Bench to bedside review: Extracorporeal carbon dioxide removal, past present and future
© BioMed Central Ltd 2012
Published: 21 September 2012
Acute respiratory distress syndrome (ARDS) has a substantial mortality rate and annually affects more than 140,000 people in the USA alone. Standard management includes lung protective ventilation but this impairs carbon dioxide clearance and may lead to right heart dysfunction or increased intracranial pressure. Extracorporeal carbon dioxide removal has the potential to optimize lung protective ventilation by uncoupling oxygenation and carbon dioxide clearance. The aim of this article is to review the carbon dioxide removal strategies that are likely to be widely available in the near future. Relevant published literature was identified using PubMed and Medline searches. Queries were performed by using the search terms ECCOR, AVCO2R, VVCO2R, respiratory dialysis, and by combining carbon dioxide removal and ARDS. The only search limitation imposed was English language. Additional articles were identified from reference lists in the studies that were reviewed. Several novel strategies to achieve carbon dioxide removal were identified, some of which are already commercially available whereas others are in advanced stages of development.
The reported incidence of acute respiratory distress syndrome (ARDS) ranges from 7 to 59 per 100,000 people [1, 2], and is associated with a mortality rate of 40 to 45%. This rate remains unacceptably high despite the introduction of lung protective ventilation and, although hospital mortality may be slowly decreasing, ICU and 28 day mortality have remained constant [1, 3]. Failure to implement lung protective ventilation (LPV) may be one of the reasons ICU mortality rates have remained unchanged [4–6]. When surveyed, health care providers reported that hypercapnia or its related effects were significant barriers to achieving LPV . Hypercapnia complicated 14% of patients in the large ARDS network on the use of LPV . However, patients with a high risk of death were excluded. In a study of severe ARDS, where tidal volumes were adjusted to target a mean airway pressure less than 28 cmH2O, all patients experienced hypercapnia . As evidence emerges that tidal volumes <6 ml.kg-1 might further reduce mortality [9, 10], alternative strategies to manage the inevitable hypercapnia must be considered.
Permissive hypercapnia is one approach, but it only improves mortality when patients are ventilated with high tidal volumes . Such volumes should no longer be used since 6 ml.kg-1 is superior to 12 ml.kg-1 and <4 ml.kg-1 might be superior to 6 ml.kg-1 [9–11]. Although hypercapnia might have beneficial effects on oxygen delivery and attenuation of inflammation , it also harms injured lung through immunosuppression and impaired pulmonary epithelial repair [13, 14]. Furthermore, hypercapnia perpetuates right heart failure  and is undesirable in patients with elevated intracranial pressure. An alternative strategy to manage hypercapnia is extracorporeal carbon dioxide removal (ECCOR), a technology pioneered four decades ago  but only recently readily accessible through commercialization of several novel devices. ECCOR therefore deserves a fresh look and this review aims to provide an overview of devices currently available and those that may be available in the near future.
ECCOR in principle
In contrast to ECMO, where the need for oxygenation requires high blood flow rates, ECCOR allows much lower blood flow rates, a result of major differences in CO2 and oxygen (O2) kinetics. First, almost all the O2 in blood is carried by hemoglobin, which displays sigmoidal saturation kinetics. Assuming normal hemoglobin and venous O2, each liter of venous blood can only carry an extra 40 to 60 ml of O2 before the hemoglobin is saturated. Blood flows of 5 to 7 L.minute-1 are therefore required to supply enough O2 for an average adult (250 ml. minute-1). Conversely, most CO2 is transported as dissolved bicarbonate, displaying linear kinetics without saturation. Thus, 1 L of blood is capable of carrying more CO2 than O2, and 250 ml of CO2 can be removed from <1 L of blood. Second, CO2 diffuses more readily than O2 across extracorporeal membranes because of greater solubility .
