Journal of Radiology Nursing 35 (2016) 261E274

Journal of Radiology Nursing 35 (2016) 261e274

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Journal of Radiology Nursing

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Carbon Dioxide Digital Subtraction Angiography: Everything You Need to Know and More

Lorena Garza, MD a, *, Christian Fauria, MD, MSW, MPH b, James G. Caridi, MD, FSIR c a Department of Radiology, Tulane University Medical Center, New Orleans, LA b Tulane University Medical Center, New Orleans, LA c Tulane University Medical Center, New Orleans, LA

abstract

Keywords: In 1971, during a routine celiac axis injection, 70 cc of room air was inadvertently injected into a patient Carbon dioxide instead of iodinated contrast. Fortunately, there were no ill effects, and despite the use of cut ﬁlm at the Contrast allergy time, Dr. Hawkins visualized the celiac axis and its branches as a negative image. Because of this incident, Nephrotoxicity in combination with his previous knowledge of carbon dioxide (CO2) in venous imaging, he began to study the intra-arterial use of CO2 in animals. After the safe and successful use in animals, he applied the same principles to humans. As technology continued to improve, CO2 evolved into a viable vascular imaging agent. Although used initially for renal failure and iodinated contrast allergy, the many unique properties of CO2 yielded multiple advantages, which are now used in a multitude of scenarios alone or in combination with traditional contrast. Despite somewhat awkward delivery devices in the past, it has now been used with great success in both adults and children for more than 3 decades with only limited reportable complications. Its safe use in children has been described, and when performed in this age group, the same principles apply as for adults. This article describes the history and technique of CO2 angiography for vascular procedures. Copyright © 2016 by the Association for Radiologic & Imaging Nursing.

History 1977; Paul, Durant, Oppenheimer, & Stauffer, 1957; Phillips, Burch, & Hellinger, 1961; Scatliff, Kummer, & Janzen, 1959). It was not long after the discovery of X-rays by Conrad Roentgen Bendib et al. (1977) performed 1,600 cases without complications, in 1895 that gas was ﬁrst used as an imaging agent. In 1914, room using a peripheral injection of 100 to 200 cc of CO2 to evaluate for air was used with radiographs in an attempt to visualize intra- pericardial effusion (Figure 1). In addition, in 1969, Hipona, Ferris, abdominal contents (Rotenberg, 1914). Less than a decade later, and Pick (1969) reported the safe use of CO2 for the evaluation of room air, oxygen, and carbon dioxide (CO2) were insufﬂated in the the inferior vena cava (IVC). retroperitoneum to evaluate for masses (Carelli & Sorddelli, 1921; Subsequently, the biggest advancement in the use of CO2 as a Rosenstein, 1921). Because of the problem of air emboli, room air contrast agent was the fortuitous epiphany by Hawkins (Figure 2). and oxygen, less soluble than CO2, were eventually replaced with After numerous safety studies in animals, he applied these princi- CO2. ples to adults and children (Caridi et al., 2003; Hawkins & Caridi, In the 1950s and 1960s, CO2 was used as a venous contrast agent 1998; Kriss, Cottrill, & Gurley, 1997). As technology continued to to evaluate for pericardial effusion (Bendib, Tourni, & Boudjella, improve, CO2 evolved into a viable vascular imaging agent. Although used initially for renal failure and iodinated contrast allergy, the many unique properties of CO2 yielded multiple advan- * Corresponding author: Lorena Garza, Department of Radiology, Tulane Univer- tages, which are now used in a multitude of scenarios alone or in sity Medical Center, 430 South Pierce Street, New Orleans, LA 70119. combination with traditional contrast. E-mail address: [email protected] (L. Garza).

This activity has been submitted to Alabama State Nurses Association for approval to award contact hours. Alabama State Nurses Association is accredited as an approver of continuing nursing education by the American Nurses Credentialing Center’s Commission on Accreditation. http://dx.doi.org/10.1016/j.jradnu.2016.09.004 1546-0843/$36.00/Copyright © 2016 by the Association for Radiologic & Imaging Nursing. 262 L. Garza et al. / Journal of Radiology Nursing 35 (2016) 261e274

Table 1

Physical properties of CO2 and physiologically related gases

Properties CO2 O2 N2 Molecular weight 42 32 28 Solubility 0.87 0.03 0.016

CO2 ¼ Carbon dioxide; O2 ¼ oxygen; N2 ¼ nitrogen.

blood displaced by the CO2 (Figure 3). Typically, smaller vessels, especially those 10 mm or smaller, demonstrate a better correlation with iodinated contrast (Figure 4)(Ehrman, Taber, Gaylord, Brown, & Hage, 1994; McLennan et al., 2001; Moresco et al., 2000). Buoyancy must also be considered when using CO2. Typically, a gas will rise to the nondependent surface of the vessel. If all the blood is not displaced from the vessel, it will readily demonstrate the anterior structures but potentially generate a spuriously smaller image of the larger feeding vessel. It is imperative to displace as much blood as possible to generate a comparable image. In addition to its buoyancy, when CO2 is administered into the vessel via a catheter, it has the potential to fragment into random bubbles depending on how it is delivered. In an attempt to avoid this, thecathetershouldbepurgedbeforedefinitive delivery, and a continuous and controlled delivery of the volume of choice should be Figure 1. Left lateral decubitus chest X-ray after the administration of intravenous given. Dr. Cho studied the best catheter to administer a uniform and carbon dioxide for pericardial evaluation. organized bolus of gas to minimalize the bubbling effect. He found that an end-hole catheter yielded the best results (Figure 5)(Cho, Properties 2007). Again with respect to buoyancy, there is one instance in which it fi To use CO2 appropriately, a basic knowledge of its properties is can be a signi cant detriment. When a blood gas interface is not essential. CO2 is a nontoxic, nonflammable, buoyant, and present in an anterior structure such as an abdominal aortic compressible gas that has low viscosity and is produced endoge- aneurysm, the CO2 may sit without dissolving and trap in that po- nously at approximately 200 to 250 cc per min. It is a natural sition (Figure 6). Trapping could potentially lead to ischemia byproduct, and there are approximately 120 L of CO2 stored in the manifested by pain. The reported incidence of this occurrence is soft tissues at one time (Roussos & Koutsoukou, 2003). negligible. Because CO2 is present endogenously, there is no concern for The incidence of gas trapping most commonly arises if a typical allergy or renal toxicity (Hawkins, 1982; Hawkins & Caridi, 1998). Its large tank (usually 3 million cc) of CO2 under pressure is mis- viscosity is 1/400 that of iodinated contrast, and therefore, it is less connected to the delivery catheter allowing unfettered flow of gas occlusive than other gases (Table 1). When administered intravas- into the vessel. It is best to wait at least 30 to 60 s between in- cularly, it tends to dissolve within a vessel in 30 s. If CO2 persists in a jections to allow for CO2 to be dissolved. vessel for more than this, it is either trapped or there is room air As with any interventional procedure, patients undergo routine contamination. procedural monitoring. As a safety measure, Cho (2007) recom- fi As opposed to traditional liquid agents, CO2 does not mix with mends monitoring blood pressure 1, 2, and 3 min after the rst CO2 blood. To render a representative image, it must displace the blood injection. in the vessel. As a result, the vessel is less dense, and a negative Asides buoyancy, another important divergent property of CO2 image is obtained with digital subtraction angiography (DSA). The when compared with liquid agents is its compressibility. Because quality and accuracy of the image will depend on the amount of CO2 is a gas it is extremely compressible under pressure. A 20 cc syringe can hold a volume of 200 cc if compressed sufficiently. Therefore, the delivery system should be purged to atmospheric pressure to eliminate the compression and avoid administering a larger dose than the amount indicated on the syringe. In addition, we have found that when a compressed dose is delivered, it can be explosive causing pain and degrade acquired images. Compression can also cause CO2 to reflux into inappro- priate vessels, potentially resulting in complication. This is especially true of the cerebral vessels in which CO2 should be avoided. Finally, to completely avoid explosive delivery, the delivery catheter should be purged of saline or blood before the definitive dose and not be under pressure. Whatever system is being used should be purged to the atmosphere for equilibrium. After this, the delivery syringe plunger should be gently advanced to purge the diagnostic catheter of saline or blood. Subsequently, the CO2 can be delivered in a controlled and nonexplosive manner. Note that unlike a liquid contrast syringe, in which a smaller syringe generates more pressure, a larger syringe Figure 2. The arrow points to negative image from room air in the celiac circulation. (usually 20 to 35 cc) should be used with CO2. If not, the gas may L. Garza et al. / Journal of Radiology Nursing 35 (2016) 261e274 263

