|Year : 2018 | Volume
| Issue : 1 | Page : 61-67
Role of inferior phrenic artery in the interventional treatment of lung metastases tumor: A report of 11 cases
Lin-Zhong Zhu, Ren-Jie Yang, Xu Zhu
Department of Interventional Therapy, Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education), Peking University Cancer Hospital and Institute, Peking, People's Republic of China
|Date of Web Publication||8-Mar-2018|
Dr. Xu Zhu
Department of Interventional Therapy, Peking University Cancer Hospital and Institute, 52 Fucheng Road, Haidian District, Peking
People's Republic of China
Source of Support: None, Conflict of Interest: None
Background: Lung metastases have been very common in advanced cancer, which were observed in 30%–40% of cancer cases. Transarterial chemoembolization (TACE) is one of the choice for treating lung cancer. In our center, 119 cases of lung metastases were treated with TACE, and we found that inferior phrenic artery (IPA) played an important role in this procedure.
Materials and Methods: From June 2011 to June 2015, 119 cases with malignant lung metastases received TACE procedure in our center. The TACE procedure was performed through bronchial artery (BA) and collateral arteries. In these 11 cases, we found that part of metastatic lesions was supplied by the IPA. Angiography and embolization technique, successful rate, safety and clinical adverse events, and survival were retrospectively studies.
Results: The lung metastases were mainly supplied by BA, thoracic artery, and intercostal artery. In 11 cases, the IPA was involved in the blood supply of lung metastases (9.2%). Right IPA (RIPA), left IPA (LIPA), and both LIPA and RIPA were involved in blood supply of 6, 3, and 2 cases of lung metastases, respectively, especially for the lesions located in the lower lobe of the lung. All lesions of the 11 cases were successfully embolized; no diaphragmatic dysfunction and spinal cord injury or other serious complications were observed. The average survival time was 14.7 months since the diagnosis of lung metastases.
Conclusion: The IPA was an important feeding artery for lung metastases, especially for lesions in the lower lung lobe. It should be searched as much as possible for achieving complete embolization of metastases.
Keywords: Inferior phrenic artery, lung metastases, transarterial chemoembolization
|How to cite this article:|
Zhu LZ, Yang RJ, Zhu X. Role of inferior phrenic artery in the interventional treatment of lung metastases tumor: A report of 11 cases. J Can Res Ther 2018;14:61-7
|How to cite this URL:|
Zhu LZ, Yang RJ, Zhu X. Role of inferior phrenic artery in the interventional treatment of lung metastases tumor: A report of 11 cases. J Can Res Ther [serial online] 2018 [cited 2022 Oct 4];14:61-7. Available from: https://www.cancerjournal.net/text.asp?2018/14/1/61/226759
| > Introduction|| |
Malignant tumor often was often companied by lung metastases., From June 2011 to June 2015, 119 cases with malignant lung metastases received transarterial chemoembolization (TACE) treatment in our center; usually, the TACE was performed through bronchial artery (BA), but in many patients, there were collateral feeding arteries such as internal mammary artery, intercostal artery, subclavian artery, axillary artery, and inferior phrenic artery (IPA). In 11 cases, we observed that metastases were supplied by the IPA.
| > Materials and Methods|| |
Of 119 patients with lung metastases, 645 cases of interventional procedure were performed. The lung metastases were supplied with IPA in 11 patients; among them, 5 were male and 6 were female, with an average age of 59.8 years. The primary cancer included hepatocellular carcinoma (9 cases), retroperitoneal leiomyosarcoma (1 case), and skin malignant melanoma (1 case). The size of metastasis lesions was ranged from 2.3 to 11 cm (average of 4.04 cm) [Table 1].
Transarterial chemoembolization procedure
All digital subtraction angiography (DSA) procedures were performed under the guidance of GE Innova 4100IQ. The right femoral artery was cannulated with a 5F vascular sheath by Seldinger technique.
