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Spinal Arterial Blood Supply Does Not Arise from the Bronchial Arteries: A Detailed Analysis of Angiographic Studies Performed for Hemoptysis
CLINICAL STUDY
Spinal Arterial Blood Supply Does Not Arise from the Bronchial Arteries: A Detailed Analysis of Angiographic Studies Performed for Hemoptysis Nicholas T. Befera, MD, James Ronald, MD, PhD, Charles Y. Kim, MD, and Tony P. Smith, MD
ABSTRACT Purpose: To determine the angiographic prevalence of spinal arteries originating directly from the bronchial arteries in the setting of embolization for hemoptysis. Materials and Methods: Over a 14-year interval, 205 patients underwent angiography for hemoptysis. Twenty-five patients were excluded because their bronchial arteries were not visualized. The remaining 180 patients underwent a total of 254 angiographic procedures (range, 1–8 per patient). Images were reviewed jointly by 2 interventional radiologists with formal fellowship training in both peripheral and neurological interventional radiology. All catheterized arteries were evaluated for arterial contribution to the spinal cord. For patients with multiple studies, each unique artery was reported only once. Embolization was performed during at least 1 procedure in 158 patients (88%). Electronic record review was used to assess neurological sequelae after the procedure. Results: One or 2 bronchial arteries originating from the aorta were identified in 57 patients (32%) on the right and in 75 patients (42%) on the left. Conjoined bronchial arteries were found in 76 patients (42%). Spinal arterial supply was absent in all. A total of 102 patients (57%) had at least 1 right and 11 patients (6%) at least 1 left intercostobronchial artery. Spinal arterial supply from the intercostal portion of an intercostobronchial artery was found in 6 patients (5 right, 1 left). Medical record review revealed no postprocedure symptoms referable to spinal cord injury in any patient. Conclusions: Spinal arterial supply does not originate directly from the bronchial artery but can originate from the intercostal portion of an intercostobronchial artery.
Bronchial artery embolization has been shown to be a reasonably efficacious treatment for hemoptysis (1–3). Although there are a number of possible complications from this procedure, spinal cord ischemia remains the most dreaded. Since its inception, the peripheral interventional teaching has been that spinal cord supply may originate
From the Division of Interventional Radiology, Department of Radiology, Duke University Medical Center, 1502 Erwin Road, Box 3838, Durham, NC 27710. Received May 15, 2019; final revision received June 27, 2019; accepted July 15, 2019. Address correspondence to T.P.S.; E-mail: [email protected] Current address for N.T.B.: Diversified Radiology of Colorado, 1746 Cole Boulevard, Suite 150, Lakewood, CO 80401. None of the authors have identified a conflict of interest. From the SIR 2019 Annual Scientific Meeting. © SIR, 2019 J Vasc Interv Radiol 2019; ▪:1–7 https://doi.org/10.1016/j.jvir.2019.07.033
directly from the bronchial arteries, resulting in neurological complications if inadvertently embolized (4–6). However, that line of thought is in conflict with the neurological interventional practice, which does not include selective bronchial artery contrast injections as part of complete spinal angiography (7). The purpose of the present study was to adjudicate these contradictory notions by retrospectively reviewing a large single-center bronchial angiography experience by interventional radiologists formally trained in both peripheral and neurological interventions, in order to determine the presence or absence of spinal cord supply originating from the bronchial arteries.
MATERIALS AND METHODS The local Institutional Review Board approved this study, and a waiver for informed written consent was obtained. The senior author (T.P.S.) wrote the first draft of the manuscript, the second author performed the statistical analysis (J.R.), and all authors vouch for the data and its analysis.
2 ▪ Angiographic Studies Performed for Hemoptysis
EDITORS’ RESEARCH HIGHLIGHTS The prevalence of spinal artery supply from bronchial arteries was studied in 180 patients using angiographically demonstrated bronchial arteries: No spinal artery supply was found from any bronchial artery. Spinal artery supply was seen from the intercostobronchial trunk beyond the origin of bronchial artery in approximately 5% of patients. It may be safe to embolize the bronchial artery for treatment of hemoptysis without any concerns about inadvertent spinal artery embolization. The intercostobronchial trunk should be embolized beyond the origin of the intercostal artery.
The interventional radiology database and the institutional electronic medical record system were queried for all patients who underwent bronchial angiography from November 2004 to October 2018 (total interval of 14 years), which was the period in which complete angiographic studies were consistently available for review on the picture archiving and communication system. Information collected from the institutional electronic medical record included indication for angiography, angiographic technique and findings, sex and age of the patient, and any neurological complications referable to the procedure up to 30 days. Only neurological complications were gathered for this report. Arteries were accessed from a common femoral route in all patients. All studies were individualized to a particular patient based on degree and laterality of symptoms; preprocedural endoscopy and imaging if performed; and review of all prior angiography, if existing. Thoracic aortography was performed at least once in 115 patients at the discretion of the interventionist. Selective catheterization was individualized to each particular patient’s clinical situation. Specifically, all bronchial arteries may not have been sought if not clinically indicated. A total of 205 unique patients underwent angiography of the systemic arterial supply to the lungs for hemoptysis during the study interval. All angiographic images of the 205 patients were reviewed using a dedicated picture archiving and communication system by 2 radiologists with fellowship training in both peripheral and neurological interventional radiology (T.P.S., 28 years, and N.T.B., 2 years of practice). Images were reviewed jointly, and decisions were reached by consensus. Twenty-five patients were excluded because the bronchial arteries were not identified, leaving a total of 180 patients as the study population. This population consisted of 101 males and 79 females. The mean age was 52.3 years old (range, 12–91 years; median, 54 years of age, including 6 patients younger than 18 years of age, as follows: 12, 15, 15, 16, 17, 17 years). A total of 254 angiographic procedures were performed in these 180 patients, ranging from 1 to 8 per patient, as
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follows: 134 patients received 1 procedure, 31 received 2, 8 received 3, 4 received 4, 2 received 5, and 1 patient underwent 8 angiographic procedures. For the 46 patients who received 2 or more angiographic studies, all images were compared among studies to ensure that each unique artery was reported only once, regardless of the number of times it was catheterized, studied, or treated. However, each angiographic study was reviewed in its entirety to determine presence of spinal arterial contribution. A bronchial artery was defined as a vessel originating from the aorta and supplying bronchial and lung tissue. An intercostobronchial artery (also known as intercostobronchial trunk) was defined as an intercostal artery that gave rise to a bronchial artery supplying bronchial and lung tissue. Spinal arteries were angiographically identified based on course, size, and configuration (8). When more than 1 angiographic view was available, the spinal artery was to overlay the spinal canal on all views. Provocative agents or somatosensory evoked potentials (9) to confirm spinal cord arterial supply were not used in any patients. Whether a particular vessel provided arterial supply to the spinal cord was determined by consensus of both image reviewers. Information collected included vessels angiographically evaluated, presence or absence of suspected spinal arterial contribution, and vessel embolization. Embolization was performed of at least 1 artery in 158 patients (88%). Bronchial artery embolization was not performed in 22 patients due to small bronchial artery size (21 patients), or vessel dissection (3 patients), or both (2 patients). Embolization was performed using polyvinyl alcohol (PVA) particles in all but 3 embolization procedures where coils alone were used. N-butyl cyanoacrylate was used additionally in 4 procedures and ethylene vinyl alcohol in 1. Descriptive statistical analyses were performed using a commonly used statistical spreadsheet (Excel software; Microsoft, Redmond, Washington). Quantitative variables were summarized by their means, medians, standard deviations, and ranges. Qualitative variables were summarized by counts and percentages. Confidence intervals (CI) for percentages were derived from the binomial distribution.
