The Role of Imaging During Extracorporeal Membrane
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1 Barnacle et al. Extracorpor eal Membrane Oxygenation in Pediatric Respiratory Failure Pediatric Imaging Review A C M E D E N T U R I C A L I M A G I N G AJR 2006; 186: X/06/ American Roentgen Ray Society Y O Alex M. Barnacle 1 Liz C. Smith 2 Melanie P. Hiorns 1 F Keywords: catheters, chest, ECMO, neonates, pediatric radiology, respiratory failure DOI: /AJR Received October 27, 2004; accepted after revision June 13, Department of Radiology, Great Ormond Street Hospital for Children, Great Ormond St., London WC1N 3JH, England. Address correspondence to A. M. Barnacle. 2 ECMO Coordinator, Great Ormond Street Hospital for Children, London WC1N 3JH, England. The Role of Imaging During Extracorporeal Membrane Oxygenation in Pediatric Respiratory Failure OBJECTIVE. Extracorporeal membrane oxygenation (ECMO) is increasingly widely used in pediatric respiratory failure. Despite playing a key part in patient management during ECMO, the role of radiology is not widely reported. We discuss the principles of ECMO support and the normal imaging appearances. Radiologic findings arising from the complications of ECMO are highlighted. CONCLUSION. Radiology has a central role in establishing well-designed imaging protocols and vigilant reporting of ECMO apparatus positions and complications. he use of extracorporeal membrane oxygenation (ECMO) as a T means of therapeutic support in infants and children with severe respiratory disease has expanded dramatically over the past two decades. Imaging plays a key role in the management of patients both before and during ECMO support. It is vital that pediatric radiologists in ECMO centers apply well-designed imaging protocols and are vigilant in the reporting of apparatus positions and complications of treatment. The role of radiology in modern ECMO support is not widely reported. Our article discusses the normal radiologic appearances during ECMO. The range of bypass cannula positions is illustrated, and appropriate imaging protocols are discussed. The radiologic findings arising from the complications of ECMO are highlighted. Background ECMO is a modified pulmonary or cardiopulmonary bypass technique used to support patients with severe cardiac or respiratory failure (or both) unresponsive to conventional ventilatory support and medical treatment. The standard indications for the use of ECMO remain neonatal conditions such as meconium aspiration, primary pulmonary hypertension, and congenital diaphragmatic hernia, and it is in the neonatal population that ECMO has been proven effective as a therapeutic intervention [1]. More recently, the indications for ECMO have broadened as techniques and survival rates have improved, with ECMO increasingly used as a temporary bridge to definitive treatment in older children with cardiac disease and in patients with overwhelming sepsis and multiorgan failure [2]. ECMO involves bypass of venous blood to an external membrane oxygenator before reintroduction either to the arterial circulation, providing heart and lung support, or to the venous circulation, providing only lung support. This allows reduction of barotrauma to the lung parenchyma, providing rest and recovery. Standard ECMO circuits use a venous-to-arterial circulation, termed VA ECMO, whereas more recently the advent of double-lumen venous cannulae has encouraged the widespread use of venovenous circuits, termed VV ECMO. Venovenous ECMO systems deliver oxygenated blood to the right side of the heart and therefore do not provide mechanical circulatory support, relying on left ventricular function for delivery of oxygenated blood to the systemic circulation. The circuit is highly dependent on optimal venous drainage to maximize the proportion of the circulating blood volume that can be oxygenated [3]. This method does, however, offer significant advantages over venous-toarterial ECMO: avoiding ligation of the carotid artery, normalizing both preload and afterload on both ventricles, maintaining pulsatile blood flow, and allowing perfusion of well-oxygenated blood to the pulmonary circulation and coronary arteries [3]. Some evidence suggests that there is an increased risk of neurologic complications with venous-to- 58 AJR:186, January 2006
