Boxstael, Sam MD*; Fret, Tom MD*; Verhelst, Hans MD; De Deyne, Cathy MD, PhD*‡; Jans, Frank MD, PhD*‡; Vanelderen, Pascal MD, PhD*‡

doi: 10.1213/ANE.0000000000001801
Anesthetic Clinical Pharmacology: Original Clinical Research Report
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BACKGROUND: In recent literature, it has been suggested that deep neuromuscular block (NMB) improves surgical conditions during laparoscopy; however, the evidence supporting this statement is limited, and this was not investigated in laparoscopic bariatric surgery. Moreover, residual NMB could impair postoperative respiratory function. We tested the hypotheses that deep NMB could improve the quality of surgical conditions for laparoscopic bariatric surgery compared with moderate NMB and investigated whether deep NMB puts patients at risk for postoperative respiratory impairment compared with moderate NMB.

METHODS: Sixty patients were evenly randomized over a deep NMB group (rocuronium bolus and infusion maintaining a posttetanic count of 1–2) and a moderate NMB group (rocuronium bolus and top-ups maintaining a train-of-four count of 1–2). Anesthesia was induced and maintained with propofol and remifentanil. The primary outcome measures were the quality of surgical conditions assessed by a single surgeon using a 5-point rating scale (1 = extremely poor, 5 = optimal), the number of intra-abdominal pressure increases >18 cmH2O and the duration of surgery. Secondary outcome measure was the postoperative pulmonary function assessed by peak expiratory flow, forced expiratory volume in 1 second, and forced vital capacity, and by the need for postoperative respiratory support. Data are presented as mean ± standard deviation with estimated treatment effect (ETE: mean difference [95% confidence interval]) for group comparisons.

RESULTS: There was no statistically significant difference in the surgeon’s rating regarding the quality of the surgical field between the deep and moderate NMB group (4.2 ± 1.0 vs 3.9 ± 1.1; P = .16, respectively; ETE: 0.4 [−0.1, 0.9]). There was no difference in the proportional rating of surgical conditions over the 5-point rating scale between both groups (P = .91). The number of intra-abdominal pressure increases >18 cmH2O and the duration of surgery were not statistically different between the deep and moderate NMB group (0.2 ± 0.9 vs 0.3 ± 1.0; P = .69; ETE: −0.1 [−0.5, 0.4] and 61.3 ± 15.1 minutes vs 70.6 ± 20.8 minutes; P = .07, ETE: −9.3 [−18.8, 0.1], respectively). All the pulmonary function tests were considerably impaired in both groups when compared with baseline (P < .001). There was no statistically significant difference in the decrease in peak expiratory flow, forced expiratory volume in 1 second, and forced vital capacity (expressed as % change from baseline) between the deep and the moderate NMB group.

CONCLUSIONS: Compared with a moderate NMB, there was insufficient evidence to conclude that deep NMB improves surgical conditions during laparoscopic bariatric surgery. Postoperative pulmonary function was substantially decreased after laparoscopic bariatric surgery independently of the NMB regime that was used. The study is limited by a small sample size.

Published ahead of print January 19, 2017.

From the Departments of *Anesthesiology and Abdominal Surgery, Intensive Care Medicine, Emergency Care and Pain Clinic, Ziekenhuis Oost-Limburg, Genk; and Faculty of Medicine and Life Sciences, Hasselt University, Diepenbeek, Belgium.

Published ahead of print January 19, 2017.

Accepted for publication October 27, 2016.

Funding: This study was funded by Merck, Sharpe & Dohme (Grant Number: 8646-085 MISP40977).

Conflicts of Interest: See Disclosures at the end of the article.

Address correspondence to Pascal Vanelderen, MD, PhD, Department of Anesthesiology, Intensive Care Medicine, Emergency Care and Pain Clinic, Ziekenhuis Oost-Limburg, Schiepse Bos 6, 3600 Genk, Belgium. Address e-mail to pascal.vanelderen@gmail.com.

Laparoscopic bariatric surgery poses special demands on the anesthesiologist and surgeon. The surgeon requires a good visualization of the surgical field to perform the operation, whereas the anesthesiologist is concerned with adequate postoperative respiratory function in these morbidly obese patients. In recent literature, it is has been suggested that deep neuromuscular block (NMB) improves surgical conditions during laparoscopy. The evidence supporting this statement, however, is limited1 and pertains mainly to laparoscopic surgery for cholecystectomy,2,3 gynecologic,4,5 and urologic6 disorders. The “pro/con” debate pertaining to the advantages of deep NMB is still ongoing.7,8 Because laparoscopy significantly reduces the time span for recovery from intraoperative NMB, deep NMB puts the patient at risk for residual postoperative NMB and associated respiratory complications.

