The steps in the middle square were performed within the patient’s room. The steps in the top and bottom squares were performed outside the patient’s room. CO2 indicates carbon dioxide; FFP, filtering face piece; Fio2, fraction of inspired oxygen; PPE, personal protective equipment.
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Avilés-Jurado FX, Prieto-Alhambra D, González-Sánchez N, et al. Timing, Complications, and Safety of Tracheotomy in Critically Ill Patients With COVID-19. JAMA Otolaryngol Head Neck Surg. Published online October 08, 2020. doi:10.1001/jamaoto.2020.3641
Is it safe to perform an early bedside surgical tracheotomy in patients with coronavirus disease 2019 (COVID-19)?
In this cohort study of 50 patients with COVID-19 who underwent consecutive bedside tracheotomies following the recommended parameters for standard protective personal equipment, the successful weaning rate was higher in the early tracheotomy group than in the late tracheotomy group, and no infections among the surgeons were identified at the end of study.
With the use of a standardized protocol to minimize risk of spread of COVID-19, early bedside surgical tracheotomy may be a safe strategy for reducing time of mechanical ventilation, sparing intensive care unit beds during the COVID-19 pandemic.
The current coronavirus disease 2019 (COVID-19) pandemic has led to unprecedented needs for invasive ventilation, with 10% to 15% of intubated patients subsequently requiring tracheotomy.
To assess the complications, safety, and timing of tracheotomy performed for critically ill patients with COVID-19.
Design, Setting, and Participants
This prospective cohort study assessed consecutive patients admitted to the intensive care unit (ICU) who had COVID-19 that required tracheotomy. Patients were recruited from March 16 to April 10, 2020, at a tertiary referral center.
A surgical tracheotomy was performed for all patients following recommended criteria for use of personal protective equipment (PPE).
Main Outcomes and Measures
The number of subthyroid operations, the tracheal entrance protocol, and use of PPE. Infections among the surgeons were monitored weekly by reverse-transcriptase polymerase chain reaction of nasopharyngeal swab samples. Short-term complications, weaning, and the association of timing of tracheotomy (early [≤10 days] vs late [>10 days]) with total required days of invasive ventilation were assessed.
A total of 50 patients (mean [SD] age, 63.8 [9.2] years; 33 [66%] male) participated in the study. All tracheotomies were performed at the bedside. The median time from intubation to tracheotomy was 9 days (interquartile range, 2-24 days). A subthyroid approach was completed for 46 patients (92%), and the tracheal protocol was adequately achieved for 40 patients (80%). Adequate PPE was used, with no infection among surgeons identified 4 weeks after the last tracheotomy. Postoperative complications were rare, with minor bleeding (in 6 patients [12%]) being the most common complication. The successful weaning rate was higher in the early tracheotomy group than in the late tracheotomy group (adjusted hazard ratio, 2.55; 95% CI, 0.96-6.75), but the difference was not statistically significant. There was less time of invasive mechanical ventilatory support with early tracheotomy compared with late tracheotomy (mean [SD], 18 [5.4] vs 22.3 [5.7] days). The reduction of invasive ventilatory support was achieved at the expense of the pretracheotomy period.
Conclusions and Relevance
In this cohort study, with the use of a standardized protocol aimed at minimizing COVID-19 risks, bedside open tracheotomy was a safe procedure for patients and surgeons, with minimal complications. Timing of tracheotomy may be important in reducing time of invasive mechanical ventilation, with potential implications to intensive care unit availability during the COVID-19 pandemic.
Since December 31, 2019, when China reported to the World Health Organization the first case of pneumonia produced by severe acute respiratory syndrome coronavirus 2, more than 2 million (2 074 529 as April 17, 2020) people have been diagnosed with coronavirus disease 2019 (COVID-19) and almost 140 000 deaths have been reported.1 The outbreak was declared a public health emergency of international concern on January 30, 2020.1
In this pandemic scenario, health care systems rapidly became overwhelmed, intensive care units (ICUs) were insufficient to provide care for all critically ill patients, and health care professionals often became infected. This convergence of events led to social distancing measures to minimize community transmission and reduce secondary infections among close contacts and health care workers.
