Predictors of pulmonary failure following severe trauma: a trauma registry-based analysis
© Geiger et al.; licensee BioMed Central Ltd. 2013
Received: 3 November 2012
Accepted: 7 April 2013
Published: 22 April 2013
The incidence of pulmonary failure in trauma patients is considered to be influenced by several factors such as liver injury. We intended to assess the association of various potential predictors of pulmonary failure following thoracic trauma and liver injury.
Records of 12,585 trauma patients documented in the TraumaRegister DGU® of the German Trauma Society were analyzed regarding the potential impact of concomitant liver injury on the incidence of pulmonary failure using uni- and multivariate analyses. Pulmonary failure was defined as pulmonary failure of ≥ 3 SOFA-score points for at least two days. Patients were subdivided according to their injury pattern into four groups: group 1: AIS thorax < 3; AIS liver < 3; group 2: AIS thorax ≥ 3; AIS liver < 3; group 3: AIS thorax < 3; AIS liver ≥ 3 and group 4: AIS thorax ≥ 3; AIS liver ≥ 3.
Overall, 2643 (21%) developed pulmonary failure, 12% (n= 642) in group 1, 26% (n= 697) in group 2, 16% (n= 30) in group 3, and 36% (n= 188) in group 4. Factors independently associated with pulmonary failure included relevant lung injury, pre-existing medical conditions (PMC), sex, transfusion of more than 10 units of packed red blood cells (PRBC), Glasgow Coma Scale (GCS) ≤ 8, and the ISS. However, liver injury was not associated with an increased risk of pulmonary failure following severe trauma in our setting.
Specific factors, but not liver injury, were associated with an increased risk of pulmonary failure following trauma. Trauma surgeons should be aware of these factors for optimized intensive care treatment.
KeywordsMultiple trauma Thoracic trauma Liver injury Pulmonary failure
Several factors such as age , base excess , number of units of fresh frozen plasma (FFP) transfused  and Injury Severity Score (ISS)  have been identified as predictors for pulmonary failure in trauma patients. The transfusion of packed red blood cells (PRBC) significantly predicted the development of respiratory complications including pneumonia and acute respiratory distress syndrome (ARDS) . In addition, a lung contusion is known to represent an independent risk factor for acute lung injury (ALI), ARDS and pulmonary failure [6, 7], with the incidence of pulmonary failure increasing if the volume of pulmonary contusion exceeds 20 per cent of the total lung volume . However, pulmonary failure is a major contributor to morbidity and mortality in trauma patients.
Abdominal trauma and solid organ injuries can result in a significant need for PRBC transfusion leading secondarily to pulmonary failure. In particular, when non-operative management in blunt hepatic injuries fails, several complications such as pneumonia, bacteremia and ARDS can occur . Nevertheless, the impact of liver injury on the incidence of pulmonary failure in multiple trauma patients remains unclear.
Thus the goal of the present study was to test the hypothesis that patients sustaining significant thoracic trauma in combination with a relevant liver injury are more likely to develop pulmonary failure when compared to patients sustaining thoracic trauma without concomitant liver injury. In addition, we intended to analyze risk factors for the development of pulmonary failure in severely injured trauma patients.
TraumaRegister DGU® of the German Trauma Society (TR-DGU)
The TraumaRegister DGU® of the German Trauma Society is a multi-center database, where severely injured patients are prospectively documented at standardized time points: (1) pre-hospital phase: mechanism of injury, initial physiology, first therapy, neurological signs, prehospital time; (2) emergency room (ER): physiology, laboratory findings, suspected pattern of injury, therapy, time sequence of diagnostics; (3) intensive care unit (ICU): status on admission, organ failure, sepsis, duration of ventilation; and (4) final outcome: hospital stay, survival, complete list of injuries including anatomic injury assessment using the ISS , operative procedures, and pre-existing medical conditions (PMCs). Interventions are documented according to the International Classification of Procedures in Medicine (current documentation sheets and participating centers available on http://www.traumaregister.de). Data collection started in 1993 by the Working Group on Polytrauma of the German Trauma Society to evaluate the quality of trauma care in Germany, Austria, the Netherlands and Switzerland . All variables are continuously entered into a web based data server. Patients eligible are those suspected to require ICU treatment after trauma and to present an ISS ≥ 16 or those that die in the emergency room. Data are submitted to a central database hosted by the Institute for Research in Operative Medicine (IFOM) at the University of Witten/Herdecke in Cologne, Germany. Data anonymity is provided both for the individual patient as well as the participating hospital [12–14]. The TR-DGU is approved by the review board of the German Trauma Society and is in compliance with the institutional requirements of its members. The TR-DGU comprises datasets of 29,353 patients documented between 1993 and 2006 from 125 participating hospitals.
