Secondary Logo

Journal Logo

The Use of Extracorporeal Membrane Oxygenation Systems in Severe Accidental Hypothermia After Drowning: A Centre Experience

Weuster, Matthias; Haneya, Assad; Panholzer, Bernd; Klüter, Tim; van der Brelie, Michael; van Laak, Ulrich; Cremer, Jochen; Haake, Nils

doi: 10.1097/MAT.0000000000000312
Clinical Critical Care
Free

Cardiopulmonary failure because of drowning with accidental hypothermia (AH) remains a major task for emergency care physicians. In this case series, we describe our experience in nine patients with cardiopulmonary failure after drowning with AH less than 35°C, who were provided on an emergency basis with extracorporeal life support (ECLS) system or extracorporeal membrane oxygenation (ECMO). Conservative rewarming methods are not considered for this study. Preclinical conditions and protocols were gathered. Surgical reports and clinical data sets were collected. Median age was 24 years (range, 6–75 years). Six patients were male. Climatic conditions mostly showed cold to frosty weather. All cases had different preclinical rescue procedures. They reached the emergency department under cardiopulmonary resuscitation (CPR). Indications for ECLS were cardiac arrest, and in one case, pulmonary failure. Mean CPR duration was 60 min (range: 15–120 min). Before implantation, the median pH value was 6.9. Two patients could be successfully weaned from the systems. Cause of death was severe neurologic damage in six patients and cardiac failure in one patient. The use of ECLS/ECMO is a therapy option for a small range of patients with cardiopulmonary failure because of drowning with AH. Nevertheless, the interval of preclinical rescue remains extensively long.

From the *Department of Trauma Surgery, Department of Cardiovascular Surgery, University Hospital Schleswig-Holstein, Campus Kiel, Kiel, Germany; Naval Institute of Maritime Medicine, Kronshagen, Germany; and §Department of Intensive Care Medicine, Imland Klinik, Rendsburg, Germany.

Submitted for consideration July 2015; accepted for publication in revised form November 2015.

Disclosure: The authors have no conflicts of interest to report.

Correspondence: Matthias Weuster, Department of Trauma Surgery, University Hospital Schleswig-Holstein, Campus Kiel, Arnold-Heller-Str. 3, 24105 Kiel, Germany. E-mail: Matthias.Weuster@uksh.de.

Drowning is still a frequent cause of accident-related deaths in Germany. The death rate totaled 417 patients (297 male, 120 female) in 2012.1 Accidental hypothermia (AH) regularly occurs among drowning patients with body core temperatures (BCTs) below 35°C.2 Accidental hypothermia is classified by its degree centigrade (°C), mild hypothermia ranges from 34°C to 32.0°C, moderate hypothermia from 31.9°C to 28.0°C, and severe hypothermia is described as temperatures below 28.0°C.3 The entity of AH affects organic systems most notably cardiovascular, pulmonary, and neuromuscular systems.2 Under the decline of temperature, the cardiac pathognomy increases; at early stage vasoconstriction and tachycardia impose, moderate AH leads to bradycardia and depression of cardiac output. Severe hypothermia causes ventricular fibrillation and cardiac arrest.4–8 People may respond to the mechanism of submersion with the mammalian reflex. It may lead to a hibernation effect by reduced metabolism, thus saving oxygen consumption of vulnerable organs.9 Pulmonary affection is outlined by an initial increase of respiratory minute volume merging to its drop-down and negative oxygen consumption. At late stage, edema and pulmonary failure occur.10 Concerning AHs impact on the cerebral and neurologic function, areflexia and paralysis impose.11 Above all, tolerance of cardiac arrest is narrow, and the positive effect (i.e., return of spontaneous circulation [ROSC]) after cardiopulmonary resuscitation (CPR) decreases as time of drowning and rescue prolongs.12 Clinical outcome because of AH in drowning patients varies. Mortality is described with rates from 20% to 70%.13–16 Once resuscitation has started and the patient is transported to a specialized hospital, the use of extracorporeal membrane oxygenation (ECMO) or extracorporeal life support (ECLS) provides a tool not only to recover cardiac and pulmonary function17 but also to establish a physiologic core temperature.2 Other methods for simply rewarming patients are still in use but not effective enough for severe injured patients.18 Unfortunately, most experiences in drowned patients with AH and correlated cardiopulmonary failure are based on a small number of studies mainly case reports.2 However, recent literature reflects that the development of extracorporeal cardiopulmonary resuscitation (ECPR) advances the issue of cardiopulmonary failure.19,20 In this case series, we describe our experience in nine individual patients with AH after drowning accidents with cardiac arrest or pulmonary failure. Indications and clinical course of the patients are displayed.