RESULTS The number of unique vessels studied in 180 patients is summarized in Table 1. Right and left bronchial arteries were identified by consensus in 57 (32%) and 75 patients (42%), respectively. Eight patients had 2 right-sided bronchial arteries, and 8 patients had 2 left-sided bronchial arteries. A conjoined bronchial artery supplying both the right and left lungs was found in 76 patients (42%). Seventy-two of those patients had a single conjoined artery, and 4 patients had 2 conjoined arteries. There was no arterial supply to the spinal cord originating from any bronchial artery (0 of 308 [0%]; 95% CI, 0%–1.1%). A right-sided intercostobronchial artery was found in 102 patients (57%), with 5 patients
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Table 1. Vessels Identified and Embolized No. of Patients
Table 1. Vessels Identified and Embolized (continued)
No. of Arteries
Right bronchial 0
123
0
–
1
49
49
38
2 total Left bronchial
8
16
13
180
65
51
0
105
0
–
1
67
67
43
2
8
16
16
180
87
69
0
104
0
–
1 2
72 4
72 8
60 4
180
80
64*
0
78
0
–
1
97
97
77
2
5
10
180
107
82
total
No. of Patients
No. Embolized Right thyrocervical branches 0 1 Left thyrocervical branches 0 1 Right vertebral 0 1 Left vertebral 0 Total
No. of Arteries
No. Embolized
176 4
0 4
– 2
177 3
0 3
– 1
179 1
0 1
– 0
180 180
0 692
– 336
Conjoined bronchial
total Right intercostobronchial
total Left intercostobronchial 0
8†
169
0
–
1
10
10
8
2
1
2
1
180
12
9
total Right intercostal 0
94
0
–
1
40
40
4
2 3
19 12
36 36
8 4
4
7
28
0
5
6
30
7
6
2
12
2
180
182
25
total Left intercostal 0
99
0
–
1 2
44 12
44 24
6 1
3
12
36
4
4
7
28
8
5
4
20
3
7
1
7
0
10
1
10
4
180
169
26
172
0
–
8
8
5
0
178
0
–
1
2
2
total Right costocervical branches 0 1 Left costocervical branches
2 continued
Note–Thyrocervical and costocervical were injected for angiography, and embolization was performed subselectively. *At least 1 of the 2 arteries was embolized. † Two arteries were embolized in 3 patients and 1 in 2 patients.
having 2 intercostobronchial arteries. Eleven patients had left-sided intercostobronchial arteries, with a single patient having 2. There was no arterial supply to the spinal cord identified from the bronchial component of any intercostobronchial artery (0 of 118 [0%]; 95% CI, 0%–3%). Thirty two arterial contributions to the spinal cord were identified in 29 patients by consensus of both reviewers (Table 2). There was conventional spinal arterial supply originating from the intercostal arteries in 23 patients, 7 from the right and 16 from the left. Spinal arterial supply arising from the intercostal portion of an intercostobronchial artery was found in 6 patients, 5 from the right, 1 from the left. Two of those patients also had intercostal supply included in the numbers above. Two patients had spinal cord supply originating from the right costocervical artery and 1 from the left thyrocervical artery, although neither trunk included arterial contributions to the lungs. The radicular branches and the spinal arteries were subjectively larger when the origin was the intercostal versus intercostobronchial, costocervical, or thyrocervical in origin (Figs 1, 2). Embolization of the bronchial artery and collateral arterial supply was performed in 336 arteries in 158 patients, whereas 22 received no embolization (Table 1). A total of 51 right and 69 left bronchial arteries were embolized. For patients with conjoined bronchial arteries, 64 had at least 1 of the arteries embolized. For the right intercostobronchial artery, a total of 82 arteries were embolized versus 9 for the left. All 5 right intercostobronchial arteries with spinal supply were embolized using PVA particles ranging in size from 150 to 700 μm (150–250 μm in 1; 300–500 μm in 3; and 500–700 μm in 1). All patients were embolized using a microcatheter placed distal to the spinal artery origin (Fig 2). The single, left intercostobronchial artery with spinal supply was not embolized as hemoptysis symptoms were clinically confined to the right. A single, left intercostal artery giving rise to spinal supply and collateral arterial supply to the lung was embolized, with PVA particles ranging in size from 355 to 500 μm
4 ▪ Angiographic Studies Performed for Hemoptysis
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Table 2. Spinal Arteries Origin of spinal arteries
No. of spinal radicular arteries
No. embolized
Intercostal artery Right
7
0
16
1
5 1
5 0
Right
2
0
Left
0
0
Right
0
0
Left
1
0
32
6
Left Intercostobronchial artery Right Left Costocervical artery
Thyrocervical artery
Total
Note–A total of 29 patients had 32 radicular arteries giving rise to spinal cord supply (1 patient had 2 radicular arteries from the left intercostal artery, 1 patient had a radicular artery from the right intercostobronchial artery and a right intercostal artery, and 1 patient had a radicular artery from the left intercostal artery and left thyrocervical artery.