Jones et al9 found that recovery from a rocuronium-induced posttetanic count (PTC) of 1 to 2 to a train-of-four ratio (TOFR) of 0.9 with a single dose of neostigmine 70 μg/kg takes 50 minutes, which is considerably longer than the time interval from the end of pneumoperitoneum to the end of skin closure. Even minimal residual NMB with a TOFR of 0.8 is associated with impaired respiratory function, as witnessed by reductions of forced expiratory volume in 1 second (FEV1) and forced vital capacity (FVC) in healthy volunteers.10,11 Moreover, a postoperative TOFR <0.7 may be associated with adverse events.12–14

Obese patients are at an even greater risk for these postoperative respiratory complications. In a recent study, 100% of patients after bariatric surgery had at least one hypoxic event (oxygen saturation <90% for more than 30 seconds).15 Restrictive ventilatory defects clearly are associated with body mass index (BMI) and obesity hypoventilation syndrome. Because respiratory failure is responsible for 12% of mortalities after bariatric surgery, optimal respiratory care for these patients is of primary importance.16 Adequate reversal of NMB plays an important role herein. Sugammadex is a cyclodextrin molecule that encapsulates and inactivates rocuronium and vecuronium, allowing a dose-dependent reversal of deep NMB within 5 minutes.9 A first indication that deep NMB and reversal with sugammadex could be beneficial in morbidly obese patients recently was presented by Carron et al17 in a high-risk cardiac patient undergoing a laparoscopic gastrectomy.

In the present randomized, double-blind, clinical trial, we build on these findings and are the first to test the hypotheses that deep NMB could improve the quality of surgical conditions for laparoscopic bariatric surgery compared with moderate NMB. The primary objective of this study was to analyze the effect of deep NMB on surgical conditions (using a 5-point rating scale, the number of intra-abdominal pressure rises >18 cmH2O, and the duration of surgery) compared with a moderate NMB. Because deep NMB puts patients at risk for residual postoperative NMB, we tested a second hypothesis that deep NMB could decrease postoperative pulmonary function. Therefore, the secondary objective was to analyze the effect of deep NMB on peak expiratory flow (PEF), FEV1, and FVC compared with moderate NMB and to assess the need for postoperative respiratory support. This study was funded by a grant from Merck, Sharp & Dohme (grant nr. 8646-085 MISP40977).

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METHODS

Study Design

In this single-center, randomized, double-blind, clinical trial, we investigated the effect of deep versus moderate NMB with rocuronium on surgical conditions and postoperative respiratory function. The trial was conducted at the Ziekenhuis Oost-Limburg after approval by the local ethics committee (Comité Medische Ethiek Ziekenhuis Oost-Limburg) and was registered on clinicaltrials.gov (registration number: NCT01748643) and EudraCT (registration number: 2012-005533-37) before patient enrollment. The study started in April 2013 and ended in January 2015 when the objective of 60 enrolled patients had been reached. Written informed consent was obtained from all patients before inclusion in the trial.

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Participants

Table 1

Table 1

Patients were recruited from a multidisciplinary weight-loss program in our hospital. Eligible patients were older 18 years of age and were obese or morbidly obese as defined by a BMI of >30 kg/m2 and >40 kg/m2, respectively, and were scheduled to undergo a laparoscopic gastric bypass surgery. Patients with an American Society of Anesthesiologist physical status class IV or greater were excluded from the study. Inclusion and exclusion criteria are presented in Table 1.

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Interventions

The surgical and anesthesia technique were the same for both study groups except for maintaining and reversing NMB. In the deep NMB-group, a PTC of 1 to 2 twitches was maintained, and NMB was reversed with sugammadex at the end of surgery. In the moderate NMB group, a TOF count of 1 to 2 was maintained and NMB was reversed with a combination of neostigmine and glycopyrolate at the end of surgery. All patients were operated by one abdominal surgeon, who was experienced in laparoscopic gastric bypass surgery. Pneumoperitoneum was obtained by insufflating CO2 through a Veress needle until a steady pressure of 18 mm Hg was reached, and this pressure was maintained throughout the procedure.