Figure 3. Comparison of carbon dioxide and contrast, respectively. Less than 10 mm vessels yield comparable images. This is a good quality CO2 image given adequate amounts of blood were displaced. simply compress in the syringe without delivery, especially if the solubility of CO2 allows for intravascular use, but the coronary, thoracic catheter is not purged. aortic, and cerebral vessels are less forgiving, and delivery into these Invisibility is the most significant property of CO2 and the one vessels should be avoided. In addition, because of the tendency of CO2 that causes the most concern and discourages competent operators to reflux, it is prudent to avoid intra-arterial injections above the dia- from using it. Because it is invisible, contamination with more phragm. To reduce the possibility of central cerebral reflux, the patient occlusive room air is a major concern of many operators. Knowl- can be placed in the Trendelenburg position. edge of the sources of contamination and how to avoid them is Other clinical scenarios that predispose a patient to untoward imperative but relatively simple. It is essential, therefore, embolization include right-to-left shunts and the combination of that disposable sources of at least medical grade CO2 be used pulmonary arterial hypertension and a patent foramen ovale. An (Table 2). additional rare contraindication is the use of nitrous oxide general Contamination may also result when a syringe of CO2 is left open anesthesia when using intravenous CO2. to room air. This can be avoided with the use of a closed delivery A recurrent concern for novice operators is the use of CO2 in system that is not open to room air. Delivery systems, especially patients with chronic obstructive pulmonary disorder (COPD). As a those that use a bag reservoir, should be purged three times to rid precautionary measure in COPD patients, it is suggested to allow the system of residual room air. Finally, delivery system connections more time between injections. Instead of the recommended 30 to should be secured, either with glue or luer lock. Loose connections 60 s between injections in most routine patients, those with COPD can lead to the aspiration of room air. Some individuals also hy- should be increased to 2 min to allow for definitive dissolution. pothesize that stopcocks are not impervious to gas introduction It is important to remember the potential increase in radiation with aspiration. Therefore, stopcocks and aspiration should be kept exposure to the operator and the patient when using CO2 DSA. It is to a minimum. recommended that the frame rate for acquiring CO2 images approximate 6/s or more. Contraindications, caveats, and disadvantages In addition to the aforementioned contraindications, there are a few minor disadvantages that exist when changing from a fluid- When using gas as an imaging agent, the biggest concern is the based vascular contrast to CO2. The primary disadvantage is possibility of embolic occlusion and secondary ischemia. The rapid learning how to use a gas-based delivery system as opposed to

Figure 4. Anterior vessels are well demonstrated by carbon dioxide digital subtraction angiography. (A) Superior mesenteric artery celiac, (B) reimplanted renal arteries, and (C) transplant renal arteries. 264 L. Garza et al. / Journal of Radiology Nursing 35 (2016) 261e274

Figure 5. End hole vs multiside hole catheters. CO2 delivery via end hole catheters (column A) demonstrates a more uniform column of CO2 than those catheters with multiple side holes (columns B and C).

iodinated contrast. CO2 is invisible, colorless, odorless, and cannot be 0.02% to 0.04% (Caro, Trindade, & McGregor, 1991; Lieberman & seen or felt; therefore, the comfort level for use is much less than Seigle, 1999; Trcka et al., 2008). iodinated contrast. The operator must learn and feel confident in the type of delivery system. In addition, CO2 vascular imaging is typically Non-nephrotoxic Quality of CO2 not as dense, and patient motion can seriously affect the final product. Undoubtedly, the best advantage of CO2 DSA is its lack of nephrotoxicity (Beese, Bees, & Belli, 2000; Caridi, Stavropolous, Hawkins, 1999; Hawkins & Caridi, 1998; Hawkins, Cho, & Advantages Caridi, 2009; Hawkins et al., 1992; Hawkins, Wilcox, Kerns, & Sabatelli, 1994; Thomson et al., 1996). Contrast-induced ne- Nonallergic Quality of CO2 phropathy (CIN) is the third leading cause of hospital-acquired renal failure behind decreased renal perfusion and nephrotoxic Because CO2 is disseminated throughout the body's soft tissues, medications (Nash, Hafeez, & Hou, 2002). The incidence of it is nonallergenic. This advantage is extremely beneficial when an hospital-acquired CIN approximates 7% (Bartholomew, Harjai, & operator is confronted with an emergent intravascular procedure in Dukkipati, 2004). a patient with a severe allergy to iodinated contrast. Currently, most Early animal studies by Hawkins (1982) and others showed operators use low osmolar nonionic contrast, which has an inci- that CO2 as an intravascular contrast agent did not affect the dence of allergic reaction of 0.7% to 3% and severe anaphylaxis of renal function. Hawkins later went on to demonstrate this in

Figure 6. (A) Cross table lateral showing carbon dioxide (CO2) pooling anteriorly in abdominal aortic aneurysm (AAA). (B) Delayed image demonstrating persistent CO2 anteriorly in an AAA. L. Garza et al. / Journal of Radiology Nursing 35 (2016) 261e274 265

Table 2 Indications: alone or as an adjunct to iodinated contrast Grades of CO2 allergy Type Purity (%)

