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The Effect of Blood Pressure Regulation During Aortic Coarctation Repair on Brain, Kidney, and Muscle Oxygen Saturation Measured by Near-Infrared Spectroscopy: A Randomized, Clinical Trial

Moerman, Annelies MD*; Bové, Thierry MD; François, Katrien MD, PhD; Jacobs, Stefan MD*; Deblaere, Isabel MD*; Wouters, Patrick MD, PhD*; De Hert, Stefan MD, PhD*

doi: 10.1213/ANE.0b013e31827f5628
Cardiovascular Anesthesiology: Society of Cardiovascular Anesthesiologists: Research Reports
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BACKGROUND: In this study, we compared the effects of 3 frequently used arterial blood pressure–regulating agents on brain (rScO2), renal (SrO2), and muscle (SmO2) oxygen saturation, during aortic coarctation repair in children. Based on the reported adverse effect of sodium nitroprusside (SNP) on left-sided rScO2 during aortic coarctation repair, we tested the hypothesis that the alterations in left rScO2 occurring with SNP would not be present with sevoflurane and nitroglycerin (NTG). Additionally, we explored the effects of blood pressure regulation with SNP, NTG, or sevoflurane on right-sided rScO2, SrO2, and SmO2.

METHODS: Children with isolated aortic coarctation undergoing surgical repair through a left thoracotomy without the use of cardiopulmonary bypass were considered eligible for the study. During aortic cross-clamping, control of mean arterial blood pressure (MAP) was conducted according to randomization by the use of SNP, NTG, or sevoflurane to obtain a mean target right brachial blood pressure of 120% to 150% of the MAP value before cross-clamping. Bilateral rScO2, SrO2, and SmO2 were recorded continuously with near-infrared spectroscopy. As a primary end point, the maximal relative change in left-sided rScO2 in response to aortic cross-clamping was compared among treatment groups.

RESULTS: Ten patients per group were included. No significant difference among treatment groups was observed in maximal relative change in left-sided rScO2 (SNP versus sevoflurane: mean difference −0.7%, 99% confidence interval [CI] −31% to 29%, P = 1.0; SNP versus NTG: mean difference −1.8%, 99% CI −32% to 28%, P = 1.0; sevoflurane versus NTG: mean difference −1.1%, 99% CI −31% to 29%, P = 1.0). Additional analyses also detected no difference between groups in right rScO2 (P = 0.4). Compared with NTG, treatment with SNP resulted in a significantly larger (−64% ± 17% vs −34% ± 25%, P = 0.01) and faster (−9 ± 4 %·min−1 vs −4 ± 3 %·min−1, P = 0.004) decrease in SmO2. Right-sided rScO2 and MAP showed a poor correlation for NTG (r = −0.2, P = 0.93), whereas borderline for sevoflurane (r = 0.44, P = 0.09) and SNP (r = 0.56, P = 0.04).

CONCLUSIONS: The mean differences in left-sided rScO2 among the patients treated with SNP, NTG, or sevoflurane for proximal hypertension during aortic cross-clamping were no more than 32%. Additional analysis demonstrated a low MAP-rScO2 dependence with the use of NTG. Because NTG also resulted in a smaller and slower decrease of oxygen saturation in peripheral tissues, our data suggest that its use might be preferable for proximal blood pressure control during surgical procedures involving aortic cross-clamping.

From the Departments of *Anesthesiology and Cardiac Surgery, Ghent University Hospital, Gent, Belgium.

Accepted for publication November 16, 2012.

Supported by a grant from the Belgian Foundation for Cardiac Surgery.

The authors declare no conflicts of interest.

Reprints will not be available from the authors.

Address correspondence to Moerman Annelies, MD, Department of Anesthesiology, Ghent University Hospital, De Pintelaan 185, 9000 Gent, Belgium. Address e-mail to annelies.moerman@UGent.be.