The 5F pigtail catheter, Cobra catheter or left gastric catheter, and headhunter catheter were applied to perform angiography in arteries originated from thoracic aorta, such as BA, subclavian artery, intercostal artery, and internal mammary artery. It aimed to find the feeding artery of lung lesions. If we could not find the feeding artery through these arteries, then we would search for arteries originated from abdominal aorta, such as celiac artery, IPA and left gastric artery, and adrenal artery. All angiography was performed with 300 mg I/ml iohexol.
Interventional treatment of lung metastases lesions
When we found the feeding artery, super-selective was achieved with a 2.2-Fr or 2.6-Fr microcatheter. In all cases, we advanced as deep as possible to avoid the cord artery and to reduce the damage to lung parenchyma. When we finally reached the branch which directly fed the tumor, lipiodol (Guerbet Corp., France) was continually injected until near stasis was observed in the artery. Dosages of lipiodol per procedure were ranged from 1 to 15 ml through IPA, mixed with 10–20 mg of doxorubicin (Pfizer Pharmaceuticals Ltd, USA). In 6 cases, Biosphere (COOK Corp., USA) was injected as supplement.
Interventional treatment of lesions in liver
Angiography was performed through celiac artery, superior mesenteric artery and IPA, renal artery, internal mammary artery, and intercostal artery. Either super-selective or super-super-selective catheter technique was adopted. Dosages of lipiodol per procedure were ranged from 4 to 18 ml, mixed with 20–40 mg of doxorubicin.
Observation of indicators and follow-up observation
On the 3rd day after the completion of TACE, adverse effects were evaluated in the patients by receiving a physical examination and laboratory testing. Besides, chest computed tomography (CT) scan was ordered within 1–3 days after TACE for evaluating potential lung injury and lipiodol deposition in the tumor of lung and liver. Tumor efficacy evaluation was performed in accordance with the WHO launched solid tumor treatment evaluation standard (modified response evaluation criteria in solid tumor standard evaluation).
| > Results|| |
Characteristics of inferior phrenic artery
Origin of feeding artery
In all 119 cases, BA was observed to be the main feeding artery. Besides, there was other collateral feeding artery, including intercostal artery and internal mammary artery. In this group, of all patients, IPA was involved in blood supply of lung metastases in 11 cases (9.2%), including 6 cases of right IPA (RIPA), 3 cases of left IPA (LIPA), and 2 cases of both LIPA and RIPA [Table 2].
Angiography appearance of inferior phrenic artery
All IPA in this group were originated from abdominal aorta, and angiography through IPA showed branch of IPA extended to lung and abnormal tumor staining in lung metastasis lesions. All lesions showed plenty of blood supply. Arteriovenous fistula was observed in only 1 case; we found bronchial vein emerged when we perform angiography through LIPA. In 3 cases, IPA supplied lesions in both liver and lung, which were all RIPA. In the other 8 cases, IPA supplied only lesions in the lung.
| > Case 1|| |
A 58-year woman, she was diagnosed as retroperitoneal leiomyosarcoma for 2 years and liver and lung metastases for 1 year, angiography through right bronchial artery showed stain of metastasis lesion, angiography through RIPA showed tumor stain in the right lower lung, embolization was performed through both arteries [Figure 1] and [Figure 2].
|Figure 1: Lung metastasis of retroperitoneal leiomyosarcoma was feed by right bronchial artery|
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|Figure 2: Lung metastasis of retroperitoneal leiomyosarcoma was feed by right inferior phrenic artery|
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| > Case 2|| |
A 46-year man with HCC and lung metastases, after liver transplantation, he suffered lung metastases. Angiography through left bronchial artery and left inferior phrenic artery showed tumor stain in the left lower lung, two arteries supply upper and lower part of the same lesion, respectively [Figure 3] and [Figure 4].
|Figure 3: Lung metastasis of liver cancer was feed by left bronchial artery|
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| > Case 3|| |
A 48-year man accepted hepatectomy 2 years ago, during the procedure, the tumor ruptured, and he suffered multiple peritoneal metastases which were controlled by TACE, 1 years later, he experienced lung metastases, angiography through bronchial artery found no stain, angiography through RIPA showed the stain in both right lower right lung and segment 8 of liver [Figure 5] and [Figure 6].