As of April 12, 2020, and according to the Spanish Health Ministry, 161 852 patients in Spain had confirmed COVID-19,2 and thus, Spain had the highest number of infected people in Europe.3 More than 60 000 patients had required hospitalization, with more than 7500 admitted to ICUs. In the US, on the same date, 492 416 patients had been diagnosed.4 Following the trend of Italy and Spain, approximately 10% (>49 000) would require ICU admission and 5% (approximately 25 000) invasive mechanical ventilation (IMV). According to published data from China,5,6 9.8% to 15% of patients receiving IMV would require a tracheotomy to manage secretions, optimize weaning, and avoid long-term laryngeal stenosis. This amount represents 700 to 1100 tracheotomies attributable to COVID-19 in a month in Spain and 2450 to 3750 cases expected in the US at the end of April 2020.
Tracheotomy for patients with COVID-19 is considered a highly infectious procedure, and adequate personal protective equipment (PPE) is needed to perform this surgery. Moreover, different scientific societies recommend avoiding or deferring its practice to minimize this risk.7,8 However, there is no information to date regarding safety, characteristics, and results of performing tracheotomy in patients with COVID-19 receiving IMV.
In the current study, we assessed the outcomes of a protocol for tracheotomy in a highly stressed COVID-19 pandemic setting. Special emphasis was placed on describing, step by step, the tracheotomy procedure, the protocol to reduce the risk of complications, and the association of tracheotomy timing with weaning progression.
This prospective cohort study assessed 50 consecutive patients with confirmed COVID-19 who were admitted to an ICU and required tracheotomy between March 16 and April 10, 2020. The study was approved by the Hospital Clínic Ethics Committee. Verbal informed consent was obtained from patient family members.
In our hospital protocol, patients who required intensive treatment were initially given high-flow nasal cannula oxygen therapy or noninvasive mechanical ventilation and progressed to IMV if their condition did not improve (ROX index, defined as the ratio of oxygen saturation as measured by pulse oximetry divided by fraction of inspired oxygen to respiratory rate, <3, <3.5, and <4 at 2, 6, and 12 hours from initial treatment). When IMV was required, the decision to perform tracheotomy was made by the treating ICU specialists following the standard protocol of our center, which is based on international recommendations and the treating physician’s decision.9 The decision was mostly influenced by the patient’s overall clinical condition, prognosis, and tolerance to wean.
Patients were followed up from the time of ICU admission until death, withdrawal of IMV, ICU discharge, or the end of the study (May 8, 2020), whichever came first. Baseline demographic and clinical characteristics, comorbidities, and laboratory variables were recorded. Ventilatory parameters (partial pressure of oxygen/fraction of inspired oxygen ratio and positive end-expiratory pressure [PEEP]) were also collected at admission, on day 7 of intubation, and at the time of tracheotomy. Disease severity and organ dysfunction or failure were estimated using the Acute Physiology and Chronic Health Evaluation II (APACHE II) and the Sequential Organ Failure Assessment (SOFA) scores at admission.
The step-by-step flowchart of the procedure is shown in Figure 1. Protection of the surgeons, location, timing of tracheotomy, type of instruments, achievement of the complete protocol, and complications were evaluated.
The PPE was classified in 3 levels. Level 1 included a disposable surgical cap, a disposable surgical mask, a work uniform, and latex gloves. Level 2 consisted of a disposable surgical cap, a disposable filtering face piece 2 (FFP2) respirator (Europe) or N95 (US), gaiters, goggles, a surgical mask with screen, a waterproof gown, and double gloves. Level 3 consisted of a disposable surgical cap or hangman, gaiters, FFP3 (Europe) or N99 (US) mask, hermetic waterproof goggles, a surgical mask with screen, a waterproof gown, and double gloves. The FFP3 (99% filter capacity) respirators were recommended in our protocol. In addition, all the surgeons attended a 1-hour training course to learn the methods for donning and doffing the PPE. Donning and doffing before and after the tracheotomy were supervised by the ICU nurse.