After we applied standard hemodynamic and respiratory monitoring (3-lead ECG, noninvasive blood pressure manometer, pulse oxymeter), an 18-gauge intravenous cannula was placed in a forearm vein and an infusion with Plasmalyte A was started. After 3 minutes of preoxygenation (100% oxygen by mask) in slight anti-Trendelenburg position, anesthesia was induced with propofol 1% (Diprivan 1%; AstraZeneca, Zoetermeer, the Netherlands) and remifentanil (Ultiva; GlaxoWellcome, Barnard Castle, UK) until the patient lost consciousness. NMB was monitored by acceleromyography of the adductor pollicis muscle with the TOF-Watch SX18 (Organon, Dublin, Ireland): after we degreased the skin, 2 electrocardiogram electrodes were placed over the ulnar nerve at the wrist. After calibration and supramaximal stimulation, an intubation dose of rocuronium (Esmeron, Merck, Sharpe and Dohme, Hoddesdon, UK) of 0.6 mg/kg (lean body mass) was administered and the patient was intubated. Assessment of NMB was performed every 5 minutes.

Anesthesia was maintained throughout the duration of surgery with propofol 1% target-controlled infusion (Alaris, CareFusion, U.K. Marsh model) and remifentanil 0.15–0.5 μg/kg/min. Dosing was left at the discretion of the attending anesthesiologist. Patients were ventilated with an oxygen/air mixture of 50:50 to achieve an end-tidal CO2 of 30–35 mm Hg. Cefazoline 2 g (Cefazoline Mylan, Mylan, Athens, Greece) and paracetamol 1 g (Perfusalgan; Bristol-Myers Squibb, Agen, France) were administered after intubation. We used the definitions by Kopman and Naguib1 for the depth of NMB (deep NMB: PTC >1 but no response to a TOF stimulation; moderate NMB: TOF count of 1–3). In the deep NMB group, a continuous rocuronium infusion of 0.6 mg/kg (lean body mass)/h was started and titrated to a PTC of 1 to 2 twitches. At the end of surgery, NMB was reversed with sugammadex 4 mg/kg (Bridion; Merck, Sharpe & Dome, Hoddesdon, UK) in the deep NMB group. In the moderate NMB group, top-ups of rocuronium (10 mg) were given to maintain a TOF count of 1 to 2.

At the end of surgery, NMB was reversed with a combination of neostigmine 50 μg/kg (lean body mass) and glycopyrolate (Robinul-Neostigmine; Eumedica, Brussels, Belgium). In both groups, patients were extubated when the TOF ratio was >0.9. Remifentanil infusion was stopped 15 minutes before the conclusion of surgery. At the same time, fentanyl 100 μg (GlaxoSmithKline, Torrile, Italy) was administered to provide initial postoperative analgesia.

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Outcome Measures

The primary outcome measure was the overall quality of surgical conditions during the entire laparoscopy procedure assessed by a single surgeon using a 5-point rating scale (1 = extremely poor, 2 = poor, 3 = acceptable, 4 = good, 5 = optimal)6 at the end of the surgery. Although used in previous studies, the 5-point surgical rating scale remains a subjective tool and different surgeons could rate the quality of the surgical conditions differently. Therefore, we added 2 more objective outcome parameters to investigate the surgical conditions. One such parameter was the number of intra-abdominal pressure increases >18 cmH2O not related to manipulation of the abdominal wall (eg, insertion of trocars) as measured by the peritoneal CO2 insufflator, and the other one was the duration of surgery measured from the first skin incision to completion of skin closure. Secondary outcome measures were the postoperative pulmonary function and the need for postoperative respiratory support.

Pulmonary function was assessed by measuring PEF, FEV1, and FVC with the Vitalograph micro model 6300 (Buckingham, UK) electronic portable peak flowmeter. Portable peak flowmeters give highly reproducible data, and the technology on which the Vitalograph is based has the least over-reading in the mid- and low-flow range.19 A mean of 3 measurements in the upright posture in bed (upper body raised 45°) before and after surgery was used for statistical analysis. Baseline pulmonary function tests were performed during the preoperative anesthesiology consultation. Postoperative tests were performed in the recovery room. A modified observer’s assessment of alertness scale20 was determined at the time of postoperative pulmonary function measurements to exclude sedation as a cause of reduced pulmonary function. Respiratory function was furthermore assessed by the need for reintubation or noninvasive respiratory support such as continuous positive airway pressure or bilevel positive airway pressure. Other registered parameters were as follows: total dose of propofol, remifentanil and rocuronium, and time interval from TOFR >0.9 to pulmonary function tests.