Surgical repair of aortic coarctation through left thoracotomy involves proximal aortic arch cross-clamping, resulting in temporary hypoperfusion of the tissues distal to the cross-clamp. This maneuver may also be associated with an abrupt increase in ventricular afterload and immediate proximal (to the aortic cross-clamp) hypertension, often necessitating pharmacologic control.1 Currently, the use of potent and short-acting vasodilators such as sodium nitroprusside (SNP) and nitroglycerin (NTG) is preferred for treating hypertension during aortic cross-clamping for this procedure. However, Azakie et al.2 have raised concerns regarding the effect of SNP on left-sided cerebral oxygen saturation (rScO2) during aortic coarctation repair. In addition, it has been demonstrated that SNP may worsen the already impaired oxygen balance of tissues below the aortic cross-clamp during surgery on the thoracic aorta.3–5

The effects of different antihypertensive agents on tissue oxygen saturation during aortic cross-clamping remain largely unexplored. The purpose of the present study was to test the hypothesis that the alterations in left rScO2 described with SNP would not be present with other arterial blood pressure–regulating agents. Second, we wanted to compare the effects of blood pressure–regulating drugs during aortic coarctation repair on the oxygen saturation of the right-sided brain and the peripheral tissues. Three agents frequently used for perioperative blood pressure control during cardiac surgery6 were included: SNP and NTG as IV vasodilating agents, and sevoflurane as an inhaled anesthetic with vasodilating effect. We hypothesized that the alterations in oxygen saturation of the brain and peripheral tissues reported with SNP would represent an agent-specific phenomenon that is not present with NTG or sevoflurane.

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METHODS

This study was a single-center, prospectively randomized, controlled trial conducted from October 2007 to March 2011. The trial was registered at ClinicalTrials.gov on September 25, 2007 (NCT00535808). After IRB approval, written informed consent was obtained from the parents or legal guardian of the child. All children with isolated aortic coarctation undergoing surgical correction through a left thoracotomy without the use of cardiopulmonary bypass were considered eligible. Patients with associated cardiac defects resulting in a hemodynamically significant intracardiac shunt were excluded. To assure uniformity of the impact of aortic cross-clamping on cerebral perfusion, the experimental protocol involved cross-clamping of the left carotid artery in all patients. If cross-clamping of the left carotid artery was surgically not indicated, patients were excluded from the study protocol. Assignment to the groups was determined by random drawing of sealed envelopes containing the labels “sevoflurane,” “sodium nitroprusside,” or “nitroglycerin.”

On the morning of the surgery, patients were allowed to take their normal daily medication. The uniform protocol of anesthesia included induction with sufentanil 0.5 µg/kg, midazolam 100 µg/kg, and rocuronium 0.9 mg/kg. Anesthesia was maintained with sevoflurane inhalation (1 minimum alveolar concentration) and additional doses of sufentanil. Mechanical ventilation was adjusted in order to obtain a PaCO2 of 40 mm Hg. Fractional inspired oxygen was set at 0.5. The body temperature was kept constant at 35.0°C to 36.0°C by using a warming mattress underneath the patient (Blanketrol® II, Cincinnati Sub-Zero Products, Inc., Cincinnati, OH) and a pediatric forced-air warming blanket surrounding the patient (Bair Hugger® Therapy; Arizant Healthcare Inc., Eden Prairie, MN). Two disposable near-infrared spectroscopy (NIRS) sensors were applied on each side of the forehead for continuous registration of the rScO2 of the corresponding brain hemisphere (INVOS 5100; Somanetics Corporation, Troy, MI). Additionally, a NIRS sensor was placed over the right flank below the costovertebral angle overlying the kidney (T10-L2) to estimate renal oxygen saturation (SrO2), and one over the right thigh to measure muscle oxygen saturation (SmO2). Arterial blood pressure was recorded continuously via an arterial line in the right brachial artery. A blood pressure cuff was placed on the left lower extremity. Central venous pressure was monitored through right internal jugular vein access.

The surgical procedure was performed in a standardized manner, with the patient in the right lateral decubitus position, using a left lateral thoracotomy approach. After extensive dissection of the aortic arch, supraaortic vessels, and descending aorta down to 4 intercostal levels, the ductus arteriosus or ligament was ligated. Subsequent to systemic heparin administration (1 mg/kg), the aortic arch was cross-clamped proximally between the innominate artery and the left carotid artery, and distally on the descending aorta below the first intercostal artery. Surgical repair consisted of resection of the coarctation segment and direct end-to-end anastomosis.