through a microcatheter placed distal to the origin of the spinal artery without neurological complication (Fig 3). A total of 75 patients remained alive as of the writing of this report. Between day 1 and day 3,717 (mean, 305 days), 103 patients died. Nine patients died within 48 hours after the procedure. Two patients were lost to follow-up. Given the focus of this study, only neurological complications were evaluated, and these were noted in only 2 patients. The first patient, a 73-year-old male complained of right leg weakness following his angiogram and embolization. The patient had a right common femoral artery access and an extensive embolization consisting of a left bronchial artery, a conjoined bronchial artery as well as left and right intercostobronchial arteries. No spinal arterial supply was noted at the time of the embolization or on review for this study. A neurology consult 1 day after the procedure concluded this represented a lumbosacral plexopathy. No spinal imaging was obtained at that time. The patient was seen as an outpatient 6 months later. MR imaging of the cervical and thoracic spine and peripheral nerve conduction studies were performed and were negative for any evidence of spinal cord ischemia. The second patient, a 52-year-old male with atherosclerotic disease, underwent embolization of bilateral bronchial arteries without complication. However, the patient required a second procedure 4 days later for recurrent hemorrhage. No therapeutic embolization was carried out; however, extensive catheterization of the proximal great vessels resulted in a neurological deficit. MR imaging confirmed scattered ischemic areas in the left cerebral and cerebellar hemispheres indicative of embolization from atherosclerotic disease of the arch. No other patients had neurologic symptoms.
Figure 1. A 72-year-old male presented with squamous cell carcinoma after left lower lobectomy and left upper lobe wedge resection, now with hemoptysis and consolidative opacities throughout the residual left lung. Bronchial artery angiography and embolization was performed which included angiography of the left thoracic-9 intercostal artery (white arrows) showing a normal arteria radicularis magna (aka, artery of Adamkiewicz [black arrows]). Note the size and configuration of the anterior spinal artery including the classic hairpin turn. Minimal supply to the left lung was noted from this intercostal, and embolization was not performed.
DISCUSSION Selective bronchial angiography was first described in 1964 by Viamonte (10), in a study of 32 patients. One year later, Feigelson and Ravin (11) published the first report of transverse myelitis after bronchial artery angiography. Those authors reported selective injection of the right fifth intercostal artery with visualization of adjacent intercostals described as an intercostobronchial artery. Spinal supply was not identified, but the patient developed bilateral lower extremity symptoms after the procedure, including weakness which improved significantly over the following month. The authors speculated that the complication was due to the use of an abundance of ionic contrast material. Today, transverse myelopathy from diagnostic spinal angiography has all but disappeared since the introduction of nonionic contrast materials (12). In 1973, Remy et al (13) first reported embolization of the bronchial arteries in 4 patients, followed by Wholey et al (4) in 5 patients 3 years later. Neither series reported spinal cord complications. However, 1 of the 5 patients in the latter study was not embolized due to the close relationship between the posterior radicular branch and the anterior spinal artery through collateralization from the bronchial artery based on the authors’ description. Currently, most bronchial artery embolization results in the peripheral literature warn of possible spinal cord complications, having occurred in up
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Figure 2. A 71-year-old male presented with diffuse alveolar hemorrhage. (a) Selective injection was performed using a 5-F catheter through a right intercostobronchial artery. The bronchial branch (white arrow) and intercostal branches (black arrowhead) are well noted. A small linear artery (black arrows) is superimposed over the spine, possibly representing the spinal arterial supply. (b) Contrast material was injected through a microcatheter (white arrow at tip) placed super-selectively in the bronchial artery (black arrow). Embolization using 500- to 710-μm polyvinyl alcohol particles was performed. (c) Contrast injected through the microcatheter into the intercostobronchial artery shows the occluded bronchial artery (white arrow) as well as filling of a spinal artery (black arrows) through the patent intercostal branches. Note the classic mid-line artery and hairpin configuration.
Figure 3. A 45-year-old female presented with aspergillosis and hemoptysis. (a) Contrast injection through the left thoracic (T)-5 intercostal artery (arrows) shows some collateral supply to the lungs. No arterial supply to the spine is noted. (b) A microcatheter placed in the proximal T-5 intercostal artery and pulmonary venous drainage (black arrows) confirm significant arterial contribution to the lungs. The intercostal artery was embolized using 355- to 500-μm polyvinyl alcohol particles to stasis. (c) A postembolization angiography through the microcatheter in the proximal intercostal artery shows the occluded distal intercostal (white arrow) and filling of the spinal artery (black arrows).
to 6% of cases in a single study (2,5,14,15). In their publication, Mal et al (15) reported spinal cord complications in 3 of 46 patients undergoing bronchial artery embolization. Those complications included Brown-Sequard syndrome that regressed after 4 months without sequelae, paraparesis with spontaneous regression after 2 weeks, and complete paraplegia without regression. However, based on the anatomic origins of the blood supply to the spinal cord, selective angiography of solely a bronchial artery should not demonstrate spinal artery supply. Neurointerventional reports consistently state that complete spinal angiography encompasses selective bilateral arteriography of the external carotid, vertebral, and subclavian and its proximal branches (thyrocervical and costocervical), intercostals at all levels, median sacral artery, and internal iliac arteries (7). No neurologically based source includes selective injection of the bronchial arteries. It is therefore
puzzling how to rectify the differences in the peripheral and neurological reports. The present publication proposes that the arterial supply to the spinal cord originates from intercostal arteries, as expected, but that the same intercostal artery may additionally give rise to a bronchial artery. To that point, in the current study of 180 patients who underwent 254 angiographic studies, no bronchial artery that originated directly from the aorta was found to provide any radiographically demonstrable arterial supply to the spinal cord. Furthermore, no spinal arterial supply was identified from the bronchial component of any intercostobronchial artery. These findings were also supported by a lack of neurological sequelae from selective bronchial artery embolization. Spinal arterial supply was identified from the intercostal arteries, as well as from the intercostal portion of intercostobronchial arteries.
