Abstract
Purpose
To assess whether partitioning the elastance of the respiratory system (E RS) between lung (E L) and chest wall (E CW) elastance in order to target values of end-inspiratory transpulmonary pressure (PPLATL) close to its upper physiological limit (25 cmH2O) may optimize oxygenation allowing conventional treatment in patients with influenza A (H1N1)-associated ARDS referred for extracorporeal membrane oxygenation (ECMO).
Methods
Prospective data collection of patients with influenza A (H1N1)-associated ARDS referred for ECMO (October 2009–January 2010). Esophageal pressure was used to (a) partition respiratory mechanics between lung and chest wall, (b) titrate positive end-expiratory pressure (PEEP) to target the upper physiological limit of PPLATL (25 cmH2O).
Results
Fourteen patients were referred for ECMO. In seven patients PPLATL was 27.2 ± 1.2 cmH2O; all these patients underwent ECMO. In the other seven patients, PPLATL was 16.6 ± 2.9 cmH2O. Raising PEEP (from 17.9 ± 1.2 to 22.3 ± 1.4 cmH2O, P = 0.0001) to approach the upper physiological limit of transpulmonary pressure (PPLATL = 25.3 ± 1.7 cm H2O) improved oxygenation index (from 37.4 ± 3.7 to 16.5 ± 1.4, P = 0.0001) allowing patients to be treated with conventional ventilation.
Conclusions
Abnormalities of chest wall mechanics may be present in some patients with influenza A (H1N1)-associated ARDS. These abnormalities may not be inferred from measurements of end-inspiratory plateau pressure of the respiratory system (PPLATRS). In these patients, titrating PEEP to PPLATRS may overestimate the incidence of hypoxemia refractory to conventional ventilation leading to inappropriate use of ECMO.
Similar content being viewed by others
Introduction
Several reports describe cases of influenza A (H1N1)-associated acute respiratory distress syndrome (ARDS) requiring extracorporeal membrane oxygenation (ECMO) for severe hypoxemia refractory to conventional treatment [1–6]. However, uncertainty regarding the appropriate indication for ECMO in these patients still remains [7–10]. Moreover, clinical evidence in support of ECMO as a rescue treatment for these patients is controversial [11].
The increase in elastance of the respiratory system [12] observed in patients with ARDS is mainly attributed to the increase in elastance of the lung (E L) [12]. Under these circumstances the elastic properties of the chest wall (E CW) contribute to the elastance of the respiratory system (E RS) by approximately 20% [13]. However, alterations in E CW have been described in patients with ARDS [13–15]. In these patients E CW may contribute to E RS by up to 50% [16]. This implies that for a value of end-inspiratory plateau pressure of the respiratory system (PPLATRS) of 30 cmH2O, the end-inspiratory transpulmonary pressure (PPLATL) will amount to 24 cmH2O in patients with a “normal” chest wall and 15 cmH2O in patients with a “stiff” chest wall [16]. This may be clinically relevant because (a) several studies suggest that mechanical ventilation should be titrated to PPLATL rather than to PPLATRS and (b) it has been suggested that the upper physiological limit of transpulmonary pressure that optimizes alveolar recruitment is 25 cmH2O [14, 15, 17].
We report a case series of patients with influenza A (H1N1)-associated ARDS that were referred for ECMO but in whom assessment of transpulmonary pressure led to a change of the ventilatory strategy that reversed refractory hypoxemia and avoided ECMO.
Methods
Further details are available in the electronic online supplement. We report patients with influenza A (H1N1)-associated ARDS referred to the Molinette Hospital (University of Turin) for ECMO in the period from September 2009 to January 2010 [18]. The institutional ethics committee approved data collection and reporting.
Patients were centralized if conventional ventilation [19], in association with nitric oxide, and/or prone positioning, and/or high frequency oscillation, resulted in HbO2 <85%; oxygenation index >25; PaO2/FiO2 <100 with PEEP ≥10 cmH2O; hypercapnia and respiratory acidosis with pH <7.25; SvO2 or SvcO2 <65% despite Ht >30% and administration of vasoactive drugs [18]. Criteria for initiating ECMO were oxygenation index >30; PaO2/FiO2 <70 with PEEP ≥15 cmH2O; pH < 7.25 for at least 2 h [18]. Exclusion criteria for ECMO were (a) intracranial bleeding and other major contraindication to anticoagulation, (b) previous severe disability; poor prognosis because of the underlying malignancy, and (c) mechanical ventilation for longer than 7 days [18].