2 Extracorporeal Membrane Oxygenation in Pediatric Respiratory Failure arterial ECMO compared with venovenous ECMO [2, 4 6], whereas other studies have failed to confirm such findings [7]. Some practitioners recommend the use of a cephalad venous catheter to improve venous outflow from the cerebral vasculature [8]. Selection criteria for consideration of ECMO may vary among institutions. The presence of potentially reversible cardiac or respiratory failure is central in determining those who will benefit from ECMO support. Parameters, such as the oxygenation index (OI), serve to provide evidence of severe respiratory failure despite maximal medical management. The OI is a calculated index of respiratory function using the values of inspired oxygen (FIO 2 [%]) and arterial oxygen (PaO 2 [mm Hg]) concentrations and mean airway pressure (MAP [cm H 2 O]) to estimate oxygen exchange and is expressed by the following formula: OI = FIO 2 MAP / PaO 2. Patient selection is based on patient weight and gestational age, underlying diagnosis, and absence of complications such as significant intracranial hemorrhage because heparinization of the ECMO circuit will only extend any preexisting intracranial bleed. Strict imaging protocols play an important role in identifying those patients with adverse intracranial features before commencement of ECMO. Pretreatment cranial sonograms are obtained in all infants with an open fontanelle. All centers exclude potential ECMO candidates with evidence of intracranial hemorrhage greater than grade 1. Attempts have been made to predict the risk of adverse neurologic events on the basis of pre-ecmo cranial sonography; it appears that infants with severe cerebral edema or periventricular leukomalacia before ECMO are at greater risk of subsequent major intracranial complications [9]. During the period of ECMO therapy itself, imaging has a limited role. Radiologic investigations serve to identify and monitor complications, a proportion of which may be clinically unsuspected [10], and imaging findings may be contributory in the decision to withdraw treatment after a prolonged course of ECMO. Recovery, however, is best assessed clinically by improvements in lung compliance and gas exchange. Levels of support are likely to be adjusted after trial weaning of ECMO therapy rather than after radiographic progress. Improvements in the appearance of the chest radiograph are often not expected until late in the course of ECMO therapy and may lag behind clinical recovery. ECMO Cannulae: Type and Position There is a wide range of pediatric ECMO cannulae in use, each with a different radiographic appearance. Familiarity of the radiologist with the type of cannulae used in each institution is essential. Both arterial and venous cannulae are usually inserted via a surgical cutdown technique, during which the cannula is sutured both to the vessel wall and to the skin, and the vessel is tied off. After removal of the cannula, reconstruction of the vessel may be attempted, depending on the method of insertion and the duration of therapy. A percutaneous insertion method without imaging guidance has been described for venous cannulae, as has an openassisted technique [11, 12]. This modified Seldinger technique obviates ligation of the jugular vein and allows flow of blood past the cannula, reducing potential impairment of cerebral venous drainage. Such a technique aims to avoid risks to the structures of the neck inherent in the non-imaging-guided percutaneous procedure. Desaturated blood is optimally drained from the right atrium through a venous cannula placed via the right internal jugular vein. The venous cannula has both end and side holes to enhance drainage. The cannula tip should lie approximately at the level of the eighth ninth ribs posteriorly (the expected level of the right atrium), thus ensuring that both tip and side holes lie within the atrium. A number of venous cannulae have a radiolucent distal segment, and the tip may therefore lie more distally than suspected on radiographic imaging; the reporting radiologist should be familiar with the cannula type in use. Some types have a radiopaque tip beyond the radiolucent segment (Fig. 1). This tip can be difficult to visualize; a conservatively collimated radiograph may fail to show the tip of a malpositioned line within the inferior vena cava. In neonates with small-caliber vessels, a venous cannula that is placed too distally will result in both obstruction to peripheral venous return and blockage of cannula side holes, leading to inadequate drainage. If the cannula tip is placed too proximally, there is a risk of the cannula side holes lying outside the vessel lumen or of dislodgement of the cannula itself, causing life-threatening air emboli and potential hemorrhage. Alternative