Resuscitation fluid practices in Brazilian intensive care units: a secondary analysis of Fluid-TRIPS

Flavio Geraldo Rezende de Freitas Naomi Hammond Yang Li Luciano Cesar Pontes de Azevedo Alexandre Biasi Cavalcanti Leandro Taniguchi André Gobatto André Miguel Japiassú Antonio Tonete Bafi Bruno Franco Mazza Danilo Teixeira Noritomi Felipe Dal-Pizzol Fernando Bozza Jorge Ibrahin Figueira Salluh Glauco Adrieno Westphal Márcio Soares Murillo Santucci César de Assunção Thiago Lisboa Suzana Margarete Ajeje Lobo Achilles Rohlfs Barbosa Adriana Fonseca Ventura Ailson Faria de Souza Alexandre Francisco Silva Alexandre Toledo Aline Reis Allan Cembranel Alvaro Rea Neto Ana Lúcia Gut Ana Patricia Pierre Justo Ana Paula Santos André Campos D. de Albuquerque André Scazufka Antonio Babo Rodrigues Bruno Bonaccorsi Fernandino Bruno Goncalves Silva Bruno Sarno Vidal Bruno Valle Pinheiro Bruno Vilela Costa Pinto Carlos Augusto Ramos Feijo Carlos de Abreu Filho Carlos Eduardo da Costa Nunes Bosso Carlos Eduardo Nassif Moreira Carlos Henrique Ferreira Ramos Carmen Tavares Cidamaiá Arantes Cintia Grion Ciro Leite Mendes Claudio Kmohan Claudio Piras Cristine Pilati Pileggi Castro Cyntia Lins Daniel Beraldo Daniel Fontes Daniela Boni Débora Castiglioni Denise de Moraes Paisani Durval Ferreira Fonseca Pedroso Ederson Roberto Mattos Edgar de Brito Sobrinho Edgar M. V. Troncoso Edison Moraes Rodrigues Filho Eduardo Enrico Ferrari Nogueira Eduardo Leme Ferreira Eduardo Souza Pacheco Euzebio Jodar Evandro L. A. Ferreira Fabiana Fernandes de Araujo Fabiana Schuelter Trevisol Fábio Ferreira Amorim Fabio Poianas Giannini Fabrício Primitivo Matos Santos Fátima Buarque Felipe Gallego Lima Fernando Antonio Alvares da Costa Fernando Cesar dos Anjos Sad Fernando G. Aranha Fernando Ganem Flavio Callil Francisco Flávio Costa Filho Frederico Toledo Campo Dall´Arto Geovani Moreno Gilberto Friedman Giulliana Martines Moralez Guilherme Abdalla da Silva Guilherme Costa Guilherme Silva Cavalcanti Guilherme Silva Cavalcanti Gustavo Navarro Betônico Gustavo Navarro Betônico Hélder Reis Helia Beatriz N. Araujo Helio Anjos Hortiz Júnior Helio Penna Guimaraes Hugo Urbano Israel Maia Ivan Lopes Santiago Filho Jamil Farhat Júnior Janu Rangel Alvarez Joel Tavares Passos Jorge Eduardo da Rocha Paranhos José Aurelio Marques José Gonçalves Moreira Filho Jose Neto Andrade José Onofre de C Sobrinho Jose Terceiro de Paiva Bezerra Juliana Apolônio Alves Juliana Ferreira Jussara Gomes Karina Midori Sato Karine Gerent Kathia Margarida Costa Teixeira Katia Aparecida Pessoa Conde Laércia Ferreira Martins Lanese Figueirêdo Leila Rezegue Leonardo Tcherniacovsk Leone Oliveira Ferraz Liane Cavalcante Ligia Rabelo Lilian Miilher Lisiane Garcia Luana Tannous Ludhmila Abrahão Hajjar Luís Eduardo Miranda Paciência Luiz Monteiro da Cruz Neto Macia Valeria Bley Marcelo Ferreira Sousa Marcelo Lourencini Puga Marcelo Luz Pereira Romano Marciano Nobrega Marcio Arbex Márcio Leite Rodrigues Márcio Osório Guerreiro Marcone Rocha Maria Angela Pangoni Alves Maria Angela Pangoni Alves Maria Doroti Rosa Mariza D’Agostino Dias Miquéias Martins Mirella de Oliveira Miriane Melo Silveira Moretti Mirna Matsui Octavio Messender Orlando Luís de Andrade Santarém Patricio Júnior Henrique da Silveira Paula Frizera Vassallo Paulo Antoniazzi Paulo César Gottardo Paulo Correia Paulo Ferreira Paulo Torres Pedro Gabrile M. de Barros e Silva Rafael Foernges Rafael Gomes Rafael Moraes Raimundo Nonato filho Renato Luis Borba Renato V Gomes Ricardo Cordioli Ricardo Lima Ricardo Pérez López Ricardo Rath de Oliveira Gargioni Richard Rosenblat Roberta Machado de Souza Roberto Almeida Roberto Camargo Narciso Roberto Marco Roberto waltrick Rodrigo Biondi Rodrigo Figueiredo Rodrigo Santana Dutra Roseane Batista Rouge Felipe Rubens Sergio da Silva Franco Sandra Houly Sara Socorro Faria Sergio Felix Pinto Sergio Luzzi Sergio Sant’ana Sergio Sonego Fernandes Sérgio Yamada Sérgio Zajac Sidiner Mesquita Vaz Silvia Aparecida Bezerra Bezerra Tatiana Bueno Tardivo Farhat Thiago Martins Santos Tiago Smith Ulysses V. A. Silva Valnei Bento Damasceno Vandack Nobre Vicente Cés de Souza Dantas Vivian Menezes Irineu Viviane Bogado Wagner Nedel Walther Campos Filho Weidson Dantas William Viana Wilson de Oliveira Filho Wilson Martins Delgadinho Simon Finfer Flavia Ribeiro Machado About the authors

RESUMO

Objetivo:

Descrever as práticas de ressuscitação volêmica em unidades de terapia intensiva brasileiras e compará-las com as de outros países participantes do estudo Fluid-TRIPS.

Métodos:

Este foi um estudo observacional transversal, prospectivo e internacional, de uma amostra de conveniência de unidades de terapia intensiva de 27 países (inclusive o Brasil), com utilização da base de dados Fluid-TRIPS compilada em 2014. Descrevemos os padrões de ressuscitação volêmica utilizados no Brasil em comparação com os de outros países e identificamos os fatores associados com a escolha dos fluidos.

Resultados:

No dia do estudo, foram incluídos 3.214 pacientes do Brasil e 3.493 pacientes de outros países, dos quais, respectivamente, 16,1% e 26,8% (p < 0,001) receberam fluidos. A principal indicação para ressuscitação volêmica foi comprometimento da perfusão e/ou baixo débito cardíaco (Brasil 71,7% versus outros países 56,4%; p < 0,001). No Brasil, a percentagem de pacientes que receberam soluções cristaloides foi mais elevada (97,7% versus 76,8%; p < 0,001), e solução de cloreto de sódio a 0,9% foi o cristaloide mais comumente utilizado (62,5% versus 27,1%; p < 0,001). A análise multivariada sugeriu que os níveis de albumina se associaram com o uso tanto de cristaloides quanto de coloides, enquanto o tipo de prescritor dos fluidos se associou apenas com o uso de cristaloides.