At arrival, all patients were ventilated according to the ARDS Network protocol [19]. Mechanics of the respiratory system was partitioned between lung and chest wall. Throughout the period of data recording all patients were orotracheally intubated and in semirecumbent position (head of bed from 30 to 45° inclination), sedated and paralyzed, as prescribed by the attending physicians.
Flow and PPLATRS were measured. The pressure required to distend the chest wall was estimated using the measurement of esophageal pressure (P ES) [20]. E RS, E CW, and E L were calculated as previously described [20]. PPLATCW and end-inspiratory plateau pressure of the lung (PPLATL) were estimated using the following equations [16]:
The shape of the airway opening pressure versus time during constant flow (the stress index) was recorded as previously described [21–24].
If values of PPLATL during conventional ventilation were less than 25 cmH2O, PEEP was further increased until PPLATL was equal to 25 cmH2O [14, 15, 17]. ECMO criteria were hence evaluated 20–30 min after the initiation of ventilation with the new PEEP setting. If values of PPLATL during conventional ventilation were at least 25 cmH2O, ECMO criteria were evaluated with ventilator settings as set on entry.
Data are presented as mean ± standard deviation. Comparisons were performed using paired and unpaired T test, as appropriate. Differences were considered significant if P < 0.05.
Results
In the period October 2009–January 2010, 36 patients with novel A (H1N1) infection were admitted to the ICUs of the Piedmont region. Among them, 20 patients had ARDS and 14 were transferred to the regional coordinating center with ECMO facilities as a result of developing the pre-established criteria.
Values of oxygenation index and of PaO2/FiO2 ratio indicated immediate use of ECMO in all patients [18]. Partitioning of respiratory mechanics showed that in seven patients PPLATL was higher than 25 cmH2O (27.2 ± 1.2 cmH2O), whereas in the other seven patients it was lower than 25 cmH2O (16.6 ± 2.9 cmH2O) (Table 1). Values of PPLATRS were similar in the groups (31.0 ± 1.0 vs. 31.5 ± 0.5 cmH2O, respectively). Whereas in the former extracorporeal support was immediately initiated (ECMO group), in the latter increasing PEEP until PPLATL reached the upper physiological limit of transpulmonary pressure (25.3 ± 1.7 cmH2O) resulted in an increase of oxygenation index and of PaO2/FiO2 to an extent that criteria for extracorporeal support were no longer met and patients were treated with conventional ventilation in association with low-flow CO2 removal [25] in four patients (no ECMO group) (Fig. 1).
Table 2 shows the physiological parameters in the ECMO and no ECMO groups. Although values of E RS did not differ, E L was higher (32.3 ± 5.3 vs. 20.2 ± 4.7 cmH2O/L; P = 0.001) and E CW was lower (6.1 ± 0.7 vs. 17.2 ± 1.7; P = 0.0001) in the ECMO than in no ECMO group. In the latter, increasing PEEP from 17.9 ± 1.2 to 22.3 ± 1.4 cmH2O (P = 0.0001) to target an increase in PPLATL from 16.6 ± 2.9 to 25.3 ± 1.7 cmH2O/L (P = 0.0001) significantly decreased the oxygenation index from 37 ± 4 to 16 ± 1 (P = 0.0001). The significant (P = 0.0001) increase of PPLATRS from 31.5 ± 0.5 to 38.4 ± 1.0 cmH2O observed with conventional ventilation and higher PEEP was associated with (a) the increase in E RS (from 37.4 ± 4.2 to 43.8 ± 3.3 cmH2O/L; P = 0.0001) and E L (from 20.2 ± 4.7 to 28.6 ± 2.3 cmH2O/L; P = 0.0001), (b) the increase of stress index (from 0.922 ± 0.033 to 1.052 ± 0.032; P = 0.0001), and (c) the reduction in PaCO2 (from 54.6 ± 8.4 to 42.9 ± 8.0; P = 0.001). Increasing PEEP significantly increased right atrial pressure (from 17 ± 2 to 20 ± 3 mmHg, P = 0.001) but did not affect mean systolic pressure, cardiac output, and cardiac index.