Patients documented between 1993 and 2006 in the TR-DGU were analyzed for eligibility. Inclusion criteria were: (1) ISS ≥ 16, (2) primary admission, (3) survival ≥ 24 hours, and (4) information available regarding (a) pulmonary failure, (b) administration of PRBC and (c) duration of mechanical ventilation. An injury was graded as severe if an Abbreviated Injury Scale (AIS) ≥ 3 was present . According to the injury pattern, patients were subdivided into the following subgroups: group 1 included multiple trauma patients, who had sustained neither a thoracic trauma nor a severe liver injury (AIS thorax < 3; AIS liver < 3); group 2 consisted of patients who had sustained a multiple injury including thoracic trauma without any liver injuries (AIS thorax ≥ 3; AIS liver < 3); multiple trauma patients who had sustained a relevant liver injury without concomitant thoracic trauma (AIS thorax < 3; AIS liver ≥ 3) were assigned to group 3 and ultimately patients with significant thoracic trauma and liver injury were assigned to group 4 (AIS thorax ≥ 3; AIS liver ≥ 3).
Selection of variables
The selection of potential predictors for the development of pulmonary failure was based on previous reports and included: age , sex , ISS  and New Injury Severity Score (NISS) , maximum AIS scores for thorax, abdomen, extremities and head, pre-hospital infusion volume , number of PRBCs transfused  and infusion volume in the ER until ICU admission , rate of multi organ failure (MOF) , defined as organ failure of two systems of ≥ 3 SOFA-score points of ≥ 2 days duration , duration of mechanical ventilation , ICU and hospital length of stay.
The following factors were dichotomized for univariate and multivariate logistic regression analysis: AIS thorax ≥ 3 versus < 3, administration of PRBCs versus non-administration, PRBC ≥ 10 versus < 10, relevant thorax injury versus no thorax injury, relevant liver injury versus no liver injury, AIS head ≥ 3 versus ≤ 1, AIS abdomen ≥ 3 versus ≤ 1, presence versus absence of PMCs, and male versus female gender.
The primary outcome parameter was the incidence of pulmonary failure defined by pulmonary failure for at least two days according to Vincent et al. . Pulmonary failure was assumed if the Sepsis-related Organ Failure Assessment (SOFA) score was ≥ 3 points for a minimum duration of two days.
The demographic and clinical characteristics comparing the previously described groups were evaluated using bivariate analysis. The p values for categorical variables were derived from the Chi-square or 2-sided Fisher’s exact test and for continuous variables from the Student's or the Mann-Whitney test. Multivariate analysis was performed to control for confounders diverging significantly (p < 0.05) between the compared groups. For continuous outcomes, analysis of covariance was used to adjust for confounders that were significant at p < 0.05.
To identify risk factors that were independently associated with the presence of pulmonary failure, a stepwise logistic regression model was utilized and risk factors from the bivariate analysis with a p value < 0.2 were included in the model.
Variables are given as mean ± standard deviation (SD) and as number and percentage for categorical variables. Odds ratios with 95% confidence intervals (CI95) were calculated for statistically significant variables. Statistical analysis was performed using the Statistical Package for Social Sciences (SPSS Windows©), version 15.0 (SPSS Inc., Chicago, IL, USA).