Research grade 99.999 Iodinated contrast allergy is explained previously. Emergent SFC grade 99.998 patients or those who for a variety of reasons did not receive Instrument grade 99.99 prednisone preparation can use CO2 DSA if necessary. Coleman grade 99.99 Anerobic grade 99.9 Medical grade 99.5 Contrast-induced Nephropathy Standard grade 99.5 There are many clinical scenarios that predispose a patient to CO2 ¼ Carbon dioxide; SFC ¼ Supercritical Fluid Chromatography. CIN. These include myeloma, diabetes, acute cardiac abnormalities, humans as well. Comparing iodinated contrast, gadolinium, and hypotension, nephrotoxic drugs, and underlying renal disease. In these patients, the incidence of CIN is increased but can be lessened CO2 in renal-insufficient patients, CO2 was the only agent not demonstrating an elevation in creatinine (Spinosa et al., 1998, with the use of CO2 DSA. Most commonly, the incidence of CIN is 2000). It should be the first-line imaging agent in patients related to the volume of iodinated contrast, the route of adminis- with renal insufficiency requiring vascular evaluation or inter- tration (intra-arterial carries higher risk than intravenous), and pre- existing renal insufficiency (Kooiman et al., 2012; Moresco et al., vention. Even if there are limitations to the CO2 imaging, it can be used in conjunction with limited diluted doses of iodinated 1998; Murakami et al., 2012; Seeger, Self, Harward, Flynn, & contrast. Hawkins, 1993). When performing procedures requiring significant volumes of contrast, CO2 can be used alone or as an adjunct to decrease this Low Viscosity possibility. It should be the preferred contrast in evaluation and intervention of the renal artery in renal transplants and renal The viscosity of CO2 is 1/400 that of iodinated contrast, arterial reimplantation cases (See Figure 11). permitting its delivery through smaller and less invasive catheters and needles. This is advantageous when using microcatheters in Hemorrhage which sufficient volumes of thicker contrast may be difficult to fi deliver. CO2 can easily be administered in signi cant doses and has CO is extremely beneficial in the demonstration of acute arte- fl fi 2 the advantage of central re ux resulting in opaci cation of the rial and venous hemorrhage (Figures 10 and 12) and is 2.5 times entire vascular structure (Figure 7). more sensitive than the thicker contrast (Hashimoto, Hashimoto, & fi Likewise, CO2 can be injected through (ultra ne) needles as Soto, 1997; Hawkins, Caridi, LeVeen, Klioze, & Mladinich, 2000; small as 27 gauge. These needles are much less invasive and have Hawkins, Caridi, Wiechman, & Kerns, 1997; Krajina et al., 2004; been used successfully with CO2 in the liver and spleen as well as Sandhu, Buckenham, & Belli, 1999). Regardless of the etiology, peripheral venography (Figure 8). whether iatrogenic, traumatic, or gastrointestinal bleed, delin- Because of its low viscosity, CO2 can be injected through a eating the origin of bleeding and treating it precipitously can lead to catheter with the wire in place using a Y-adapter (Figure 9). This is significantly less morbidity and mortality. Hawkins reported that advantageous when performing invasive procedures and at times the use of CO2 DSA has approximately 2.5 times the sensitivity for when it is preferable to maintain wire access. defining the acute hemorrhage when compared with iodinated contrast (Hawkins et al., 1997). Other Peripheral Arterial Occlusive Disease Finally, one of the biggest advantages of CO2 is its cost. The typical cost for CO2 is 3 cents per 100 cc, which is exponentially The incidence of peripheral arterial occlusive disease (PAD), cheaper than iodinated contrast. chronic limb ischemia, and endovascular repair is increasing. CO2

Figure 7. (A and B). The low viscosity of carbon dioxide permits delivery between wire and balloon to allow assessment of stenosis and position. (C) Follow-up imaging does not require removal of the guidewire. 266 L. Garza et al. / Journal of Radiology Nursing 35 (2016) 261e274

Figure 8. (A) Large patient with poor opaciﬁcation of central structures using iodinated contrast. (B) Carbon dioxide that can be delivered via 25-gauge peripheral needle, does not mix with blood, and readily demonstrates central structures.

DSA is vital and extremely useful in this clinical scenario, but it is renal failure that is permanent and cumulative (Chao et al., 2007; currently underused. Successful correlation of CO2 and iodinated Criado, Kabbani, & Cho, 2008; Gahlen et al., 2001; Walsh, Tang, & contrast in PAD was demonstrated by Seeger's group in the mid Boyle, 2008). The typical EVAR patient is usually older than 1990s (Seeger et al., 1993). They demonstrated a 92% correlation 70 years. This group of individuals has approximately a 30% inci- with an increase to 100% when a small amount of iodinated contrast dence of abnormally low glomerular filtration rate that may not be was administered (Figure 13). reflected by serum creatinine levels alone. They also tend to have A large number of patients with PAD/chronic limb ischemia comorbid conditions that predispose them to renal insult. The inci- commonly have concomitant renal artery disease and other pre- dence of renal insufficiency in patients undergoing EVAR approxi- disposition to renal insufficiency. Considering these facts and the mates 7% to 25% with acute renal failure occurring in 2% to 16%, susceptibility of this group to CIN, it would seem intuitive to use resulting in an associated mortality of 30% to 50%. CO2 can be used as CO2 as a contrast agent whenever possible. the exclusive contrast agent or in addition to smaller volumes of iodinated contrast, allowing accurate and complete endovascular Endovascular Abdominal Aneurysm Repair repair without inducing renal compromise. In addition, because of its low viscosity, it has also been noted by several of the aforementioned authors that CO is more sensitive for detecting endoleaks. One current use of CO2 DSA has been in the placement and 2 evaluation of abdominal aortic endografts. This use has been proliferating among numerous operators for a variety of reasons, including decrease of iodinated contrast load, more sensitive eval- Interventional oncology uation of endoleaks, safety, and cost (Beese et al., 2000; Caro et al., 1991; Hawkins et al., 1994, 2009). Interventional oncology is a recent catchall phrase for a specialty With the maturation of endovascular abdominal aneurysm repair that includes a multitude of minimally invasive procedures in the (EVAR), it has become clear that there is a propensity for developing treatment of a variety of tumors. One aspect of this specialty is

Figure 9. (A) Arteriovenous ﬁstula (AVF) from previous common femoral artery approach. Nonselective injection demonstrates an early draining vein. (B) Magniﬁed view with a more selective injection. (C) After stent placement demonstrating resolution of the AVF, all with carbon dioxide. L. Garza et al. / Journal of Radiology Nursing 35 (2016) 261e274 267