Conclusão:

Nossos resultados sugerem que cristaloides são usados mais frequentemente do que coloides para ressuscitação no Brasil, e essa discrepância, em termos de frequências, é mais elevada do que em outros países. A solução de cloreto de sódio 0,9% foi o cristaloide mais frequentemente prescrito. Os níveis de albumina sérica e o tipo de prescritor de fluidos foram os fatores associados com a escolha de cristaloides ou coloides para a prescrição de fluidos.

Descritores:
Hidratação; Cuidados críticos; Coloides; Soluções cristaloides; Hemodinâmica; Choque

Abstract

Objective:

To describe fluid resuscitation practices in Brazilian intensive care units and to compare them with those of other countries participating in the Fluid-TRIPS.

Methods:

This was a prospective, international, cross-sectional, observational study in a convenience sample of intensive care units in 27 countries (including Brazil) using the Fluid-TRIPS database compiled in 2014. We described the patterns of fluid resuscitation use in Brazil compared with those in other countries and identified the factors associated with fluid choice.

Results:

On the study day, 3,214 patients in Brazil and 3,493 patients in other countries were included, of whom 16.1% and 26.8% (p < 0.001) received fluids, respectively. The main indication for fluid resuscitation was impaired perfusion and/or low cardiac output (Brazil: 71.7% versus other countries: 56.4%, p < 0.001). In Brazil, the percentage of patients receiving crystalloid solutions was higher (97.7% versus 76.8%, p < 0.001), and 0.9% sodium chloride was the most commonly used crystalloid (62.5% versus 27.1%, p < 0.001). The multivariable analysis suggested that the albumin levels were associated with the use of both crystalloids and colloids, whereas the type of fluid prescriber was associated with crystalloid use only.

Conclusion:

Our results suggest that crystalloids are more frequently used than colloids for fluid resuscitation in Brazil, and this discrepancy in frequencies is higher than that in other countries. Sodium chloride (0.9%) was the crystalloid most commonly prescribed. Serum albumin levels and the type of fluid prescriber were the factors associated with the choice of crystalloids or colloids for fluid resuscitation.

Keywords:
Fluid therapy; Critical care; Colloids; Crystalloid solutions; Hemodynamics; Shock

INTRODUCTION

Fluid resuscitation is defined as intravenous fluid administration with the aim of improving tissue perfusion in shock states. It is one of the most common interventions in critically ill patients. Despite being a frequent intervention, fluid resuscitation lacks a clear definition. The choice of fluid to be administered as well as the dose and speed are not well determined, leading to differences in bedside practices.(11 Finfer S, Myburgh J, Bellomo R. Intravenous fluid therapy in critically ill adults. Nat Rev Nephrol. 2018;14(9):541-57.,22 Myburgh JA, Mythen MG. Resuscitation fluids. N Engl J Med. 2013;369(13):1243-51.)

In the last 15 years, multiple randomized controlled trials and subsequent meta-analyses have shown that the type of fluid used for resuscitation, particularly hydroxyethyl starch (HES), may negatively affect outcomes.(33 Myburgh JA, Finfer S, Bellomo R, Billot L, Cass A, Gattas D, Glass P, Lipman J, Liu B, McArthur C, McGuinness S, Rajbhandari D, Taylor CB, Webb SA; CHEST Investigators; Australian and New Zealand Intensive Care Society Clinical Trials Group. Hydroxyethyl starch or saline for fluid resuscitation in intensive care. N Engl J Med. 2012;367(20):1901-11.

4 Perner A, Haase N, Guttormsen AB, Tenhunen J, Klemenzson G, Aneman A, Madsen KR, Møller MH, Elkjær JM, Poulsen LM, Bendtsen A, Winding R, Steensen M, Berezowicz P, Søe-Jensen P, Bestle M, Strand K, Wiis J, White JO, Thornberg KJ, Quist L, Nielsen J, Andersen LH, Holst LB, Thormar K, Kjældgaard AL, Fabritius ML, Mondrup F, Pott FC, Møller TP, Winkel P, Wetterslev J; 6S Trial Group; Scandinavian Critical Care Trials Group. Hydroxyethyl starch 130/0.42 versus Ringer's acetate in severe sepsis. N Engl J Med. 2012;367(2):124-34.

5 Yates DR, Davies SJ, Milner HE, Wilson RJ. Crystalloid or colloid for goal-directed fluid therapy in colorectal surgery. Br J Anaesth. 2014;112(2):281-9.

6 Annane D, Siami S, Jaber S, Martin C, Elatrous S, Declère AD, Preiser JC, Outin H, Troché G, Charpentier C, Trouillet JL, Kimmoun A, Forceville X, Darmon M, Lesur O, Reignier J, Abroug F, Berger P, Clec'h C, Cousson J, Thibault L, Chevret S; CRISTAL Investigators. Effects of fluid resuscitation with colloids vs crystalloids on mortality in critically ill patients presenting with hypovolemic shock: the CRISTAL trial. JAMA. 2013;310(17):1809-17.

7 Caironi P, Tognoni G, Masson S, Fumagalli R, Persenti A, Romero M, Fanizza C, Caspani L, Faenza S, Grasselli G, Iapichino G, Antonelli M, Parrini V, Fiore G, Latini R, Gattinoni L; ALBIOS Study Investigators. Albumin replacement in patients with severe sepsis or septic shock. N Engl J Med. 2014;370(15):1412-21.

8 Zarychanski R, Abou-Setta AM, Turgeon AF, Houston BL, McIntyre L, Marshall JC, et al. Association of hydroxyethyl starch administration with mortality and acute kidney injury in critically ill patients requiring volume resuscitation: a systematic review and meta-analysis. JAMA. 2013;309(7):678-88.

9 Gattas DJ, Dan A, Myburgh J, Billot L, Lo S, Finfer S; CHEST Management Committee. Fluid resuscitation with 6% hydroxyethyl starch (130/0.4) in acutely ill patients: an updated systematic review and meta-analysis. Anesth Analg. 2012;114(1):159-69.

10 Gillies MA, Habicher M, Jhanji S, Sander M, Mythen M, Hamilton M, et al. Incidence of postoperative death and acute kidney injury associated with i.v. 6% hydroxyethyl starch use: systematic review and meta-analysis. Br J Anaesth. 2014;112(1):25-34.