Whenever possible, a subthyroid approach with electrocautery was used to speed the surgery and reduce the risk of thyroid bleeding. The surgical steps to open the trachea were performed according to scientific recommendations for the COVID-19 scenario (Figure 1).10-12 The surgical team consisted of 2 expert seniors or 1 senior plus 1 junior otolaryngologist assisted by an ICU nurse (F.X.A.-J., N.G.-S., J.d.O., C.A., M.J.R.-L., L.R.-S., J.R., E.L.-C., M.L.-C., C.L., J.M.G., F.L., I.A., and I.V.). The entire team was composed of 14 different surgeons. Surgical instruments used included electrocautery only, soft tissues with electrocautery and trachea access with cold scalpel, or cold instruments only. In terms of timing of surgery, early tracheotomy was defined as tracheotomy performed during the first 10 days of mechanical ventilation and late tracheotomy was from the 10th day onward, as established by previous Cochrane recommendations.13
During the surgery, a cuffed tracheotomy tube with inner cannula was inserted. In case of problems, an extra-large tracheotomy tube was provided. Once mechanical ventilation was withdrawn, the cuff was progressively deflated according to patient requirements. When management of secretions was adequate, a fenestrated cannula was promoted. If the patient was able to breathe normally with a plugged cannula for 24 to 48 hours, decannulation was considered. No routine laryngoscopy was performed to assess the upper airway patency.
Intraoperative and postoperative complications were determined. Minor bleeding was defined as diffuse bleeding that could be fixed with local compressive measures and major as bleeding that required surgical revision or blood transfusion.
The numbers of days from intubation to tracheotomy, from tracheotomy to the end of mechanical ventilation (at least 24 hours without ventilatory support), and from intubation to the end of mechanical ventilation were calculated. The percentage of patients withdrawn from IMV was compared between the early and late tracheotomy groups. The percentage of patients undergoing decannulation at the end of the study was also calculated.
Categorical variables are reported as number (percentage) and continuous variables as mean (SD) or median (interquartile range [IQR]). A Kolmogorov-Smirnov test was performed to evaluate distribution of the assessed variables. Differences between groups were assessed using the χ2 test or Fisher exact test for categorical variables and the t test or Mann-Whitney test for continuous and ordinal variables according to distribution. Kaplan-Meier functions were used to depict cumulative weaning probability over time, stratified by timing of the tracheotomy. The follow-up period was 28 days starting from the day of orotracheal intubation (time 0).
Univariable and multivariable Cox proportional hazards regression models were fitted to estimate hazard ratios (HRs) and 95% CIs for time to weaning or withdrawal of IMV according to time of tracheotomy using late tracheotomy as the reference group and early tracheotomy as the target intervention. Multivariable adjustment included comorbidities, lymphocyte count, anticoagulant treatment, and APACHE II score, following the variables that were relevant in the univariate analysis. Backward stepwise elimination was used to generate a parsimonious model and minimize the risk of overfitting. In addition, under clinical criteria, we included pronation requirements and PEEP values in the equation.
All statistical analyses were performed with SPSS software, version 20.0 (IBM Inc). Effect size and 95% CIs were used to evaluate significance.
A total of 50 patients (mean [SD] age, 63.8 [9.2] years; 33 [66%] male) participated in the study. These patients were the first 50 patients with COVID-19 who received IMV and required tracheotomy at our hospital, representing 50 of 308 patients (16%) receiving IMV until the end of the study. The characteristics of the series are summarized in Table 1. Patients had a mean (SD) body mass index of 30 (5.9) (calculated as weight in kilograms divided by height in meters squared); 27 patients (54%) had hypertension. The mean (SD) APACHE II score at admission was 13.3 (4.2), and the mean (SD) SOFA score was 6.2 (2.3).
All tracheotomies were performed at the bedside (in the ICU) because of prolonged ventilatory support and facilitation of weaning from IMV. No urgent tracheotomy was needed. The median length of intubation at the time of tracheotomy was 9 days (IQR, 2-4 days). Early tracheotomy was performed for 32 patients (64%) and late tracheotomy for 18 (36%). Baseline characteristics between patients in the early and late tracheotomy groups were not different except that patients in the early tracheotomy group presented with lower mean (SD) PEEP levels at day 7 (8.4 [3.3] vs 13.1 [2.4] cm H2O) and had fewer pronation requirements (44% vs 77%).
The characteristics of the surgical procedure, ventilatory parameters, weaning, and postoperative complication rates are summarized in Table 2. A total of 46 tracheotomies (92%) were performed with subthyroid access using a combination of electrocautery and cold instruments (48 [96%]) and with the apnea protocol to enter the trachea completely achieved (40 [80%]) (Figure 1). For 10 patients (20%), difficulties occurred in the tracheal protocol, mostly regarding difficulties handling the ventilator during the procedure. Postoperative complications were rare, with the most frequent being minor diffuse bleeding (in 6 patients [12%]). No severe complications occurred, and all complications were resolved with conservative management, without revision surgery needed. At the end of the study, with a mean (SD) follow-up of 73.8 (5.9) days, 8 patients (16%) had died of COVID-19 and IMV withdrawal had been achieved for all who remained alive.