Figure 10. (A) Posthepatic trauma, no evidence of acute hemorrhage with liquid contrast. (B) Gross carbon dioxide extravasation demonstrating site of bleeding for embolization. catheter directed and requires angiography/venography and significant underlying liver disease and are at risk for hepatorenal embolization. The contrast load for these patients is often high. compromise. Approximately 75% of patients with cirrhosis will have renal insufficiency at some time during the course of their Transarterial Chemoembolization, Drug-eluting Beads, and Yttrium-90 disease. Commonly, a large volume of contrast is required for interro- There are procedures that use angiographically direc- gation of the vasculature, treatment, and follow-up examination. ted therapy predominantly for liver tumors. Transarterial che- These risks can be exacerbated by postembolization syndrome moembolization, drug-eluting beads, and yttrium-90 therapy are followed by decreased oral intake or very rarely nontarget embo- used with liver tumor patients, who tend to be older and usually lization and tumor lysis syndrome. All these factors, especially the have other comorbidities, such as renal insufficiency, diabetes, and high volume of contrast, place the patient at risk for CIN. Probably, hypertension. Patients with primary hepatic tumors also have the most significant scenario is that some of these patients may be

Figure 11. Renal transplant carbon dioxide (CO2) digital subtraction angiography demonstrating ostial stenosis treated with a stent. All performed with CO2 without insulting the transplant kidney. 268 L. Garza et al. / Journal of Radiology Nursing 35 (2016) 261e274

Figure 12. Renal angiogram after robotic surgery for renal cell carcinoma and potential postoperative bleeding. (A) Traditional contrast not only does make the diagnosis but also jeopardizes a compromised kidney. (B and C) Arrows indicate source of bleeding using carbon dioxide digital subtraction angiography. denied life-prolonging therapy because of their elevated creatinine transarterial therapy can be precluded if there is an elevation of the and risk for CIN (Figure 14). serum creatinine. In fact, renal insufﬁciency is listed as one of the Another procedure, uterine ﬁbroid embolization, is usually relative contraindications (Stokes et al., 2010) and has been performed in young and healthy individuals. Less invasive described (Rastogi, Wu, Shlansky-Goldberg, & Stavropoulos, 2004).

Figure 13. Advanced arterial disease can be demonstrated using reﬁned imaging techniques. L. Garza et al. / Journal of Radiology Nursing 35 (2016) 261e274 269

Figure 14. (A) Patient had previous transarterial chemoembolization and needs repeat delivery in a right hepatic artery branch. Iodinated contrast injected goes peripherally, and tumor is not seen. (B) Carbon dioxide digital subtraction angiography demonstrates central reﬂux and ﬁlling of the culprit vessel so inadvertent embolization is avoided and the catheter can be redirected for appropriate treatment.

As with transarterial chemoembolization procedures, they may also Venous evaluation and treatment be subjected to high volumes of iodinated contrast and develop postembolization syndrome (Figure 15). As noted, CO2 was used safely in the venous system early in the Similarly, some patients with renal cell carcinoma require 1960s. Since the discovery and refinement of DSA, the myriad uses embolization of the primary tumor or the hypervascular for CO2 as a venous vascular contrast agent have proliferated. The metastasis. Obviously, many of these patients are susceptible gaseous properties noted previously make it an ideal venous to CIN. contrast agent. In each of the clinical scenarios delineated previously, CO2 In the extremities, the low viscosity of CO2 permits delivery of can usually be used as the predominant contrast agent with the sufficient volumes through smaller 25-gauge needles. This is less addition of a small or limited amount of dilute iodinated invasive and less painful to the patient. Because CO2 does not mix contrast. with blood, it is not diluted, and a peripheral hand injection will yield good opacification centrally. This is unlike contrast.

Figure 16. Right upper extremity venogram demonstrating central venous occlusion Figure 15. Carbon dioxide digital subtraction angiography of pelvis demonstrating and patency of collaterals and right internal jugular vein. This can be used to plan hypertrophied uterine arteries and tumor vascularity in the uterine ﬁbroid. access in patients with limited veins. 270 L. Garza et al. / Journal of Radiology Nursing 35 (2016) 261e274

Figure 17. Fistulagram. (A) Central veins. (B and C) Peripheral vein with stenosis. (D) Balloon waist from stenosis.

In the presence of venous occlusion, the properties of low vis- A common venous use of CO2 involves a variety of clinical sce- cosity and reflux will often demonstrate collateral cervical and narios in the liver and spleen. It has been shown by Culp and thoracic veins bilaterally (Figure 16). This is critical in patients with Hawkins that, as opposed to iodinated contrast, CO2 does not have renal insufficiency and chronic venous occlusive disease. Because of any negative effect on the splenocytes or hepatocytes when injec- CIN and nephrogenic systemic fibrosis, respectively, venous ted directly into the respective parenchyma (Culp, Mladinich, & computed tomography and magnetic resonance cannot be used for Hawkins, 1999). Hawkins showed that an injection of as little as a road map before venous access procedures. This can be circum- 12 cc/s had a negative effect as compared with CO2 at 200 cc/s. vented nicely with CO2 extremity venography. It can help deter- One of the more unusual but effective uses of CO2 is in patients mine venous patency and potential access sites. CO2 venography with abnormalities of the splenoportal system (Figure 19)(Burke, can also be used in patients with iodinated contrast allergy. Weeks, Mauro, & Jaques, 2004; Caridi et al., 2003; Cho & Cho, CO2 DSA can be extremely useful in the examination of dialysis 2003; Teng et al., 2006). The low viscosity of CO2 will cause opa- fistulas or interposition grafts (Figure 17). It is excellent at cification the small caliber splenoportal system, identifying the demonstrating the veins and central circulation. anatomy without significant bleeding (Burke et al., 2004; Caridi Another good use is in IVC evaluation, especially for filter et al., 2003; Cho & Cho, 2003; Teng et al., 2006). placement. Many times, these are emergent and patients may have More commonly, it has become routine for many operators to allergy, have elevated creatinine, or do not need the additional use CO2 in transjugular intrahepatic portosystemic shunt (TIPS) volume of iodinated contrast boluses. CO2 has been shown to be a procedures (Figure 20). The incidence of renal compromise after very effective imaging agent for the evaluation of the IVC (Figure 18) TIPS approximates 2% to 3%. The entire procedure, including hepatic (Boyd-Kranis, Sullivan, Eschelman, Bonn, & Gardiner, 1999; and portal venography as well as tract measurement, portal local- Holtzman et al., 2003; Pessanha de Rezende et al., 2011; Sing, ization, and post-TIPS placement, can be performed with CO2, Stackhouse, Jacobs, & Heniford, 2001). reducing the possibility of CIN (Hawkins & Caridi, 1998). Where CO2 CO2 renal venography can also be performed in other procedures is most helpful in TIPS is in the localization of the portal vein. The (adrenal vein sampling and balloon-occluded retrograde trans- low viscosity permits excellent visualization of the portal vein in venous obliteration of varices) where evaluation of veins is greater than 80% of cases and visualizes more of the system than essential. iodinated contrast without most of the consequences. However, because of a few complications of capsular rupture with catheter-

Figure 18. Intravenous cavagram from jugular approach. Figure 19. Splenoportography using a 25-gauge spinal needle and carbon dioxide. L. Garza et al. / Journal of Radiology Nursing 35 (2016) 261e274 271

Figure 20. Transjugular intrahepatic portosystemic shunt procedure using only carbon dioxide.