11 Perel P, Roberts I, Ker K. Colloids versus crystalloids for fluid resuscitation in critically ill patients. Cochrane Database Syst Rev. 2013;(2):CD000567.
-1212 Rochwerg B, Alhazani W, Sindi A, Heels-Ansdell D, Thabane L, Fox-Robichaud A, Mbuagbaw L, Szczeklik W, Alshamsi F, Altayyar S, Ip WC, Li G, Wang M, Wludarczyk A, Zhou Q, Guyatt GH, Cook DJ, Jaeschke R, Annane D; Fluids in Sepsis and Septic Shock Group. Fluid resuscitation in sepsis: a systematic review and network meta-analysis. Ann Intern Med. 2014;161(5):347-55.) Even with recent published guidelines including new evidences,(1313 Cecconi M, De Backer D, Antonelli M, Beale R, Bakker J, Hofer C, et al. Consensus on circulatory shock and hemodynamic monitoring. Task force of the European Society of Intensive Care Medicine. Intensive Care Med. 2014;40(12):1795-815.,1414 Rhodes A, Evans LE, Alhazzani W, Levy MM, Antonelli M, Ferrer R, et al. Surviving Sepsis Campaign: International Guidelines for Management of Sepsis and Septic Shock: 2016. Intensive Care Med. 2017;43(3):304-77.) delays and failures with translating recommendations into practice are common, leading to variability in care.(1515 Vander Schaaf EB, Seashore CJ, Randolph GD. Translating Clinical Guidelines Into Practice: Challenges and Opportunities in a Dynamic Health Care Environment. N C Med J. 2015;76(4):230-4.,1616 Lira A, Pinsky MR. Choices in fluid type and volume during resuscitation: impact on patient outcomes. Ann Intensive Care. 2014;4:38.) The Saline versus Albumin Fluid Evaluation - Translation of Research Into Practice Study (SAFE-TRIPS), a cross-sectional study conducted in 2007 including 391 intensive care units (ICUs) across 25 countries, reported that resuscitation practices varied significantly. Although colloid solutions were more expensive and may possibly be harmful in some patients, they were administered to more patients and during more resuscitation episodes than crystalloids.(1717 Finfer S, Liu B, Taylor C, Bellomo R, Billot L, Cook D, Du B, McArthur C, Myburgh J; SAFE TRIPS Investigators. Resuscitation fluid use in critically ill adults: an international cross-sectional study in 391 intensive care units. Crit Care. 2010;14(5):R185.)

Recently, the same group conducted a similar observational study in a convenience sample of ICUs: the Fluid-TRIPS.(1818 Hammond NE, Taylor C, Finfer S, Machado FR, An Y, Billot L, Bloos F, Bozza F, Cavalcanti AB, Correa M, Du B, Hjortrup PB, Li Y, McIntryre L, Saxena M, Schortgen F, Watts NR, Myburgh J; Fluid-TRIPS and Fluidos Investigators; George Institute for Global Health, The ANZICS Clinical Trials Group, BRICNet, and the REVA research Network. Patterns of intravenous fluid resuscitation use in adult intensive care patients between 2007 and 2014: An international cross-sectional study. PLoS One. 2017;12(5):e0176292.) This study demonstrated an important change in clinical practice, with a preferential use of crystalloids, specifically buffered salt solutions, over colloids. Another interesting finding of this study was that fluid choice was determined by local practice rather than by any identifiable patient characteristic.

The number of contributing ICUs from Brazil in the Fluid-TRIPS was just over half of all participating units, allowing the unique opportunity to separately analyze Brazilian data. Our hypothesis was that Brazilian ICUs would have different standards for fluid resuscitation, mainly regarding the choice of crystalloids.

Thus, the objective of this study was to describe current practices on fluid resuscitation in Brazilian ICUs and to compare Brazil with the other countries participating in the study.

METHODS

This secondary analysis of a prospective, international, cross-sectional, observational study was carried out in a convenience sample of ICUs in 27 countries using the Fluid-TRIPS database, compiled in 2014.(1818 Hammond NE, Taylor C, Finfer S, Machado FR, An Y, Billot L, Bloos F, Bozza F, Cavalcanti AB, Correa M, Du B, Hjortrup PB, Li Y, McIntryre L, Saxena M, Schortgen F, Watts NR, Myburgh J; Fluid-TRIPS and Fluidos Investigators; George Institute for Global Health, The ANZICS Clinical Trials Group, BRICNet, and the REVA research Network. Patterns of intravenous fluid resuscitation use in adult intensive care patients between 2007 and 2014: An international cross-sectional study. PLoS One. 2017;12(5):e0176292.)

In Brazil, we recruited participating sites at critical care meetings through the Brazilian Research in Critical Care network (BRICNet) website and contacts and personal contacts with key opinion leaders. Participation was voluntary, and any hospital willing to join the study was considered eligible, with no exclusion criteria. The coordinating center was the Universidade Federal de São Paulo, and the institution’s Ethics and Research Committee approved the study protocol under the number CAAE 36093314.4.1001.5505 with a waiver for Informed Consent considering the observational nature of the study.

Participants and data collection

In Brazil, the sites collected data on any single day between December 9th and 11th 2014. Methodological details were previously published.(1818 Hammond NE, Taylor C, Finfer S, Machado FR, An Y, Billot L, Bloos F, Bozza F, Cavalcanti AB, Correa M, Du B, Hjortrup PB, Li Y, McIntryre L, Saxena M, Schortgen F, Watts NR, Myburgh J; Fluid-TRIPS and Fluidos Investigators; George Institute for Global Health, The ANZICS Clinical Trials Group, BRICNet, and the REVA research Network. Patterns of intravenous fluid resuscitation use in adult intensive care patients between 2007 and 2014: An international cross-sectional study. PLoS One. 2017;12(5):e0176292.) Briefly, the study day was defined as a 24-hour period. The investigators included all patients over 16 years old who required one or more fluid resuscitation episodes during the study period. There were no exclusion criteria. The total number of patients being treated in the ICUs on the study day was also recorded. We defined a fluid resuscitation episode as an hour during which a patient received a specifically prescribed intravenous fluid bolus of any crystalloid or colloid solution, a continuous infusion of 5mL/kg/hour or greater of crystalloid and/or any dose of colloid by continuous infusion.(1818 Hammond NE, Taylor C, Finfer S, Machado FR, An Y, Billot L, Bloos F, Bozza F, Cavalcanti AB, Correa M, Du B, Hjortrup PB, Li Y, McIntryre L, Saxena M, Schortgen F, Watts NR, Myburgh J; Fluid-TRIPS and Fluidos Investigators; George Institute for Global Health, The ANZICS Clinical Trials Group, BRICNet, and the REVA research Network. Patterns of intravenous fluid resuscitation use in adult intensive care patients between 2007 and 2014: An international cross-sectional study. PLoS One. 2017;12(5):e0176292.)

We recorded information on fluid availability in the participating ICUs as well as data related to patients, including demographic data, illness severity scores, admission diagnosis, laboratory test data, clinical data on the study day, predefined subgroup characteristics (trauma, traumatic brain injury - TBI, sepsis, and acute respiratory distress syndrome - ARDS), and information on the type and volume of fluids for resuscitation. The reason for fluid resuscitation and the prescriber characteristics were also recorded. We defined specialist or assistant physician as the board-certified intensivist or the physician responsible for the ICU on the study day. We defined senior resident or fellow as graduated students or residents in the last years of their residency, and we defined residents as those in the first years of their residency regardless of the specialty as it is usual in Brazil to have residents of different specialties in training.

We collected all data using an electronic data capture system (REDCap, Vanderbilt University, Tennessee, USA), hosted at Instituto D’Or de Ensino e Pesquisa, Rio de Janeiro, Brazil.