Basic characteristics: patients were assigned to four different groups according to their AIS lung and AIS liver
AIS lung < 3
AIS lung ≥ 3
AIS lung < 3
AIS lung ≥ 3
AIS liver < 3
AIS liver < 3
AIS liver ≥ 3
AIS liver ≥ 3
(n = 5347; 42.5%)
(n = 6528; 51.9%)
(n = 188; 1.5%)
(n = 522; 4.1%)
Age, years (mean ± SD)
42.1 ± 21.1a
40.5 ± 18.6c
31.1 ± 14.2d
34.8 ± 16.8e
24.1 ± 9.1
31.3 ± 11.1
27.4 ± 9.5
40.8 ± 11.6
31.5 ± 12.9
36.1 ± 12.8
34.6 ± 12.3
44.8 ± 12.6
Duration of ventilation (days)
7.3 ± 12.1
8.3 ± 11.2
13.7 ± 17.4
ICU length of stay (days)
11.5 ± 14.6
15.1 ± 15.8
13.1 ± 13.2
19.8 ± 22.3
In hospital length of stay (days)
28.5 ± 31.7b
32.2 ± 35.3
29 ± 24.5d
35 ± 29.9f
MOF (%) (defined as organ failure of two systems of >2 SOFA-score points of ≥ 2 days duration)16
19 ± 39
25 ± 43
26 ± 44
39 ± 49
In hospital mortality rate (%)
Pulmonary failure ≥ 2 days (%)
Bivariate analysis of selected parameters in patients with and without pulmonary failure
No pulmonary failure
(n = 12,585 )
(n = 10,000)
(n = 2,585)
40.8 ± 19.7
40.1 ± 19.6
43.7 ± 19.7
28.6 ± 11.1
27.3 ± 10.5
33.7 ± 12.1
34.5 ± 13.2
33 ± 12.7
40.1 ± 13.5
Length of ventilation (days)
9.0 ± 12.8
6.4 ± 10
19.4 ± 16.5
Stay in ICU (days)
13.7 ± 15.8
10.9 ± 13.2
24.91 ± 19.5
In hospital stay (days)
30.7 ± 33.5
28.1 ± 32.5
40.6 ± 35.4
PRBC before ICU adminission (Units)
2.5 ± 6.2
2.0 ± 4.9
4.8 ± 9.4
Prehospital volume substitution (ml)
1,414 ± 1,155
1,338 ± 1,106
1,707 ± 1,285
2,948 ± 3,061
2,702 ± 2,645
2,947 ± 3,061
Incidence of pulmonary failure in univariate conditions
ISS ≥ 25
Early termination of regular ER diagnostics due to emergency operation
Glasgow coma scale ≤ 8
Lung injury (AISthorax ≥3)
Liver injury (AISadomen ≥3)
Age ≥ 60 years
AIShead ≥ 3
AISthorax ≥ 3
AISabdomen ≥ 3
AISextremity ≥ 3
Prehospital blood pressure ≤ 90 mmHg
Blood pressure in the ER ≤ 90 mmHg on admission
Administration of PRBC
Ttransfusion of ≥ 10 PRBC s
Admission during night shift
List of independent predictors for pulmonary failure as dependent variable in multivariate logistic regression analysis
Odds ratio (CI95)
Lung injury (AISthorax ≥3)
Transfusion of ≥10 PRBC
Administration of PRBC
Glasgow coma scale ≤ 8
ISS per point
Age per year
In this retrospective study evaluating 12,585 multiple traumatized patients, the presence of concomitant liver injury in thoracic trauma had no impact on the development of pulmonary failure. However, we found several factors which revealed a significant association with the incidence of pulmonary failure confirming previously published findings [8, 24]. In the current analysis, the presence of lung injury (AIS thorax ≥ 3) and other PMCs, sex, and the administration of more than 10 PRBCs increased the incidence of pulmonary failure following thoracic trauma.
To the best of our knowledge, this is the first study addressing the question of whether relevant liver injury in patients with thoracic trauma has a significant impact on clinical outcome in terms of pulmonary failure.