Control of blood pressure during aortic cross-clamping was performed according to the randomization sequence by the use of sevoflurane, SNP, or NTG. Drug dose was titrated to obtain a mean target right brachial blood pressure of 120% to 150% of the mean arterial blood pressure (MAP) value before aortic cross-clamping. The vasodilator therapy was started immediately after heparin administration (start of administration of SNP/NTG in the SNP and NTG groups, respectively, or increasing the concentration of sevoflurane in the sevoflurane group). Two minutes before anticipated completion of the anastomosis, administration of the vasoactive treatment was stopped to attenuate the hypotensive response upon clamp release.

Heart rate, invasive systemic blood pressure, and central venous pressure, in- and end-expiratory gas tensions, pulse oximetry, and NIRS data (bilateral rScO2, SrO2, SmO2) were recorded continuously and integrated digitally with the RUGLOOP® software (Demed, Temse, Belgium). Analysis of hematocrit, arterial and venous blood gas partial pressures, and lactate levels was performed just before surgical incision, after heparin administration, 5 minutes after aortic cross-clamping, 5 minutes after aortic declamping, and postoperatively at arrival in the intensive care unit. Types and volumes of all fluids administered, doses of any drugs given, and blood loss were recorded.

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Data Description

In the present study, we compared the effects of 3 blood pressure–regulating agents on rScO2, SrO2, and SmO2. Because no data from the literature were available allowing sample size calculation for changes in SrO2 and SmO2 during aortic cross-clamping, we had to rely for the expected treatment effects and the sample size calculation on reported rScO2 changes during aortic cross-clamping. Azakie et al.2 demonstrated a relative decrease of left-sided rScO2 of 10.4% with the use of SNP during aortic cross-clamping. Assuming a baseline mean rScO2 and standard deviation of 71% and 6%, respectively,7 a sample size of 7 patients per group was calculated to detect a minimal difference of 10% in left rScO2 among treatment groups with a power of 0.8 and an α of 0.05. To account for possible dropouts, 10 patients per group were included.

Absolute NIRS values have a wide range of variability among patients when measured with the INVOS technology.8 Therefore, only measures of the relative changes in NIRS variables were analyzed, defined as the relative percentage of the lowest (in case of decrease) or highest (in case of increase) value during the cross-clamp period versus the value just before aortic cross-clamping.

The primary outcome variable of the present study was the maximal relative change in left rScO2 after aortic cross-clamping. Secondary NIRS variables included the maximal relative change in right rScO2, SrO2, and SmO2 after aortic cross-clamping. Further secondary analyses included the rate of decrease in SrO2 and SmO2 in each treatment group, and the integrated rScO2, SrO2, and SmO2 for each treatment group. The rate of decrease in SrO2 and SmO2 was determined by the average rate of decay, calculated by dividing the maximal change in SrO2 or SmO2 by the time to reach its nadir, expressed in percentage per minute. The integrated rScO2, SrO2, or SmO2, or area under the curve (AUC), was calculated with reference to the value just before aortic cross-clamping, using measurement intervals of 5 seconds, and is expressed in %·second. Subsequently, the AUC accounts for both depth and duration of change in oxygen saturation.

Because rScO2 and blood pressure have been reported to be correlated,9 we also evaluated the relationship between right-sided rScO2 and MAP in the 3 treatment groups. The extent of collateral circulation has been shown to be age-related,10 therefore the relationship between age and changes in SrO2 and SmO2 was also evaluated.

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Statistical Analysis

Statistical analysis was performed using the statistical software SPSS Statistics 20 (SPSS Inc., Chicago, IL). The raw data were tested for normality using the Shapiro-Wilk test and were considered normally distributed if P > 0.05. Homogeneity of variances was tested with Levene’s test. Additionally, residuals were tested as well and normality has been confirmed. Normally distributed continuous data are presented as mean ± SD. Nonparametric data are presented as median (range).

Comparison of demographic data among the 3 treatment groups was performed with the Kruskal-Wallis test for continuous data and with the χ2 test for categorical data. Intraoperative data, absolute rScO2, SrO2, and SmO2 values, and blood gas values among the 3 treatment groups were compared with analysis of variance. For pairwise comparisons among groups, Tukey correction was used with 99% confidence intervals (CIs).