|Figure 5: Celiac metastasis of HCC was feed by superior mesenteric artery|
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|Figure 6: Lung metastasis of liver cancer was feed by right inferior phrenic artery|
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| > Case 4|| |
A 53-year woman with malignant melanoma, as well as both liver and lung metastases, RIPA supply metastatic lesion in the right lower lung, which was embolized with lipiodol; patients reported chest tightness in the night, emergency chest CT scan showed lipiodol accumulation inside the metastases lesion, and she had pleural effusion and limitation atelectasis, no high density was observed in pulmonary parenchymal and signs of pneumonia; the symptom was relieved 2 days later [Figure 7], [Figure 8], [Figure 9], [Figure 10], [Figure 11], [Figure 12], [Figure 13], [Figure 14].
|Figure 8: Lung metastasis was feed by branch of right inferior phrenic artery|
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|Figure 13: Right lung metastasis was feed by right inferior phrenic artery|
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|Figure 14: Left lung metastasis was feed by left inferior phrenic artery|
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| > Case 5|| |
The right lung metastatic lesion was supplied by both bronchial artery and the right inferior phrenic artery. For the lesion in the left lung, we failed to find the bronchial artery, the lower part of the metastases was supplied by the left inferior phrenic artery, angiography showed arteriovenous fistula, lipiodol flowed to the direction of hilar during embolization, and we stopped timely; no sign of pumonary embolization was found.
Transarterial chemoembolization session for finding the inferior phrenic artery
The average TACE session for finding IPA was 3.5 times (ranged 1–8 times). In 6 cases, IPA was found to supply lung metastasis lesions in the first TACE session; in 4 cases, IPA was found in the second TACE session due to the insufficient deposit of lipiodol in metastases lesion; and in 1 case, IPA was found at the fifth TACE session.
Relationship between inferior phrenic artery and bronchial artery
In 3 cases, IPA and BA supplied a same lesion; in 5 cases, they supplied different lesions; in 3 cases, IPA was the only feeding artery. All lesions supplied by IPA were in the lower lobe of the lung, which was closed to the diaphragm.
Embolization through IPA was achieved in all 11 cases, and all patients were regularly examined with chest CT scan. Compared with preoperative imaging, all lesions supplied by IPA became smaller after first TACE session, and long-term follow-up showed complete response (CR) in 0 case, partial response (PR) in 6 cases, stable disease (SD) in 2 cases, and progression disease (PD) in 3 cases; the result of other lesions in the lung was not that better, and the result was CR in 0 case, PR in 2 cases, SD in 2 cases, and PD in 7 cases. Average survival time since the date of diagnoses of lung metastases was 14.7 months.
No deposition of lipiodol was observed in lung parenchyma or other organs. There were 5 cases of chest pain, 1 case of pleural effusion which lasted for 5 days, and 6 cases of transient chest tightness. No hiccup, kin damage, and spinal cord injury was observed. There were 7 cases of moderate or high fever lasted for 1–5 days, which was relieved by antipyretics. All cases died of liver dysfunction or gastrointestinal bleeding.
| > Discussion|| |
BA was the main artery of the primary/metastatic lung cancer. In general, blood supply of visceral pleura was originated from the BA while that of parietal pleura was originated from the systemic artery. Bronchial arteries and other arteries may form vascular anastomosis, such as intercostal arteries, thyrocervical trunk, subclavian artery, axillary artery, and internal mammary artery. Besides, IPA, left gastric artery, and other arteries may also be the potential artery for blood supply of lung lesions.
Technical failure of transcatheter BA embolization was observed due to the collateral supply in many cases, resulted from systemic supply of the lesion such as the IPA, intercostal, mammary, or subclavian arteries.,
In our center, we found that IPA was an important collateral artery. IPA usually originated from abdominal aorta, celiac,, occasionally from renal artery., Gwon et al. reported both LIPA and RIPA were originated from a common trunk in 29.5% patients. The majority of LIPA and RIPA were originated independently from the celiac axis. Aslaner et al. reported that inferior phrenic arteries gave off small branches to the diaphragm, liver, adrenal glands, esophagus, stomach, inferior vena cava, and retroperitoneum. Loukas et al. found that the RIPA ascending branch could be separated as branch and the inferior vena cava diaphragmatic hiatus branch, LIPA ascending branch, and sub-branch could be separated as esophagus spleen branch.
