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1 All authors: Department of Radiology, Kyoto Prefectural University of Medicine, 465 Kajii-chyo, Kawaramachi-Hirokoji, Kamigyo, Kyoto, 602-8566, Japan.
Received February 19, 2002;
accepted after revision May 30, 2002.
Address correspondence to T. Yamagami.
Abstract
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SUBJECTS AND METHODS. Eighty-six patients (56 men, 30 women; mean age, 62.1 years) with unresectable advanced liver cancer underwent percutaneous implantation of a port-catheter system. In the 75 patients who had not undergone gastrectomy, right gastric artery embolization was performed before port-catheter system placement to prevent gastric mucosal lesions. In 43 patients, the approach for embolization was through a microcatheter inserted from the hepatic artery site, and in the remaining 32 patients, the approach was from the left gastric artery. The success rates of these two groups were compared.
RESULTS. Embolization was successfully accomplished at the first attempt in 72.1% of the 43 patients in whom the microcatheter was inserted from the hepatic artery site. In contrast, in 93.8% of 32 patients, embolization was successfully performed through the left gastric artery. The success rate of embolization was significantly higher in the latter group (p = 0.0173, chi-square test). A second attempt in which the catheter was redirected to another approach, performed on the same day in a majority of patients, resulted in successful embolization in an additional eight patients, with a final success rate of 92.0%.
CONCLUSION. Embolization of the right gastric artery using microcoils through a microcatheter advanced through the left gastric artery may be the preferred method for the preparation of repeated hepatic artery infusion.
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A frequent complication is reactive gastric or duodenal mucosal lesions caused by irritation resulting from infusion of chemotherapeutic agents into adjacent organs through arteries originating from the common hepatic artery, such as the gastroduodenal artery and the right gastric artery [5,6,7,8,9,10,11,12,13,14]. To prevent this complication, some investigators contend that it is efficacious to selectively embolize arteries supplying blood to these organs, at the time of implantation of the port-catheter system [11, 15,16,17]. However, it is our experience and that of others [11, 18, 19] that the origin of the right gastric artery, which is one of the arteries supplying adjacent organs (i.e., the stomach), is, in many cases, diminutive and angulated with anatomic variations [18, 20, 21]. Thus, it is occasionally difficult to insert a catheter selectively into the right gastric artery from the hepatic artery, and this problem results in failure to embolize the right gastric artery with coils. Through trial and error, we found a method to embolize the right gastric artery through a microcatheter advanced through the left gastric artery. The aim of our study was to evaluate whether this approach was more useful than that through the site of the hepatic artery.
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Of the 86 patients, 34 had primary liver cancer, and 52 had metastatic liver cancer that originated from colorectal (n = 22), breast (n = 13), gastric (n = 8), lung (n = 3), gallbladder (n = 2), pancreatic (n = 1), ovarian (n = 1), anal (n = 1), and jejunal (n = 1) cancers. In all patients, there were diffuse or multiple (> five) malignant lesions or a few large (> 5 cm) malignant lesions in both the right and left lobes of the liver, making surgical resection impossible. Most of these patients had been administered systemic chemotherapy or other interventional treatments, only to develop intractable disease.
In 75 patients, as the first step in the port-catheter implantation procedure or on the day before port-catheter implantation, the right gastric artery was embolized to prevent infusion of chemotherapeutic agents into the stomach. Gastrectomy was performed previously in the remaining 11 patients (gastric cancer, n = 8; gastric ulcer, n = 3), and the right gastric artery had been ligated at the time of surgery. Thus, embolization was not required in these patients.
Procedures
Percutaneous placement of long-term indwelling catheters was performed for
frequent arterial infusion chemotherapy, according to the procedure of Arai et
al. [16]
(Fig. 1), as follows: First, a
5-French catheter was inserted from a branch of the left subclavian artery or
the right femoral artery, both of which were exposed by minimally invasive
surgery using local anesthetic, and was advanced to the common hepatic artery
through the celiac artery. Second, a microcatheter (Renegade-18; Boston
Scientific, Watertown, MA) was inserted coaxially, after which the
posterosuperior pancreaticoduodenal artery was embolized with microcoils
(Diamond Coil, Boston Scientific; or Trufill, Cordis, Miami, FL) to prevent
infusion of chemotherapeutic agents into the duodenum and pancreas. Third,
using the catheter exchange method, we inserted an indwelling catheter with a
side hole with the tip into the gastroduodenal artery. The side hole was
placed into the common hepatic artery. Fourth, the distal lumen of the
indwelling catheter was occluded with a 1.2-cm microcoil (Hilal Embolization
Microcoils; Cook Europe, Bjaeverskov, Denmark) through a coaxial microcatheter
advanced inside the indwelling catheter beyond the side hole. Fifth, the
gastroduodenal artery was embolized with microcoils (Diamond Coil [2.3-8.0 cm
long when straightened], Boston Scientific; or Trufill [2.0-6.0 cm long when
straightened], Cordis) through a microcatheter inserted through the side hole
of the indwelling catheter coaxially into the gastroduodenal artery outside
the indwelling catheter. In many cases, 0.5-1.5 mL of n-butyl
cyanoacrylate (Histoacryl-Blue; Braun, Melsungen, Germany) mixed with Lipiodol
([iodized oil] Laboratoire Guerbet, Roissy, France) was added for sufficient
embolization. Finally, the proximal end of the indwelling catheter was
connected to a port (Septum Port; Sumitomo Bakelite, Akita, Japan) implanted
subcutaneously. A 5-French polyurethane-covered catheter with a tapered tip
(Anthron P-U catheter; Toray Medical, Tokyo, Japan) was used in 80 patients as
the indwelling catheter. The operator made a side hole at the region in which
the diameter was tapered, using a small scissors after folding the indwelling
catheter, and then cut off the redundant distal part of the catheter tip. In
the remaining six patients, a Gently catheter (Solution, Tokyo, Japan) in
which a side hole is created during manufacturing was used.