Between-group comparisons of maximal relative changes in rScO2, SrO2, and SmO2 were done in a general linear model with adjustment for baseline oxygen saturations, and Bonferroni correction for multiple comparisons (3 in the Bonferroni denominator). The same statistical method was applied for analysis of the rate of decay for SrO2 and SmO2. AUCs for rScO2, SrO2, and SmO2 were analyzed with the Kruskal-Wallis test. Pairwise differences in AUC among treatment groups were examined for significance by using Mann-Whitney U test.

For the correlation between changes in right rScO2 and MAP, Kendall τ test of concordance was used. The relationship between age and changes in SrO2 and SmO2 was evaluated by simple linear regression analysis.

The level of statistical significance was set at corrected 2-sided P value <0.05 for the primary analyses. A P value of <0.01 was considered significant for secondary end points regarding multiple comparisons after Bonferroni correction with denominator 3.

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RESULTS

Thirty-one patients were considered eligible. One patient was excluded before randomization to a treatment group because cross-clamping of the left carotid artery was surgically not indicated. Patient characteristics are summarized in Table 1. There were no differences among groups in the listed variables. Intraoperative data are reported in Table 2. As expected, during aortic cross-clamping, the mean end-tidal sevoflurane concentration was higher in the sevoflurane group compared with the SNP group and the NTG group (P = 0.01 for each). There was no difference in sevoflurane concentration between the SNP and NTG groups. Sufentanil total dose and arterial and venous blood gas results were similar among the 3 groups. The mean total doses of SNP and NTG necessary for maintaining the target MAP were 14.3 ± 11.2 µg/kg and 18.6 ± 14.5 µg/kg, respectively. No significant differences in MAP were observed among the 3 groups at any time of measurement, indicating that the different blood pressure–regulating strategies allowed for a comparable proximal blood pressure control during aortic cross-clamping.

Table 1

Table 1

Table 2

Table 2

No difference among groups was observed in mean left-sided rScO2 values before aortic cross-clamping (72% ± 10%, 77% ± 13%, and 77% ± 11% for sevoflurane, SNP, and NTG, respectively, P = 0.57). Three possible responses to aortic cross-clamping were observed in left rScO2 measurements: a decrease of left rScO2 in 2 patients of each group (maximal relative decrease of −5% and −17% for sevoflurane, −5% and −47% for SNP, −28% and −33% for NTG, P = 0.58 between groups), no change in left rScO2 in 1 patient in the sevoflurane group, 2 patients in the SNP group, and in 2 patients in the NTG group, whereas an increase in left rScO2 was observed in the remaining patients (sevoflurane, n = 7, 10% ± 7%; SNP, n = 6, 13% ± 4%; NTG, n = 6, 17% ± 19%, P = 0.32 between groups). No differences among groups were observed in the maximal relative changes in left rScO2 values in response to aortic cross-clamping (SNP versus sevoflurane: mean difference −0.7%, 99% CI −31% to 29%, P = 1.0; SNP versus NTG: mean difference −1.8%, 99% CI −32% to 28%, P = 1.0; sevoflurane versus NTG: mean difference −1.1%, 99% CI −31% to 29%, P = 1.0).

The following additional observations were made regarding changes in right rScO2, SrO2, and SmO2. No differences among groups were observed in mean right rScO2 values before aortic cross-clamping (P = 0.69) and in maximal relative change in right rScO2 values in response to aortic cross-clamping (P = 0.4) (Table 3). SrO2 and SmO2 showed a rapid and significant decrease after aortic cross-clamping in all groups, reaching a plateau phase for SrO2 within 8.6 minutes, 7.4 minutes, and 10.0 minutes for sevoflurane, SNP, and NTG, respectively (P = 0.08 among groups) and within 9.4 minutes, 6.8 minutes, and 9.9 minutes for SmO2 for sevoflurane, SNP, and NTG, respectively (P = 0.02 among groups). All tissue oxygen saturations recovered promptly after release of the aortic cross-clamp. For SmO2, the maximal relative changes were larger and the rate of decay was faster in the SNP group compared with the NTG group (Table 3).