venous cannulation sites include the left internal jugular vein and the femoral veins. In large children, a second venous cannula is required to allow adequate exchange of the patient s circulating volume. In such cases, two venous cannulae are placed simultaneously, usually within the jugular and femoral veins. The line tips must be placed a sufficient distance from each other to reduce recirculation of oxygenated blood (Fig. 2). Arterial cannulae are usually inserted via the right common carotid artery with the tip lying within the innominate artery. The tip of the cannula has a single end hole and is typically radiopaque; it should lie at the origin of the common carotid artery to maximize delivery of oxygenated blood to the aortic circulation without causing obstruction to flow within the aortic lumen. In cases in which dense lung parenchymal opacification obscures the cardiovascular landmarks, the cannula tip should therefore lie at the level of the second third ribs posteriorly because this position correlates with the origin of the common carotid artery. The exact position of the cannula tip is difficult to determine on chest radiographs and is confirmed by echocardiography after placement. Failure to adequately advance the arterial catheter within the carotid artery increases the risk of inadvertent dislodgement (Fig. 3). Equally, cannulae that are placed too far into the vessel may obstruct aortic flow and increase afterload on the left ventricle. Note that, as with various venous catheters, some types of arterial cannulae also have a distal radiolucent segment with a radiopaque tip to confirm the distal position of the cannula (Fig. 4). Venovenous ECMO, via a single cannula with a double lumen, is increasingly popular, with 12- to 18-French cannulae now available allowing support in patients with a body weight of up to 15 kg. The small-caliber lumens possible within a single catheter limit the volume of venous exchange possible; therefore, use of double-lumen venovenous ECMO is restricted by the size of the patient. The tip of the venovenous cannula should lie within the right atrium with the smaller arterial lumen directed toward the tricuspid valve to maximize delivery of oxygenated blood during systole; orientation of the catheter can be determined on chest radiography or echocardiography (Fig. 5). Suturing the cannula within the vessel and patient positioning can cause inadvertent kinking or narrowing of the catheter, leading to suboptimal circuit drainage (Fig. 6). This is particularly common in soft-walled venovenous cannulae, many of AJR:186, January
3 Barnacle et al. Fig. 1 Chest radiograph of 2-day-old male shows venous cannula with radiopaque tip (arrow) just below level of ninth rib, within right atrium. Fig. 3 Chest radiograph of 29-month-old female illustrates incorrect placement of arterial cannula (arrow), which is too high and resulted in inadvertent displacement of cannula with subsequent life-threatening hemorrhage. Fig. 2 Chest radiograph of 23-month-old male shows optimal positioning of two venous cannulae and also shows expected lung white out present during extracorporeal membrane oxygenation. Fig. 4 Chest radiograph of 1-month-old male shows arterial cannula has distal radiolucent segment. Tip of cannula is gauged by position of radiopaque tip (arrow), which lies approximately at level of aortic arch. Echocardiography (not shown) would confirm position of cannula. There is also kink in upper venous catheter. which are made of a material with inherent memory so that kinked cannulae cannot be salvaged and may have to be replaced. Normal Radiographic Appearances During Therapy Generalized lung opacification typically occurs when patients in respiratory failure are commenced on ECMO. This phenomenon does not correlate with severity of lung dis- 60 AJR:186, January 2006
4 Extracorporeal Membrane Oxygenation in Pediatric Respiratory Failure Fig. 5 Chest radiograph of 20-month-old female illustrates optimal position of cannula for venovenous extracorporeal membrane oxygenation. Fig. 7 Sonographic images of 2-day-old female. A, Cranial image shows intraparenchymal hemorrhage within right frontal lobe (between calipers). B, Coronal image shows large left-sided extraaxial hemorrhage (arrows). A Fig. 6 Chest radiograph of 3-week-old male reveals kinking of venovenous cannula (arrow) within soft tissues of neck. B ease, but is likely to reflect changes in pulmonary hemodynamics and physiology and the abrupt decrease in airway pressure [13 15]. Dense opacification of the lung parenchyma hinders the assessment of the position of support apparatus, with loss of normal mediastinal landmarks; hence, bone landmarks (rib and vertebral body levels) become more important. Particular care should be taken to correctly analyze the positions of ECMO cannulae and other catheters, recognizing that poor patient positioning and differing radiographic AJR:186, January