IPA was not only an important extrahepatic collateral artery for hepatocellular carcinomas, especially those located in the bare area of the liver,, but also an important supply artery for lung.
IPA was generally searched in embolization in primary lung cancer and hemoptysis. However, for lung metastases, role of IPA was underestimated. In our study, we found IPA feeding the lung metastases in 9.2% of cases. What factors may be contributed to the involvement of IPA in the feeding artery of lung metastases?First, all lesions supplied by IPA were in the lower lobe of the lung and closed to the diaphragm. Second, there was rich blood supply for all the lesions, which was quickly developed with a strong ability to induce tumor angiogenesis. The branch of IPA and BA or other arteries may be attracted and migrated. Third, the size of the metastases was relatively large, with 5 cases of <3 cm, 4 cases of 3–5 cm, and 2 cases of larger than 5 cm. The more demand for blood supply leads to hyperplasia of branch of IPA.
How can we determine the collateral artery before TACE? With the development of CT angiography (CTA), existence of IPA may be guided before TACE procedure. Recent advances in CTA allowed for better visualization of small vessels and have replaced DSA in many clinical algorithms of the abdominal vasculature.,, The origin of IPA can be also revealed, providing guidance for TACE procedure.
All the cases died of liver dysfunction or gastrointestinal bleeding. Average survival time since the date of diagnoses of lung metastases was 14.7 months. Long-term follow-up was observed for IPA supplied lesions. We achieved a result that 0 case of CR, 6 cases of PR, 2 cases of SD, and 3 cases of PD. For other metastatic lesions in the lung, the result was not that better, and the result was CR in 0 case, PR in 2 cases, SD in 2 cases, and PD in 7 cases. This may contribute to the complete embolization through IPA.
What the relationship between IPA and BA? In 3 cases, IPA and BA supplied a same lesion; in 5 cases, they supplied different lesions. In other 3 cases, we failed to find BA and other arteries originated from thoracic aorta; thus, IPA was the only feeding artery. Most IPA was found at the first or second TACE session for lung metastases; obviously, IPA was not compensatory artery of BA after embolization. This was independent phenomenon. We owed it to the anatomy factor.
As the IPA was relatively tortuous and slim and might supply lung parenchyma, spinal cord, pericardium, and diaphragm, carefully operation and observation would be required. We need advanced as deep as possible and perform high-quality angiography to identified normal tissue and potential arteriovenous shunts. Doctor must be continually watching the X-ray fluoroscopy when giving lipiodol.
The most common complications for the embolization of lung cancer were chest pain, dysphagia, bronchial necrosis, and spinal cord ischemia. Tajima et al. reported transarterial hepatic chemoembolization through the IPA frequently resulted in lung CT changes, including lipiodol accumulation in the lung field, consolidation, and pleural effusion or even respiratory symptoms. They suggested that it might contribute to arteriovenous shunts. In our cases, the average TACE session through IPA was 3.5 times (ranged 1–8). We found arteriovenous shunts only in 1 case, and embolization was stopped in time; no ectopic embolization was observed. Follow-up CT proved no accumulation of lipiodol in lung parenchyma. Seven cases suffered moderate or high fever lasted for 1–5 days which was relieved by antipyretics. Five cases reported slight-to-moderate pain and 5 cases with moderate fever. Six cases experienced transient chest tightness. No hiccup, skin damage, and spinal cord injury was observed. In 1 case, whose metastatic lesion lay in right cardiophrenic angle, the patient suffered from chest tightness for one night, CT scan showed pleural effusion and limitation atelectasis, and the symptom disappeared in the next day. Moreover, the pleural effusion and atelectasis disappeared 5 days later.
| > Conclusion|| |
In TACE treatment of lung metastases, especially for those in the lower lobe, IPA should be considered. TACE through IPA was a safe procedure, and the lesion could be controlled satisfactorily. The limitations of this study included its retrospective design, the small sample size. A multicenter prospective study with a large sample size of patients would be necessary to definitively establish the benefits of TACE management.