wedged CO2 injections, balloon occlusion of the hepatic vein with can be used percutaneously to separate organs before and during venous CO2 injections became the preferred method of choice ablative procedures. (Figure 21)(Rees, Niblettt, Lee, Diamond, & Crippin, 1994; Semba, Saperstein, Nyman, & Dake, 1996; Taylor, Smith, Watkins, Kohne, CO2 delivery & Suh, 1999; Theuerkauf et al., 2001). Complications are fewer with the advantage of better portal visualization. Since the advent of intravascular CO2 delivery, there has been Visualizing the portal vein has also become more important anumberofinnovativemethodsofdeliverydeveloped with the rise in interventional oncology. Transhepatic portal vein (Alexander, 2011; Cherian et al., 2009; Cronin, Patel, Kessel, fi access is necessary for certain procedures. More speci cally, it is Robertson, & McPherson, 2005; Hawkins, Caridi, & Kerns, critical in performing selective portal vein embolization to generate 1995; Mendes, Wolosker, & Krutman, 2013). CO2 delivery be- hepatic parenchymal hypertrophy of the remaining future liver gins with a source. As stated previously, a medical-grade CO2 remnant when extended hepatectomy is necessary. should be used, and because of potential impurities over time, Finally, there have been additional reports of limited numbers of thesourceshouldalsobedisposable.Next,theremustbea patients using CO for atypical procedures. One of these is in pain 2 mechanism to deliver the CO2 from the source. One must be management. CO2 has been used instead of iodinated contrast aware that many of the commercial canisters contain 3 million before neurolysis when the patient is highly allergic (Hirata, Higa, cc of pressurized gas. Shono, Hirota, & Shinokuma, 2003). Another newer area of use To avoid the inadvertent overload of pressurized gas and the requiring additional investigation is for intraosseous venography in cumbersome presence of a large canister, we introduced the use of a percutaneous vertebroplasty (Tanigawa, Komemushi, Kariya, flaccid reservoir bag with a series of one-way valves (Figures 22). Kojima, & Sawada, 2005). CO2 can also be used in angioscopy This method used a converted fluid management system by (Silverman, Mladinich, Hawkins, Abela, & Seeger, 1989). It persists Angiodynamics called the Angioflush III system (Angiodynamics, longer than saline, giving a clearer view of the vessel. Similarly, it Inc., Queensbury, NY). A similar system by Merit Medical is also used successfully (Figure 23). The theory behind these systems was that they would be a nonpressurized flaccid reservoir of CO2 that would avoid explosive delivery and excessive volumes. The one-way glued valves are intended to eliminate stopcocks, prevent room air contamination, and eliminate the necessity to remove the delivery syringe. The inherent problem in each appa- ratus is that the systems required assembly. Regardless of the training and simplicity, incorrect assembly can result in air embolus. In addition, the bag must be filled and purged three times to remove residual room air. This step is somewhat cumbersome and time consuming, especially when the decision to use CO2 oc- curs spontaneously during the procedure. Other similar systems do exist. For years, we have reported that the patient should never be connected directly to the cylinder. This has been modified recently because of the development of a K valve stopcock that precludes the possibility of CO2 passing directly from the canister to the patient (Figure 24). The next generation of delivery systems uses a compact regulator that uses a small 10,000 cc canister of pharmaceutical-grade CO2 (Figure 25). The smaller system can be placed in a sterile sleeve or left beneath the sterile drape. It is Figure 21. Capsular rupture with wedged hepatic venography using carbon dioxide. connected to a series of two tubes with one-way valves, as well as 272 L. Garza et al. / Journal of Radiology Nursing 35 (2016) 261e274

Figure 22. AngioFill Bag Collection System and Angioflush (Angiodynamics, Inc., Queensbury, NY). 1,500 cc nondistended plastic bag is attached to a three-port fitting with two one- way check valves. The three-port fitting is connected to a 100 cm tubing, then to a second fitting with two inline check valves and a three-way stopcock. This system is no longer available. a K valve and a reservoir and delivery syringe. The K valve pre- on the delivery catheter. The system does not require assembly vents direct communication with the patient. CO2 is introduced and is extremely user friendly. Setup for use takes approximately into the reservoir syringe. From the reservoir, the gas should be 1 min. pushed, not aspirated, to the delivery syringe to avoid the unlikely Another recently developed type of delivery is the Angiodroid possibility of air contamination through the K valve. Equilibrium CO2 injector (Angiodroid, Angiodynamics, Inc., Queensbury, NY), with the atmosphere can be achieved with a three-way stopcock which uses digital versus hand injection. Finally, some operators filter the CO2 before it enters the vasculature. CO2 can be delivered and has been delivered without filtration for arteriography and venography, as the gas is not injected as an arterial contrast agent above the diaphragm. However, the use of a filter (0.2 mm pore size) can effectively remove particulate contamination and bacteria (0.5 to 5.0 mm).

Conclusion

CO2 is not the quintessential imaging agent, but it offers unique properties when used alone or in combination with iodinated contrast that can expand diagnostic and therapeutic options in a variety of clinical scenarios. Used appropriately, it is safe and can not only prevent CIN but also offer life-extending procedures to patients who would otherwise have been precluded because of their underlying renal status. It can also be used less invasively or when traditional contrast fails to make diagnoses and avoids more signiﬁcant intervention. Current technology permits simple and Figure 23. Merit Medical Custom Waste Bag and Contrast Delivery Set (Merit Medical Systems, Inc., South Jordan, UT). This system is not approved by the Food and Drug safe administration with images comparable to liquid contrast. It is Administration. Similar to the AngioFill, it uses a ﬂaccid plastic bag, one-way valves, an inexpensive and versatile tool that should be added to every and tubing attached to a three-way stopcock for delivery. interventionist's toolbox. L. Garza et al. / Journal of Radiology Nursing 35 (2016) 261e274 273

Figure 24. Proprietary K valve. Product can only be transferred along the lines of the valve stem. Product cannot go from the original source to patient directly. It must traverse both the reservoir and delivery syringe.