Table 3

Table 3

AUC for oxygen saturation from each site is depicted in Figure 1. No differences were observed among the 3 treatment groups in AUC for left-sided and right-sided rScO2 (P = 0.74 and P = 0.17, respectively). For renal AUC, there was a difference between the NTG and the SNP group (P = 0.009). There were no differences in muscle AUC among the treatment groups (P = 0.05 for NTG versus sevoflurane, and P = 0.03 for NTG versus SNP). Right-sided rScO2 and MAP showed a poor correlation for NTG (r = −0.2, P = 0.93), whereas the correlation was borderline for sevoflurane (r = 0.44, P = 0.09) and SNP (r = 0.56, P = 0.04).

Figure 1

Figure 1

An effect of age was observed on the maximal relative decrease of SrO2 (unstandardized β = 0.06, 99% CI −0.02 to 0.14, P = 0.06) and SmO2 (unstandardized β = 0.07, 99% CI 0.01–0.13, P = 0.03). This effect was independent of the study product used (unstandardized β = 1.5, 99% CI −12.4 to 15.4, P = 0.76 for SrO2 and unstandardized β = 6.3, 99% CI −7.9 to 20.6, P = 0.23 for SmO2).

Analysis of hematocrit, blood gas partial pressures, and lactate levels performed 5 minutes after aortic cross-clamp removal is presented in Table 4. There were no differences among the treatment groups. In all patients, clinical recovery was uneventful. Postoperative lactate levels and blood creatinine levels were comparable among groups.

Table 4

Table 4

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DISCUSSION

In this randomized, clinical study, the effects of blood pressure–regulating strategies with SNP, NTG, or sevoflurane on rScO2, SrO2, and SmO2 were investigated during aortic cross-clamping in children undergoing aortic coarctation repair. Although no differences in rScO2 values were observed among the 3 strategies, the mean differences in left-sided rScO2 among the 3 treatment groups was no more than 32%. Decreases in SrO2 and SmO2 were larger and had a faster rate of decay in SNP-treated patients. For both SNP and sevoflurane MAP-rScO2 dependence was higher than for NTG.

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Effects on Cerebral Oxygen Saturation

In this study, aortic cross-clamping always involved temporary occlusion of the left carotid artery. This maneuver was associated with a variable response of the left-sided rScO2, ranging from a decrease to an increase in rScO2. CIs for pairwise comparisons between groups were wide. Although our study design did not allow us to comment on possible underlying mechanisms, it is conceivable that this phenomenon merely reflects the functional adequacy of the circle of Willis.

In a study on 18 patients undergoing aortic coarctation repair, Azakie et al.2 observed a pronounced decrease in left rScO2 in 2 patients treated with SNP, in whom the left carotid artery was clamped during the intervention. They attributed this finding to an SNP-induced disruption of cerebral autoregulation. However, because in that study no simultaneous recording of both left and right hemispheres was obtained, it cannot be determined whether this rScO2 decrease is the result of an agent-specific effect or rather a deficient circle of Willis.

We observed no significant differences in right rScO2 values among the different blood pressure–regulating strategies; however, with NTG treatment, changes in rScO2 were less dependent on changes in MAP than with SNP and sevoflurane. A higher correlation between MAP and rScO2 has been reported to be indicative of impaired cerebral autoregulation, whereas values around zero and negative values could be considered as representative of intact autoregulation.11,12 In line with this reasoning, the higher correlation between MAP and rScO2 in the SNP and sevoflurane groups compared with the NTG group would suggest that SNP and sevoflurane may interfere to a larger extent with cerebral autoregulation than NTG. This is in accordance with previous work reporting on dose-dependent impairment of cerebral autoregulation with SNP,13 whereas there was no significant impairment with NTG.14,15 Data on the effect of sevoflurane on cerebral autoregulation are controversial. It is generally assumed that cerebral autoregulation is maintained at low concentrations of sevoflurane, whereas higher doses seem to decrease autoregulatory capacity.16

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Effects on Renal and Muscle Oxygen Saturation