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Blinding and Randomization

Patients were randomized within 3 strata (BMI 30–34 kg/m2, BMI 35–39 kg/m2, BMI >40 kg/m2) so that the treatment assignments were balanced within each stratum. Randomization was performed by the anesthesiologist responsible for the anesthesia and consisted of pulling a closed envelope from 1 of the 3 boxes labeled “BMI 30–34 kg/m2,” “BMI 35–39 kg/m2,” or “BMI > 40 kg/m2.” Each box contained an equal amount of cards reading deep and moderate NMB in closed envelopes. The cards were made unreadable by wrapping them in aluminum foil. The anesthesiologist performing the anesthesia was not involved in outcome assessment. The patient and the surgeon were both blinded to the treatment. To blind the surgeon, each patient had a syringe marked “rocuronium” in a syringe pump attached to the intravenous line. In the moderate NMB group, the syringe contained normal saline 0.9%, whereas in the deep NMB group, the syringe contained actual rocuronium. During surgery, the “rocuronium” syringe pumps in both groups were operated by the anesthesiologist as if they contained the active drug. The hand of the patient used to monitor NMB was hidden from the view of the surgeon under the sterile drapes.

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Statistical Methods

All analyses were preceded by tests for normality (D’Agostino and Pearson).21 Differences in the primary outcome measure (quality of surgical conditions) assessed by a 5-point surgical rating scale, the number of intra-abdominal pressure rises >18 cmH2O, and the duration of surgery were analyzed by a Mann-Whitney U test. Differences in proportion in the different surgical ratings between the 2 study groups also were examined with the Mann-Whitney U test. No adjustment was made to the significance criterion for having 3 primary outcome variables. The secondary outcome measure was assessed by comparing the mean percent change from baseline in PEF, FEV1, and FVC in both groups with the Student t test. Data are presented as mean ± standard deviation with estimated treatment effect (ETE: mean difference [95% confidence interval]) for group comparisons. P < .05 was considered statistically significant. Statistical analyses were performed using Prism 5.0d (GraphPad Software, San Diego, CA).

The clinically meaningful difference in quality of surgical conditions on a 5-point surgical rating scale has not been determined. We proposed that a difference of 2 points on a 5-point rating scale could be considered clinically meaningful. To detect this difference with a standard deviation of 3 and a power of 90% with a significance level set at α = 0.05, we calculated that a sample size of 24 patients per group would be needed.22 To compensate for an estimated dropout rate of 20%, we included 30 patients per group.

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RESULTS

Study Population

Table 2

Table 2

Figure 1

Figure 1

Seventy-four patients were assessed for eligibility. Fourteen patients were excluded: 11 patients declined to participate, 1 patient had renal insufficiency, and 2 patients had previous gastric banding surgery. Sixty patients were randomized, 30 to each treatment group. Each treatment group contained an equal amount of patients per stratum: 1 patient in the BMI 30–34 kg/m2 stratum, 20 patients in the BMI 35–39 kg/m2 stratum, and 9 patients in the BMI >40 kg/m2 stratum. All patients received the allocated treatment and none were lost to follow-up. In total, 60 patients completed the study (Figure 1). The baseline characteristics of the 2 study groups were similar (Table 2).

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Primary Outcome

Figure 2

Figure 2

The distribution of patients over the 5-point surgical rating scale in the deep and moderate NMB group is presented in Figure 2. There was no statistically significant difference in the surgeon’s rating regarding the quality of the surgical field between the deep and moderate NMB group (4.2 ± 1.0 vs 3.9 ± 1.1; P = .16, respectively; ETE: 0.4 [−0.1, 0.9]). There was no difference in the proportional rating of surgical conditions over the 5-point rating scale between both groups (P = .91). The number of intra-abdominal pressure rises >18 cmH2O were not statistically different between the deep and moderate NMB-group (0.2 ± 0.9 vs 0.3 ± 1.0; P = .69, respectively; ETE: −0.1 [−0.5, 0.4]). The duration of surgery was not different between the deep NMB group and the moderate NMB group (61.3 ± 15.1 minutes vs 70.6 ± 20.8 minutes; P = .07, respectively; ETE: −9.3 minutes [−18.8, 0.1]).