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The right gastric artery was embolized in 75 patients. In the first 43 patients, the right gastric artery was embolized with microcoils (Diamond Coil [2.3 or 4.1 cm long when straightened], Boston Scientific; or Trufill [2.0 or 4.0 cm long when straightened], Cordis) through a microcatheter advanced through the common or proper hepatic artery, coaxially inserted from a 5-French catheter positioned in the celiac or common hepatic artery. Then, in the subsequent 32 patients, we performed embolization from the left gastric artery site after noticing the usefulness of such an approach. With this modification, embolization of the right gastric artery was performed through a microcatheter advanced through the left gastric artery, coaxially inserted from a 5-French catheter positioned in the celiac axis or the origin of the left gastric artery (Fig. 2A,2B,2C,2D,2E). Before embolization, celiac arteriography was performed in all 75 patients to delineate the precise anatomy.
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These procedures were performed in the interventional radiology suite, by one of three experienced interventional radiologists, after written informed consent was obtained from the patient.
Parameters Investigated
The rates of success of the two approaches (through the common or proper
hepatic artery and through the left gastric artery) of embolization of the
right gastric artery were compared. The chi-square test was additionally used
for statistical comparison of these two groups. Moreover, when embolization
failed at the first approach, future management of the right gastric artery,
thereafter, was investigated.
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Overall, in 61 (81.3%) of the 75 patients, the right gastric artery was successfully embolized at the first trial; an additional trial resulted in successful embolization in an additional eight patients, with a final success rate of 92.0% (69/75).
In 31 (72.1%) of the 43 patients in whom the microcatheter was advanced through the site of the hepatic artery, the right gastric artery was successfully catheterized at the first trial. In six of the remaining 12 patients, the right gastric artery was catheterized by changing the route for advancement of the microcatheter to the left gastric artery, and embolization was accomplished, whereas in the other six patients, attempts at embolization were abandoned because we had not yet noticed the usefulness of the approach from the left gastric artery.
On the other hand, of the 32 patients in whom the microcatheter was advanced through the left gastric artery, the right gastric artery was successfully catheterized at the first trial in 30 patients (93.8%). In one of the two patients in whom catheterization by this route was not accomplished, there was no communication between the right and left gastric arteries. In the second patient, mild intimal injury occurred while the microcatheter was advanced to the right gastric artery from the left gastric artery, thus preventing embolization by this pathway. In these two patients, embolization was achieved after changing the approach route to that from the hepatic artery site.
In summary, the success rate at the first trial to selectively advance a microcatheter into the right gastric artery was significantly higher when the approach was through the left gastric artery than through the hepatic artery (p = 0.0173, chisquare test).
The mean number of microcoils used among all patients in whom embolization was accomplished was 2.2 ± 0.8 (mean ± SD; range, 1-4). When the microcatheter was inserted through the hepatic artery, the mean number of microcoils used was 1.8 ± 0.8 (mean ± SD; range, 1-3), whereas the mean number was 2.4 ± 0.7 (mean ± SD; range, 1-4) when the microcatheter was advanced through the left gastric artery.
Gastrointestinal symptoms developed acutely after hepatic artery infusion chemotherapy in four patients who also had gastric mucosal lesions as revealed on endoscopy. Two (33.3%) were among the six patients in whom embolization of the right gastric artery could not be accomplished; embolization had been successful in the other two. In the former two patients, severe gastric ulcers occurred, necessitating abandonment of further hepatic artery infusion chemotherapy. In the latter two patients, both gastric ulcers and gastritis occurred. Arteriography performed while contrast material was infused through the port revealed recanalization of the right gastric artery in one of these patients; in the other patient, the right gastric artery was sufficiently embolized. In both patients, chemotherapy through the port-catheter system was withdrawn, and the gastric ulcers were treated. In addition, in the patient whose right gastric artery was recanalized, embolization was again performed. After an interval, intraarterial infusion chemotherapy was resumed.