Statistical analysis

Continuous variables are expressed as the mean ± standard deviation - SD or the median [interquartile range]. Categorical variables are expressed as counts (percentages). The comparison of the data between Brazil and other countries and between the administration of colloids and crystalloids in Brazilian patients were performed using a t-test or Wilcoxon rank-sum test for continuous data or Pearson’s chi-squared test for categorical data, as appropriate. Differences in the proportions of crystalloid and colloid episodes were tested using generalized estimating equations (GEEs), accounting for clustering at the patient level.

As in the main study,(1818 Hammond NE, Taylor C, Finfer S, Machado FR, An Y, Billot L, Bloos F, Bozza F, Cavalcanti AB, Correa M, Du B, Hjortrup PB, Li Y, McIntryre L, Saxena M, Schortgen F, Watts NR, Myburgh J; Fluid-TRIPS and Fluidos Investigators; George Institute for Global Health, The ANZICS Clinical Trials Group, BRICNet, and the REVA research Network. Patterns of intravenous fluid resuscitation use in adult intensive care patients between 2007 and 2014: An international cross-sectional study. PLoS One. 2017;12(5):e0176292.) multivariable analyses using GEEs accounting for clustering at the patient level were conducted to determine associations between patient demographics, clinical characteristics and the type of fluid administered. We used 2 binary outcomes in the analysis: 1) crystalloid episode Yes versus crystalloid episode No, and 2) colloid episode Yes versus colloid episode No. The denominators of these two outcomes were the total number of fluid episodes; thus, as a given patient could have received crystalloids as well as colloids within the same hour (the same fluid episode), the total number of fluid episodes was higher than the sum of crystalloid episodes and colloid episodes. As these outcomes were analyzed separately, two different sets of odds ratios (ORs) were generated for each variable. Variables meeting a predetermined level of statistical significance (p < 0.1) with the administration of crystalloids or colloids in univariate models were included in the final multivariable model. Associations were considered statistically significant if p < 0.01. The results of the multivariable analysis are presented as adjusted ORs and 95% confidence intervals (95%CI). Details regarding the handling of missing data are provided in the main paper.(1818 Hammond NE, Taylor C, Finfer S, Machado FR, An Y, Billot L, Bloos F, Bozza F, Cavalcanti AB, Correa M, Du B, Hjortrup PB, Li Y, McIntryre L, Saxena M, Schortgen F, Watts NR, Myburgh J; Fluid-TRIPS and Fluidos Investigators; George Institute for Global Health, The ANZICS Clinical Trials Group, BRICNet, and the REVA research Network. Patterns of intravenous fluid resuscitation use in adult intensive care patients between 2007 and 2014: An international cross-sectional study. PLoS One. 2017;12(5):e0176292.) All analyses were carried out using the R statistical software package, version 3.1.0 (2014-04-10).

RESULTS

In Brazil, 217 ICUs participated in the study (participating centers are listed at the end of this manuscript). The overall summary of FLUID-TRIPS data is shown in table 1. Data on the participation of other countries can be found in detail in the main study.(1818 Hammond NE, Taylor C, Finfer S, Machado FR, An Y, Billot L, Bloos F, Bozza F, Cavalcanti AB, Correa M, Du B, Hjortrup PB, Li Y, McIntryre L, Saxena M, Schortgen F, Watts NR, Myburgh J; Fluid-TRIPS and Fluidos Investigators; George Institute for Global Health, The ANZICS Clinical Trials Group, BRICNet, and the REVA research Network. Patterns of intravenous fluid resuscitation use in adult intensive care patients between 2007 and 2014: An international cross-sectional study. PLoS One. 2017;12(5):e0176292.) During the 24-hour study period, 3,214 patients were included in Brazil, of whom 519 (16.1%) received fluids. Almost half of the patients received fluids within the first two days of ICU admission (46%). The baseline characteristics of patients in Brazil and those of patients in the other countries are shown in table 2.

Table 1
Overall summary of Fluid-TRIPS
Table 2
Baseline characteristics of patients in Brazil and other countries

In 880 fluid resuscitation episodes in Brazil, a specialist was the main fluid prescriber (82.3%), and the main indication for fluid resuscitation was impaired perfusion and/or low cardiac output (71.7%) (Table 3 and Table 1S in Supplementary material). The total volume of resuscitation fluid received and net fluid balance on the survey day were higher in Brazil than in other countries (Table 4).

Table 3
Indications for fluid resuscitation in Brazil and in other countries
Table 4
Characteristics of fluids received per patient in Brazil and other countries

Compared to other countries, crystalloid solutions were more frequently used than colloid solutions in Brazil (Figure 1). In Brazil, 0.9% sodium chloride was significantly more commonly used than in other countries (62.5% versus 27.1%, p < 0.0001) (Table 1S - Supplementary material), despite the availability of different fluids at the participating ICUs (Table 2S - Supplementary material). In Brazil and other countries, the most commonly used balanced crystalloid solution was Ringer’s lactate. Plasma Lyte was used more frequently in other countries than in Brazil (Table 1S - Supplementary material). The percentage of patients receiving crystalloid or colloid solutions or the number of crystalloid or colloid episodes were not modified in the presence of trauma, TBI, sepsis or ARDS. These conditions did not lead to significant changes in the total volume of resuscitation fluid received on the survey day. However, patients with sepsis and ARDS had a higher net fluid balance on the survey day (Table 3S to Table 6S - Supplementary material).

Figure 1
Percentage of fluid resuscitation episodes in Brazil and other countries. (A) Comparison of the choice of fluid in each of the fluid episodes. (B) Comparison of the choice of crystalloids in episodes in which crystalloids were used. (C) Comparison of the choice of colloids in episodes in which colloids were used. Percentages may not add to 100%, as patients can be administered more than one type of fluid during resuscitation episodes. HES - hydroxyethyl starch.

We analyzed the factors associated with the choice of crystalloids or colloids for fluid resuscitation episodes. The multivariable analysis (Table 5) suggested that, in Brazil, lower albumin levels (i.e., < 27g/dL, ≥ 27g/dL, or missing), in general, were associated with both the use of crystalloids and colloids (p = 0.001 and < 0.0001, respectively).

Table 5
Multivariate analysis of factors associated with the choice of crystalloid or colloid for fluid resuscitation episodes in Brazilian patients

Among the patients who received crystalloids, the odds of having an albumin level ≥ 2g/dL were 9.4 times (OR = 8.6 [0.8 - 89.8]) that of having an albumin level < 27g/dL.

There was also a higher chance of having unknown/missing values for albumin (OR = 7.2, 95%CI = 2.5 - 20.7) than having an albumin level < 27g/dL. Similarly, among those who received colloids, the odds of having an albumin level ≥ 27g/dL was one-fiftieth (OR = 0.2 [0.0 - 0.9]) that of having levels < 27g/dL. In addition, for patients receiving crystalloids, the odds of them being prescribed by a senior resident/fellow was 9.9 times higher (OR = 9.9, 95%CI = 3.6 - 27.7) than that of them being prescribed by a specialist/assistant physician. For patients receiving colloids, there was no clear association with fluid prescriber. The univariate analysis is available in table 7S (Supplementary material).