Pulmonary failure is a well-known complication after multiple trauma and has also been described following major hepatic surgery with an incidence of up to 82% [8, 24]. It is commonly associated with poor survival and quality of life, a significant increase in morbidity as well as increased health care costs . There is growing evidence that organ interactions must be taken into account to understand the determinants of ARDS. Among extra-pulmonary organs, the liver plays a central role in regulating cytokine kinetics relevant to acute lung injury. Since various studies in both, ARDS patients as well as ALI rodent models, revealed elevated leukotriene (LT) levels in lung edema fluid, it is proposed that LT levels have a substantial impact on the pathophysiology of ARDS [26–29]. The liver is the principle organ for metabolic leukotrien B4 [LTB4] inactivation. Impairment of liver function, e.g. due to relevant abdominal trauma, may therefore result in a limited and/or delayed catabolism of LTB4, which ultimately increases the risk of ARDS as well as pulmonary failure.
In addition, it has been shown that there is a high incidence of sepsis-induced acute lung injury in patients with end-stage liver failure emphasizing a close correlation between ARDS and liver failure . Hence, one can expect that additional liver injury following thoracic trauma promotes the incidence of pulmonary failure and ARDS, respectively. Unlike Matuschak and co-workers in their cohort of 29 patients with end-stage liver failure, we did not find liver injury to be a significant trigger for pulmonary failure in thoracic trauma when applied to the data of the TR-DGU in our setting.
As reported two decades ago in a series of 185 patients with blunt traumatic hepatic injury, class I-III hepatic injuries are relatively negligible as a cause of death or serious complications. In these populations the associated patterns of organ injury, such as brain and chest injuries are more likely to play a major role in the induction of serious complications, i.e. ARDS, which is frequently associated with high mortality . Although in our population liver injury was simply classified according to the AIS score and information regarding the classification of Moore  was missing, we likewise found severe liver injury, defined as AIS liver ≥ 3, not to be significantly associated with the development of severe pulmonary complications following thoracic trauma. Comparing thoracic trauma patients with and without liver injury did not reveal a statistically significant difference in the incidence of pulmonary failure and the overall in-hospital mortality.
Massive transfusion is commonly suggested as a major risk factor for the development of ARDS and pulmonary failure due to interaction between non-specific systemic inflammatory mediators, anti-granulocyte antibodies or depressed immune response [35–37]. We were able to confirm that the transfusion of ≥10 units of PRBCs until ICU admission is an independent predictor for the development of ARDS, as previously reported by Chaiwat and co-workers . They further demonstrated that one additional unit of PRBCs in patients receiving more than 10 units accounted for a 6% higher risk of ARDS . However, in our analysis, liver injury (AIS ≥ 3) was not associated with pulmonary failure but revealed a significant association with transfusion of PRBCs, whereas transfusion of PRBCs was significantly associated with pulmonary failure.
Although this is one of the largest studies investigating the association of liver injury and the development of pulmonary failure, there are some methodological issues and limitations, the most important being the retrospective nature of data analysis. All data were obtained from the database of the German Trauma Society, which was founded in the early 1990s. This database is not specifically developed for the documentation of patients with thoracic and/or liver trauma, but rather for the documentation of multiply traumatized patients in general. Moreover, we excluded patients who experienced pulmonary failure for only one day, because many trauma patients require initial lung function support during the first hours in hospital and on ICU. However, data were recruited from more than 120 hospitals in Germany, Austria, Switzerland and the Netherlands. Since we included almost 13,000 patients we believe that the patient population is representative.
Finally, the applied definitions of PMCs, for example, may vary widely among the different participating hospitals. While some diseases were clearly defined in our setting, others should be more specified in future studies. Although specifically designed clinical studies could reveal much more detail of the disease and its consequences, registry studies are from our point of view still considerable, since a large and representative number of patients is available for the analysis of even minor effects.
To conclude, in the current analysis, liver injury did not prove to be independently associated with the presence of pulmonary failure. Basic trauma research should focus on those identified risk factors to further explore their impact and pathophysiology to approach an improved and individualized therapeutic regime.