Concerning the effects on peripheral tissue oxygen saturation, a larger and faster decrease in both SrO2 and SmO2 was observed in children treated with SNP. Previous studies have suggested that SNP-induced hypotension might worsen the impaired oxygen balance of tissues below the aortic cross-clamp.3–5 These findings could not be readily explained. Of interest, an experimental study on striated hamster muscle conducted by Endrich et al.17 demonstrated that SNP dilated preferentially precapillaries and caused a consistent increase in intravascular pressure within the venules. Consequently, the arteriolar-venular pressure gradient was reduced and functional capillary density decreased, leading to skeletal muscle tissue hypoxia. In contrast, NTG dilated both arterioles and venules, leaving the functional capillary density and local PO2 unchanged. Our findings are in accordance with the results of Endrich et al.17 and suggest that NTG may be preferable to SNP in terms of tissue oxygenation.

In all patients, both SrO2 and SmO2 declined to a plateau phase, which indicated that oxygen delivery no longer met metabolic oxygen requirements, likely resulting in anaerobic metabolism. The duration of the nadir of oxygenation has been demonstrated to be directly related to the extent of tissue injury.18,19 Sakamoto et al.18 demonstrated that nadir times of <25 minutes did not induce tissue injury. It can therefore be expected that the nadir times in our study were too short to translate into changes of biomarkers indicative for tissue injury, such as serum lactate, base excess, and creatinine levels.

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Study Limitations

The results of the present study should be interpreted within the constraints of the methodology. First, because of absence of evident adverse clinical events due to the short aortic cross-clamp times, the clinical implications of the current study on outcome remain to be determined. Second, the current study population comprised only young patients. Because the extent of collateral circulation has been shown to be age-related,10 the validity of the current results in older patients with a possibly more developed collateral circulation needs to be confirmed. Third, the reliability of NIRS to measure specific renal oxygen saturation can be questioned because of the uncertainty related to the depth of penetration of the near-infrared light in relation to the kidney. However, a number of studies have suggested that placement of an NIRS sensor over the flank might indeed reflect SrO2. Ortmann et al.20 demonstrated a strong correlation between flank NIRS values and renal vein saturation in children weighing <10 kg. Also, low renal tissue oxygen saturations measured with NIRS were associated with renal dysfunction after pediatric cardiac surgery21 and after aortic coarctation repair.22

In conclusion, although no significant differences were observed in rScO2 values among the different blood pressure–regulating strategies, mean differences in left-sided rScO2 among the 3 treatment groups was no more than 32%. With NTG treatment, changes in rScO2 were less dependent on changes in MAP than with SNP and sevoflurane. Decreases in SrO2 and SmO2 were larger and had a faster rate of decay in SNP-treated patients. Based on the lower MAP-rScO2 dependence and the smaller and slower decreases in SrO2 and SmO2, our data suggest that NTG might be preferable for blood pressure control during surgical procedures involving aortic cross-clamping.

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DISCLOSURES

Name: Annelies Moerman, MD.

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

Attestation: Annelies Moerman attests to the integrity of the original data and the analysis reported in this manuscript, approved the final manuscript, and is the author responsible for archiving the study files.

Name: Thierry Bové, MD.

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

Attestation: Thierry Bové attests to the integrity of the original data and the analysis reported in this manuscript, and approved the final manuscript.

Name: Katrien François, MD, PhD.

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

Attestation: Katrien François approved the final manuscript.

Name: Stefan Jacobs, MD.

Contribution: This author helped conduct the study.

Attestation: Stefan Jacobs approved the final manuscript.

Name: Isabel Deblaere, MD.

Contribution: This author helped conduct the study.

Attestation: Isabel Deblaere approved the final manuscript.

Name: Patrick Wouters, MD, PhD.

Contribution: This author helped design the study and write the manuscript.

Attestation: Patrick Wouters approved the final manuscript.

Name: Stefan De Hert, MD, PhD.

Contribution: This author helped analyze the data and write the manuscript.

Attestation: Stefan De Hert attests to the integrity of the original data and the analysis reported in this manuscript, and approved the final manuscript.

This manuscript was handled by: Charles W. Hogue, Jr., MD.

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ACKNOWLEDGMENTS

The authors are grateful to Marc De Buyzere for his valuable guidance and assistance regarding statistical review.

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