References Cronin, P., Patel, J.V., Kessel, D.O., Robertson, I., & McPherson, S.J. (2005). Carbon dioxide angiography: A simple and safe system of delivery. Clinical Radiology, 60(1), 123-125. Alexander, J.Q. (2011). CO angiography in lower extremity arterial disease. Endo- 2 Culp, W.C., Mladinich, C.R., & Hawkins, I.F., Jr. (1999). Comparison of hepatic damage vascular Today, pp. 27-34. Retrieved from http://evtoday.com/2011/09/ from direct injections of iodinated contrast agents and carbon dioxide. Journal of cosub2sub-angiography-in-lower-extremity-arterial-disease. Vascular and Interventional Radiology, 10(9), 1265-1270. Bartholomew, B.A., Harjai, K.J., & Dukkipati, S. (2004). Impact of nephropathy after Ehrman, K.O., Taber, T.E., Gaylord, G.M., Brown, P.B., & Hage, J.P. (1994). Comparison percutaneous coronary intervention and a method for risk stratification. of diagnostic accuracy with carbon dioxide versus iodinated contrast material in American Journal of Cardiology, 93(12), 1515-1519. the imaging of hemodialysis access fistulas. Journal of Vascular and Interven- Beese, R.C., Bees, N.R., & Belli, A.M. (2000). Renal angiography using carbon dioxide. tional Radiology, 5(5), 771-775. British Journal of Radiology, 73, 3-6. Gahlen, J., Hansmann, J., Schumacher, H., Seelos, R., Richter, G.M., & Allenberg, J.R. Bendib, M., Tourni, M., & Boudjellab, A. (1977). CO angiography and enlarged CO angi- 2 2 (2001). Carbon dioxide angiography for endovascular grafting in high risk pa- ography in cardiology (author's transl) AnnalesdeRadiologie(Paris),20, 673-686. tients with infrarenal abdominal aortic aneurysms. Journal of Vascular Surgery, Boyd-Kranis, R., Sullivan, K.L., Eschelman, D.J., Bonn, J., & Gardiner, G.A. (1999). 33(3), 646-649. Accuracy and safety of carbon dioxide inferior vena cavography. Journal of Hashimoto, S., Hashimoto, K., & Soto, M. (1997). CO as an intra-arterial digital Vascular and Interventional Radiology, 10(9), 1183-1189. 2 subtraction angiography (IADSA) agent in the management of trauma. Seminars Burke, C.T., Weeks, S.M., Mauro, M.A., & Jaques, P.F. (2004). CO splenoportography 2 in Interventional Radiology, 14, 163-173. for evaluating the splenic and portal veins before or after liver transplantation. Hawkins, I.F. (1982). Carbon dioxide digital subtraction arteriography. AJR. American Journal of Vascular and Interventional Radiology, 15(10), 1161-1165. Journal of Roentgenology, 139(1), 19-24. Carelli, H.H., & Sorddelli, E. (1921). A new procedure for examining the kidney. Hawkins, I.F., & Caridi, J.G. (1998). Carbon dioxide (CO2) digital subtraction angi- Revista de la Asociacion Medica Argentina, 34, 18-24. ography: 26 year experience at the University of Florida. European Radiology, Caridi, J.G., Hawkins, I.F., Jr., Cho, K., et al. (2003). CO2 splenoportography: Pre- 8(3), 391-402. liminary results. AJR. American Journal of Roentgenology, 180(5), 1375-1378. Hawkins, I.F., Jr., Caridi, J.G., & Kerns, S.R. (1995). Plastic bag delivery system for hand in- Caridi, J.G., Stavropolous, W., & Hawkins, I.F., Jr. (1999). CO digital subtraction 2 jectionofcarbondioxide.AJR. American Journal of Roentgenology, 165(6), 1487-1489. angiography for renal artery angioplasty in high-risk patients. AJR. American Hawkins, I.F., Jr., Caridi, J.G., LeVeen, R.F., Klioze, S.D., & Mladinich, C.R.J. (2000). Use Journal of Roentgenology, 173(6), 1551-1556. of carbon dioxide for the detection of gastrointestinal bleeding. Techniques in Caro, J.J., Trindade, E., & McGregor, M. (1991). The risks of death and of severe Vascular and Interventional Radiology, 3(3), 130-138. nonfatal reactions with high- vs low-osmolality contrast media: A meta-anal- Hawkins, I.F., Caridi, J.G., Wiechman, B.N., & Kerns, S.R. (1997). Carbon dioxide (CO ) ysis. AJR. American Journal of Roentgenology, 156(4), 825-832. 2 digital subtraction angiography in trauma patients. Seminars in Interventional Chao, A., Major, K., Kumar, S.R., et al. (2007). Carbon dioxide digital subtraction Radiology, 14, 175-180. angiography-assisted endovascular aortic aneurysm repair in the azotemic pa- Hawkins, I.F., Cho, K.J., & Caridi, J.G. (2009). Carbon dioxide in angiography to reduce tient. Journal of Vascular Surgery, 45(3), 451-460. the risk of contrast-induced nephropathy. Radiologic Clinics of North America, Cherian, M.P., Mehta, P., Gupta, P., Kalyanpur, T.M., Jayesh, S.R., & Rupa, R. (2009). 47(5), 813-825. Technical note: A simple and effective CO2 delivery system for angiography Hawkins, I.F., Mladinich, C.J., Drane, W.E., et al. (1992). Effects of CO angiography on using a blood bag. Indian Journal of Radiology and Imaging, 19(3), 203-205. 2 renal function. Journal of Vascular and Interventional Radiology, 3,6. Cho, K.J. (2007). CO2 as a venous contrast agent: Safety and tolerance. In K.J. Cho, & Hawkins, I.F., Jr., Wilcox, C.S., Kerns, S.R., & Sabatelli, F.W. (1994). CO2 digital angi- I.F. Hawkins (Eds.), Carbon dioxide angiography: Principles, techniques and prac- ography: A safer contrast agent for renal vascular imaging? American Journal of tices (pp. 37-44). New York: Informa Healthcare. Kidney Diseases, 24(4), 685-694. Cho, K.J., & Cho, D.R. (2003). CO digital subtraction splenoportography with the 2 Hipona, F.A., Ferris, E.J., & Pick, R. (1969). Capnocavography: A new technique for “skinny” needle experimental study in a swine model. Cardiovascular and examination of the inferior vena cava. Radiology, 92, 606-609. Interventional Radiology, 26(3), 273-276. Hirata, K., Higa, K., Shono, S., Hirota, K., & Shinokuma, T. (2003). Splanchnic neu- Criado, E., Kabbani, L., & Cho, K. (2008). Catheter-less angiography for endovascular rolysis using carbon dioxide as the contrast agent. Regional Anesthesia and Pain aortic aneurysm repair: A new application of carbon dioxide as a contrast agent. Medicine, 28(1), 68-69. Journal of Vascular Surgery, 48(3), 527-534. Holtzman, R., Lottenberg, L., Bass, T., Saridakis, A., Bennett, V.J., & Carrillo, E.H. (2003). Comparison of carbon dioxide and iodinated contrast for cavography prior to inferior vena cava filter placement. American Journal of Surgery, 185(4), 364-368. Kooiman, J., Pasha, S.M., Zondag, W., et al. (2012). Meta-analysis: Serum creatinine changes following contrast-enhanced CT imaging. European Journal of Radiology, 81(10), 2554-2561. Krajina, A., Lojík, M., Rejchrt, S., et al. (2004). Carbon dioxide arteriography in the detection of acute massive gastrointestinal bleeding. Folia Gastroenterology Hepatology, 2(1), 8-12. Kriss, V.M., Cottrill, C.M., & Gurley, J.C. (1997). Carbon dioxide (CO2) angiography in children. Pediatric Radiology, 27(10), 807-810. Lieberman, P.L., & Seigle, R.L. (1999). Reactions to radiocontrast material: Anaphy- lactoid events in radiology. Clinical Reviews in Allergy & Immunology, 17(4), 469- 496. McLennan, G., Moresco, K.P., Patel, N.H., et al. (2001). Accuracy of CO2 angiography in vessel diameter assessment: A comparative study of CO2 versus iodinated contrast material in a porcine model. Journal of Vascular and Interventional Radiology, 12(8), 985-989. Mendes, C.A., Wolosker, N., & Krutman, M. (2013). A simple home-made carbon Figure 25. Commander and AngiAssist delivery system. This uses a dedicated phar- dioxide delivery system for endovascular procedures in the iliofemoral arteries. maceutical grade carbon dioxide 10,000 cc cylinder containing a compact user-friendly Circulation Journal, 77(3), 831. compressor. The AngiAssist is one piece preassembled containing one-way valves and a Moresco, K.P., Patel, N., Johnson, M.S., Trobridge, D., Bergan, K.A., & Lalka, S.G. priority K valve, which prevents direct delivery from the source to the patient. (2000). Accuracy of CO2 angiography in vessel diameter assessment: A 274 L. Garza et al. / Journal of Radiology Nursing 35 (2016) 261e274