In the univariate analysis, comorbidities, lymphocyte count, anticoagulant treatment, APACHE II score, and timing of tracheotomy were associated with IMV (Table 1). Mean (SD) time of IMV was shorter in the early tracheotomy group than in the late tracheotomy group (18 [5.4] vs 22.3 [5.7] days). The shortening was attained in the pretracheotomy period only, suggesting that the indication for timing of the tracheotomy was crucial for the overall ventilation time. The mean (SD) PEEP value at day 7 of orotracheal intubation was also lower in the early group (9.5 [3.3] vs 13 [2.5] cm H2O).
In the multivariate analysis, the successful weaning rate was higher in the early tracheotomy group than in the late tracheotomy group, but the difference was not statistically significant (unadjusted HR, 1.8; 95% CI, 0.95-3.44) (Figure 2). After adjustment for confounding clinical variables, including PEEP values and pronation requirements, the adjusted HR was 4.04 (95% CI, 0.93-17.54).
With regard to PPE use, in all cases, at least level 2 PPE was worn. No incidents with PPE were identified during the surgical procedures. Because of disposable equipment shortage, hermetic goggles and FFP3 respirators were reused up to 8 hours. Ten operations had to be performed with FFP2. Despite these limitations, no COVID-19 cases were identified among the surgical team during the study period (which included weekly evaluation with reverse-transcriptase polymerase chain reaction up to 4 weeks after the last tracheotomy).
Recommendations derived from previous experience in China do not establish the best approach for tracheotomy in patients with COVID-19. Some clinicians believe that tracheotomy should never be performed before 3 weeks given the high risk of transmission and poor prognosis for patients.7,8 However, an association between tracheotomy and improved prognosis has been suggested in Europe,14 and after the first cases in our hospital, ICU specialists and the otolaryngologist surgical team decided to perform tracheotomy following our normalized protocol, with some changes adjusted to the COVID-19 scenario and specific risks.10-12 To our knowledge, this is the largest series evaluating the feasibility and safety of a standardized bedside open tracheotomy protocol for ICU-admitted patients with COVID-19.
All procedures were performed at bedside as open tracheotomies. Most series15,16 comparing surgical with percutaneous tracheotomy in patients without COVID-19 have not found significant differences, although the latter is favored for cases with more anatomical necks and adequate exposure.16 In patients with COVID-19, several factors could favor the surgical approach. Percutaneous tracheotomy is conceptually less invasive, but the serial dilations required may involve more extensive manipulation. In case of difficulties that lead to a change to open surgery, the need of PPE and critical respiratory status may be associated with additional risk for the patient and/or surgeon. From this point of view, open tracheostomies were favored over percutaneous tracheostomies during the severe acute respiratory syndrome outbreak and also seem to currently be favored.17-19 Furthermore, obesity is a risk factor for severe COVID-1920; mean body mass index in our cohort was 30. It is not uncommon that these patients present with thrombotic events that require anticoagulation therapy,21 and open tracheotomy is also preferred in this scenario. Because of the high amount of ICU admissions and hospital requirements attributable to the COVID-19 pandemic, surgical teams, including otolaryngologists, decreased their programmed operations, whereas intensivists’ work increased exponentially. Therefore, availability of surgeons was higher.
One of the main concerns of this procedure is the safety of the surgical team. According to data from the Spanish Ministry of Health, 26% of those infected in Spain were health care professionals. This finding is not exclusive of Spain3; more than 100 physicians have died in Italy, and infections among health care professionals represent approximately 10% of all diagnosed cases.22 Tracheotomy is considered a high-risk procedure. In an observational study23 during the severe acute respiratory syndrome epidemic, the odds ratio for transmission among those who performed tracheotomies compared with those who did not was 4.15. Substantial evidence indicates that adequate PPE is significantly associated with reduced infection rates among health care workers.24 Official recommendations from the World Health Organzation25,26 and the European Centre for Disease Prevention and Control27 suggest wearing an FFP3 respirator. We followed the standard recommendations for a high-risk procedure, and PPE was systematically used, although the shortage of disposable equipment led us to reuse part of the equipment. However, recent evidence seems to indicate that FFP2 and FFP3 maintain their protection even when they are used for a long time.25 Of interest, none of the members of the surgical team became infected during the study period. Therefore, our data suggest that with adequate PPE, tracheotomy is a safe procedure in patients with COVID-19.