Table 3 shows the clinical and demographic characteristics of the patients. Except for age (35.4 ± 11.1 vs. 53.3 ± 11.7 years; P = 0.01) and fluid balance prior to admission to the referral center (718 ± 270 vs. 1,384 ± 332 mL; P = 0.01), Murray’s score [26] (3.82 ± 0.19 vs. 3.61 ± 0.43) and other clinical variables did not differ between the ECMO and no ECMO groups.
Discussion
The present case series shows that partitioning of respiratory mechanics between lung and chest wall revealed a subset of patients with influenza A (H1N1)-associated ARDS in whom hypoxemia was refractory to the conventional treatment not because of a profound alteration of the lung parenchyma but because a large amount of the pressure applied at the airways was not transmitted to the lung parenchyma but dissipated against a “stiff” chest wall. In these patients, targeting PEEP to reach the upper physiological limit of transpulmonary pressure (25 cmH2O) [14, 15, 17], instead of the “safe” limit of PPLATRS (30 cmH2O) [19], improved oxygenation to an extent that ECMO criteria were no longer met.
The reported incidence of patients with influenza A (H1N1)-associated ARDS transitioning from conventional ventilation to ECMO is extremely variable. Reports from Australia and New Zealand [1] and from France [2] indicate that patients on ECMO were 34 and 50% of the mechanically ventilated patients, respectively. In Hong Kong [3] and Canada [4] only 6% of the patients were shifted from conventional ventilation to ECMO. In the present study, 14 patients were referred to the regional center to initiate ECMO for refractory hypoxemia. Partitioning of respiratory mechanics between lung and chest wall allowed us to identify seven patients that responded to conventional treatment and avoided ECMO provided that PEEP was sufficiently high to be transmitted to the collapsed lungs and to overcome chest wall stiffness. By doing so, the incidence of ECMO in the Piedmont region went from the possible 39% (14 out of a total of 36 mechanically ventilated patients) to the observed 19% (7 of the 36 mechanically ventilated patients) (Fig. 1).
Both in the ECMO and in the no ECMO group the oxygenation index was equally compromised (Table 2) suggesting equal impairment of lung function. However, the oxygenation index is calculated using mean airway pressure. Indeed, the mean transpulmonary pressure during conventional mechanical ventilation was lower in the no ECMO than in the ECMO group (13.4 ± 1.6 vs. 21.4 ± 1.7, P = 0.01) and therefore the oxygenation index calculated using the mean transpulmonary pressure was significantly lower in the no ECMO than in the ECMO group (19.8 ± 1.6 vs. 28.7 ± 4.8 P = 0.01).
The “open lung” approach aims at maximizing alveolar recruitment and counteracting tidal recruitment of unstable alveoli by setting PEEP as high as possible to match a PPLATRS of 30 cmH2O [27–29]. A recent meta-analysis suggests that this approach may reduce mortality in patients with ARDS in comparison to the conventional approach [30]. Recently, Mercat and co-workers [28] proposed an open lung protocol in which PEEP was individually set as high as possible to match a PPLATRS target of 30 cmH2O. The open lung strategy adopted in the present report is based on the same rationale but, in order to overcome the bias induced by chest wall stiffness, aimed at an end-inspiratory transpulmonary pressure of 25 cmH2O. Note that this value is regarded as the upper physiological limit of transpulmonary pressure [14, 15, 17] and is the value recorded in patients with ARDS and normal E CW (E CW/E RS ratio of 0.2) at a PPLATRS of 30 cmH2O. This approach differs from the one proposed by Talmor and co-workers [20] that titrated PEEP in order to obtain values of end-expiratory transpulmonary pressure ranging between 0 and 10 cmH2O.