Back to Top | Article Outline

Methods

Setting

This retrospective study is performed at the Department of Cardiovascular Surgery, University Hospital of Schleswig-Holstein, Christian-Albrechts University of Kiel, Germany. The intensive care unit (ICU) of the department counts 24 beds. The centre provides a broad experience in ECMO and ECLS particularly besides its use in cardiac surgery. Patients were primarily surveyed in the shock area and immediately transferred from the Emergency Department (ED) to the operating room. Indications for ECMO/ECLS were made by an interdisciplinary team of cardiac surgeons, intensive care specialists, trauma surgeons, and anesthesiologists in the ED.

Back to Top | Article Outline

Ethics

Institutional Review Board approval was obtained, but the requirement of individual patient consent was waived because of the study’s retrospective design.

Back to Top | Article Outline

Inclusion and Exclusion Criteria

Study period was from 2003 to 2012 including nine patients of different ages. Only drowning accidents were considered. The included patients sustained severe AH (<32°C). Eight patients suffered from cardiac failure/arrest, and one patient suffered from pulmonary failure (acute respiratory distress syndrome, ARDS) after drowning. Patients who were indicated for implantation of ECMO or ECLS with cardiac arrest all sustained long and extensive CPR, and the patient with ARDS was treated through intensive respiratory management in a rural hospital for about 12 hours. In case of pulmonary failure, preclinical data were missing. Preclinical settings and rescue procedures were different in each patient. Transfer happened either by helicopter or by ground rescue systems. No common treatment protocols existed among paramedics and surrounding external hospitals. Exclusion criteria include patients with existing vital signs that approached the hospital under mild or moderate AH. No patients with AH because traumatic reasons. Patients of extreme age, i.e., geriatric, were excluded as well.

Back to Top | Article Outline

Data

Data sets were gathered by the patients’ hospital files with preclinical reports, admission and surgery protocols, laboratory and blood gas parameters, and hospital discharge documents. Results are shown in mean with standard deviation. As the number of patients is small (n = 9), we did not perform statistical analyses. This study is a description of a case series. Missing data are displayed cross-marked.

Back to Top | Article Outline

Accidental Hypothermia

The organ dysfunctions increase as BCT declines. Cardiac symptoms include tachycardia, bradycardia, general arrhythmias, vasoconstriction, low cardiac output, minor contractility, and cardiac arrest. Pulmonary complications impress and lead to basically apnoe and higher pulmonary secretion. Coagulopathy sets in with mainly thrombocytes’ malfunctions. Cerebral function fades with reduced electroencephalograph (EEG) activity, lower cerebral perfusion and finally cerebral coma. Peripheral neuropathy occurs. Electrolytes are unbalanced with metabolic acidosis. Gastrointestinal disorders predominate with lower bowl motility and ulcerations.21

Back to Top | Article Outline

Drowning

Drowning” is described as a process resulting in primary respiratory impairment from submersion/immersion in a liquid medium. A liquid/air interface is present at the entrance of the patient’s airway, preventing the patient from breathing air. The patient may live or die after this process.22 Water aspiration is usually small because of early laryngospasm preventing further entry of water. As the hypoxic phase prolongs, the laryngospasm will end. Aspirated water will lead to pulmonary disorders. Primarily surfactant gets washed out. The pulmonary capillary barrier leaks, lung edema follows, and the risk of ARDS increases. The longer patients are exposed to cold water by immersion or submersion AH becomes the major threat.

Back to Top | Article Outline

Extracorporeal Membrane Oxygenation and Extracorporeal Life Support

Two systems were used in this study. Either ECLS or ECMO were implanted. The ECLS system was “Emergency Life Support Cardiohelp” (MAQUET Cardiopulmonary, Hirrlingen, Germany). It is a portable and thus lightweight extracorporeal perfusion system. The system can work independently with battery packs for about 90 min. Its circuits are preconnected and suitable for a rapid setup and priming. A plasma-tight polymethylpentene (PMP) diffusion membrane oxygenator, an integrated centrifugal pump and a drive and steering unit make up the system. Heparin coats all blood contact surfaces, and thus, systemic anticoagulation can be kept low. The activated partial thromboplastin time (aPTT) is intended to be in the range of 50 and 60 sec. The priming volume is less than 600 ml normal saline. The drive and steering units incorporate flow sensing and bubble detecting modalities. Basically, a long cannula (55 cm, 21–23 Fr) was percutaneously inserted into the femoral vein up to the right atrium using Seldinger’s technique. The arterial return was achieved with a short cannula (15 cm, 15–17 Fr) via the femoral artery. The ECMO system displays an equal modulation like the ECLS. The difference is based on the venovenous cannulation in case of acute respiratory failure. Surgical approach is usually percutaneously by femoral or jugular veins. Adequate oxygenation and ventilation of the patient can be achieved. Blood gases have to be controlled. All components are Heparin coated as well.