The membrane lung
The membrane lung made long-term extracorporeal gas exchange feasible. Before membrane lungs, extracorporeal circuits achieved gas exchange by creating a direct air-blood interface, either bubbling air through blood or creating a thin film of blood on the surface of a rotating cylinder/disc. However, blood-air interfaces denature proteins, activate clotting and inflammatory pathways, and damage circulating cells . Consequently, devices relying on blood-air interfaces cannot be used more than a few hours without serious complications.
The concept of placing a barrier between blood and air began with the observation that gas exchange occurred across cellophane tubing in hemodialysis machines . This led to the development of membrane lungs consisting of gas permeable silicone-rubber mounted on a nylon mesh . The nylon mesh provided structural strength and decreased leakage from random pinhole defects, which occur during the manufacture of thin silicone-rubber membranes . Three major factors determine the amount of gas crossing membranes: the diffusion gradient, the membrane-blood contact time and the membrane diffusion characteristics.
Extracorporeal carbon dioxide removal circuit components
Impeller elevated in electromagnetic field
Levotronix LLC Waltham, MA, USA
Impeller driven by electromagnetic field and has single sapphire bearing
Maquet, Rastatt, Germany
Impeller drive shaft supported by sealed bearings
Medtronic, Eden Praire, MN, USA
Diagonally streamed impeller, sealed bearings
Medos Medizintechnik AG, Stolberg, Germany
1.8 m2 surface area, 250 ml priming volume
Maquet, Rastatt, Germany
iLA membrane ventilator
1.3 m2 surface area, 175 ml priming volume
Novalung GmbH, Heilbronn, Germany
1.9 m3 surface area, 275 ml priming volume
Medos Medizintechnik AG, Stolberg, Germany
2.5 m2 surface area, 270 ml priming volume
Medtronic, Eden Praire, MN, USA
Blood flow through ECCOR circuits can be achieved in one of two ways. In patients with sufficient arterial pressure, a pumpless system can be used where blood is driven out of an arterial cannula by high arterial pressures and returned through a venous cannula, often called arteriovenous CO2 removal (AVCO2R). Pumpless systems result in less blood trauma, but require large bore arterial cannulas and an adequate cardiac output. The alternative is to use a mechanical pump.
Early devices used roller or peristaltic pumps. Although cheap and reliable, these pumps were prone to blood trauma - for example, hemolysis - from compression and heating of blood components. Blood trauma is less of a problem at lower blood flow rates - for example, those used in dialysis. The introduction of rotary pumps has resulted in simpler yet effective systems that cause less blood trauma. Two main types of rotary pumps are used in ECCOR devices, centrifugal and diagonal flow pumps.
Centrifugal pumps use a radial rotating impeller to create a suction vortex that draws blood into the center of the pump and spins it outwards, imparting centrifugal momentum, which is converted into driving pressure. In diagonal flow pumps, impellor design is a mix of radial and axial geometry. Centrifugal pumps tend to generate high pressures and low flows, whereas diagonal pumps produce both high flows and high pressures . Impellors are connected to a drive shaft, requiring bearings to support the rotational movement. Exposure of blood to typical bearings promotes clotting, causing deposition of coagulation debris that can seize the bearing. Some pumps use seals to protect the bearings, but these can wear out; other designs use biocompatible materials to construct the bearings. In the most advanced centrifugal pumps impellors are completely suspended in an electromagnetic field, eliminating the need for a drive shaft or bearings and reducing heating, minimizing blood trauma and lowering the incidence of mechanical failure.
Early clinical trials placed separate drainage and return cannulas in the saphenous veins [29, 30]. Modern cannulas are placed percutaneously in a femoral-femoral or femoral-jugular orientation. To maintain flow and minimize blood trauma, heparin-coated wire-reinforced cannulas are used. Recently, a high flow, wire-reinforced double-lumen catheter has been developed. It is placed via the right internal jugular vein and the drainage port (tip of the cannula) is advanced into the intra-hepatic inferior vena cava using ultrasound guidance . In this orientation the return port aligns with the right atrium, minimizing recirculation. New ECCOR devices with flow rates comparable to those in dialysis use double-lumen cannulas similar to dialysis catheters [32, 33].