In patients with ARDS, the increase of E RS is mainly attributed to E L [31]. However, alterations in E CW have been also described in these patients [13, 15]. Moreover, influenza A (H1N1)-associated ARDS frequently occurs in obese subjects [32], a category of patients that often present a compromised E CW [33]. Under these circumstances: (a) part of PPLATRS may be “wasted” to distend the chest wall and only a fraction of the pressure applied at the airways will inflate the lung [14]; (b) the amount of pressure that will result in lung recruitment depends on the E CW/E RS ratio [16]. In normal adults the E CW/E RS ratio is approximately 0.4 [16]. In patients with ARDS, Gattinoni and co-workers [13] described patients with a normal chest wall and a E CW/E RS ratio of 0.2 and patients with a substantial impairment of the elastic properties of the chest wall and a E CW/E RS ratio of 0.5 in patients with compromised chest wall mechanics [16]. Mergoni et al. [34], Ranieri et al. [15], and Grasso et al. [14] later confirmed these findings. We show that in seven of our patients, the impairment of the elastic properties of the respiratory system (E RS = 38.4 ± 5.2 cmH2O/L) was due to a profound and substantial alteration of the lung parenchyma. In these patients the E CW/E RS ratio was 0.16 ± 0.03 and PPLATL during conventional ventilation was 27.2 ± 1.2 cmH2O (Table 2), hypoxemia was refractory to conventional treatments and ECMO was required to re-establish oxygenation. In the remaining patients, chest wall mechanics substantially contributed to the observed values of E RS (37.4 ± 4.2 cmH2O/L) with an E CW/E RS ratio of 0.47 ± 0.08 (Table 2). In these patients, during conventional ventilation and with a PEEP of 17.9 ± 1.2 cmH2O, baseline PPLATL was 16.6 ± 2.9 cmH2O. Raising PEEP to 22.3 ± 1.4 cmH2O to target the upper physiological limit of PPLATL (25.3 ± 1.7 cmH2O) decreased oxygenation index (from 37 ± 4 to 16 ± 1; P = 0.0001) reverting the indication for ECMO and allowing treatment with conventional ventilation. The significant improvement in oxygenation (Table 2) with a relatively small increase of PEEP (4.4 ± 1.4 cmH2O, range 4–6 cmH2O) suggests a high potential for alveolar recruitment in the no ECMO group [35].
Recent evidence [36] accounts for significant alveolar hyperinflation at PPLATRS levels higher than 28 cmH2O. However several arguments support the lack of any direct or indirect evidence of hyperinflation observed in the present study even if we did not directly assess recruitment and hyperinflation. First, PPLATL was significantly lower than PPLATRS, due to high E cw. Second, stress index went from the range of values associated with tidal recruitment (0.922 ± 0.033) to the range of values associated with protective ventilation (1.052 ± 0.032; P = 0.0001). Third, although a decrease in cardiac output could have per se decreased shunt and improved oxygenation [37], we found that cardiac output remained unchanged. Fourth, despite the slight but significant increase of E L with the higher PEEP strategy could be explained by assuming that in these patients the increase of PEEP shifted tidal ventilation close to the upper inflection point of the pulmonary volume–pressure curve [38–41], recent evidence suggests that “regional elastance” of lung tissue previously collapsed and re-expanded by applied pressure is higher than the elastance of the normally patent lung regions [42].
The observational nature of the present study limits the interpretation of its results. First, alterations of E CW in patients with ARDS have been associated with excessive and unopposed abdominal pressure [43] or with pleural effusions due to a positive fluid balance [14]. Moreover, in normal subjects E RS increases with age, due to an increase of E CW [44]. Although we found that patients with impaired chest wall mechanics were older (53.3 ± 11.7 vs. 35.4 ± 11.1 years; P = 0.01) and had a more pronounced positive fluid balance (1,384 ± 332 vs. 718 ± 270 mL; P = 0.01) than the patients that had a normal chest wall, the small number of patients included in the study does not allow one to identify clinical or physiological variables that could predict the alteration of impairment of chest wall mechanics. Second, we report on a cohort of patients with a particularly diffuse and recruitable form of ARDS. Third, portioning E RS between E CW and E L is based on the measurement of P ES and on the assumption that this measurement (a) represents the average pleural pressure [45], (b) is insensitive to changes in lung volume [46] and to local gradients in pleural pressure [12]. Unfortunately none of these assumptions have ever been verified in patients with ARDS [47]. Fourthly, several other methods have been proposed to set up an open lung approach [48, 49]. Borges and co-workers [50] showed that applying distending pressures up to 60 cmH2O could successfully recruit the lung in ARDS patients considered not responders to conventional lung-distending pressures. Therefore, it is conceivable that targeting a PPLATL higher than 25 cmH2O would have successfully recruited patients also in the ECMO group. Finally, we must point out that reducing tidal volume from 6 to 4 mL/kg would have allowed higher PEEP levels at baseline in both groups [51].