Back to Top | Article Outline

Results

The characteristics of the patients (mean age of 24 years) differed with a range from 3 to 75 years (6 male and 3 female patients). Body weight varied with a mean body mass index of 20.8. Glasgow Coma Scale (GCS) was 3 in all cases. Body core temperature was significantly low ranging from 13.4°C to 29.4°C. Patients were approached by water- or air-rescue systems and rescued from a wet spot, lakes, ponds, and the Baltic Sea by paramedics. Procedures showed a mean of 115.5 min until admission to the ED. Climatic surroundings mainly displayed icy and frosty conditions. Seven patients were found submersed with unknown amounts of aspirated water. Two patients did not submerse.

Details on clinical course and parameters are shown in Table 2. Leading indication in all cases for ECMO/ECLS were persistent cardiac arrest (n = 8) and pulmonary failure with severe hypoxic state (n = 1) because of severe AH, despite aggressive techniques in advanced life support. All patients required CPR, basically suffering from long-time exposure to extreme cold, wet environment. One patient who suffered from ARDS was treated by invasive and aggressive respiratory therapy by a rural hospital. Once admitted to the shock room, the initial blood gases showed signs of severe shock. Mean results of arterial blood gases displayed values of arterial pH, 6.9; lactate, 20.8 mmol/L; base excess, 17 mmol/L. Until ECMO/ECLS were placed, eight patients received continuous CPR, and in one case, the LUCAS system (Physio-Control Inc./Jolife AB, Lund, Sweden) was required. Nine patients were endotracheal intubated. The female patient received aggressive respiratory therapy. No adequate ventilation could be obtained. Here, secondary transfer was indicated for ECMO implantation. Vasopressor and inotropes were applied in all cases. Venoarterial cannulation (n = 7) was performed either by open chest surgery or by percutaneous inguinal approach. Venovenous cannulation (n = 1) was performed by percutaneous technique in case of ARDS. Further ICU treatment involved a complex therapy. Mean duration of ECMO/ECLS treatment was 56 (3–260) hours. Seven patients could not be successfully resuscitated. Cranial computed tomography (CT) scans and regular neurological re-/evaluations were performed. Severe neurological outcome with major brain edema occurred in these seven patients. Two patients were successfully weaned, one male patient after cardiac arrest and one female patient after ARDS. At discharge from the hospital, they showed no neurological deficit, stable cardiopulmonary status with physiologic laboratory parameters.

Back to Top | Article Outline

Discussion

The incidence of cardiac arrest because of severe AH after drowning remains a rare but immense problem. The clinical course of these patients displays severe complications and has high rates of mortality.1,2 Nevertheless, patients drowned by immersion or submersion still have to be found and rescued from the water. Newspaper headlines during the summer season underline this problem.