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Secondary Outcomes

Table 3

Table 3

Table 4

Table 4

After surgery, all the pulmonary function tests were considerably impaired in both groups when compared with baseline (Table 3). There was no statistically significant difference in the decrease in PEF, FEV1, and FVC (expressed as % change from baseline) between the deep and the moderate NMB group (PEV: 51.3% ± 31.6% vs 51.5% ± 19.0%; P = .97, respectively; ETE: −0.2% [−13.8, 15.6], FEV1: 45.2% ± 36.4% vs 48.8% ± 19.6%; P = .64, respectively; ETE: −3.6% [−15.0, 11.0] and FVC: 51.9% ± 16.4% vs 49.0% ± 22.6%; P = .58, respectively; ETE: 2.9% [−7.2, 17.6]). The modified observer’s assessment of alertness scale at the time of pulmonary function testing was not different between the 2 groups (4.9 ± 0.5 vs 4.9 ± 0.3; P = .76). In the deep NMB group, 2 patients required postoperative noninvasive continuous positive airway pressure versus 1 patient in the moderate NMB-group (P = .6). No patient needed reintubation after surgery. The total dose of propofol, remifentanil and rocuronium, and time from a TOFR >0.9 to pulmonary function testing in both groups are presented in Table 4.

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DISCUSSION

Deep NMB failed to improve the surgeon’s rating of operating conditions when compared with moderate NMB in patients undergoing laparoscopic gastric bypass surgery. There was no difference in the number of intra-abdominal pressure increases or the duration of surgery between both groups.

Investigators whom reported an improved effect of deep NMB during laparoscopy often compared it with a very shallow or no NMB.2,4,5 This, however, does not reflect clinical practice, where a certain degree of muscle relaxation is maintained during laparoscopic procedures. So, the question we should be asking ourselves is as follows: “is there an added value of deep NMB compared over moderate NMB” rather than “is deep NMB superior to a shallow or no NMB”? To complicate matters even further, investigators frequently use various definitions of deep, moderate, and shallow NMB adding to the difficulty of comparing these studies. Often the term “moderate NMB” is used for conditions following a single intubation dose of rocuronium after which neuromuscular function is spontaneously allowed to return to normal over the course of the surgery. With TOF stimulation, however, T1 reappears 21 minutes after an intubation dose of 0.6 mg/kg rocuronium and after 28 minutes T1 is at 25% of its initial value23 corresponding to a shallow NMB for the remainder of the operation. Therefore, studies comparing deep NMB to a “true” moderate NMB are scarce.

In one such study, Staehr-Rye et al3 investigated whether deep NMB was associated with a greater proportion of optimal surgical conditions during low-pressure pneumoperitoneum (8 mm Hg) for laparoscopic cholecystectomy compared with moderate NMB. Optimal surgical space conditions were found in 28% of patients in the deep NMB group versus 4% in the moderate NMB group (P = .05). The conversion rate to a high-pressure pneumoperitoneum (12 mm Hg) and median duration of anesthesia were similar between the 2 groups. The authors concluded that deep NMB marginally improved surgical conditions.

Our findings and those by Staehr-Rye et al3 are in line with an earlier observation that deep NMB only minimally enlarged the surgical space (distance from the sacral promontory to the edge of the trocar) by 0.3 cm compared with no NMB.4 The effect of such a small improvement on the quality of the surgical field is indeed questionable. In contrast, Martini et al6 found improved surgical conditions with deep NMB (PTC 1–2, compared with a moderate NMB: TOF-count 1–2) in patients undergoing laparoscopic prostatectomy or nephrectomy. Nonetheless, the improved surgical conditions did not result in a shorter duration of surgery.

Several explanations are possible for the discrepancy with our results. First, the retroperitoneal localization of the surgical field for prostatectomy and nephrectomy is more confined and surrounded by muscles than an intraperitoneal surgical field and consequently could benefit more from deep NMB. Second, different surgeons could rate operating conditions differently, as was demonstrated in the same study. Finally, the range of end-tidal CO2 pressures was less controlled in the study by Martini et al6 (33–56 mm Hg). Because high end-tidal CO2 pressures stimulate the respiratory center in the brainstem, which in turn activates the phrenic nerve and the diaphragm,24 this could induce a bias. The percentage of optimal surgical ratings in our study (55%) is lower than previously reported with deep NMB (68%–88%).5,25 This can be explained by the obesity of our patients. The increased abdominal wall mass and intraperitoneal fat can lead to decreased intraperitoneal volume expansion and therefore visibility for equal pneumoperitoneum pressures.