ECCOR in practice
The first clinical trial of extracorporeal respiratory support was published in 1979, and used the Kolobow spiral-coil membrane lung, a roller pump and venoarterial access to provide ECMO . This trial found no difference between conventional treatment and ECMO. At about the same time Gattinoni and coworkers introduced ECCOR , but did not publish the first clinical trial until 1986, where patients with severe ARDS were selected for LPV combined with ECCOR (Kolobow spiral-coil membrane lung, and a roller pump). Observed mortality was 51% using this technique . Subsequent work was initially encouraging  but a randomized controlled study in 1994 concluded that ECCOR conferred no survival advantage . Importantly, complication rates were high with ECCOR, being discontinued in 33% of cases owing to bleeding, and 20% experiencing circuit clotting. Recently, new devices with lower complication rates have demonstrated improved survival when combined with ultra-protective ventilation ; some are already available whilst others are in advanced development. They can be broadly categorized into i) arteriovenous devices, ii) venovenous devices, iii) gas exchange catheters and iv) respiratory dialysis.
Arteriovenous carbon dioxide removal
Pumpless systems require an arteriovenous pressure gradient ≥60 mmHg, which is unsuitable for hemodynamically unstable patients. Further, cannulation of a major artery can result in distal ischemia , although measuring the artery diameter with ultrasound and selecting a cannula that occupies no more than 70% of the lumen reduces this risk . AVCO2R has been successfully used to facilitate LPV in patients with ARDS [41–43], severe asthma  and as a bridge to lung transplantation .
Venovenous carbon dioxide removal
Venovenous carbon dioxide removal (VVCO2R) requires a mechanical pump to propel blood through the circuit and can be broadly divided depending on whether the pump and membrane lung are separate components or incorporated into a single console. When separate components are used, the circuit is set up as described in Figure 1. Table 1 shows some of the different components that can be used. These circuits are more complicated to operate, often need flow rates >1 L.minute-1 and may need multidisciplinary support. The growth of programs in more general settings has provided impetus to simplify ECCOR, resulting in several devices where the pump and membrane lung are combined into one console.
The iLA Activve mounts the Novalung and a diagonal flow pump together in one device. At higher blood flow rates this device can provide venovenous ECMO. Conceptually, this is the simplest method of providing ECCOR via a console, and although it does not provide any special benefits over separate components, the pump is designed to provide reliable flows throughout a large range of flow rates.
Several gas-exchange catheters have been developed but only one, the intravenocaval oxygenator and carbon dioxide removal device (IVOX), has been used clinically. These devices package hollow fiber membrane lungs into a catheter that is small enough to be placed in the vena cava, that is, <15 mm in diameter. Intracorporeal catheters are conceptually attractive because they are exposed to 2 to 3 L.minute-1 of blood flow and therefore CO2 removal is not flow limited.
The IVOX was designed for both oxygenation and CO2 removal. Orienting 'crimped' membrane fibers in a spiral arrangement maximized gas exchange by increasing surface area and creating disturbed blood flow patterns over the membrane . Disturbed blood flow provides convection velocity towards the fiber surfaces, reducing diffusional resistance. The membrane surface of the IVOX ranged from 0.2 to 0.5 m2  and gas flow was applied under negative pressure; an important safety feature in intracorporeal devices since there is no other opportunity to prevent air embolism if the membrane is disrupted.
In animal trials the IVOX consistently removed 40 ml.minute-1 of CO2, but oxygen delivery was less reliable. Clinical experience was mixed; the IVOX facilitated lower ventilator settings in some studies , but made no difference in others [53, 54]. On the whole, gas exchange was too limited and placement associated with high complication rates from bleeding and thrombosis . Commercial development has subsequently ceased.