In addition to correct PPE, 3 other points deserve comment regarding the safety of the technique for surgeons. First, some authors advise against the use of electrocautery because it may increase the number of aerosolized particles.19 However, it may facilitate bleeding control and subsequently reduce surgical time. Bleeding control is crucial in the COVID-19 scenario because of the high percentage of patients with obesity and poor coagulation. The additional risk of aerosol exposure compared with the reduced time of surgery and bleeding control provided by the electrocautery has not yet been assessed to our knowledge. Second, all the tracheotomies in our study were performed at the bedside of the patient. Rooms in ICUs are suboptimal for the surgeon because of reduced space, poor illumination, and small bed size. Conversely, bedside surgery avoids patient transfers, reducing the risk of transmission. Third, PPE may be associated with vision impairment because of condensation in the goggles and with reduced tactile sensation and motility. Thus, it is importance to minimize the duration of the procedure, to prepare instrumentation in advance, and to include adequately trained support staff. Tracheotomy was also safe for the patients. The rate of perioperative complications was unremarkable, and the postoperative bleeding or cannula dislocation rates were similar to those reported in the literature.28
Median time to tracheotomy since intubation in our cohort was 9 days. Despite decades of experience, the ideal timing for a tracheotomy in patients receiving mechanical ventilation is still controversial. A Cochrane review13 found lower mortality rates among patients undergoing early (≤10 days) tracheotomy and a higher probability of discharge from the ICU at day 28. More recently, in a meta-analysis,29 early tracheotomy was associated with shorter mechanical ventilation duration and hospital stay, without differences in mortality rate. Our study was not designed to find differences in outcome regarding time to tracheotomy, but a shorter mechanical ventilation duration was seen in the early tracheotomy group independent of ventilatory parameters at admission or at the time of tracheotomy. The decrease in time of IMV did not occur in the posttracheotomy period but rather before tracheotomy, suggesting that the indication of the tracheotomy was a key factor. Patients in the early and late tracheotomy groups had similar characteristics at admission. Of note, the latter had more prone position hours and higher PEEP levels at day 7, suggesting slower respiratory improvement. The presence of a tracheotomy tube may make posture changes difficult in patients with high prone position requirements, which is a common scenario in COVID-19. In addition, PEEP values at approximately day 7 are usually taken into account by the ICU specialists when deciding whether a tracheotomy should be performed. High PEEP values may indicate severe respiratory failure and perhaps put the patient at risk in case of surgery. In the multivariate analysis of our study, early or late tracheotomy and PEEP values were independent factors associated with overall IMV withdrawal. In addition, early surgery was safe, with no differences in complications in the sample. If confirmed in other series, early tracheotomy may be considered preferable when possible to favor a more efficient use of mechanical ventilators and spare ICU beds.
Strengths of the study are the prospective collection of data, the standardization of the procedure that includes the recommended protection measures, the careful strategy during the tracheal opening, and the monitoring of risk of infection for the surgical team. Among the limitations of the current study are the limited sample size and short follow-up of patients, precluding robust conclusions on uncommon outcomes or long-term complications. Another limitation is the lack of randomization for the timing of surgery, leading to potential confounding by indication. Despite no obvious differences in key parameters, we conducted a multivariable regression model to adjust for observed imbalances in relevant clinical features between early vs late tracheotomy recipients. Our findings that early tracheotomy was safe and potentially associated with reduced duration of mechanical ventilation require confirmation in randomized clinical trials. However, such trials are unlikely to be completed during the current COVID-19 crisis because ICU beds are overwhelmed and need to be strategically allocated.
The findings suggest that with the use of a standardized protocol, bedside open tracheotomy may be safe for patients with COVID-19 receiving IMV at ICUs and their surgeons. Moreover, early indication of tracheotomy, when clinically appropriate, may be associated with decreased use of ICU beds in the COVID-19 pandemic.
Corresponding Author: Isabel Vilaseca, MD, PhD, Otorhinolaryngology Head Neck Surgery Department, Institut Clínic d'Especialitats Mèdiques i Quirúrgiques. Hospital Clínic, Hospital Clínic, Villarroel 170, 08036 Barcelona, Spain (firstname.lastname@example.org).