DISCUSSION

Our results demonstrated that in Brazil, crystalloids were more frequently used than colloids for fluid resuscitation. In other countries, crystalloids were also the fluid of choice, but in Brazil, the proportion was significantly higher. Sodium chloride (0.9%) was the most prescribed crystalloid in Brazil, despite the availability of balanced solutions. In other countries, balanced solutions were the preferred crystalloids. The availability of serum levels and the current albumin level were the factors associated with the choice of crystalloids or colloids for fluid resuscitation. In addition, the type of fluid prescriber was significantly associated with crystalloid use.

The results in Brazil are consistent with more recent studies regarding fluid resuscitation practices. Fluid resuscitation aims at improving tissue perfusion by restoring the perfusion pressure of vital organs and ensuring adequate cardiac output.(1313 Cecconi M, De Backer D, Antonelli M, Beale R, Bakker J, Hofer C, et al. Consensus on circulatory shock and hemodynamic monitoring. Task force of the European Society of Intensive Care Medicine. Intensive Care Med. 2014;40(12):1795-815.) Aligned with these principles, the main indications for fluid administration in Brazilian ICUs were similar to those found in the main study and in other studies addressing this issue.(1818 Hammond NE, Taylor C, Finfer S, Machado FR, An Y, Billot L, Bloos F, Bozza F, Cavalcanti AB, Correa M, Du B, Hjortrup PB, Li Y, McIntryre L, Saxena M, Schortgen F, Watts NR, Myburgh J; Fluid-TRIPS and Fluidos Investigators; George Institute for Global Health, The ANZICS Clinical Trials Group, BRICNet, and the REVA research Network. Patterns of intravenous fluid resuscitation use in adult intensive care patients between 2007 and 2014: An international cross-sectional study. PLoS One. 2017;12(5):e0176292.,1919 Cecconi M, Hofer C, Teboul JL, Pettila V, Wilkman E, Molnar Z, Della Rocca G, Aldecoa C, Artigas A, Jog S, Sander M, Spies C, Lefrant JY, De Backer D; FENICE Investigators; ESICM Trial Group. Fluid challenges in intensive care: the FENICE study: A global inception cohort study. Intensive Care Med. 2015;41(9):1529-37.) Our results also showed a reduction in the use of colloid solutions.(1818 Hammond NE, Taylor C, Finfer S, Machado FR, An Y, Billot L, Bloos F, Bozza F, Cavalcanti AB, Correa M, Du B, Hjortrup PB, Li Y, McIntryre L, Saxena M, Schortgen F, Watts NR, Myburgh J; Fluid-TRIPS and Fluidos Investigators; George Institute for Global Health, The ANZICS Clinical Trials Group, BRICNet, and the REVA research Network. Patterns of intravenous fluid resuscitation use in adult intensive care patients between 2007 and 2014: An international cross-sectional study. PLoS One. 2017;12(5):e0176292.

19 Cecconi M, Hofer C, Teboul JL, Pettila V, Wilkman E, Molnar Z, Della Rocca G, Aldecoa C, Artigas A, Jog S, Sander M, Spies C, Lefrant JY, De Backer D; FENICE Investigators; ESICM Trial Group. Fluid challenges in intensive care: the FENICE study: A global inception cohort study. Intensive Care Med. 2015;41(9):1529-37.
-2020 Hammond NE, Taylor C, Saxena M, Liu B, Finfer S, Glass P, et al. Resuscitation fluid use in Australian and New Zealand Intensive Care Units between 2007 and 2013. Intensive Care Med. 2015;41(9):1611-9.) The evidence of harm from recent randomized clinical trials (RCTs) with synthetic colloids such as HES (3-12) could explain the preference for crystalloid solutions in Brazil and in other countries. It is interesting to note that the higher proportion of the use of colloids in other countries is represented by the use of albumin. As albumin is expensive, the costs may have limited its use in Brazil, a middle-income country.(2121 Falcão H, Japiassú AM. Uso de albumina humana em pacientes graves: controvérsias e recomendações. Rev Bras Ter Intensiva. 2010;23(1):87-95.)

Another aspect that differentiates Brazil from other countries was the use of 0.9% sodium chloride as the crystalloid solution of choice. Although Plasmalyte is a high-cost balanced solution in Brazil, there are low-cost balanced solutions available (e.g., Ringer’s lactate). Our study was not designed to assess the potential reasons for this difference between Brazil and other countries. It is possible that this was influenced by the variation in availability among the sites and countries, which would bias any further analysis. The relatively small number of patients and variables in our database might also compromise the reliability of eventual findings. Another possible explanation is a cultural preference derived from years of using saline potentially associated with a reduced awareness of the potential adverse effects of hyperchloremic solutions, as the controversy around balanced vs. unbalanced crystalloids was not as intense as it is currently.(2222 Young P, Bailey M, Beasley R, Henderson S, Mackle D, McArthur C, McGuinness S, Mehrtens J, Myburgh J, Psirides A, Reddy S, Bellomo R; SPLIT Investigators; ANZICS CTG. Effect of a Buffered Crystalloid Solution vs Saline on Acute Kidney Injury Among Patients in the Intensive Care Unit: The SPLIT Randomized Clinical Trial. JAMA. 2015;314(16):1701-10.

23 Semler MW, Self WH, Rice TW. Balanced Crystalloids versus Saline in Critically Ill Adults. N Engl J Med. 2018;378(20):1951.
-2424 Self WH, Semler MW, Wanderer JP, Wang L, Byrne DW, Collins SP, Slovis CM, Lindsell CJ, Ehrenfeld JM, Siew ED, Shaw AD, Bernard GR, Rice TW; SALT-ED Investigators. Balanced Crystalloids versus Saline in Noncritically Ill Adults. N Engl J Med. 2018;378(9):819-28.) We believe our findings are potentially useful for hypothesis generation, and further studies are necessary to better evaluate potential factors associated with this choice.

