- Email: [email protected]
Spinal Dural Arteriovenous Fistula: Is There a Role for Intraoperative Contrast-Enhanced Ultrasound?
Accepted Manuscript Spinal Dural Arteriovenous Fistula: Is There A Role For Intra-operative Contrast Enhanced Ultrasound? Francesco Prada, MD, Massimiliano Del Bene, MD, Giuseppe Faragò, Francesco DiMeco, MD PII:
S1878-8750(17)30058-X
DOI:
10.1016/j.wneu.2017.01.045
Reference:
WNEU 5142
To appear in:
World Neurosurgery
Received Date: 6 November 2016 Revised Date:
7 January 2017
Accepted Date: 10 January 2017
Please cite this article as: Prada F, Del Bene M, Faragò G, DiMeco F, Spinal Dural Arteriovenous Fistula: Is There A Role For Intra-operative Contrast Enhanced Ultrasound?, World Neurosurgery (2017), doi: 10.1016/j.wneu.2017.01.045. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Spinal Dural Arteriovenous Fistula: Is There A Role For Intra-operative Contrast Enhanced Ultrasound?
Francesco Prada MD1, Massimiliano Del Bene MD1, Giuseppe Faragò2, Francesco
RI PT
DiMeco MD1,3
1 Department of Neurosurgery, Fondazione IRCCS Istituto Neurologico C. Besta, Milan;
2 Department of Neuroradiology, Fondazione IRCCS Istituto Neurologico C. Besta,
SC
Milan;
3 Department of Neurological Surgery, Johns Hopkins Medical School, Baltimore,
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EP
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M AN U
Maryland
Corresponding Author: Francesco Prada, MD.
Department of Neurosurgery, Fondazione IRCCS Istituto Neurologico “C. Besta”, Milan, Italy Via Celoria n.11, 20133, Milan, Italy Phone +39 02 23942421 Mobile +39 3394269011 Fax +39 02 5990 2239 e-mail: [email protected]
ACCEPTED MANUSCRIPT ABSTRACT Background Intra-operative imaging during surgical ligation of a spinal dural arteriovenous fistula (SDAVF) is usually based on fluorescence angiography, intra-operative ultrasound with Doppler modality and intra-operative digital subtraction angiography.
ultrasound (CEUS) during surgical management of SDAVF.
RI PT
The aim of our work was to explore the potential role of contrast enhanced
SDAVF main features in CEUS prior to treatment are described together with their modifications after surgical ligation
SC
Case Description
CEUS was performed using harmonic imaging with a second generation ultrasound contrast agent (SonoVue) in a case of right D6 spinal dorsal arterio-venous fistula.
M AN U
An initial CEUS scan demonstrated the location of the arterialized vein draining in the dilated peri-medullary plexus together with an augmented enhancement of the spinal cord because of intra-medullary capillary congestion and augmented flow. The post-ligation scan demonstrated the interruption of the arterialized vein together with normal blood flow restoration in spinal cord and in peri-medullary plexus.
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Conclusions
CEUS allowed both pre- and post-ligation real-time visualization of site of the fistula and blood flow changes occurring in the spinal cord and peri-medullary plexus. In our opinion CEUS is definitely a valuable tool in SDAVF surgery, that encompass
EP
limitations of Doppler imaging and that might be integrated with other imaging
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modalities such as fluorescence.
Keywords Spinal dural arteriovenous fistula, Contrast enhanced ultrasound, vascular malformation, intra-operative ultrasound, surgical ligation.
ACCEPTED MANUSCRIPT INTRODUCTION Spinal dural arteriovenous fistulas (SDAVFs) represent the most common spinal vascular malformation (SVMs) accounting for 70% of the cases (2). Numerous classifications exist for SVMs, consequently the definition for SDAVFs may appear confusing. In this article we will focus on intradural dorsal spinal arteriovenous fistulas as defined by Spetzler and colleagues, in the past defined as Type I spinal
RI PT
arteriovenous fistulas in Di Chiro classification or Type III in Borden classification.
Typically these malformations are characterized by a pathological connection between a dural branch of a radicular artery and the coronal venous plexus, usually in the dural sleeve of the nerve root (Figure 1 and 2). This shunt allows high pressure
SC
arterial flow within the venous compartment, thus inducing coronal plexus congestion and capillary spinal cord hypertension related to increased resistance to medullary venous outflow with consequent myelopathy (1).
M AN U
Common presentation encompasses gait instability, numbness and paresthesias having a stepwise deterioration: up to 50% of the patients has a severe disability after 3 years from the diagnosis. Latter stages involve limb paralysis, pain, bowel, bladder and sexual dysfunction.
Diagnosis is based on imaging findings in magnetic resonance imaging (MRI) and digital subtraction angiography (DSA) (5).