May our data influence physicians’ attitudes to implement ECMO in patients with ARDS? Unfortunately, available data come from case series [1–5, 18, 52] and only one randomized clinical trial tested the efficacy of ECMO in patients with severe ARDS [53]. Table 4 presents the main ECMO criteria of these studies together with the ECMO criteria proposed by the Extracorporeal Life Support Organization guidelines [54]. As can be seen all our patients would have been treated with ECMO according to the existing criteria. Results of the present study may therefore suggest that (a) liberal and inclusive criteria for centralizing patients with H1N1-induced ARDS to centers with ECMO facilities [1–5, 18, 52] should not be considered prima facie grounds to actually implement ECMO, (b) titrating PEEP to target a PPLATL value of 25 cmH2O [14, 15, 17] instead of a PPLATRS of 30 cmH2O [27, 28] may optimize oxygenation and prevent inappropriate use of ECMO in those patients with influenza A (H1N1)-associated ARDS that have abnormal chest wall mechanics. Further studies are required to evaluate whether these conclusions may apply to a general population of ARDS patients.
References
Davies A, Jones D, Bailey M, Beca J, Bellomo R, Blackwell N, Forrest P, Gattas D, Granger E, Herkes R, Jackson A, McGuinness S, Nair P, Pellegrino V, Pettila V, Plunkett B, Pye R, Torzillo P, Webb S, Wilson M, Ziegenfuss M (2009) Extracorporeal membrane oxygenation for 2009 influenza A(H1N1) acute respiratory distress syndrome. JAMA 302:1888–1895
Roch A, Lepaul-Ercole R, Grisoli D, Bessereau J, Brissy O, Castanier M, Dizier S, Forel JM, Guervilly C, Gariboldi V, Collart F, Michelet P, Perrin G, Charrel R, Papazian L (2010) Extracorporeal membrane oxygenation for severe influenza A (H1N1) acute respiratory distress syndrome: a prospective observational comparative study. Intensive Care Med 36:1899–1905
Chan KK, Lee KL, Lam PK, Law KI, Joynt GM, Yan WW (2010) Hong Kong’s experience on the use of extracorporeal membrane oxygenation for the treatment of influenza A (H1N1). Hong Kong Med J 16:447–454
Freed DH, Henzler D, White CW, Fowler R, Zarychanski R, Hutchison J, Arora RC, Manji RA, Legare JF, Drews T, Veroukis S, Kesselman M, Guerguerian AM, Kumar A (2010) Extracorporeal lung support for patients who had severe respiratory failure secondary to influenza A (H1N1) 2009 infection in Canada. Can J Anaesth 57:240–247
Holzgraefe B, Broome M, Kalzen H, Konrad D, Palmer K, Frenckner B (2010) Extracorporeal membrane oxygenation for pandemic H1N1 2009 respiratory failure. Minerva Anestesiol 76:1043–1051
Noah MA, Peek GJ, Finney SJ, Griffiths MJ, Harrison DA, Grieve R, Sadique MZ, Sekhon JS, McAuley DF, Firmin RK, Harvey C, Cordingley JJ, Price S, Vuylsteke A, Jenkins DP, Noble DW, Bloomfield R, Walsh TS, Perkins GD, Menon D, Taylor BL, Rowan KM (2011) Referral to an extracorporeal membrane oxygenation center and mortality among patients with severe 2009 influenza A(H1N1). JAMA 306:1659–1668
Dalton HJ, MacLaren G (2010) Extracorporeal membrane oxygenation in pandemic flu: insufficient evidence or worth the effort? Crit Care Med 38:1484–1485
Hubmayr RD, Farmer JC (2010) Should we “rescue” patients with 2009 influenza A(H1N1) and lung injury from conventional mechanical ventilation? Chest 137:745–747
Morris AH, Hirshberg E, Miller RR 3rd, Statler KD, Hite RD (2010) Counterpoint: efficacy of extracorporeal membrane oxygenation in 2009 influenza A(H1N1): sufficient evidence? Chest 138:778–781 (Discussion 782–774)
Park PK, Dalton HJ, Bartlett RH (2010) Point: efficacy of extracorporeal membrane oxygenation in 2009 influenza A(H1N1): sufficient evidence? Chest 138:776–778