- Bulger EM, Arneson MA, Mock CN, Jurkovich GJ: Rib Fractures in the Elderly. J Trauma. 2000, 48: 1040-1047. 10.1097/00005373-200006000-00007.View ArticlePubMedGoogle Scholar
- Estenssoro E, Dubin A, Laffaire E, Canales HC, Saenz G, Moseinco M, Pozo M, Gomez A, Baredes N, Jannello G, Osatnik J: Incidence, clinical course, and outcome in 217 patients with acute respiratory distress syndrome. Crit Care Med. 2002, 30: 2450-2456. 10.1097/00003246-200211000-00008.View ArticlePubMedGoogle Scholar
- Watson GA, Sperry JL, Rosengart MR, Minei JP, Harbrecht BG, Moore EE, Cuschieri J, Maier RV, Billiar TR, Peitzman AB, The Inflammation and the Host Response to Injury I: Fresh Frozen Plasma Is Independently Associated With a Higher Risk of Multiple Organ Failure and Acute Respiratory Distress Syndrome. J Trauma. 2009, 67: 221-230. 10.1097/TA.0b013e3181ad5957. 210.1097/TA.1090b1013e3181ad5957View ArticlePubMedGoogle Scholar
- Edens JW, Chung KK, Pamplin JC, Allan PF, Jones JA, King BT, Cancio LC, Renz EM, Wolf SE, Wade CE: Predictors of Early Acute Lung Injury at a Combat Support Hospital: A Prospective Observational Study. J Trauma. 2010, 69: S81-S86. 10.1097/TA.0b013e3181e44a32. 10.1097/TA.1090b1013e3181e1044a1032View ArticlePubMedGoogle Scholar
- Englehart M, Cho S, Morris M, Gee A, Riha G, Underwood S, Differding J, Luem N, Wiesberg T, Boshkov L, Schreiber M: Use of Leukoreduced Blood Does Not Reduce Infection, Organ Failure, or Mortality Following Trauma. World J Surg. 2009, 33: 1626-1632. 10.1007/s00268-009-0076-5.View ArticlePubMedGoogle Scholar
- Ashbaugh DG, Bigelow DB, Petty TL, Levine BE: Acute respiratory distress in adults. Lancet. 1967, 2: 319-323.View ArticlePubMedGoogle Scholar
- Ware LB, Matthay MA: The acute respiratory distress syndrome. N Engl J Med. 2000, 342: 1334-1349. 10.1056/NEJM200005043421806.View ArticlePubMedGoogle Scholar
- Miller PR, Croce MA, Bee TK, Qaisi WG, Smith CP, Collins GL, Fabian TC: ARDS after pulmonary contusion: accurate measurement of contusion volume identifies high-risk patients. J Trauma. 2001, 51: 223-228. 10.1097/00005373-200108000-00003. discussion 229-230View ArticlePubMedGoogle Scholar
- Velmahos GC, Toutouzas K, Radin R, Chan L, Rhee P, Tillou A, Demetriades D: High Success With Nonoperative Management of Blunt Hepatic Trauma: The Liver Is a Sturdy Organ. Arch Surg. 2003, 138: 475-481. 10.1001/archsurg.138.5.475.View ArticlePubMedGoogle Scholar
- Baker SP, O'neill B, Haddon W, Long WB: The injury severity score: a method for describing patients with multiple injuries and evaluating emergency care. J Trauma. 1974, 14: 187-196. 10.1097/00005373-197403000-00001.View ArticlePubMedGoogle Scholar
- "Scoring" study committee of the German Society of Trauma Surgery: [Trauma register of the German Society of Trauma Surgery. Unfallchirurg. 1994, 97: 230-237.