5 Barnacle et al. Fig. 8 Coronal cranial sonographic image of 6-week-old female illustrates typical widening of CSF spaces around both frontal lobes (arrows). projections can significantly alter projected line tip positions. The patient is usually ventilated via an endotracheal tube on minimal airway pressures, in air, with a rate of approximately 10 breaths per minute. Alternatively, continuous positive airway pressure techniques may be used in patients with significant air leaks or multiple chest drains in situ. Regular chest physiotherapy and progressive tissue healing lead to a gradual improvement in lung aeration over time, monitored via serial chest radiographs. Currently, CT is rarely used in the evaluation of the chest during treatment. Imaging of the lung parenchyma during the first 7 14 days of ECMO support is of limited value, given that a period of normal lung recovery must be allowed before treatment withdrawal can be Fig. 9 Sagittal sonographic image of 4-week-old male shows echogenic hemorrhagic focus within posterior fossa (arrows). Fig. 10 Cranial sonographic image of 4-day-old male obtained using highfrequency linear probe shows right-sided echogenic subdural hemorrhage abutting falx (arrow). Extraaxial space (between calipers) on left side remains typically widened. considered. Recent work suggests that crosssectional imaging may have a role in complex cases, particularly in patients with an unexplained delay in clinical improvement [16, 17]. Such imaging requires transportation of the patient to the radiology department, thereby increasing the risk of complications such as cannula dislodgement. Contrast medium must be administered via the arterial side of the circuit, 62 AJR:186, January 2006
6 Extracorporeal Membrane Oxygenation in Pediatric Respiratory Failure Fig. 11 Chest radiographs of two infants with pneumothorax. A, 5-week-old male. Image shows spontaneous right-sided tension pneumothorax that occurred during treatment. B, 12-month-old female. Image shows mediastinal free air and left-sided pneumothorax, with thymus gland (arrows) outlined by mediastinal air. distal to the membrane oxygenator, or directly into the arterial circulation to prevent dilution of contrast medium in the ECMO system [16]. Abdominal radiographs may be requested to show the position of femoral cannulae. Radiographs show relatively little air within the abdomen during ECMO. This is a normal finding during treatment due in part to sedation of the A patient with reduced or absent air swallowing. If available, abdominal radiographs should be closely evaluated for the presence of necrotizing enterocolitis during support of preterm infants. The Role of Sonography Sonography is often the most useful imaging investigation of both the chest and the Fig. 12 Chest sonographic image of 5-day-old female shows small pleural effusion (short arrow) with associated consolidation of right lower lobe (long arrow). abdomen once lung parenchymal opacification has occurred and the volume of bowel gas within the abdomen becomes limited. Sonography is readily available within the intensive care setting, allowing minimal disturbance of the patient or support apparatus. Fluid collections are well depicted, and there may be clues as to the complexity of B AJR:186, January
7 Barnacle et al. the collection: The sonographic appearances may include fluid collections that are anechoic, septated, hyperechoic, mixed, or complex. Some studies have shown that collections that are anechoic or only have a few simple septa are less likely to be infected, and therefore just represent transudates, than those that show increased echogenicity or a complex pattern of septations [18], which may indicate infection. Other series have shown that neither sonography nor CT can reliably identify the stage of pleural infection [19] and that therefore sonography findings need to be interpreted in their clinical context. Acute hemothorax is usually identified by a fluid collection of homogeneous hyperechogenicity, subsequently showing fluid fluid levels as the blood products separate. Sonography provides a useful tool for intracranial imaging in infants during treatment