Mitchell MD, Mikkelsen ME, Umscheid CA, Lee I, Fuchs BD, Halpern SD (2010) A systematic review to inform institutional decisions about the use of extracorporeal membrane oxygenation during the H1N1 influenza pandemic. Crit Care Med 38:1398–1404
Hubmayr RD, Rodarte JR, Walters BJ, Tonelli FM (1987) Regional ventilation during spontaneous breathing and mechanical ventilation in dogs. J Appl Physiol 63:2467–2475
Gattinoni L, Pelosi P, Suter PM, Pedoto A, Vercesi P, Lissoni A (1998) Acute respiratory distress syndrome caused by pulmonary and extrapulmonary disease. Different syndromes? Am J Respir Crit Care Med 158:3–11
Grasso S, Mascia L, Del Turco M, Malacarne P, Giunta F, Brochard L, Slutsky AS, Marco Ranieri V (2002) Effects of recruiting maneuvers in patients with acute respiratory distress syndrome ventilated with protective ventilatory strategy. Anesthesiology 96:795–802
Ranieri VM, Brienza N, Santostasi S, Puntillo F, Mascia L, Vitale N, Giuliani R, Memeo V, Bruno F, Fiore T, Brienza A, Slutsky AS (1997) Impairment of lung and chest wall mechanics in patients with acute respiratory distress syndrome: role of abdominal distension. Am J Respir Crit Care Med 156:1082–1091
Gattinoni L, Chiumello D, Carlesso E, Valenza F (2004) Bench-to-bedside review: chest wall elastance in acute lung injury/acute respiratory distress syndrome patients. Crit Care 8:350–355
Colebatch HJ, Greaves IA, Ng CK (1979) Exponential analysis of elastic recoil and aging in healthy males and females. J Appl Physiol 47:683–691
Patroniti N, Zangrillo A, Pappalardo F, Peris A, Cianchi G, Braschi A, Iotti GA, Arcadipane A, Panarello G, Ranieri VM, Terragni P, Antonelli M, Gattinoni L, Oleari F, Pesenti A (2011) The Italian ECMO network experience during the 2009 influenza A(H1N1) pandemic: preparation for severe respiratory emergency outbreaks. Intensive Care Med 37:1447–1457
The Acute Respiratory Distress Network (2000) Ventilation with lower tidal volumes as compared with traditional tidal volumes for acute lung injury and the acute respiratory distress syndrome. The Acute Respiratory Distress Syndrome Network. N Engl J Med 342:1301–1308
Talmor D, Sarge T, Malhotra A, O’Donnell CR, Ritz R, Lisbon A, Novack V, Loring SH (2008) Mechanical ventilation guided by esophageal pressure in acute lung injury. N Engl J Med 359:2095–2104
Ranieri VM, Giuliani R, Fiore T, Dambrosio M, Milic-Emili J (1994) Volume-pressure curve of the respiratory system predicts effects of PEEP in ARDS: “occlusion” versus “constant flow” technique. Am J Respir Crit Care Med 149:19–27
Ranieri VM, Zhang H, Mascia L, Aubin M, Lin CY, Mullen JB, Grasso S, Binnie M, Volgyesi GA, Eng P, Slutsky AS (2000) Pressure-time curve predicts minimally injurious ventilatory strategy in an isolated rat lung model. Anesthesiology 93:1320–1328
Grasso S, Stripoli T, De Michele M, Bruno F, Moschetta M, Angelelli G, Munno I, Ruggiero V, Anaclerio R, Cafarelli A, Driessen B, Fiore T (2007) ARDSnet ventilatory protocol and alveolar hyperinflation: role of positive end-expiratory pressure. Am J Respir Crit Care Med 176:761–767
Grasso S, Terragni P, Mascia L, Fanelli V, Quintel M, Herrmann P, Hedenstierna G, Slutsky AS, Ranieri VM (2004) Airway pressure-time curve profile (stress index) detects tidal recruitment/hyperinflation in experimental acute lung injury. Crit Care Med 32:1018–1027
Terragni PP, Del Sorbo L, Mascia L, Urbino R, Martin EL, Birocco A, Faggiano C, Quintel M, Gattinoni L, Ranieri VM (2009) Tidal volume lower than 6 ml/kg enhances lung protection: role of extracorporeal carbon dioxide removal. Anesthesiology 111:826–835
Murray JF, Matthay MA, Luce JM, Flick MR (1988) An expanded definition of the adult respiratory distress syndrome. Am Rev Respir Dis 138:720–723