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Although the current study reports the absence of arterial contribution to the spinal cord from the bronchial artery, this is not the first publication to mention such considerations. Remy et al (16) in a 1977 review of 104 patients found the presence of supply to the anterior spinal artery arising from the cervicointercostal trunk, from an intercostal artery and from an intercostobronchial trunk, which in their opinion constituted an absolute contraindication to embolization. Bookstein et al (17) in that same year also suggested the source of embolic injury to the spine might have been the right intercostobronchial trunk. It was proposed by Marshal and Jackson in 1997 (18) that spinal supply may originate from the intercostobronchial artery and was, fortunately, more common than direct supply from the bronchial artery, implying that such direct bronchial supply does rarely exist. Similarly, in a systematic review of studies published between 1976 and 2016, Panda et al (1) concluded that spinal cord ischemia leading to transient or permanent paraparesis could be attributed to inadvertent embolization of spinal arteries arising from bronchial or intercostobronchial arteries. The current study found the existence of a right intercostobronchial artery in 57% of the patients. This is clearly in agreement with the study by Kocbek and Rakusa (19) who performed dissections in 43 cadavers and found the right bronchial artery originated from the second to the fifth posterior intercostal artery in 58% of cases. It is generally held that spinal cord issues from bronchial artery embolization procedures have deceased over time (1,5,20). This is perhaps attributable to the present widespread use of nonionic contrast material and subselective catheterization of the bronchial artery for embolization (21). Early embolization was performed using 5-F or larger catheters and would clearly increase the likelihood of occlusion of a spinal artery originating from an intercostobronchial artery (21,22). Additionally, such large catheters may not seat well in the bronchial artery origin, thus heightening the possibility for reflux, particularly when coupled with comparatively lower quality fluoroscopy/imaging (22,23). Such reflux could readily track into a more inferiorly located intercostal artery that, in turn, gives rise to the principle arterial supply to the lower thoracic anterior spinal artery (arteria radicularis magna; aka, the artery of Adamkiewicz) (Fig 1). The latter usually arises from the thoracic T6–T12 level and thus at or closely inferior to most bronchial arteries, which generally arise at the T5– T6 level (24). In patients in the current study in whom the spinal artery was visualized through intercostobronchial origin, the appearance of the radicular and spinal arteries was subjectively smaller (Fig 1, 2) than that of the arteria radicularis magna and corresponding anterior spinal artery (Fig 3). To that end, neurological complications from bronchial artery embolization have been reported even when the spinal supply is not angiographically visualized (25,26). This clearly supports the need to selectively catheterize the bronchial artery as distally as possible to achieve both an
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adequate embolization and prevent reflux into the intercostal artery which may give rise to spinal cord supply. This study has a number of limitations. It is a retrospective study, thus, much of the imaging was less than ideal to definitively determine spinal cord arterial supply. The image reviewers arrived at decisions by consensus but were often limited to single radiographic views. Although all patients were inpatients, follow-up might not have mentioned a neurologic examination specifically. Additionally, 9 patients died within 48 hours of the bronchial procedure due to their underlying illnesses. All bronchial and intercostal arteries were not systematically studied in all patients, but rather selection was based on a particular patient’s clinical needs. The imaging reviewers chose to limit the search to bronchial arteries originating from the aorta, although all vessels injected were reviewed for spinal supply including the intercostal and intercostobronchial arteries. In conclusion, the spinal cord arterial supply originated from conventional sites in all patients undergoing angiography in the current study. These conventional sites included intercostal arteries and the intercostal portion of intercostobronchial arteries. No bronchial artery contributed supply to the spinal cord by either image review or presence of spinal cord neurological symptoms following bronchial artery embolization.
REFERENCES 1. Panda A, Bhalla AS, Goyal A. Bronchial artery embolization in hemoptysis: a systematic review. Diagn Interv Radiol 2017; 23:307–317. 2. Shao H, Wu J, Wu Q, Sun X, Xing Z, Sun H. Bronchial artery embolization for hemoptysis: a retrospective observation study of 344 patients. Chinese Med J 2015; 128:58–62. 3. Han K, Yoon KW, Kim JH, Kim GM. Bronchial artery embolization for hemoptysis in primary lung cancer: a retrospective review of 84 patients. J Vasc Interv Radiol 2019; 30:428–434. 4. Wholey MH, Chamorro HA, Rao G, Ford WB, Miller WN. Bronchial artery embolization for massive hemoptysis. JAMA 1976; 236:2501–2504. 5. Sidhu M, Wieseler K, Burdick TR, Shaw DWW. Bronchial artery embolization for hemoptysis. Semin Intervent Radiol 2008; 25:310–318. 6. Brown AC, Ray CE. Anterior spinal cord infarction following bronchial artery embolization. Semin Intervent Radiol 2012; 29:241–244. 7. Morris P. Practical neuroangiography. In: Spinal Angiography: Technical Aspects. 3rd edition. Philadelphia: Lippincott Williams & Wilkins; 2013. p. 52–57. 8. Santillan A, Nacarino V, Greenberg E, Riina HA, Gobin YP, Patsalides A. Vascular anatomy of the spinal cord. J Neurointerv Surg 2012; 4:67–74. 9. Schrodt JE, Becker GJ, Scott JA, Warren CH, Benenati SV. Bronchial artery embolization: monitoring with somatosensory evoked potentials work in progress. Radiology 1987; 164:135–139. 10. Viamonte M. Selective bronchial angiography in man. Radiology 1964; 83: 830–839. 11. Feigelson HH, Ravin HA. Transverse myelitis following selective bronchial arteriography. Radiology 1965; 85:663–665. 12. Chen J, Gailloud P. Safety of spinal angiography: complication rate analysis of 302 diagnostic angiograms. Neurology 2011; 77:1235–1240. my J, Voisin C, Ribet M, et al. Treatment, by embolization, of severe or 13. Re repeated hemoptysis associated with systemic hypervascularization. Nouv Presse Med 1973; 8:2060. 14. Sopko DR, Smith TP. Bronchial artery embolization for hemoptysis. Semin Intervent Radiol 2011; 28:48–62. 15. Mal H, Rullon I, Mellot F, et al. Immediate and long-term results of bronchial artery embolization for life-threatening hemoptysis. Chest 1999; 115:996–1001.