Sepsis, ARDS, trauma and TBI did not influence the choice between colloids and crystalloids. The uncertainty about the ideal fluid for these specific diseases could explain this finding.(2525 Martin C, Cortegiani A, Gregoretti C, Martin-Loeches I, Ichai C, Leone M, et al. Choice of fluids in critically ill patients. BMC Anesthesiol. 2018;18(1):200.) However, in Brazilian ICUs, albumin serum levels had a clear role in guiding the choice of fluid. This preference is not supported by the available evidence. The results from high-quality RCTs suggest that intravenous albumin administration does not reduce the mortality rate in mixed populations of critically ill patients, including those who have hypoalbuminemia.(2626 SAFE Study Investigators, Finfer S, Bellomo R, McEvoy S, Lo SK, Myburgh J, Neal B, et al. Effect of baseline serum albumin concentration on outcome of resuscitation with albumin or saline in patients in intensive care units: analysis of data from the saline versus albumin fluid evaluation (SAFE) study. BMJ. 2006;333(7577):1044.) Even albumin supplementation in addition to crystalloids targeting serum concentrations higher than 30g per liter in septic patients did not improve survival at 28 and 90 days.(2727 Caironi P, Tognoni G, Masson S, Fumagalli R, Pesenti A, Romero M, Fanizza C, Caspani L, Faenza S, Grasselli G, Iapichino G, Antonelli M, Parrini V, Fiore G, Latini R, Gattinoni L; ALBIOS Study Investigators. Albumin replacement in patients with severe sepsis or septic shock. N Engl J Med. 2014;370(15):1412-21.) Thus, we believe that this finding probably reflects local practice patterns rather than solid evidence. It is worth mentioning that senior residents and fellows were more likely to prescribe crystalloid fluids to patients than specialists, probably suggesting that academic exposure to scientific evidence promotes changes in practice behaviors.(2828 Institute of Medicine (US) Committee on Standards for Developing Trustworthy Clinical Practice Guidelines; Graham R, Mancher M, Miller Wolman D, et al., editors. Clinical Practice Guidelines We Can Trust. Washington (DC): National Academies Press (US); 2011. 6, Promoting Adoption of Clinical Practice Guidelines. [cited 2020 Jan 13]. Available from: https://www.ncbi.nlm.nih.gov/books/NBK209543/
https://www.ncbi.nlm.nih.gov/books/NBK20...
) Another potential explanation is the generation difference. The specialists were previously exposed to a cultural environment in which colloids were heavily used based on their potential better effect on oncotic pressure. In contrast, the new generation, composed of residents and fellows, was exposed to scientific evidence of harm with colloid use. This also suggests that continuous training, even for specialists, is important to ensure better quality of care.

This study has strengths and some limitations, some of which were mentioned in the main study.(1818 Hammond NE, Taylor C, Finfer S, Machado FR, An Y, Billot L, Bloos F, Bozza F, Cavalcanti AB, Correa M, Du B, Hjortrup PB, Li Y, McIntryre L, Saxena M, Schortgen F, Watts NR, Myburgh J; Fluid-TRIPS and Fluidos Investigators; George Institute for Global Health, The ANZICS Clinical Trials Group, BRICNet, and the REVA research Network. Patterns of intravenous fluid resuscitation use in adult intensive care patients between 2007 and 2014: An international cross-sectional study. PLoS One. 2017;12(5):e0176292.) This is the first study to describe resuscitation fluid practices in a large sample of Brazilian ICUs. The use of standard case report forms and definitions across all countries and detailed information on clinical factors that may potentially influence the choice of fluid for resuscitation at the time of the fluid episode allowed not only comparisons with other countries but also analyses of national practice patterns. Among the limitations of the study, it is important to mention the generalizability of the results. Even with a large sample of ICUs, the use of convenience sampling might have not reflected practices adopted in all Brazilian ICUs. Another limitation is the definition of fluid resuscitation episodes.(1818 Hammond NE, Taylor C, Finfer S, Machado FR, An Y, Billot L, Bloos F, Bozza F, Cavalcanti AB, Correa M, Du B, Hjortrup PB, Li Y, McIntryre L, Saxena M, Schortgen F, Watts NR, Myburgh J; Fluid-TRIPS and Fluidos Investigators; George Institute for Global Health, The ANZICS Clinical Trials Group, BRICNet, and the REVA research Network. Patterns of intravenous fluid resuscitation use in adult intensive care patients between 2007 and 2014: An international cross-sectional study. PLoS One. 2017;12(5):e0176292.) Finally, the interpretation of fluid administration practices in specific patient populations, such as those with sepsis, requires caution due to relatively small patient numbers.

CONCLUSION

Crystalloids were more frequently used than colloids for fluid resuscitation in Brazilian intensive care units. Sodium chloride (0.9%) was the most prescribed crystalloid in Brazil, despite the availability of balanced solutions. The availability of serum levels and the low albumin level were the factors that influenced the choice between crystalloid or colloid for fluid resuscitation. In addition, senior residents/fellows were more likely to prescribe crystalloid fluids to patients than specialists.

  • Clinical Trials register: Clinicaltrials.gov: Fluid-Translation of research into practice study (Fluid-TRIPS) - NCT02002013.

ACKNOWLEDGMENTS

The original study was partially supported by unrestricted fluid grants from Baxter Healthcare and CSL Behring paid to the George Institute for Global Health. NH received a National Health and Medical Research Council of Australia Postgraduate Scholarship (2012±2014) that supported part of this work [APP1039312]. The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation of the manuscript; or decision to submit the manuscript for publication.

Brazilian participating sites

Country coordinator: Flavia R Machado.