Our study describes a period of 10 years. We could include nine patients who reached the hospital with the diagnosis of severe AH after drowning accidents. Past studies are rare and reported on similar case series in which patients were rescued from either lakes or ponds or from maritime waters.5,6 The event of drowning is still a challenge for paramedics and emergency care physicians to shorten the time interval in which early hypothermia affects the patients’ physiology. A long lasting AH has a huge impact on the cardiovascular system.18,21 Most patients suffered from cold and frosty conditions in our study. The process of drowning starts with immersion. At the beginning, the patient is influenced by sudden effects of the cold water such as shivering and quick movements of the body. With submersion among others cold water, body fat, clothing, and the patients’ behavior in the water interact with each other. Further cooling follows as tissue isolation weakens. The majority in our study group suffered from submersion. Studies reported on protective effects of body fat.6 We observed a very low body mass index of our severe hypothermic group. Cardiac arrest occurred in eight cases. The question remains whether female patients have higher potential for resisting severe hypothermic conditions, although we had more male than female patients in our observation.6 The average time schedule until patients were admitted to our ED lasted up to 2 hours. The preclinical course is probably not changeable because of rescue procedures.23 The complex and difficult demands of water rescue supports this fact. In cases of mild to moderate hypothermia, it is of utmost neccessarity to make early use of traditional rewarming methods. They have to be applied in preclinical and at latest in clinical settings. Warm liquids and prewarmed blanket are the easiest and quickest techniques to stop further cooling. Especially trauma patients profit from preventing hypothermia suggested by common guidelines.24 The combination of hemorrhagic shock and AH aggravates the patients’ clinical outcome after polytrauma.25 Long exposure, forced volume management, metabolic disorders are predisposed factors. Coagulopathy with impaired platelet function and reduced clotting factor activity is observed.26 The restoration of clotting factors and an improved oxygenation are the upper goals after polytrauma.27 When it comes to severe hypothermia with cardiopulmonary failure, the recommendations describe techniques such as the use of ECLS.28 Extracorporeal life support even provides support after severe trauma in patients with bleeding shock.19 Experiences in severe AH basically rely upon case reports and single centre studies.2,5,6 Rewarming treatments vary a lot described in detail by the working group of van der Ploeg et al.2 They were able to study on a large group of more than 80 hypothermic patients admitted to the hospital with a large variety of BCT; as many as 14 rewarming techniques were used. Only six patients received cardiopulmonary bypass operation for rewarming. Indications were mostly severe hypothermia with death counts of two patients. The leading and most frequently used tools remain the application of any kind of warm blankets/mattresses and prewarmed liquids. Our observed group of cardiopulmonary bypasses (n = 9) is comparable with their study group concerning BCT and preclinical courses. Other investigations describe similar settings considering preclinical procedures, the ages of patients, the range of BCT, and initial laboratory parameters because of AH.29 Our patients were all admitted to the shock room with severe hypothermia (in maximum 29.4°C BCT) and mainly cardiac arrest (n = 8). One female patient was transferred from another hospital because of a therapy resistant ARDS. The preclinical treatment of these patients was highly qualified with CPR as suggested by current guidelines.30 Intensive telephone communication happened before admission between paramedics and cardiac surgeons. The indications for ECMO were clear in all cases. As techniques of ECMO have advanced over the years, knowledge and experience have widened. It has become an essential tool especially concerning patients with cardiac arrest, severe pulmonary failure respectively ARDS, and even in patients with bleeding shock after trauma.19,31–35 It provides sufficient blood flow, restores oxygenation, and ventilation parameters, and it rewarms the BCT with a definite rate.7,28,29 Besides, the positive effects complications are re-/bleeding, vessel ruptures, limb ischemia, and infections.19 Careful cannulation and safe surgical approaches reduce such risks. We observed rebleeding as the inguinal region is predisposed. Besides, surgical problems’ further complications were observed during the clinical course on ICU. In addition to coagulopathy and metabolic disorders, patients are in danger of pneumonia, liver and kidney failure, and decreased immunologic functions.2,36,37 The survivors in our group (n = 2) showed pneumonia and lung edema. One patient38 had slight peripheral neuropathy of his hands and a hearing loss, both in regression at discharge. Lung edema was reported in four patients. These complications occurred after rewarming. Among others, we treated five children after drowning with poor outcome. The time of CPR was extended. All children had been in submersion. This might explain the poor outcome. Neither severe AH nor sufficient CPR was able to restore a response in circulation. Past studies have reported on similar results.18 Blood gases of lactate, bases excess, and arterial pH displayed the severity of injury because AH (Tables 1 and 2). Neurological outcome resulted in brain hypoxia, which required profound neurological evaluation and reassessment by brain CT scans. In three patients, fatal outcome was the result of cerebral death. Reason for the hypoxic state in the patients is most likely the prolonged period of oxygen deficit before and during rescue.

Table 1

Table 1

Table 2

Table 2

We conclude that the accident of drowning with cardiac arrest under AH is a very rare but life threatening problem. The rescue procedure until patients are adequately treated by the up-to-date therapy of ECLS is difficult and complex. Many patients are simply not rescued from the water in time and do not even reach the hospital. In case of rescue, severe clinical complications influence patients’ recovery: massive lung edema, brain hypoxic states, and no-cardiac response after rewarming are observed. Nevertheless, our report has some limitations. The report is a single center experience, and the number of patients is small. This is in accordance with past and similar studies. The retrospective data collection is a major limitation. The findings and results are based on data and hospital files, which often lack important information. However, ECMO/ECLS remains a therapy option to recover from severe AH. It may reestablish cardiopulmonary functions. But as only two patients survived in our study (one after cardiac arrest and one after ARDS), the therapy through ECMO/ECLS is clearly limited to small range of patients after drowning and AH. Nevertheless, ECMO/ECLS is restricted to level one trauma centers that provide cardiovascular surgery facilities. The future focus should be based on multicenter investigations. Treatment regime for this group of patients needs to be forwarded as essential information and recommendations for emergency care medicine.