Volume ▪ ▪ Number ▪ ▪ Month ▪ 2019 my J, Arnaud A, Fardou H, Giraud R, Voisin C. Treatment of hemop16. Re tysis by embolization of bronchial arteries. Radiology 1977; 122:33–37. 17. Bookstein JJ, Moser KM, Kalafer ME, et al. The role of bronchial arteriography and therapeutic embolization in hemoptysis. Chest 1977; 72:658–661. 18. Marshall TJ, Jackson JE. Vascular intervention in the thorax: bronchial artery embolization for hemoptysis. Eur Radiol 1997; 7:1221–1227. 19. Kocbek L, Rakusa M. The right intercostobronchial trunk: anatomical study in respect of posterior intercostal artery origin and its clinical application. Surg Radiol Anat 2018; 40:67–73. 20. Zuckerman D, Marks C. Arteriography and endovascular intervention in the lungs. In: Pua BB, Covey AM, Madoff DC, editors. Interventional Radiology: Fundamentals of Clinical Practice. New York: Oxford University Press; 2019. p. 341–350. 21. Tanaka N, Yamaladp K, Takeda K, et al. Superselective bronchial artery embolization for hemoptysis with a coaxial microcatheter system. J Vasc Intervent Radiol 1997; 8:65–70.
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22. Swanson KL, Johnson M, Prakash UBS, McKusic MA, Andrews JC, Stanson AW. Bronchial artery embolization: experience with 54 patients. Chest 2002; 121:789–795. 23. Fraser KL, Grossman Hyland RH, Tullis DE. Transverse myelitis: a reversible complication of bronchial artery embolisation in cystic fibrosis. Thorax 1997; 52:99–101. 24. Hoehmann CL, Hitscherich K, Cuoco JA. The artery of Adamkiewicz: vascular anatomy, clinical significance and surgical considerations. Int J Cardiovasc Res 2016; 5:1–5. 25. Ramakantan R, Bandekar VG, Gandhi MS, Aulakh BG, Deshmukh HL. Massive hemoptysis due to pulmonary tuberculosis: control with bronchial artery embolization. Radiology 1996; 200:691–694. 26. Wang GR, Ensor JE, Gupta S, Hicks ME, Tam AL. Bronchial artery embolization for the management of hemoptysis in oncology patients: utility and prognostic factors. J Vasc Interv Radiol 2009; 20: 722–729.
Spinal Arterial Blood Supply Does Not Arise from the Bronchial Arteries: A Detailed Analysis of Angiographic Studies Performed for Hemoptysis Nicholas T. Befera, MD, James Ronald, MD, PhD, Charles Y. Kim, MD, and Tony P. Smith, MD
ABSTRACT Purpose: To determine the angiographic prevalence of spinal arteries originating directly from the bronchial arteries in the setting of embolization for hemoptysis. Materials and Methods: Over a 14-year interval, 205 patients underwent angiography for hemoptysis. Twenty-five patients were excluded because their bronchial arteries were not visualized. The remaining 180 patients underwent a total of 254 angiographic procedures (range, 1–8 per patient). Images were reviewed jointly by 2 interventional radiologists with formal fellowship training in both peripheral and neurological interventional radiology. All catheterized arteries were evaluated for arterial contribution to the spinal cord. For patients with multiple studies, each unique artery was reported only once. Embolization was performed during at least 1 procedure in 158 patients (88%). Electronic record review was used to assess neurological sequelae after the procedure. Results: One or 2 bronchial arteries originating from the aorta were identified in 57 patients (32%) on the right and in 75 patients (42%) on the left. Conjoined bronchial arteries were found in 76 patients (42%). Spinal arterial supply was absent in all. A total of 102 patients (57%) had at least 1 right and 11 patients (6%) at least 1 left intercostobronchial artery. Spinal arterial supply from the intercostal portion of an intercostobronchial artery was found in 6 patients (5 right, 1 left). Medical record review revealed no postprocedure symptoms referable to spinal cord injury in any patient. Conclusions: Spinal arterial supply does not originate directly from the bronchial artery but can originate from the intercostal portion of an intercostobronchial artery.
Bronchial artery embolization has been shown to be a reasonably efficacious treatment for hemoptysis (1–3). Although there are a number of possible complications from this procedure, spinal cord ischemia remains the most dreaded. Since its inception, the peripheral interventional teaching has been that spinal cord supply may originate
From the Division of Interventional Radiology, Department of Radiology, Duke University Medical Center, 1502 Erwin Road, Box 3838, Durham, NC 27710. Received May 15, 2019; final revision received June 27, 2019; accepted July 15, 2019. Address correspondence to T.P.S.; E-mail: [email protected] Current address for N.T.B.: Diversified Radiology of Colorado, 1746 Cole Boulevard, Suite 150, Lakewood, CO 80401. None of the authors have identified a conflict of interest. From the SIR 2019 Annual Scientific Meeting. © SIR, 2019 J Vasc Interv Radiol 2019; ▪:1–7 https://doi.org/10.1016/j.jvir.2019.07.033
directly from the bronchial arteries, resulting in neurological complications if inadvertently embolized (4–6). However, that line of thought is in conflict with the neurological interventional practice, which does not include selective bronchial artery contrast injections as part of complete spinal angiography (7). The purpose of the present study was to adjudicate these contradictory notions by retrospectively reviewing a large single-center bronchial angiography experience by interventional radiologists formally trained in both peripheral and neurological interventions, in order to determine the presence or absence of spinal cord supply originating from the bronchial arteries.
MATERIALS AND METHODS The local Institutional Review Board approved this study, and a waiver for informed written consent was obtained. The senior author (T.P.S.) wrote the first draft of the manuscript, the second author performed the statistical analysis (J.R.), and all authors vouch for the data and its analysis.