Albert Sabin Hospital e Maternidade - SR Zajac; Associação Beneficente Hospital Unimar - A Campos, D de Albuquerque; Associação Hospitalar Beneficente São Vicente de Paulo - J Gomez; Casa de Caridade de Carangola - S Vaz; Casa de Saúde Campinas - B Campos, W Delgadinho; Casa de Saúde Santa Lúcia - RT Amâncio, VC Souza-Dantas; Clínica Campo Grande - V Damasceno, J dos Santos; Clínica Dom Rodrigo - F de Araújo, I do Nascimento; Complexo Hospitalar Ortotrauma de Mangabeira - F de Araújo, I do Nascimento; Fundação Doutor Amaral Carvalho - M Higashi, E Mattos; Fundação Pio XII- Hospital de Câncer de Barretos - CP Amendola, UVA Silva; Hospital São José - F Dal-Pizzol, C Ritter; Hospital 9 de Julho - UTI 10a andar - MD D’Agostino; Hospital 9 de Julho - UTI 11a andar - C Moreira; Hospital 9 de Julho - UTI 1a andar - C Moreira; Hospital 9 de Julho - UTI 8a andar - L da Cruz Neto; Hospital 9 de Julho - UTI 9a andar - F Ganem; Hospital Adventista de Belém - ME de Oliveira, E Sobrinho; Hospital Adventista de Manaus - P Ferreira, R Rabelo; Hospital Alemão Oswaldo Cruz - R Cordioli, F Zampieri; Hospital Alvorada Brasília - ACC Cembranel, EJ Nascimento; Hospital Alvorada Taguatinga - RS Biondi, E Milhomem; Hospital Amecor - Unidade Coronariana - M Bley; Hospital Amecor - UTI Geral - M Bley; Hospital Anis Rassi - G Canedo, R Filho; Hospital Assunção - M Fukushima, L Miilher; Hospital Beneficência Portuguesa - UTI do Choque - S Houly; Hospital Brigadeiro - EC Maitan, OL Santarém; Hospital Carlos da Silva Lacaz - A Ferreira, E Ferreira; Hospital Casa de Saúde de Santos - P Rosateli, A Scazufka; Grupo Hospitalar Nossa Senhora da Conceição - W Nedel, VM Oliveira; Hospital Copa D’Or - CTI Amarelo - L Rabello, W Viana; Hospital Copa D’Or UPO 2 - AP Santos, W Viana; Hospital Copa D’Or - UTI Azul - L Tanaka, W Viana; Hospital Copa D’Or - UTI Pós-Operatória - L Salles, AP Santos; Hospital Copa D’Or - CTI Verde - K Ebecken, W Viana; Hospital Copa D’Or - Neurointensiva - D Musse, L Rabello; Hospital Copa D’Or - UTI Lilás - L Rabello, L Tanaka; Hospital da Luz Vila Mariana - F Filho, F dos Santos Borges; Hospital da Restauração - K Monteiro, F Buarque; Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo - UTI Emergências Clínicas - P Mendes, L Taniguchi; Hospital das Clínicas da Faculdade de Medicina de Botucatu - L de Stefano, A Gut; Hospital das Clínicas da Faculdade Ribeirão Preto - M Auxiliadora-Martins, ML Puga; Hospital das Clínicas da Universidade Federal de Minas Gerais - V Nobre; Hospital das Clínicas da Universidade Federal do Espírito Santo - LM Caixeta, PF Vassallo; Hospital das Clínicas de Porto Alegre - RB Moraes, J Vidart; Hospital de Base - Faculdade de Medicina de São José do Rio Preto - H Batista, SM Lobo; Hospital de Caridade Astrogildo de Azevedo - CB da Silva, C Kmohan; Hospital de Clínicas Gaspar Vianna - C da Rocha, H Reis; Hospital de Urgência - UTI Geral 1 - D Pedroso, J Sobrinho; Hospital de Urgência - UTI Geral 4 - S Faria; Hospital de Urgência - UTI Neurológica 3 - J Sobrinho; Hospital de Urgência - UTI Trauma 2 - S Faria, D Pedroso; Hospital Distrital Evandro Ayres de Moura - L Figueiredo, H Magalhaes; Hospital do Coração - MLP Romano, R Vasconcelos; Hospital do Coração do Brasil - H Araújo, M de Araújo; Hospital do Rim e Hipertensão - AT Bafi, FGR Freitas; Hospital do Servidor Público Estadual - S Luzzi, D Ortega; Hospital do Servidor Público Municipal de São Paulo - T Farhat; Hospital do Servidor Público Municipal de São Paulo - UTI 7a andar - KM Sato; Hospital do Subúrbio - J Motta, C Lins; Hospital do Trabalhador - A Rea-Neto, F Reese; Hospital Dom Hélder - RAF Gomes, ARA Macedo Júnior; Hospital Dom Vicente Scherer - EM Rodrigues Filho, M Hadrich; Hospital e Maternidade Municipal Dr. Odelmo Leão Carneiro - C Arantes, MAS Toneto; Hospital e Maternidade Otaviano Neves - B Fernandino, A Pereira; Hospital e Pronto-Socorro 28 de Agosto - L Cavalcante, A Matos; Hospital Ecoville - L Araújo, A Rea-Neto; Hospital Escola da Faculdade de Medicina de Jundiaí - E Ferreira; Hospital Estadual de Urgência e Emergência de Vitória - L Dornelas, L Tcherniacovsk; Hospital Estadual Getúlio Vargas - UTI 1 - A Rodrigues, K Schechter; Hospital Estadual Getúlio Vargas - UTI 2 - F Montesanto, B Vidal; Hospital Estadual Getúlio Vargas - UTI 3 - C Frambach, G Moralez; Hospital Estadual Getúlio Vargas - UTI 4 - F Callil, V Montez; Hospital Estadual Rocha Faria - CHF Ramos; Hospital Evangélico de Londrina - J Festti, C Grion; Hospital Evangélico de Sorocaba - A de Souza, M Marabezi; Hospital Federal dos Servidores do Estado RJ - M Bissoli, J Marques; Hospital Felício Rocho - D Fontes, C Ranyere; Hospital Fernandes Távora - A Batista, L Martins; Hospital e Maternidade Galileo - W Delgadinho, M Rocha; Hospital Geral de Fortaleza - UTI Azul - C Feijó, V Araújo; Hospital Geral de Goiânia - D Pedroso, G Silva; Hospital Geral de Vitória da Conquista - M Martins, M Ribeiro II; Hospital Geral Dr. César Cals - A Justo, A Macedo; Hospital Goiânia Leste - M Nobrega, M Nobrega; Hospital Hélio Anjos Ortiz - H Júnior, M Lazzarotto; Hospital IBR - J Andrade, L Souza; Hospital Estadual Ipiranga - S Fernandes, F Lombardi; Hospital Israelita Albert Einstein - TD Correa, M Assunção; Hospital Jardim Amália - C Arbex, M Arbex; Hospital Estadual Jayme Santos Neves - F dos Anjos Sad, E Stucchi; Hospital M’Boi Mirim - A Andrade, C de Abreu Filho; Hospital Madre Regina Prottman - D Colodetti, M Rodrigues; Hospital Marcelino Champagnat - M de Oliveira, A Rea-Neto; Hospital de Clínicas Mário Lioni - P Galhardo, A Japiassú; Hospital Maternidade e Pronto-Socorro Santa Lucia - R Bergo, F Dall’Orto; Hospital Maternidade São José - P Bernardes, R Figueiredo; Hospital Memorial São José - G Costa, K Monteiro; Hospital Moinhos de Vento - M Rosa, JHD Barth; Hospital Municipal de Paracatu - T Neiva, R de Souza; Hospital Municipal Dr. Munir Rafful - M Arbex, L de Oliveira; Hospital Municipal Irmã Dulce - D Boni, MOG Douglas; Hospital Municipal Dr. José Soares Hungria - K Conde, N Quintino; Hospital Municipal Padre Germano Lauck - R Almeida, J Fuck; Hospital Municipal Pedro II - E Paranhos, J Soares; Hospital Municipal Santa Isabel - A de Carvalho, C Tavares; Hospital Municipal São José - D Possamai, G Westphal; Hospital Nereu Ramos - E Berbigier, I Maia; Hospital Norte D’Or - J Pinto, S Sant’Anna; Hospital Nossa Senhora da Conceição - JM de Araújo, F Schuelter-Trevisol; Hospital Nossa Senhora dos Prazeres - A Gargioni, R Gargioni; Hospital Nossa Senhora Monte Serrat - MAP Alves; Hospital Novo Atibaia - A Bemfica, R Franco; Hospital Ortopédico - L da Silva, M Nobrega; Hospital Paulistano - I Campos, DT Noritomi; Hospital Paulo Sacramento - ELA Ferreira; Hospital PIO XII de São José dos Campos - Unidade Coronariana - M Durval, A Silva; Hospital Português - R Hermes, O Messeder; Hospital Primavera - J Feijó, E Nogueira; Hospital Professor Edmundo Vasconcelos - E Jodar, R Pereira; Hospital Regional de Sousa - P da Silveira, A Lunguinho; Hospital Regional de Itapetininga São Camilo - V Irineu, R Seabra; Hospital Regional de Jundiaí - G Cavalcanti, M Leão; Hospital Regional de Presidente Prudente - GN Betônico, LA Garcia; Hospital Regional de Samambaia - UTI 1 - F Amorim, C de Carvalho; Hospital Regional de Samambaia - UTI 2 - S Margalho, F Santos; Hospital Renascentista - D Beraldo, R dos Santos; Hospital Samaritano Rio de Janeiro - J Freitas, R Lima; Hospital Samaritano São Paulo - UTI 6a andar - B Mazza, S Almeida; Hospital Samaritano São Paulo - 3a andar - B Mazza, R Rocha; Hospital Samaritano João Pessoa - P Gottardo, C Mendes; Hospital Santa Helena - R Narciso, S Pantaleão; Hospital Santa Isabel - K Gerent; Hospital Santa Izabel - R Marco, D Vinho; Hospital Santa Juliana - EMV Troncoso, KLN Vilassante; Hospital Santa Lúcia - A Ventura, M da Silva; Hospital Santa Maria - M Nobrega, F Oliveira; Hospital Santa Maria - Intensibarra - I Santiago, A Lima; Hospital Santa Rita - F da Costa, M Vilela; Hospital Santa Rita - T Lisboa, A Torelly; Hospital São Camilo Ipiranga - M Dutra, F Giannini; Hospital São Camilo Pompéia - A Ramacciot, AT Maciel; Hospital São Francisco de Assis - GA da Silva, M da Silva; Hospital São João de Deus - G Gussen, M Rocha; Hospital São Lucas - UTI cirúrgica - C Santos, T Smith; Hospital São Lucas - UTI clínica - A Sobrinho, T Smith; Hospital São Lucas da Pontifícia Universidade Católica do Rio Grande do Sul - S Baldiserotto, M Moretti; Hospital São Marcos - UTI A - W Dantas, L Ishiy; Hospital São Marcos - UTI B - W Dantas, L Ishiy; Hospital São Mateus - JG Moreira Filho; Hospital Saúde da Mulher - N Machado, L Rezegue; Hospital Sepaco - AT Bafi, ES Pacheco; Hospital SOS Cárdio - F Aranha, R Saorin; Hospital Tereza Ramos - K de Paula, R Waltrick; Hospital TotalCor - A Batista, P de Barros e Silva; Hospital Uniclinic - M Serpa, J Terceiro; Hospital Unimed ABC - MOG Douglas, R Rosenblat; Hospital Unimed de Belo Horizonte - A Barbosa, C Nogueira; Hospital Unimed de Limeira - A de Carvalho, L Paciência; Hospital Unimed de Macaé - JT Passos, PTS Almeida; Hospital Unimed de Manaus - WO Filho, MM Lippi; Hospital Unimed Rio de Janeiro - M Assad, F Miranda; Hospital Unimed Rio de Janeiro - UTI Cardio - R Gomes, P Nogueira; Hospital Unimed Salto - MAP Alves; Hospital Universitário Cajuru - V Bernardes, L Tannous; Hospital Universitário Ciências Médicas - R Dutra, G Mirachi; Hospital Universitário da Universidade Federal de Juiz de Fora - BV Pinheiro, EV Carvalho; Hospital Universitário da Universidade Federal de São Paulo - UTI Clínica Médica - H Guimaraes, L Vendrame; Hospital Universitário da Universidade Federal de São Paulo - UTI Geral - F Machado, A Nascente; Hospital Universitário da Universidade Federal de São Paulo - UTI Neuro - F Machado, J Polezei; Hospital Universitário da Universidade Federal de São Paulo - UTI Pronto-Socorro - AFT de Góis, KMC Teixeira; Hospital Universitário da Faculdade de Medicina de Jundiaí - G Cavalcanti, M Leão; Hospital Universitário de Maringá - A Germano, S Yamada; Hospital Universitário de Santa Cruz do Sul - P de Moraes, R Foernges; Hospital Universitário de Santa Maria - L Garcia, S Ribeiro; Hospital Universitário Getúlio Vargas - WO Filho, A Matos; Hospital Universitário Júlio Müller - D Castiglioni, G da Silva; Hospital Universitário Lauro