Back to Top | Article Outline

References

1. Bundesamt S:. Todesursachen in Deutschland 2012. Statistisches Bundesamt. 2013
2. van der Ploeg GJ, Goslings JC, Walpoth BH, Bierens JJ. Accidental hypothermia: rewarming treatments, complications and outcomes from one university medical centre. Resuscitation. 2010;81:1550–1555
3. Kobbe P, Lichte P, Wellmann M, et al. [Impact of hypothermia on the severely injured patient]. Unfallchirurg. 2009;112:1055–1061
4. Gilbert M, Busund R, Skagseth A, Nilsen PA, Solbø JP. Resuscitation from accidental hypothermia of 13.7 degrees C with circulatory arrest. Lancet. 2000;355:375–376
5. Walpoth BH, Walpoth-Aslan BN, Mattle HP, et al. Outcome of survivors of accidental deep hypothermia and circulatory arrest treated with extracorporeal blood warming. N Engl J Med. 1997;337:1500–1505
6. Wanscher M, Agersnap L, Ravn J, et al. Outcome of accidental hypothermia with or without circulatory arrest: experience from the Danish Præstø Fjord boating accident. Resuscitation. 2012;83:1078–1084
7. Suominen PK, Vallila NH, Hartikainen LM, Sairanen HI, Korpela RE. Outcome of drowned hypothermic children with cardiac arrest treated with cardiopulmonary bypass. Acta Anaesthesiol Scand. 2010;54:1276–1281
8. Lønning PE, Skulberg A, Abyholm F. Accidental hypothermia. Review of the literature. Acta Anaesthesiol Scand. 1986;30:601–613
9. Giesbrecht GG. Cold stress, near drowning and accidental hypothermia: a review. Aviat Space Environ Med. 2000;71:733–752
10. Morales CF, Strollo PJ. Noncardiogenic pulmonary edema associated with accidental hypothermia. Chest. 1993;103:971–973
11. Segers MJ, Diephuis JC, van Kesteren RG, van der Werken C. Hypothermia in trauma patients. Unfallchirurg. 1998;101:742–749
12. Baumgartner FJ, Janusz MT, Jamieson WR, Winkler T, Burr LH, Vestrup JA. Cardiopulmonary bypass for resuscitation of patients with accidental hypothermia and cardiac arrest. Can J Surg. 1992;35:184–187
13. Farstad M, Andersen KS, Koller ME, Grong K, Segadal L, Husby P. Rewarming from accidental hypothermia by extracorporeal circulation. A retrospective study. Eur J Cardiothorac Surg. 2001;20:58–64
14. Kornberger E, Mair P. Important aspects in the treatment of severe accidental hypothermia: the Innsbruck experience. J Neurosurg Anesthesiol. 1996;8:83–87
15. Martin RS, Kilgo PD, Miller PR, Hoth JJ, Meredith JW, Chang MC. Injury-associated hypothermia: an analysis of the 2004 National Trauma Data Bank. Shock. 2005;24:114–118
16. Bierens JJ, Warner DS. Drowning resuscitation requires another state of mind. Resuscitation. 2013;84:1467–1469
17. Phillips SJ, Ballentine B, Slonine D, et al. Percutaneous initiation of cardiopulmonary bypass. Ann Thorac Surg. 1983;36:223–225
18. Bierens JJ, Uitslager R, Swenne-van Ingen MM, van Stiphout WA, Knape JT. Accidental hypothermia: incidence, risk factors and clinical course of patients admitted to hospital. Eur J Emerg Med. 1995;2:38–46
19. Arlt M, Philipp A, Voelkel S, et al. Extracorporeal membrane oxygenation in severe trauma patients with bleeding shock. Resuscitation. 2010;81:804–809
20. Ried M, Bein T, Philipp A, et al. Extracorporeal lung support in trauma patients with severe chest injury and acute lung failure: a 10-year institutional experience. Crit Care. 2013;17:R110
21. Hildebrand F, Probst C, Frink M, Huber-Wagner S, Krettek C. [Importance of hypothermia in multiple trauma patients]. Unfallchirurg. 2009;112:959–964
22. Layon AJ, Modell JH. Drowning: update 2009. Anesthesiology. 2009;110:1390–1401