Future directions and devices in development
Current active trials from clinicaltrials.gov accessed April 2012
Extracorporeal CO2 removal in COPD (DECOPD)
University of Turin, Italy
Pulmonary and Renal Support during Acute Respiratory Distress Syndrome (PARSA)
Neonatal membrane lung (HiLite 800 LT, Medos) within dialysis circuit (Multifiltrate kit 7, CVVH 1000, Fresenius)
Hopital Ambroise Pare, France
Low-flow ECCO2-R and 4 ml/kg Tidal Volume vs. 6 ml/kg Tidal Volume to Enhance Protection From Ventilator Induced Lung Injury in Acute Lung Injury (ELP)
University of Turin, Italy
Not yet recruiting
Gas-exchange catheters in development
Active mixing can also be achieved by rotating the fiber bundle; a strategy used in the dynamic intravascular lung assist device (D-ILAD) . Although the D-ILAD was almost twice as efficient as balloon-pulsating catheters, rotating fibers could damage vessel walls upon contact. Recently, the Hattler catheter has been modified by replacing the balloon with a series of small impellers. It has been successfully used in animals and has CO2 exchange rates similar to the D-ILAD .
Finally, in addition to active mixing, CO2 exchange has been improved by covalent immobilization of carbonic anhydrase to the surface of the hollow fiber membrane . As a result, CO2 is more rapidly generated from bicarbonate, facilitating removal.
In the 1980s, several groups reported the results of animal experiments using dialysis to remove CO2 in the form of bicarbonate. This approach is appealing because CO2 is transported in the form of bicarbonate, which moves freely across dialysis membranes. Conventional hemodialysis uses bicarbonate-containing dialysates to correct the metabolic acidosis accompanying renal failure, but bicarbonate-free dialysates can remove enough CO2 to replace pulmonary ventilation in dog models . Currently, respiratory dialysis is limited by the inability to maintain electrolyte concentrations and pH whilst removing bicarbonate. Several approaches to replace bicarbonate have been attempted using sodium hydroxide, tromethamine (THAM), and organic anions. However, fluid gain, hyperchloremic acidosis, hemolysis, cardiac arrhythmias and acid-base derangements have prevented successful long-term use [64, 65].
Recently, hemofiltration has been used to remove bicarbonate. One group used sodium hydroxide in a post-filter replacement fluid and maintained pH and CO2 within physiological range for 18 hours in hypoventilated sheep. However, hyperchloremic acidosis developed and blood flow rates exceeding 500 ml.minute-1 would be needed to remove sufficient CO2 in humans . Another group removed bicarbonate by using pre-filter replacement fluid containing THAM. Physiologic CO2 levels and pH were maintained for 1.5 hours, but it was not determined whether THAM had the same long-term problems seen in the hemodialysis models . Nonetheless, respiratory dialysis holds much promise if the problems of electrolyte and acid-base disturbances can be solved.
Several modalities of providing ECCOR are now either available or in development. As evidence favoring low-volume, low-pressure ventilation in ARDS accumulates, the argument for applying these ventilation strategies in all critically ill patients will gather momentum. However, successful application is dependent upon a safe, reliable approach for CO2 removal.
Simpler more efficient ECCOR devices requiring lower blood flow rates and smaller access cannulas promise to improve safety and ease of use. Novel designs, such as the Decap, can serve the dual purpose of renal support and ECCOR. However, other solutions currently in development, gas exchange catheters and respiratory dialysis, promise to be minimally invasive, easy to initiate and well tolerated. They may even eliminate the need for intubation in some forms of respiratory failure, where CO2 is the primary problem . Familiarity with devices already available can change our approach to ARDS and prime the ICU for the arrival of devices that may revolutionize our approach to respiratory failure.
acute respiratory distress syndrome
arteriovenous CO2 removal
dynamic intravascular lung assist device
extracorporeal carbon dioxide removal
extracorporeal membrane oxygen
interventional lung assist
lung protective ventilation
venovenous carbon dioxide removal.
MEC acknowledges support from NIH grant HL07820. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Heart, Lung, And Blood Institute or the National Institutes of Health. The authors acknowledge Marquet (Rastatt, Germany) Medos (Medizintechnik AG, Stolberg, Germany), Novalung GmbH (Heilbronn, Germany) and Hemolung (Alung Technologies, Pittsburgh, USA) for their assistance in producing the figures.
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