Published Online: October 8, 2020. doi:10.1001/jamaoto.2020.3641
Author Contributions: Drs Avilés-Jurado and Vilaseca contributed equally to this article. Drs Avilés-Jurado and Vilaseca had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.
Concept and design: Avilés-Jurado, Prieto-Alhambra, de Ossó, Lehrer, Alobid, Bernal-Sprekelsen, Castro, Vilaseca.
Acquisition, analysis, or interpretation of data: Avilés-Jurado, Prieto-Alhambra, González Sánchez, Arancibia, Rojas-Lechuga, Ruiz-Sevilla, Remacha, Sánchez, Lehrer, López-Chacón, Langdon, Guilemany, Larrosa, Alobid, Castro, Vilaseca.
Drafting of the manuscript: Avilés-Jurado, Prieto-Alhambra, Arancibia, Lehrer, Alobid, Vilaseca.
Critical revision of the manuscript for important intellectual content: Avilés-Jurado, Prieto-Alhambra, González Sánchez, de Ossó, Rojas-Lechuga, Ruiz-Sevilla, Remacha, Sánchez, López-Chacón, Langdon, Guilemany, Larrosa, Alobid, Bernal-Sprekelsen, Castro, Vilaseca.
Statistical analysis: Avilés-Jurado, Prieto-Alhambra, González Sánchez, Vilaseca.
Administrative, technical, or material support: Avilés-Jurado, de Ossó, Arancibia, Rojas-Lechuga, Ruiz-Sevilla, Remacha, Sánchez, Lehrer, López-Chacón, Larrosa.
Supervision: Avilés-Jurado, Prieto-Alhambra, Lehrer, Langdon, Alobid, Bernal-Sprekelsen, Castro.
Conflict of Interest Disclosures: Dr Prieto-Alhambra reported receiving grants and speaker honorarium from Amgen and UCB outside the submitted work. Dr Bernal-Sprekelsen reported receiving speaker honorarium from Olympus outside the submitted work. No other disclosures were reported.
Additional Contributions: The following COVID-19 Clinic Critical Care Group members from Hospital Clínic of Barcelona provided substantial collaboration to the work: Alex Almuedo, MD, PhD; Joan Ramon Alonso, MD, PhD; Rut Andrea MD, PhD; Fatima Aziz, MD; Joan Ramon Badia MD, PhD; Enric Barbeta, MD; Raquel Berger, MD; Xavier Borrat, MD, PhD; Ernest Bragulat, MD, PhD; Carmen Cañueto, RN; Inmaculada Carmona, RN; Manel Castellà, MD, PhD; Oriol De Diego, MD; Marta Farrero, MD, PhD; Javier Fernández, MD, PhD; Sara Fernández, MD; Carlos Ferrando, MD, PhD; Miguel Ferrer MD, PhD; Maria Forga, MD, PhD; Ignacio Grafiá, MD; Lídia Gómez, MD; Eduard Guasch, MD, PhD; María Hernández-Tejero, MD, PhD; Adriana Jacas, MD; Pere Leyes, MD, PhD; Teresa López, MD; Javier Marco, MD; Jose Antonio Martínez, MD, PhD; Graciela Martínez-Palli, MD, PhD; Ricard Mellado, MD, PhD; Jordi Mercadal, MD, PhD; Guillermo Muñoz, MD; José Muñoz, MD, PhD; Ricard Navarro, MD, PhD; Josep Maria Nicolás MD, PhD; José T Ortiz, MD, PhD; Esteban Poch, MD, PhD; Margalida Pujol, MD; Eduard Quintana, MD, PhD; Enric Reverter, MD, PhD; Irene Rovira, MD, PhD; Pablo Ruiz, MD; Xavier Sala-Blanch, MD PhD; Elena Sandoval, MD, PhD; Stefan Schneider, MD; Ferran Seguí, MD; Oriol Sibila, MD, PhD; Cristina Sierra, MD, PhD; Alex Soriano, MD, PhD; Dolors Soy, Pharm D, PhD; María Suárez, MD; Adrián Téllez, MD; David Toapanta MD; Antoni Torres MD, PhD; Xavier Urra MD, PhD; and Carles Zamora, MD. They were not compensated for their work.
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