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A weak point in this system is the inability to easily and safely withdraw the indwelling catheter if either the patient or the referring physician wants the catheter to be retracted during follow-up or after successful treatment of hepatic malignant lesions. However, despite this disadvantage, among various methods to implant port-catheter systems using interventional techniques [16, 23,24,25,26, 30, 31], the fixed-catheter-tip technique as described by Arai et al. [16], which we used, is advantageous because of the low frequency of hepatic artery occlusion, which was shown to occur in only 5.3% of 115 patients [28]. Such a low rate of hepatic artery occlusion is mainly due to the lack of mechanical stimulation of the hepatic artery wall by movement of the catheter tip because the catheter is fixed in the gastroduodenal artery.
In our previous research [32], the rate of catheter dislocation with the fixed-catheter-tip technique was only 4.4% of the 45 patients. In the most common interventional procedure, in which the indwelling catheter tip is positioned in the proper or the common hepatic artery, catheter dislocation occurs at a relatively higher rate (6-18%) [23, 26, 30, 31]. Thus, the procedure we report is also useful to avoid catheter dislocation because the distal tip of the catheter is tightly fixed to the gastroduodenal artery with embolic agents such as coils and n-butyl cyanoacrylate.
Another advantage of the fixed-catheter-tip technique is the prevention of some gastroduodenal mucosal lesions and of damage to the pancreas caused by the intraarterial infusion of chemotherapeutic agents to adjacent organs supplied from the common hepatic artery, such as the duodenum and pancreas, because the gastroduodenal artery is embolized during indwelling catheter placement.
However, there remains the problem of gastromucosal lesions, which are reported to occur in 3.2-47.5% of these patients [5,6,7,8,9,10,11], caused by opening the right gastric artery, through which chemotherapeutic agents are distributed to the wall of the stomach. To avoid this drug-induced complication, researchers have strongly proposed embolization of the right gastric artery [11, 16, 17]. Inaba et al. [17] conducted a review of 217 patients who underwent repeated hepatic artery infusion chemotherapy and found that only 2.6% of 192 patients in whom the right gastric artery was sufficiently embolized before percutaneous port-catheter placement developed gastric mucosal lesions, whereas 36.0% of 25 patients without sufficient embolization developed such lesions. This difference was statistically significant. In our study, definite gastric lesions developed in only two (2.9%) of 69 patients having gastric artery embolization.
The right gastric artery is usually small (<2 mm in diameter), angulated, and rich in anatomic variations [11]. Hence, it is sometimes difficult to selectively advance catheters from the site of the hepatic artery into the right gastric artery. Regarding anatomic variations, the most commonly reported sites of divergence of the right gastric artery are the proper hepatic artery with a frequency of 40-52% [11, 20, 21] and the right or left hepatic artery with a frequency of 21-42% [11, 20, 21]. Divergence has also been reported in the common hepatic artery (1.5-10%) [20, 21] and gastroduodenal artery (1.5%) [21]. These sites correspond to sites from which the right gastric artery diverged in subjects of our study; this correspondence suggests that our subjects did not differ appreciably from those of other cohorts.
The right gastric artery generally anastomoses with the left gastric artery [19]. This fact led us to speculate that advancing the microcatheter to the right gastric artery through the left gastric artery would be possible, even though the hepatic artery was usually used for this purpose. In our study, the rate of successful embolization at the first trial was significantly higher in patients in whom the microcatheter was advanced through the left gastric artery instead of through the hepatic artery. In addition, in six (50%) of 12 patients in whom embolization of the right gastric artery through the hepatic artery site failed, a change in approach to the left gastric artery resulted in success.
Our technique (i.e., advancing the microcatheter through the left gastric artery to the right gastric artery) might be useful in other scenarios as well. Embolization of the right gastric artery using this approach might be applied in patients who have undergone port-catheter placement at surgical laparotomy with failure of right gastric artery ligation or in patients undergoing episodic hepatic artery infusion chemotherapy. This technique might be used to protect the right gastric artery from any agents used for hepatic artery embolization. Our new approach might also serve as a more direct collateral pathway, allowing transcatheter hepatic artery chemoembolization of the hepatic artery for liver malignancies in patients with common or proper hepatic artery stenosis or occlusion. These patients otherwise might undergo chemoembolization from the superior mesenteric artery through pancreaticoduodenal pathways.
The results of our study show that advancement of microcatheters through the left gastric artery into the right gastric artery is a useful method for the preparation of long-term hepatic artery infusion chemotherapy. This route may also be used as an alternative approach when the usual route via the site of the hepatic artery fails. The limitation of using this route is that the anastomosis between the right and left gastric artery may be too small to advance the microcatheter or may not exist.
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