2 ▪ Angiographic Studies Performed for Hemoptysis
EDITORS’ RESEARCH HIGHLIGHTS The prevalence of spinal artery supply from bronchial arteries was studied in 180 patients using angiographically demonstrated bronchial arteries: No spinal artery supply was found from any bronchial artery. Spinal artery supply was seen from the intercostobronchial trunk beyond the origin of bronchial artery in approximately 5% of patients. It may be safe to embolize the bronchial artery for treatment of hemoptysis without any concerns about inadvertent spinal artery embolization. The intercostobronchial trunk should be embolized beyond the origin of the intercostal artery.
The interventional radiology database and the institutional electronic medical record system were queried for all patients who underwent bronchial angiography from November 2004 to October 2018 (total interval of 14 years), which was the period in which complete angiographic studies were consistently available for review on the picture archiving and communication system. Information collected from the institutional electronic medical record included indication for angiography, angiographic technique and findings, sex and age of the patient, and any neurological complications referable to the procedure up to 30 days. Only neurological complications were gathered for this report. Arteries were accessed from a common femoral route in all patients. All studies were individualized to a particular patient based on degree and laterality of symptoms; preprocedural endoscopy and imaging if performed; and review of all prior angiography, if existing. Thoracic aortography was performed at least once in 115 patients at the discretion of the interventionist. Selective catheterization was individualized to each particular patient’s clinical situation. Specifically, all bronchial arteries may not have been sought if not clinically indicated. A total of 205 unique patients underwent angiography of the systemic arterial supply to the lungs for hemoptysis during the study interval. All angiographic images of the 205 patients were reviewed using a dedicated picture archiving and communication system by 2 radiologists with fellowship training in both peripheral and neurological interventional radiology (T.P.S., 28 years, and N.T.B., 2 years of practice). Images were reviewed jointly, and decisions were reached by consensus. Twenty-five patients were excluded because the bronchial arteries were not identified, leaving a total of 180 patients as the study population. This population consisted of 101 males and 79 females. The mean age was 52.3 years old (range, 12–91 years; median, 54 years of age, including 6 patients younger than 18 years of age, as follows: 12, 15, 15, 16, 17, 17 years). A total of 254 angiographic procedures were performed in these 180 patients, ranging from 1 to 8 per patient, as
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follows: 134 patients received 1 procedure, 31 received 2, 8 received 3, 4 received 4, 2 received 5, and 1 patient underwent 8 angiographic procedures. For the 46 patients who received 2 or more angiographic studies, all images were compared among studies to ensure that each unique artery was reported only once, regardless of the number of times it was catheterized, studied, or treated. However, each angiographic study was reviewed in its entirety to determine presence of spinal arterial contribution. A bronchial artery was defined as a vessel originating from the aorta and supplying bronchial and lung tissue. An intercostobronchial artery (also known as intercostobronchial trunk) was defined as an intercostal artery that gave rise to a bronchial artery supplying bronchial and lung tissue. Spinal arteries were angiographically identified based on course, size, and configuration (8). When more than 1 angiographic view was available, the spinal artery was to overlay the spinal canal on all views. Provocative agents or somatosensory evoked potentials (9) to confirm spinal cord arterial supply were not used in any patients. Whether a particular vessel provided arterial supply to the spinal cord was determined by consensus of both image reviewers. Information collected included vessels angiographically evaluated, presence or absence of suspected spinal arterial contribution, and vessel embolization. Embolization was performed of at least 1 artery in 158 patients (88%). Bronchial artery embolization was not performed in 22 patients due to small bronchial artery size (21 patients), or vessel dissection (3 patients), or both (2 patients). Embolization was performed using polyvinyl alcohol (PVA) particles in all but 3 embolization procedures where coils alone were used. N-butyl cyanoacrylate was used additionally in 4 procedures and ethylene vinyl alcohol in 1. Descriptive statistical analyses were performed using a commonly used statistical spreadsheet (Excel software; Microsoft, Redmond, Washington). Quantitative variables were summarized by their means, medians, standard deviations, and ranges. Qualitative variables were summarized by counts and percentages. Confidence intervals (CI) for percentages were derived from the binomial distribution.
RESULTS The number of unique vessels studied in 180 patients is summarized in Table 1. Right and left bronchial arteries were identified by consensus in 57 (32%) and 75 patients (42%), respectively. Eight patients had 2 right-sided bronchial arteries, and 8 patients had 2 left-sided bronchial arteries. A conjoined bronchial artery supplying both the right and left lungs was found in 76 patients (42%). Seventy-two of those patients had a single conjoined artery, and 4 patients had 2 conjoined arteries. There was no arterial supply to the spinal cord originating from any bronchial artery (0 of 308 [0%]; 95% CI, 0%–1.1%). A right-sided intercostobronchial artery was found in 102 patients (57%), with 5 patients
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Table 1. Vessels Identified and Embolized No. of Patients
Table 1. Vessels Identified and Embolized (continued)
No. of Arteries
Right bronchial 0
123
0
–
1
49
49
38
2 total Left bronchial
8
16
13
180
65
51
0
105
0
–
1
67
67
43
2
8
16
16
180
87
69
0
104
0
–
1 2
72 4
72 8
60 4
180
80
64*
0
78
0
–
1
97
97
77
2
5
10
180
107
82
total
No. of Patients
No. Embolized Right thyrocervical branches 0 1 Left thyrocervical branches 0 1 Right vertebral 0 1 Left vertebral 0 Total
No. of Arteries
No. Embolized
176 4
0 4
– 2
177 3
0 3
– 1
179 1
0 1
– 0
180 180
0 692
– 336
Conjoined bronchial
total Right intercostobronchial
total Left intercostobronchial 0
8†
169
0
–
1
10
10
8
2
1
2
1
180
12
9
total Right intercostal 0
94
0
–
1
40
40
4
2 3
19 12
36 36
8 4
4
7
28
0
5
6
30
7
6
2
12
2
180
182
25
total Left intercostal 0
99
0
–
1 2
44 12
44 24
6 1
3
12
36
4
4
7
28
8
5
4
20
3
7
1
7
0
10
1
10
4
180
169
26
172
0
–
8
8
5
0
178
0
–
1
2
2
total Right costocervical branches 0 1 Left costocervical branches
2 continued
Note–Thyrocervical and costocervical were injected for angiography, and embolization was performed subselectively. *At least 1 of the 2 arteries was embolized. † Two arteries were embolized in 3 patients and 1 in 2 patients.