- Ruchholtz S: [The Trauma Registry of the German Society of Trauma Surgery as a basis for interclinical quality management. A multicenter study of the German Society of Trauma Surgery]. Unfallchirurg. 2000, 103: 30-37. 10.1007/s001130050005.View ArticlePubMedGoogle Scholar
- Ruchholtz S: [External quality management in the clinical treatment of severely injured patients]. Unfallchirurg. 2004, 107: 835-843. 10.1007/s00113-004-0814-y.View ArticlePubMedGoogle Scholar
- Ruchholtz S, Nast-Kolb D, Waydhas C, Lefering R: [The trauma register of the 'Polytrauma' Committee of the German Society of Trauma Surgery as the basis for quality management in the management of severely injured patients]. Langenbecks Arch Chir Suppl Kongressbd. 1997, 114: 1265-1267.PubMedGoogle Scholar
- American Association for Automotive Medicine: Abbreviated Injury Scale - Revision 90. 1995, Morton Grove, Illinois, USA: The American Association For Automotive MedicineGoogle Scholar
- Battle CE, Hutchings H, Evans PA: Risk factors that predict mortality in patients with blunt chest wall trauma: a systematic review and meta-analysis. Injury. 2012, 43: 8-17. 10.1016/j.injury.2011.01.004.View ArticlePubMedGoogle Scholar
- Rincon F, Ghosh S, Dey S, Maltenfort M, Vibbert M, Urtecho J, Mcbride W, Moussouttas M, Bell R, Ratliff JK, Jallo J: Impact of acute lung injury and acute respiratory distress syndrome after traumatic brain injury in the United States. Neurosurgery. 2012, 71: 795-803. 10.1227/NEU.0b013e3182672ae5.View ArticlePubMedGoogle Scholar
- Miller PR, Croce MA, Kilgo PD, Scott J, Fabian TC: Acute respiratory distress syndrome in blunt trauma: identification of independent risk factors. Am Surg. 2002, 68: 845-850. discussion 850-841PubMedGoogle Scholar
- Osler T, Baker SP, Long W: A modification of the injury severity score that both improves accuracy and simplifies scoring. J Trauma. 1997, 43: 922-925. 10.1097/00005373-199712000-00009. discussion 925-926View ArticlePubMedGoogle Scholar
- Navarrete-Navarro P, Ruiz-Bailen M, Rivera-Fernandez R, Guerrero-Lopez F, Pola-Gallego-De-Guzman MD, Vazquez-Mata G: Acute respiratory distress syndrome in trauma patients: ICU mortality and prediction factors. Intensive Care Med. 2000, 26: 1624-1629. 10.1007/s001340000683.View ArticlePubMedGoogle Scholar
- Wutzler S, Wafaisade A, Maegele M, Laurer H, Geiger EV, Walcher F, Barker J, Lefering R, Marzi I: Lung Organ Failure Score (LOFS): probability of severe pulmonary organ failure after multiple injuries including chest trauma. Injury. 2012, 43: 1507-1512. 10.1016/j.injury.2010.12.029.View ArticlePubMedGoogle Scholar
- Laudi S, Donaubauer B, Busch T, Kerner T, Bercker S, Bail H, Feldheiser A, Haas N, Kaisers U: Low incidence of multiple organ failure after major trauma. Injury. 2007, 38: 1052-1058. 10.1016/j.injury.2007.03.020.View ArticlePubMedGoogle Scholar
- Vincent JL, Moreno R, Takala J, Willatts S, De Mendonca A, Bruining H, Reinhart CK, Suter PM, Thijs LG: The SOFA (Sepsis-related Organ Failure Assessment) score to describe organ dysfunction/failure. On behalf of the Working Group on Sepsis-Related Problems of the European Society of Intensive Care Medicine. Intensive Care Med. 1996, 22: 707-710. 10.1007/BF01709751.View ArticlePubMedGoogle Scholar
- Chapman WC, Debelak JP, Wright Pinson C, Washington MK, Atkinson JB, Venkatakrishnan A, Blackwell TS, Christman JW: Hepatic cryoablation, but not radiofrequency ablation, results in lung inflammation. Ann Surg. 2000, 231: 752-761. 10.1097/00000658-200005000-00016.PubMed CentralView ArticlePubMedGoogle Scholar