fl comparative study of CO2 versus iodinate contrast material in an aortoiliac ow Suggested Reading model. Journal of Vascular and Interventional Radiology, 11(4), 437-444. Moresco, K.P., Patel, N.H., Namyslowski, Y., Shah, H., Johnson, M.S., & Trerotola, S.O. Castaneda-Zuniga, W.R., Jauregui, H., Rysavy, J.A., Formanek, A., & Amplatz, K. (1998). Carbon dioxide angiography to the transplanted kidney: Technical (1978). Complications of wedge hepatic venography. Radiology, 126(1), 53-56. considerations and imaging findings. AJR. American Journal of Roentgenology, Choudhri, A.H., Cleland, J.G., Rowlands, P.C., Tran, T.L., McCarty, M., & al- 171(5), 1271-1276. Kutoubi, M.A. (1990). Unsuspected renal artery stenosis in peripheral vascular Murakami, R., Hayashi, H., Sugizaki, K., et al. (2012). Contrast- induced nephropathy disease. British Medical Journal, 301(6762), 1197-1198. in patients with renal insufficiency undergoing contrast-enhanced MDCT. Eu- Coffey, R., Quisling, R.G., Mickle, J.P., Hawkins, I.F., Jr., & Ballinger, W.B. (1984). The ropean Radiology, 22(10), 2147-2152. cerebrovascular effects of intraarterial CO in quantities required for diagnostic Nash, K., Hafeez, A., & Hou, S. (2002). Hospital-acquired renal insufficiency. Amer- 2 imaging. Radiology, 151(2), 405-410. ican Journal of Kidney Diseases, 39(5), 930-936. Dimakakos, P., Stefanopoulos, T., Doufas, A., et al. (1998). The cerebral effects of Paul, R.E., Durant, T.M., Oppenheimer, M.J., & Stauffer, H.M. (1957). Intravenous carbon dioxide digital subtraction angiography in the aortic arch and its carbon dioxide intracardiac gas contrast in the roentgen diagnosis of pericardial branches in rabbits. AJNR. American Journal of Neuroradiology, 19(2), 261-266. effusion and thickening. American Journal of Roentgenology, Radium Therapy, and Hawkins, I.F. (2007). Aortogram and runoff. In K.J. Cho, & I.F. Hawkins (Eds.), Carbon Nuclear Medicine, 78(2), 224-225. dioxide angiography: Principles, techniques, and practices (pp. 53-68). New York: Pessanha de Rezende, M., Massiere, B., Von Ristow, A., et al. (2011). Carbon dioxide Informa Healthcare. use as contrast for vena cava filter implantation: Case series. Journal of Vascular Heye, S., Maleux, G., & Marchal, G.J. (2006). Upper-extremity venography: CO Brasileira, 11(1), 18-21. 2 versus iodinated contrast media. Radiology, 241(1), 291-297. Phillips, J.H., Burch, G.E., & Hellinger, R. (1961). The use of intracardiac carbon di- Huo, T.I., Wu, J.C., Lee, P.C., Chang, F.Y., & Lee, S.D. (2004). Incidence and risk factors oxide in the diagnosis of pericardial disease. American Heart Journal, 61, 748- for acute renal failure in patients with hepatocellular carcinoma undergoing 755. transarterial chemoembolization: A prospective study. Liver International, 24(3), Rastogi, S., Wu, Y.H., Shlansky-Goldberg, R.D., & Stavropoulos, S.W. (2004). Acute 210-215. renal failure after uterine artery embolization. Cardiovascular and Interventional Jang, B.K., Lee, S.H., Chung, W.J., et al. (2008). Incidence and risk factors of acute Radiology, 27(5), 549-550. renal failure after transcatheter arterial chemoembolization for hepatocellular Rees, C.R., Niblettt, R.L., Lee, S.P., Diamond, N.G., & Crippin, J.S. (1994). Use of carbon carcinoma. Korean Journal of Hepatology, 14(2), 168-177. dioxide as a contrast medium for transjugular intrahepatic portosystemic shunt Kappel, J., & Calissi, P. (2002). Nephrology: Safe drug prescribing for patients with procedures. Journal of Vascular and Interventional Radiology, 5(2), 383-386. renal insufficiency. CMAJ, 166(4), 473-477. Rosenstein, P. (1921). Pneumoradiology of kidney positioneA new technique for the Liss, P., Eklof, H., Hellberg, O., et al. (2005). Renal effects of CO and iodinated radiological representation of the kidneys and neighboring organs (suprarenal 2 contrast media in patients undergoing renovascular intervention: A prospec- gland, spleen, liver). Journal of Urology, 15,447. tive, randomized study. Journal of Vascular and Interventional Radiology, 16(1), Rotenberg, E. (1914). Rontgenophotographie der leber, der milz, und des zwerch- 57-65. fells. Deutsch Med Wschr, 40, 1205. Marenzi, G., Lauri, G., Assanelli, E., et al. (2004). Contrast-induced nephropathy in Roussos, C., & Koutsoukou, A. (2003). Respiratory failure. European Respiratory patients undergoing primary angioplasty for acute myocardial infarction. Jour- Journal, 22(Suppl 47), 3s-14s. nal of the American College of Cardiology, 44(9), 1780-1785. Sandhu, C., Buckenham, T.M., & Belli, A.M. (1999). Using CO -enhanced arteriog- 2 McCullough, P.A. (2008). Contrast-induced acute kidney injury. Journal of the raphy to investigate acute gastrointestinal hemorrhage. AJR. American Journal of American College of Cardiology, 51(15), 1419-1428. Roentgenology, 173(5), 1399-1401. Missouris, C.G., Buckenham, T., Cappuccio, F.P., & MacGregor, G.A. (1994). Renal Scatliff, J.H., Kummer, A.J., & Janzen, A.H. (1959). The diagnosis of pericardial effu- artery stenosis: A common and important problem in patients with peripheral sion with intracardiac carbon dioxide. Radiology, 73, 871-883. vascular disease. American Journal of Medicine, 96(1), 10-14. Seeger, J.M., Self, S., Harward, T.R., Flynn, T.C., & Hawkins, I.F., Jr. (1993). Carbon Moos, J.M., Ham, S.W., Han, S.M., et al. (2011). Safety of carbon dioxide digital dioxide gas as an arterial contrast agent. Annals of Surgery, 217(6), 697-698. subtraction angiography. Archives of Surgery, 146(12), 1428-1432. Semba, C.P., Saperstein, L., Nyman, U., & Dake, M.D. (1996). Hepatic