Brower RG, Lanken PN, MacIntyre N, Matthay MA, Morris A, Ancukiewicz M, Schoenfeld D, Thompson BT (2004) Higher versus lower positive end-expiratory pressures in patients with the acute respiratory distress syndrome. N Engl J Med 351:327–336
Mercat A, Richard JC, Vielle B, Jaber S, Osman D, Diehl JL, Lefrant JY, Prat G, Richecoeur J, Nieszkowska A, Gervais C, Baudot J, Bouadma L, Brochard L (2008) Positive end-expiratory pressure setting in adults with acute lung injury and acute respiratory distress syndrome: a randomized controlled trial. JAMA 299:646–655
Meade MO, Cook DJ, Guyatt GH, Slutsky AS, Arabi YM, Cooper DJ, Davies AR, Hand LE, Zhou Q, Thabane L, Austin P, Lapinsky S, Baxter A, Russell J, Skrobik Y, Ronco JJ, Stewart TE (2008) Ventilation strategy using low tidal volumes, recruitment maneuvers, and high positive end-expiratory pressure for acute lung injury and acute respiratory distress syndrome: a randomized controlled trial. JAMA 299:637–645
Briel M, Meade M, Mercat A, Brower RG, Talmor D, Walter SD, Slutsky AS, Pullenayegum E, Zhou Q, Cook D, Brochard L, Richard JC, Lamontagne F, Bhatnagar N, Stewart TE, Guyatt G (2010) Higher vs lower positive end-expiratory pressure in patients with acute lung injury and acute respiratory distress syndrome: systematic review and meta-analysis. JAMA 303:865–873
Brander L, Ranieri VM, Slutsky AS (2006) Esophageal and transpulmonary pressure help optimize mechanical ventilation in patients with acute lung injury. Crit Care Med 34:1556–1558
Fezeu L, Julia C, Henegar A, Bitu J, Hu FB, Grobbee DE, Kengne AP, Hercberg S, Czernichow S (2011) Obesity is associated with higher risk of intensive care unit admission and death in influenza A (H1N1) patients: a systematic review and meta-analysis. Obes Rev 12:653–659
Salome CM, King GG, Berend N (2010) Physiology of obesity and effects on lung function. J Appl Physiol 108:206–211
Mergoni M, Martelli A, Volpi A, Primavera S, Zuccoli P, Rossi A (1997) Impact of positive end-expiratory pressure on chest wall and lung pressure-volume curve in acute respiratory failure. Am J Respir Crit Care Med 156:846–854
Fan E, Wilcox ME, Brower RG, Stewart TE, Mehta S, Lapinsky SE, Meade MO, Ferguson ND (2008) Recruitment maneuvers for acute lung injury: a systematic review. Am J Respir Crit Care Med 178:1156–1163
Terragni PP, Rosboch G, Tealdi A, Corno E, Menaldo E, Davini O, Gandini G, Herrmann P, Mascia L, Quintel M, Slutsky AS, Gattinoni L, Ranieri VM (2007) Tidal hyperinflation during low tidal volume ventilation in acute respiratory distress syndrome. Am J Respir Crit Care Med 175:160–166
Matamis D, Lemaire F, Harf A, Teisseire B, Brun-Buisson C (1984) Redistribution of pulmonary blood flow induced by positive end-expiratory pressure and dopamine infusion in acute respiratory failure. Am Rev Respir Dis 129:39–44
Ranieri VM, Giuliani R, Cinnella G, Pesce C, Brienza N, Ippolito EL, Pomo V, Fiore T, Gottfried SB, Brienza A (1993) Physiologic effects of positive end-expiratory pressure in patients with chronic obstructive pulmonary disease during acute ventilatory failure and controlled mechanical ventilation. Am Rev Respir Dis 147:5–13
Maggiore SM, Jonson B, Richard JC, Jaber S, Lemaire F, Brochard L (2001) Alveolar derecruitment at decremental positive end-expiratory pressure levels in acute lung injury: comparison with the lower inflection point, oxygenation, and compliance. Am J Respir Crit Care Med 164:795–801
Jonson B, Richard JC, Straus C, Mancebo J, Lemaire F, Brochard L (1999) Pressure-volume curves and compliance in acute lung injury: evidence of recruitment above the lower inflection point. Am J Respir Crit Care Med 159:1172–1178