- Angus DC, Clermont G, Linde-Zwirble WT, Musthafa AA, Dremsizov TT, Lidicker J, Lave JR: Healthcare costs and long-term outcomes after acute respiratory distress syndrome: A phase III trial of inhaled nitric oxide. Crit Care Med. 2006, 34: 2883-2890.PubMedGoogle Scholar
- Stephenson AH, Lonigro AJ, Hyers TM, Webster RO, Fowler AA: Increased concentrations of leukotrienes in bronchoalveolar lavage fluid of patients with ARDS or at risk for ARDS. Am Rev Respir Dis. 1988, 138: 714-719. 10.1164/ajrccm/138.3.714.View ArticlePubMedGoogle Scholar
- Amat M, Barcons M, Mancebo J, Mateo J, Oliver A, Mayoral JF, Fontcuberta J, Vila L: Evolution of leukotriene B4, peptide leukotrienes, and interleukin-8 plasma concentrations in patients at risk of acute respiratory distress syndrome and with acute respiratory distress syndrome: mortality prognostic study. Crit Care Med. 2000, 28: 57-62. 10.1097/00003246-200001000-00009.View ArticlePubMedGoogle Scholar
- Westcott JY, Thomas RB, Voelkel NF: Elevated urinary leukotriene E4 excretion in patients with ARDS and severe burns. Prostaglandins Leukot Essent Fatty Acids. 1991, 43: 151-158. 10.1016/0952-3278(91)90162-X.View ArticlePubMedGoogle Scholar
- Masclans JR, Sabater J, Sacanell J, Chacon P, Sabin P, Roca O, Planas M: Possible prognostic value of leukotriene B(4) in acute respiratory distress syndrome. Respir Care. 2007, 52: 1695-1700.PubMedGoogle Scholar
- Matuschak GM, Rinaldo JE: Organ interactions in the adult respiratory distress syndrome during sepsis. Role of the liver in host defense. Chest. 1988, 94: 400-406. 10.1378/chest.94.2.400.View ArticlePubMedGoogle Scholar
- Rivkind AI, Siegel JH, Dunham CM: Patterns of organ injury in blunt hepatic trauma and their significance for management and outcome. J Trauma. 1989, 29: 1398-1415. 10.1097/00005373-198910000-00019.View ArticlePubMedGoogle Scholar
- Moore EE, Edgar J: Poth Lecture. Critical decisions in the management of hepatic trauma. Am J Surg. 1984, 148: 712-716. 10.1016/0002-9610(84)90422-7.View ArticlePubMedGoogle Scholar
- Erickson S, Schibler A, Numa A, Nuthall G, Yung M, Pascoe E, Wilkins B: Acute lung injury in pediatric intensive care in Australia and New Zealand: a prospective, multicenter, observational study. Pediatr Crit Care Med. 2007, 8: 317-323. 10.1097/01.PCC.0000269408.64179.FF.View ArticlePubMedGoogle Scholar
- Vincent JL, Zambon M: Why do patients who have acute lung injury/acute respiratory distress syndrome die from multiple organ dysfunction syndrome? Implications for management. Clin Chest Med. 2006, 27: 725-731. 10.1016/j.ccm.2006.06.010. abstract x-xiView ArticlePubMedGoogle Scholar
- Barrett NA, Kam PC: Transfusion-related acute lung injury: a literature review. Anaesthesia. 2006, 61: 777-785. 10.1111/j.1365-2044.2006.04742.x.View ArticlePubMedGoogle Scholar
- Nathens AB: Massive transfusion as a risk factor for acute lung injury: association or causation?. Crit Care Med. 2006, 34: S144-S150. 10.1097/01.CCM.0000214309.95032.65.View ArticlePubMedGoogle Scholar
- Carson JL, Altman DG, Duff A, Noveck H, Weinstein MP, Sonnenberg FA, Hudson JI, Provenzano G: Risk of bacterial infection associated with allogeneic blood transfusion among patients undergoing hip fracture repair. Transfusion. 1999, 39: 694-700. 10.1046/j.1537-2995.1999.39070694.x.View ArticlePubMedGoogle Scholar
- Chaiwat O, Lang JD, Vavilala MS, Wang J, Mackenzie EJ, Jurkovich GJ, Rivara FP: Early packed red blood cell transfusion and acute respiratory distress syndrome after trauma. Anesthesiology. 2009, 110: 351-360. 10.1097/ALN.0b013e3181948a97.View ArticlePubMedGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.