Declaration of patient consent
The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.
We wish to thank Siwen Dong for her contribution to the language editing of this manuscript and Hongzhi Zhang for his collecting service and support rendered during the preparation of this manuscript.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| > References|| |
Nichols FC. Pulmonary metastasectomy. Thorac Surg Clin 2012;22:91-9, vii.
Hornbech K, Ravn J, Steinbrüchel DA. Current status of pulmonary metastasectomy. Eur J Cardiothorac Surg 2011;39:955-62.
Pietrasik K, Bakon L, Zdunek P, Wojda-Gradowska U, Dobosz P, Kolesnik A, et al.
Clinical anatomy of internal thoracic artery branches. Clin Anat 1999;12:307-14.
Krokidis M, Sabharwal T, editors. Challenging Concepts in Interventional Radiology. Oxford UK: Oxford University Press; 2015.
He G, Liu W, Gao Z, Gao Z, Gao H, Wang Y, et al.
Intervention treatment on massive hemoptysis of pulmonary aspergilloma. Exp Ther Med 2017;13:2259-62.
Gürses İA, Gayretli Ö, Kale A, Öztürk A, Usta A, Şahinoǧlu K, et al.
Inferior phrenic arteries and their branches, their anatomy and possible clinical importance: An experimental cadaver study. Balkan Med J 2015;32:189-95.
Song SY, Chung JW, Yin YH, Jae HJ, Kim HC, Jeon UB, et al.
Celiac axis and common hepatic artery variations in 5002 patients: Systematic analysis with spiral CT and DSA. Radiology 2010;255:278-88.
Loukas M, Hullett J, Wagner T. Clinical anatomy of the inferior phrenic artery. Clin Anat 2005;18:357-65.
Miyayama S, Yamashiro M, Yoshie Y, Okuda M, Nakashima Y, Ikeno H, et al.
Inferior phrenic arteries: Angiographic anatomy, variations, and catheterization techniques for transcatheter arterial chemoembolization. Jpn J Radiol 2010;28:502-11.
Gwon DI, Ko GY, Yoon HK, Sung KB, Lee JM, Ryu SJ, et al.
Inferior phrenic artery: Anatomy, variations, pathologic conditions, and interventional management. Radiographics 2007;27:687-705.
Aslaner R, Pekcevik Y, Sahin H, Toka O. Variations in the origin of inferior phrenic arteries and their relationship to celiac axis variations on CT angiography. Korean J Radiol 2017;18:336-44.
Kim HC, Chung JW, Lee W, Jae HJ, Park JH. Recognizing extrahepatic collateral vessels that supply hepatocellular carcinoma to avoid complications of transcatheter arterial chemoembolization. Radiographics 2005;25 Suppl 1:S25-39.
Lee AJ, Gomes AS, Liu DM, Kee ST, Loh CT, McWilliams JP, et al.
The road less traveled: Importance of the lesser branches of the celiac axis in liver embolotherapy. Radiographics 2012;32:1121-32.
Ozbülbül NI. CT angiography of the celiac trunk: Anatomy, variants and pathologic findings. Diagn Interv Radiol 2011;17:150-7.
Liu PS, Platt JF. CT angiography in the abdomen: A pictorial review and update. Abdom Imaging 2014;39:196-214.
So YH, Chung JW, Yin Y, Jae HJ, Jeon UB, Cho BH, et al.
The right inferior phrenic artery: Origin and proximal anatomy on digital subtraction angiography and thin-section helical computed tomography. J Vasc Interv Radiol 2009;20:1164-71.
Tajima T, Honda H, Kuroiwa T, Yabuuchi H, Okafuji T, Yosimitsu K, et al.
Pulmonary complications after hepatic artery chemoembolization or infusion via the inferior phrenic artery for primary liver cancer. J Vasc Interv Radiol 2002;13:893-900.
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9], [Figure 10], [Figure 11], [Figure 12], [Figure 13], [Figure 14]
[Table 1], [Table 2]