and for documenting complications (Fig. 7). Widening of the interhemispheric fissure during ECMO is recognized in up to 59% of cases [17, 20 22] (Fig. 8). Typically, the finding resolves once ECMO is discontinued [20]. Some authors believe this to be an intracranial manifestation of generalized edema [20]. Other authors suggest that raised sagittal sinus pressures associated with internal jugular vein ligation may contribute to the appearance [17, 23]. A Fig. 13 Chest radiographs of two infants. A, 5-month-old male. Image illustrates displacement of mediastinal soft tissues and support apparatus to right with intercostal drain decompressing left-sided hemothorax. B, 7-month-old male. Image shows displacement of mediastinum to left secondary to collapse of left lung. Complications of Treatment Complications of ECMO are divided into mechanical and patient factors. Given that ECMO is generally used as a rescue therapy in critically ill infants and children, complication rates during treatment can be significant. Typically, patients are severely hypoxemic, hypotensive, and acidotic before commencement of ECMO and thus are already at particular risk of cerebrovascular injury. Successful use of ECMO requires adequate anticoagulation to prevent thrombus formation in the extracorporeal circuits, but systemic heparinization places patients at significant risk of hemorrhagic complications involving a range of organ systems. Furthermore, platelets are continuously consumed during ECMO, with implications for coagulation. Platelet transfusions are administered regularly to maintain an adequate platelet count. Acute changes in hemodynamics during cannulation and in fluid balance during therapy contribute to the risk of hemorrhage and fluid collections. Several novel therapies have been used to minimize the risk of bleeding complications. In North America, for instance, the use of an antifibrinolytic drug, aminocaproic acid, in patients undergoing surgery before or while on ECMO appears to significantly reduce the risk of surgical site bleeding [24], although there is no proven benefit on intracranial hemorrhage rates. CNS Complications Systemic anticoagulation makes intracranial hemorrhage the primary risk of ECMO. Some authors have suggested CNS injury may be compounded by ligation of the internal jugular vein and common carotid artery. Series suggest an incidence of intracranial hemorrhage of approximately 14% during ECMO [25, 26]. Both intracranial hemorrhage and ischemic injury can be detected and monitored in infants by cranial sonography. Particular attention should be paid to the posterior fossa, where sonography views may be limited; and the echogenic tentorium, vermis, and subarachnoid spaces may mask acute hemorrhage [27] (Fig. 9). Care must be taken to examine the extraaxial spaces at the periphery of the field of view where large extraaxial collections may be missed. This includes the routine use of a high-resolution linear probe to examine the near field (Fig. 10). Although sonography remains a cornerstone in the monitoring of the CNS during treatment, CT studies may provide additional information in up to 73% of cases [17]. Generalized edema, acute hypoxic ischemic injury, and small hemorrhages may not be visible sonographically. In addition, cranial sonography may not be possible in older patients because of closure of the fontanelle. In the neonatal population, however, sonography remains highly sensitive for the detection of ma- B 64 AJR:186, January 2006
8 Extracorporeal Membrane Oxygenation in Pediatric Respiratory Failure jor intracranial hemorrhage, an event that can affect the acute management of the patient. Thoracic Complications Thoracic complications of ECMO are relatively common [27] and include migration of support apparatus, air collections, pleural effusions, and hemorrhage. A proportion of complications may be unsuspected, and the clinical significance of these sequelae varies widely. Chest sonography is often a useful adjunct to portable radiography in such cases. Migration of cannulae and chest drains can occur in small infants as increasing soft-tissue edema displaces catheters that are sutured to the skin. Intrathoracic air leaks can complicate management and are common due to the underlying lung disease present in a large proportion of patients. Such sequelae may be clinically apparent and are readily detected on chest radiography (Fig. 11). Large air collections can dramatically compromise venous drainage and need to be addressed urgently. Hemorrhage into the pleural and