Richard JC, Brochard L, Vandelet P, Breton L, Maggiore SM, Jonson B, Clabault K, Leroy J, Bonmarchand G (2003) Respective effects of end-expiratory and end-inspiratory pressures on alveolar recruitment in acute lung injury. Crit Care Med 31:89–92
Grasso S, Stripoli T, Sacchi M, Trerotoli P, Staffieri F, Franchini D, De Monte V, Valentini V, Pugliese P, Crovace A, Driessen B, Fiore T (2009) Inhomogeneity of lung parenchyma during the open lung strategy: a computed tomography scan study. Am J Respir Crit Care Med 180:415–423
Hess DR, Bigatello LM (2008) The chest wall in acute lung injury/acute respiratory distress syndrome. Curr Opin Crit care 14:94–102
Frank NR, Mead J, Ferris BG Jr (1957) The mechanical behavior of the lungs in healthy elderly persons. J Clin Investig 36:1680–1687
Milic-Emili J, Mead J, Turner JM, Glauser EM (1964) Improved technique for estimating pleural pressure from esophageal balloons. J Appl Physiol 19:207–211
Rehder K, Abboud N, Rodarte JR, Hyatt RE (1975) Positive airway pressure and vertical transpulmonary pressure gradient in man. J Appl Physiol 38:896–899
Hubmayr RD (2010) Is there a place for esophageal manometry in the care of patients with injured lungs? J Appl Physiol 108:481–482
Suarez-Sipmann F, Bohm SH, Tusman G, Pesch T, Thamm O, Reissmann H, Reske A, Magnusson A, Hedenstierna G (2007) Use of dynamic compliance for open lung positive end-expiratory pressure titration in an experimental study. Crit Care Med 35:214–221
Hodgson CL, Tuxen DV, Davies AR, Bailey MJ, Higgins AM, Holland AE, Keating JL, Pilcher D, Westbrook AJ, Cooper DJ, Nichol A (2011) A randomised controlled trial of an open lung strategy with staircase recruitment, titrated PEEP and targeted low airway pressures in patients with acute respiratory distress syndrome. Crit Care 15:R133
Borges JB, Okamoto VN, Matos GF, Caramez MP, Arantes PR, Barros F, Souza CE, Victorino JA, Kacmarek RM, Barbas CS, Carvalho CR, Amato MB (2006) Reversibility of lung collapse and hypoxemia in early acute respiratory distress syndrome. Am J Respir Crit Care Med 174:268–278
Hager DN, Krishnan JA, Hayden DL, Brower RG (2005) Tidal volume reduction in patients with acute lung injury when plateau pressures are not high. Am J Respir Crit Care Med 172:1241–1245
Norfolk SG, Hollingsworth CL, Wolfe CR, Govert JA, Que LG, Cheifetz IM, Hollingsworth JW (2010) Rescue therapy in adult and pediatric patients with pH1N1 influenza infection: a tertiary center intensive care unit experience from April to October 2009. Crit Care Med 38:2103–2107
Peek GJ, Mugford M, Tiruvoipati R, Wilson A, Allen E, Thalanany MM, Hibbert CL, Truesdale A, Clemens F, Cooper N, Firmin RK, Elbourne D (2009) Efficacy and economic assessment of conventional ventilatory support versus extracorporeal membrane oxygenation for severe adult respiratory failure (CESAR): a multicentre randomised controlled trial. Lancet 374:1351–1363
Extracorporeal Life Support Organization (ELSO) (2009) ELSO guidelines. Available via http://www.elso.med.umich.edu/Guidelines.html. Accessed 13 Apr 2011
Acknowledgments
This study was supported by grants from the Ministero dell’Università, Programmi di Ricerca di Interesse Nazionale # VMRLM98, 2007–2009.
Author information
Authors and Affiliations
Corresponding author
Additional information
S. Grasso and P. Terragni contributed equally to this work and should be both considered as first author.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Grasso, S., Terragni, P., Birocco, A. et al. ECMO criteria for influenza A (H1N1)-associated ARDS: role of transpulmonary pressure. Intensive Care Med 38, 395–403 (2012). https://doi.org/10.1007/s00134-012-2490-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00134-012-2490-7