Wanderley - P Gottardo, C Mendes; Hospital Universitário Maria Aparecida Pedrossian - S Pinto; Hospital Universitário São Francisco de Paula - M Guerreiro, L Teixeira; Hospital Universitário -Universidade Federal Grande Dourados - M Matsui, E Neto; Hospital Vila da Serra - F Anselmo, H Urbano; Hospital Vita Batel - R Deucher, A Rea-Neto; Instituto do Coração, Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo - J Ferreira, E Costa; Instituto do Coração, Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo - REC - FRBG Galas, LA Hajjar; Instituto do Coração, Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo - FG Lima, VRB Benites; Instituto de Infectologia Emílio Ribas II - R Borba, M Douglas; Instituto de Ortopedia e Traumatologia - CPP Castro, AB Saraiva; Instituto de Pesquisa Clínica Evandro Chagas - Instituto de Pesquisa Clínica Evandro Chagas da Fundação Oswaldo Cruz - FA Bozza, A Japiassú; Instituto do Câncer do Estado de São Paulo - JP Almeida, LA Hajjar; Instituto Estadual do Cérebro Paulo Niemeyer - C Righy, B Goncalves; Instituto D’Or de Ensino e Pesquisa - G Viana, A Reis; Instituto Latino Americano de Sepse - F Carrara, A Carvalho Júnior; Instituto Nacional de Cardiologia - M de Freitas, R Felipe; Instituto Ortopédico - L Caetano, M Nobrega; Instituto de Pesquisa Hospital do Coração - D de Moraes Paisani; Irmandade de Misericórdia de Guaxupé - SA Bezerra, DRB Pereira; Irmandade Misericórdia Hospital Santa Casa de Monte Alto - L Cassimiro, W Filho; Lifecenter - M Hermeto, B Pinto; Samur - L Ferraz, L Melo; Santa Casa de Angra dos Reis - V Bogado, S Silva; Santa Casa de Belém do Pará - R Batista, N Fonseca; Santa Casa de Belo Horizonte - P Correia, G Reis; Santa Casa de Caridade de Diamantina - MF Sousa, MMF Souza; Santa Casa de Misericórdia de Assis - GN Betônico, AL Leonardi; Santa Casa de Caridade de Don Pedrito - J Alvarez, A Tarouco; Santa Casa de Misericórdia de Paraguaçu Paulista - JA Alves, PRG Silva; Santa Casa de Misericórdia de Porto Alegre - G Friedman, T Lisboa; Santa Casa de Misericórdia de Presidente Prudente - C Bosso, G Plantier; Santa Casa de Misericórdia de Ribeirão Preto - P Antoniazzi, F Ostini; Santa Casa de Misericórdia de Santana do Livramento - J Alvarez, D de Souza; Santa Casa de Misericórdia de Santo Amaro - P Chaves, J Farhat Júnior; Santa Casa de Misericórdia de São Paulo - R Marco, E Peixoto; Santa Casa de Misericórdia de Vitória da Conquista - G Moreno; Santa Casa Maringá - Universidade Estadual Maringá - D Bolognese, P Torres; São Bernardo Apart Hospital - R López, M Rodrigues; Sociedade Beneficente de Senhoras Hospital Sírio-Libanês - LCP Azevedo, F Ramos; Universidade Estadual de Campinas - UTI da Disciplina de Emergências Clínicas - C Gontijo-Coutinho, T Santos; Universidade Estadual de Londrina - C Grion, M Tanita; Vitória Apart Hospital - A Muniz, C Piras

The other countries sites are mentioned in the original publication.

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Publication Dates

  • Publication in this collection
    05 July 2021
  • Date of issue
    Apr-Jun 2021

History

  • Received
    19 Sept 2020
  • Accepted
    08 Dec 2020
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