mediastinal spaces is well recognized. Sonography aids in the evaluation of pleural collections (Fig. 12) and may show hemorrhage, which appears echogenic and complex [27, 28]. Although the lungs remain opacified, significant mediastinal shift due to pleural collections or lung collapse can be detected only by the displacement of the support lines and tubing [29] (Fig. 13). Occasionally, CT may play a role in the detection of thoracic abnormalities such as pleural and pericardial collections, mediastinal hemorrhage, lung abscess, and bronchopleural fistulas [16]. It is important to stress, however, that complications detected during routine examinations in stable patients may not require treatment until ECMO support has been weaned; insertion of catheters or drains for air leaks or collections may cause unnecessary and life-threatening hemorrhage. Other Complications Other less-well-recognized complications during ECMO include adrenal gland hemorrhage [16, 30]; hepatic infarction [16]; intraperitoneal hemorrhage; and, occasionally, retinal hemorrhage [31]. Rapid splenic enlargement has been documented in a series of infants after commencement of ECMO therapy [32]. The authors of that study propose that splenomegaly may have been secondary to hemolysis and platelet aggregation during ECMO support. In two cases, splenomegaly impeded repair of a congenital diaphragmatic hernia. Periosteal reactions of the ribs have been reported and are thought to be secondary to subperiosteal edema during therapy [33]. Imaging Protocols ECMO imaging protocols vary among centers. The importance of regular surveillance for cannula migration and hemorrhagic complications cannot be overstated but must be balanced by a regard for minimizing radiation dose. It may be reassuring to remember that cannula position is routinely assessed during regular echocardiography examinations performed while a patient is on ECMO support. The current imaging protocol at our institution involves a cranial sonography examination before commencement of ECMO as a baseline study and to exclude a preexisting intracranial condition and again within 24 hr of cannula insertion because of potentially significant changes in hemodynamics and blood clotting after anticoagulation. Repeat cranial sonography examinations are then performed at weekly intervals or in the event of clinical deterioration. This protocol was established after an extensive review of our practice that had shown a very low yield of significant new intracranial findings after the first 24-hr period. However, different centers have different protocols and there is no consensus in the literature; some centers perform cranial sonography on a daily basis for the duration of the admission. Similarly, chest radiographs are obtained immediately before and after commencement of ECMO and thereafter at 2- to 3-day intervals while the patient remains stable because improvement in lung aeration is best assessed clinically. The advent of anticipated pathways of recovery has led to a further reduction in the number of examinations requested. Conclusions ECMO is a highly invasive treatment commonly used as a rescue therapy in critically ill patients; complications are varied and frequent. The radiologist must be able to recognize the normal radiographic appearances of ECMO support and should be vigilant in the detection of complications. Given the extensive range of cannulae currently available and the lack of information provided by manufacturers regarding the radiographic appearances of each catheter, close liaison with the clinical team is essential in sharing information and allowing accurate assessment of catheter type and position. Appropriate imaging protocols should be implemented to ensure maximal efficiency and safety during therapy and, given the rapid expansion in this field of life support, should be reassessed as practice evolves in individual centers. References 1. [No authors listed]. UK collaborative randomised trial of neonatal extracorporeal membrane oxygenation. UK Collaborative ECMO Trial Group. Lancet 1996; 348: Langham MR, Kays DW, Beierle EA, Chen MK, Stringfellow K, Talbert JL. Expanded application of extracorporeal membrane oxygenation in a pediatric surgery population. Ann Surg 2003; 237: Kugelman A, Gangitano E, Pincros J, Tantivit P, Taschuk R, Durand M. Venovenous versus venoarterial extracorporeal membrane oxygenation in congenital diaphragmatic hernia. J Pediatr Surg 2003; 38: Dimmitt RA, Moss RL, Rhine WD, et al. 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