23. Timm A, Maegele M, Lefering R, Wendt K, Wyen HTraumaRegister DGU®. . Pre-hospital rescue times and actions in severe trauma. A comparison between two trauma systems: Germany and the Netherlands. Injury. 2014;45(Suppl 3):S43–S52
24. . Advanced trauma life support (ATLS(R)): the ninth edition. J Trauma Acute Care Surg. 2013;74:1363–1366
25. Mommsen P, Zeckey C, Frink M, Krettek C, Hildebrand F. [Accidental hypothermia in multiple trauma patients]. Zentralbl Chir. 2012;137:264–269
26. Mohr J, Ruchholtz S, Hildebrand F, et al. Induced hypothermia does not impair coagulation system in a swine multiple trauma model. J Trauma Acute Care Surg. 2013;74:1014–1020
27. Nast-Kolb D, Ruchholtz S, Waydhas C, Taeger G. [Management of polytrauma]. Chirurg. 2006;77:861–872; quiz 873
28. Soar J, Deakin CD, Nolan JP, et al.European Resuscitation Council. [Cardiac arrest with special circumstances. Section 7 in the Guidelines for Resuscitation 2005 of the European Resuscitation Council]. Unfallchirurg. 2009;112:236–264
29. Oberhammer R, Beikircher W, Hörmann C, et al. Full recovery of an avalanche victim with profound hypothermia and prolonged cardiac arrest treated by extracorporeal re-warming. Resuscitation. 2008;76:474–480
30. Bossaert L, O’Connor RE, Arntz HR, et al.Acute Coronary Syndrome Chapter Collaborators. Part 9: acute coronary syndromes: 2010 International Consensus on Cardiopulmonary Resuscitation and Emergency Cardiovascular Care Science with Treatment Recommendations. Resuscitation. 2010;81(Suppl 1):e175–e212
31. Arlt M, Philipp A, Zimmermann M, et al. Emergency use of extracorporeal membrane oxygenation in cardiopulmonary failure. Artif Organs. 2009;33:696–703
32. Conseil français de réanimation cardiopulmonaire; Société française d'anesthésie et de réanimation; Société française de cardiologie; Société française de chirurgie thoracique et cardiovasculaire; Société française de médecine d'urgence; Société française de pédiatrie; Groupe francophone de réanimation et d'urgence pédiatriques; Société française de perfusion; Société de réanimation de langue française. . Guidelines for indications for the use of extracorporeal life support in refractory cardiac arrest. French Ministry of Health. Ann Fr Anesth Reanim. 2009;28:182–190
33. Ruttmann E, Weissenbacher A, Ulmer H, et al. Prolonged extracorporeal membrane oxygenation-assisted support provides improved survival in hypothermic patients with cardiocirculatory arrest. J Thorac Cardiovasc Surg. 2007;134:594–600
34. Shin TG, Choi JH, Jo IJ, et al. Extracorporeal cardiopulmonary resuscitation in patients with inhospital cardiac arrest: A comparison with conventional cardiopulmonary resuscitation. Crit Care Med. 2011;39:1–7
35. Terragni P, Faggiano C, Ranieri VM. Extracorporeal membrane oxygenation in adult patients with acute respiratory distress syndrome. Curr Opin Crit Care. 2014;20:86–91
36. Tang XN, Yenari MA. Hypothermia as a cytoprotective strategy in ischemic tissue injury. Ageing Res Rev. 2010;9:61–68
37. Wagner F, Wagner K, Weber S, et al. Inflammatory effects of hypothermia and inhaled H2S during resuscitated, hyperdynamic murine septic shock. Shock. 2011;35:396–402
38. Kroppenstedt SN, Thomale UW, Griebenow M, et al. Effects of early and late intravenous norepinephrine infusion on cerebral perfusion, microcirculation, brain-tissue oxygenation, and edema formation in brain-injured rats. Crit Care Med. 2003;31:2211–2221
Keywords:

accidental hypothermia; drowning; extracorporeal membrane oxygenation; cardiac arrest; acute respiratory distress syndrome

Copyright © 2016 by the American Society for Artificial Internal Organs