having 2 intercostobronchial arteries. Eleven patients had left-sided intercostobronchial arteries, with a single patient having 2. There was no arterial supply to the spinal cord identified from the bronchial component of any intercostobronchial artery (0 of 118 [0%]; 95% CI, 0%–3%). Thirty two arterial contributions to the spinal cord were identified in 29 patients by consensus of both reviewers (Table 2). There was conventional spinal arterial supply originating from the intercostal arteries in 23 patients, 7 from the right and 16 from the left. Spinal arterial supply arising from the intercostal portion of an intercostobronchial artery was found in 6 patients, 5 from the right, 1 from the left. Two of those patients also had intercostal supply included in the numbers above. Two patients had spinal cord supply originating from the right costocervical artery and 1 from the left thyrocervical artery, although neither trunk included arterial contributions to the lungs. The radicular branches and the spinal arteries were subjectively larger when the origin was the intercostal versus intercostobronchial, costocervical, or thyrocervical in origin (Figs 1, 2). Embolization of the bronchial artery and collateral arterial supply was performed in 336 arteries in 158 patients, whereas 22 received no embolization (Table 1). A total of 51 right and 69 left bronchial arteries were embolized. For patients with conjoined bronchial arteries, 64 had at least 1 of the arteries embolized. For the right intercostobronchial artery, a total of 82 arteries were embolized versus 9 for the left. All 5 right intercostobronchial arteries with spinal supply were embolized using PVA particles ranging in size from 150 to 700 μm (150–250 μm in 1; 300–500 μm in 3; and 500–700 μm in 1). All patients were embolized using a microcatheter placed distal to the spinal artery origin (Fig 2). The single, left intercostobronchial artery with spinal supply was not embolized as hemoptysis symptoms were clinically confined to the right. A single, left intercostal artery giving rise to spinal supply and collateral arterial supply to the lung was embolized, with PVA particles ranging in size from 355 to 500 μm
4 ▪ Angiographic Studies Performed for Hemoptysis
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Table 2. Spinal Arteries Origin of spinal arteries
No. of spinal radicular arteries
No. embolized
Intercostal artery Right
7
0
16
1
5 1
5 0
Right
2
0
Left
0
0
Right
0
0
Left
1
0
32
6
Left Intercostobronchial artery Right Left Costocervical artery
Thyrocervical artery
Total
Note–A total of 29 patients had 32 radicular arteries giving rise to spinal cord supply (1 patient had 2 radicular arteries from the left intercostal artery, 1 patient had a radicular artery from the right intercostobronchial artery and a right intercostal artery, and 1 patient had a radicular artery from the left intercostal artery and left thyrocervical artery.
through a microcatheter placed distal to the origin of the spinal artery without neurological complication (Fig 3). A total of 75 patients remained alive as of the writing of this report. Between day 1 and day 3,717 (mean, 305 days), 103 patients died. Nine patients died within 48 hours after the procedure. Two patients were lost to follow-up. Given the focus of this study, only neurological complications were evaluated, and these were noted in only 2 patients. The first patient, a 73-year-old male complained of right leg weakness following his angiogram and embolization. The patient had a right common femoral artery access and an extensive embolization consisting of a left bronchial artery, a conjoined bronchial artery as well as left and right intercostobronchial arteries. No spinal arterial supply was noted at the time of the embolization or on review for this study. A neurology consult 1 day after the procedure concluded this represented a lumbosacral plexopathy. No spinal imaging was obtained at that time. The patient was seen as an outpatient 6 months later. MR imaging of the cervical and thoracic spine and peripheral nerve conduction studies were performed and were negative for any evidence of spinal cord ischemia. The second patient, a 52-year-old male with atherosclerotic disease, underwent embolization of bilateral bronchial arteries without complication. However, the patient required a second procedure 4 days later for recurrent hemorrhage. No therapeutic embolization was carried out; however, extensive catheterization of the proximal great vessels resulted in a neurological deficit. MR imaging confirmed scattered ischemic areas in the left cerebral and cerebellar hemispheres indicative of embolization from atherosclerotic disease of the arch. No other patients had neurologic symptoms.
Figure 1. A 72-year-old male presented with squamous cell carcinoma after left lower lobectomy and left upper lobe wedge resection, now with hemoptysis and consolidative opacities throughout the residual left lung. Bronchial artery angiography and embolization was performed which included angiography of the left thoracic-9 intercostal artery (white arrows) showing a normal arteria radicularis magna (aka, artery of Adamkiewicz [black arrows]). Note the size and configuration of the anterior spinal artery including the classic hairpin turn. Minimal supply to the left lung was noted from this intercostal, and embolization was not performed.
DISCUSSION Selective bronchial angiography was first described in 1964 by Viamonte (10), in a study of 32 patients. One year later, Feigelson and Ravin (11) published the first report of transverse myelitis after bronchial artery angiography. Those authors reported selective injection of the right fifth intercostal artery with visualization of adjacent intercostals described as an intercostobronchial artery. Spinal supply was not identified, but the patient developed bilateral lower extremity symptoms after the procedure, including weakness which improved significantly over the following month. The authors speculated that the complication was due to the use of an abundance of ionic contrast material. Today, transverse myelopathy from diagnostic spinal angiography has all but disappeared since the introduction of nonionic contrast materials (12). In 1973, Remy et al (13) first reported embolization of the bronchial arteries in 4 patients, followed by Wholey et al (4) in 5 patients 3 years later. Neither series reported spinal cord complications. However, 1 of the 5 patients in the latter study was not embolized due to the close relationship between the posterior radicular branch and the anterior spinal artery through collateralization from the bronchial artery based on the authors’ description. Currently, most bronchial artery embolization results in the peripheral literature warn of possible spinal cord complications, having occurred in up
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Figure 2. A 71-year-old male presented with diffuse alveolar hemorrhage. (a) Selective injection was performed using a 5-F catheter through a right intercostobronchial artery. The bronchial branch (white arrow) and intercostal branches (black arrowhead) are well noted. A small linear artery (black arrows) is superimposed over the spine, possibly representing the spinal arterial supply. (b) Contrast material was injected through a microcatheter (white arrow at tip) placed super-selectively in the bronchial artery (black arrow). Embolization using 500- to 710-μm polyvinyl alcohol particles was performed. (c) Contrast injected through the microcatheter into the intercostobronchial artery shows the occluded bronchial artery (white arrow) as well as filling of a spinal artery (black arrows) through the patent intercostal branches. Note the classic mid-line artery and hairpin configuration.