Pulmonary function was impaired significantly after laparoscopic bariatric surgery in the deep as well as the moderate NMB group. There was no difference between both groups with respect to the extent of impairment (45%–52% decrease from baseline) in PEF, FEV1, and FVC. Given that respiratory function tests are highly dependent on patient cooperation, we determined the alertness of patients before testing the pulmonary function. In both groups, we found mean sedation scores of 5, ie, the patients responded readily to their name spoken in a normal tone. Blobner et al2 found similar decreases in PEF, FEV1, and FVC after laparoscopic cholecystectomy in nonobese patients irrespective of the use of deep NMB. The pulmonary function tests showed no sign of recovery within the first 24 hours after surgery. The investigators found no difference in postoperative pain scores related to the use of deep NMB. In the latter study, patients were also extubated when TOFR was >0.9.

These findings suggest that the use of NMB agents is not responsible for postoperative respiratory impairment as long as NMB is adequately monitored and reversed at the end of surgery. Pulmonary atelectasis is probably the main cause of decreased postoperative pulmonary function. Baltieri et al26 found that atelectasis was present in 25% of patients after laparotomy for bariatric surgery. This number may be even higher after laparoscopic bariatric surgery because of the cranial displacement of the diaphragm caused by the pneumoperitoneum. Only postoperative bilevel positive airway pressure decreased the incidence of atelectasis. A major limitation is the fact that the study was underpowered. Ideally, the sample size should have been a total of 98 patients. As such, negative results should not be interpreted as lack of an effect but more studies are needed to definitively answer the research question.

In conclusion, there was insufficient evidence to conclude that deep NMB improves surgical conditions during laparoscopic bariatric surgery compared with a moderate NMB. Postoperative pulmonary function is substantially decreased after laparoscopic bariatric surgery independently of the NMB regime that is used.

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DISCLOSURES

Name: Sam Baete, MD.

Contribution: This author helped conduct the study, collect the data, analyze the data, and prepare the manuscript.

Conflicts of Interest: None.

Name: Gerd Vercruysse, MD.

Contribution: This author helped conduct the study, collect the data, analyze the data, and prepare the manuscript.

Conflicts of Interest: None.

Name: Margot Vander Laenen, MD.

Contribution: This author helped design the study, conduct the study, collect the data, analyze the data, and prepare the manuscript.

Conflicts of Interest: None.

Name: Pieter De Vooght, MD.

Contribution: This author helped collect the data and prepare the manuscript.

Conflicts of Interest: None.

Name: Jeroen Van Melkebeek, MD.

Contribution: This author helped design the study, conduct the study, collect the data, and prepare the manuscript.

Conflicts of Interest: None.

Name: Dimitri Dylst, MD.

Contribution: This author helped design the study, conduct the study, collect the data, and prepare the manuscript.

Conflicts of Interest: None.

Name: Maud Beran, MD.

Contribution: This author helped design the study, conduct the study, collect the data, and prepare the manuscript.

Conflicts of Interest: None.

Name: Jan Van Zundert, MD, PhD.

Contribution: This author helped design the study, conduct the study, collect the data, analyze the data, and prepare the manuscript.

Conflicts of Interest: None.

Name: René Heylen, MD, PhD.

Contribution: This author helped design the study, conduct the study, collect the data, analyze the data, and prepare the manuscript.

Conflicts of Interest: None.

Name: Willem Boer, MD.

Contribution: This author helped design the study, analyze the data, and prepare the manuscript.

Conflicts of Interest: None.

Name: Sam Van Boxstael, MD.

Contribution: This author helped anaylze the data and prepare the manuscript.

Conflicts of Interest: None.

Name: Tom Fret, MD.

Contribution: This author helped design the study, conduct the study, collect the data, and prepare the manuscript.

Conflicts of Interest: None.

Name: Hans Verhelst, MD.

Contribution: This author helped design the study, conduct the study, and prepare the manuscript.

Conflicts of Interest: None.

Name: Cathy De Deyne, MD, PhD.

Contribution: This author helped design the study, conduct the study, collect the data, analyze the data, and prepare the manuscript.

Conflicts of Interest: None.

Name: Frank Jans, MD, PhD.

Contribution: This author helped design the study, conduct the study, collect the data, analyze the data, and prepare the manuscript.

Conflicts of Interest: None.

Name: Pascal Vanelderen, MD, PhD.

Contribution: This author helped design the study, conduct the study, collect the data, analyze the data, and prepare the manuscript.

Conflicts of Interest: Pascal Vanelderen received a grant of 70.968,85€ from Merck, Sharpe & Dohme for the execution of this study.

This manuscript was handled by: Ken B. Johnson, MD.

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