laceration from Nikolsky, E., Mehran, R., Turcot, D.B., et al. (2004). Impact of chronic kidney disease wedged venography performed before transjugular intrahepatic portosystemic on prognosis of patients with diabetes mellitus treated with percutaneous shunt placement. Journal of Vascular and Interventional Radiology, 7(1), 143-146. coronary intervention. American Journal of Cardiology, 94(3), 300-305. Silverman, S.H., Mladinich, C.J., Hawkins, I.F., Jr., Abela, G.S., & Seeger, J.M. (1989). Penzkofer, T., Slebocki, K., Grommes, J., et al. (2013). Carbon dioxide-contrasted The use of carbon dioxide gas to displace flowing blood during angioscopy. computed tomography angiography: High pitch protocols and adapted detec- Journal of Vascular Surgery, 10(3), 313-317. tion parameters improve imaging quality. Rofo, 185(2), 128-135. Sing, R.F., Stackhouse, D.J., Jacobs, D.G., & Heniford, B.T. (2001). Safety and accuracy of Rashid, S.T., Salman, M., Agarwal, S., & Hamilton, G. (2006). Occult renal impairment bedside carbon dioxide cavography for the insertion of inferior vena cava filters in is common in patients with peripheral vascular disease and normal serum the intensive care unit. Journal of American College of Surgery, 192(2), 168-171. creatinine. European Journal of Vascular and Endovascular Surgery, 32(3), 294- Spinosa, D.J., Angle, J.F., Hagspiel, K.D., Kern, J.A., Hartwell, G.D., & Matsumoto, A.H. 299. (2000). Lower extremity arteriography with use of iodinated contrast material Rihal, C.S., Textor, S.C., Grill, D.E., et al. (2002). Incidence and prognostic importance or gadodiamide to supplement CO angiography in patients with renal insuf- 2 of acute renal failure after percutaneous coronary intervention. Circulation, ficiency. Journal of Vascular and Interventional Radiology, 11(1), 35-43. 105(19), 2259-2264. Spinosa, D.J., Matsumoto, A.H., Angle, J.F., et al. (1998). Gadolinium-based contrast Rolland, Y., Duvauferrier, R., Lucas, A., et al. (1998). Lower limb angiography: A and carbon dioxide angiography to evaluate renal transplants for vascular prospective study comparing carbon dioxide with iodinated contrast material in causes of renal insufficiency and accelerated hypertension. Journal of Vascular 30 patients. AJR. American Journal of Roentgenology, 171(2), 333-337. and Interventional Radiology, 9(6), 909-916. Shifrin, E., Plich, M., Verstandig, A.G., & Gomori, M. (1990). Cerebral angiography Stokes, L.S., Wallace, M.J., Godwin, R.B., et al. (2010). Quality improvement guide- with gaseous carbon dioxide CO . Journal of Cardiovascular Surgery, 31(5), 603- lines for uterine artery embolization for symptomatic leiomyomas. Journal of 2 606. Vascular and Interventional Radiology, 21(8), 1153-1163. Sonoda, A., Nitta, N., Ushio, N., et al. 320-row multidetector CT angiography for Tanigawa, N., Komemushi, A., Kariya, S., Kojima, H., & Sawada, S. (2005). Intra- hepatocellular carcinoma using CO2 gas instead of iodinated contrast agents: osseous venography with carbon dioxide contrast agent in percutaneous ver- Experiment and preliminary clinical study. Poster presented at: European tebroplasty. AJR. American Journal of Roentgenology, 184(2), 567-570. Congress of Radiology, March 3-7, 2011, Vienna, Austria. Poster C-1123. Taylor, F.C., Smith, D.C., Watkins, G.E., Kohne, R.E., & Suh, R.D. (1999). Balloon occlusion Stram, E., & Molgaard, C.P. (1999). Use of a compression paddle to displace bowel versus wedged hepatic venography using carbon dioxide for portal vein opacifica- gas for carbon dioxide digital subtraction angiography. Journal of Vascular and tion during TIPS. Cardiovascular and Interventional Radiology, 22(2), 150-151. Interventional Radiology, 10(4), 405-408. Teng, G.J., Deng, G., Liu, Z.S., et al. (2006). Ultrafine needle CO splenoportography: A 2 Sullivan, K., Bonn, J., Shapiro, M., & Gardiner, G.A. (1995). Venography with carbon comparative investigation with transarterial portography and MR portography. dioxide as a contrast agent. Cardiovascular and Interventional Radiology, 18(3), European Journal of Radiology, 59(3), 393-400. 141-145. Theuerkauf, I., Strunk, H., Brensing, K.A., et al. (2001). Infarction and laceration of Wilson, A.J., & Boxer, M.M. (2002). Neurotoxicity of angiographic carbon dioxide in liver parenchyma caused by wedged CO venography before TIPS insertion. 2 the cerebral vasculature. Investigative Radiology, 37(10), 542-551. Cardiovascular and Interventional Radiology, 24(1), 64-67. Wong, A.A., Charalel, R.A., Louie, J.D., & Sze, D.Y. (2013). Carbon dioxide contrast Thomson, K.R., Tello, R., Sullivan, R., Dixon, R.G., Becker, G., & Mitchell, P.J. (1996). enhancement for c-arm CT utility for treatment planning during hepatic Carbon dioxide angiography. Asian Oceanian Journal of Radiology, 1, 20-23. embolization procedures. Journal of Vascular and Interventional Radiology, 24(7), Trcka, J., Schmidt, C., Seitz, C.S., Brocker,€ E.-B., Gross, G.E., & Trautmann, A. (2008). 975-980. Anaphylaxis to iodinated contrast material: Nonallergic hypersensitivity or IgE- Yamazaki, H., Oi, H., Matsushita, M., et al. (2001). Renal cortical retention on delayed mediated allergy? AJR. American Journal of Roentgenology, 190(3), 666-670. CT and nephropathy following transcatheter arterial chemoembolisation. British Walsh, S.R., Tang, T.Y., & Boyle, J.R. (2008). Renal consequences of endovascular Journal of Radiology, 74(884), 695-700. abdominal aortic aneurysm repair. Journal of Endovascular Therapy, 15(1), 73-82.