Figure 3. A 45-year-old female presented with aspergillosis and hemoptysis. (a) Contrast injection through the left thoracic (T)-5 intercostal artery (arrows) shows some collateral supply to the lungs. No arterial supply to the spine is noted. (b) A microcatheter placed in the proximal T-5 intercostal artery and pulmonary venous drainage (black arrows) confirm significant arterial contribution to the lungs. The intercostal artery was embolized using 355- to 500-μm polyvinyl alcohol particles to stasis. (c) A postembolization angiography through the microcatheter in the proximal intercostal artery shows the occluded distal intercostal (white arrow) and filling of the spinal artery (black arrows).
to 6% of cases in a single study (2,5,14,15). In their publication, Mal et al (15) reported spinal cord complications in 3 of 46 patients undergoing bronchial artery embolization. Those complications included Brown-Sequard syndrome that regressed after 4 months without sequelae, paraparesis with spontaneous regression after 2 weeks, and complete paraplegia without regression. However, based on the anatomic origins of the blood supply to the spinal cord, selective angiography of solely a bronchial artery should not demonstrate spinal artery supply. Neurointerventional reports consistently state that complete spinal angiography encompasses selective bilateral arteriography of the external carotid, vertebral, and subclavian and its proximal branches (thyrocervical and costocervical), intercostals at all levels, median sacral artery, and internal iliac arteries (7). No neurologically based source includes selective injection of the bronchial arteries. It is therefore
puzzling how to rectify the differences in the peripheral and neurological reports. The present publication proposes that the arterial supply to the spinal cord originates from intercostal arteries, as expected, but that the same intercostal artery may additionally give rise to a bronchial artery. To that point, in the current study of 180 patients who underwent 254 angiographic studies, no bronchial artery that originated directly from the aorta was found to provide any radiographically demonstrable arterial supply to the spinal cord. Furthermore, no spinal arterial supply was identified from the bronchial component of any intercostobronchial artery. These findings were also supported by a lack of neurological sequelae from selective bronchial artery embolization. Spinal arterial supply was identified from the intercostal arteries, as well as from the intercostal portion of intercostobronchial arteries.
6 ▪ Angiographic Studies Performed for Hemoptysis
Although the current study reports the absence of arterial contribution to the spinal cord from the bronchial artery, this is not the first publication to mention such considerations. Remy et al (16) in a 1977 review of 104 patients found the presence of supply to the anterior spinal artery arising from the cervicointercostal trunk, from an intercostal artery and from an intercostobronchial trunk, which in their opinion constituted an absolute contraindication to embolization. Bookstein et al (17) in that same year also suggested the source of embolic injury to the spine might have been the right intercostobronchial trunk. It was proposed by Marshal and Jackson in 1997 (18) that spinal supply may originate from the intercostobronchial artery and was, fortunately, more common than direct supply from the bronchial artery, implying that such direct bronchial supply does rarely exist. Similarly, in a systematic review of studies published between 1976 and 2016, Panda et al (1) concluded that spinal cord ischemia leading to transient or permanent paraparesis could be attributed to inadvertent embolization of spinal arteries arising from bronchial or intercostobronchial arteries. The current study found the existence of a right intercostobronchial artery in 57% of the patients. This is clearly in agreement with the study by Kocbek and Rakusa (19) who performed dissections in 43 cadavers and found the right bronchial artery originated from the second to the fifth posterior intercostal artery in 58% of cases. It is generally held that spinal cord issues from bronchial artery embolization procedures have deceased over time (1,5,20). This is perhaps attributable to the present widespread use of nonionic contrast material and subselective catheterization of the bronchial artery for embolization (21). Early embolization was performed using 5-F or larger catheters and would clearly increase the likelihood of occlusion of a spinal artery originating from an intercostobronchial artery (21,22). Additionally, such large catheters may not seat well in the bronchial artery origin, thus heightening the possibility for reflux, particularly when coupled with comparatively lower quality fluoroscopy/imaging (22,23). Such reflux could readily track into a more inferiorly located intercostal artery that, in turn, gives rise to the principle arterial supply to the lower thoracic anterior spinal artery (arteria radicularis magna; aka, the artery of Adamkiewicz) (Fig 1). The latter usually arises from the thoracic T6–T12 level and thus at or closely inferior to most bronchial arteries, which generally arise at the T5– T6 level (24). In patients in the current study in whom the spinal artery was visualized through intercostobronchial origin, the appearance of the radicular and spinal arteries was subjectively smaller (Fig 1, 2) than that of the arteria radicularis magna and corresponding anterior spinal artery (Fig 3). To that end, neurological complications from bronchial artery embolization have been reported even when the spinal supply is not angiographically visualized (25,26). This clearly supports the need to selectively catheterize the bronchial artery as distally as possible to achieve both an
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adequate embolization and prevent reflux into the intercostal artery which may give rise to spinal cord supply. This study has a number of limitations. It is a retrospective study, thus, much of the imaging was less than ideal to definitively determine spinal cord arterial supply. The image reviewers arrived at decisions by consensus but were often limited to single radiographic views. Although all patients were inpatients, follow-up might not have mentioned a neurologic examination specifically. Additionally, 9 patients died within 48 hours of the bronchial procedure due to their underlying illnesses. All bronchial and intercostal arteries were not systematically studied in all patients, but rather selection was based on a particular patient’s clinical needs. The imaging reviewers chose to limit the search to bronchial arteries originating from the aorta, although all vessels injected were reviewed for spinal supply including the intercostal and intercostobronchial arteries. In conclusion, the spinal cord arterial supply originated from conventional sites in all patients undergoing angiography in the current study. These conventional sites included intercostal arteries and the intercostal portion of intercostobronchial arteries. No bronchial artery contributed supply to the spinal cord by either image review or presence of spinal cord neurological symptoms following bronchial artery embolization.
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