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Treatment resides in obliteration of the arterialized vein at and it can be achieved with endovascular technique or with open surgery. In the latter cases identification of the target vessel is mandatory: intra-operative imaging is usually based on fluorescence angiography, intra-operative ultrasound (ioUS) with Doppler modality
EP
and intra-operative DSA (7).
We report for the first time the use of intra-operative contrast enhanced ultrasound (CEUS) in SDAVF surgery, presenting its principals features prior treatment and the
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modifications after surgical ligation. CASE DESCRIPTION
We present the case of a 72-year-old man who suffered from worsening paraparesis, lower limbs hypo-aesthesia, gait instability and incontinence in the 3 years before admission in our Institution. An MRI demonstrated a T2 hyperintensity of the spinal cord between T3 and the conus, associated to peri-medullary flow-void compatible with SDAVF. A DSA confirmed the presence of a D6 right spinal dorsal arterio-venous fistula (Figure 1). After spinal level identification, surgery was performed through a posterior approach with D5-D6 laminectomy (Figure 2). In order to identify the correct point to open the
ACCEPTED MANUSCRIPT dura we performed a trans-dural US scan with Doppler to evaluate perimedullary flow. We then performed CEUS as described in other papers from our group (4, 6), visualizing the arterialized vein with inverted flow bridging from the right D6 radicular dural sleeve to the congested and distended peri-medullary plexus. The dura was then opened and spinal cord appeared covered and dislocated by the engorged coronal venous plexus in continuity to the arterialized D6 right radicular vein (Figure
RI PT
2). A new scan was performed with CEUS in order to confirm pre-ligation blood flow dynamics. The arterialized bridging vein was highlighted by CEUS: in particular the direction of the microbubbles (MB) was evident, showing the inverted flow from the radicular sleeve toward the perimedullary coronal plexus. The plexus appeared
SC
engorged and dilated, characterized by chaotic high flow of MB. CEUS signal of the spinal cord seemed increased if compared to physiological conditions. This was probably due to the inverted high blood flow from the coronal plexus to the
M AN U
intramedullary capillaries that were consequently enlarged (Figure 3).
After this evaluation, the arterialized vein was coagulated and divided close to the dura, while a post-ligation CEUS control was performed (Figure 2). CEUS demonstrated the interruption of the arterialized vein together with normal blood flow restoration in peri-medullary plexus that appeared no more congested. CEUS signal of the spinal cord at the level of the fistula revealed the restitution of normal signal,
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without inverted flow in the capillary district (Figure 4).
The post-operative period was uneventful and the patient demonstrated a prompt relief from the symptoms.
EP
DISCUSSION
In this case of SDAVF CEUS permitted to visualize the site of the fistula prior dural opening, to understand the pathophysiology of this condition and the modification of
AC C
blood flow dynamics that take place after fistula disconnection. Before ligation, blood freely flows from the fistula in the radicular dural sleeve through the arterialized radicular vein (characterized by inverted high flow) towards the perimedullary plexus. The latter presents chaotic high velocity flow that pour out in medullary capillary (Figure 3). This flow dynamics might explain the medullary edema seen as T2 hyperintensity or T1 gadolinium enhancement in MRI, that is consequence of the inverted flow and subsequent capillary increased pressure with interstitial fluid extravasation (Figure 1).
After ligation, the reduction of spinal cord contrast
enhancement in CEUS demonstrates that the medullary capillaries regain physiological pressure and flow, therefore permitting the correct fluid balance in the medullary interstitial space (Figure 4)
ACCEPTED MANUSCRIPT Regarding the surgical procedure itself CEUS permits to find the fistula with great accuracy, then allowing a targeted opening of the dura mater and safe identification of the fistula position (Figure 1). Other intra-operative imaging modalities applicable in SVMs are intra-operative DSA (IODSA), indocyanine green videoangiography (ICG), intra-operative Doppler ultrasound.
RI PT
IODSA is an extremely valuable tool capable to highlight the SVM angio-architecture also outside the operative field and demonstrated high sensitivity for flow dynamics changes and lesion localization. On the other hand it is an invasive procedure that uses radiation and a demanding technique that requires experience and specific
SC
operating room (3).
ICG is less invasive and time consuming if compared to IODSA, is able to identify the SVM, to confirm the exclusion of the fistula and through specific analysis can lead to
M AN U
a quantitative assessment of flow dynamics. A major drawback of ICG, as for the other fluorescence techniques, is the need to expose the area of interest in order to value the fluorescence, thus the vessels not already exposed are not evaluable. Microdoppler and more recently Doppler ultrasound have been proposed in order to study flow dynamics changes after ligation and lesion location. It must be underlined that Doppler imaging is negatively influenced by artifacts onset and angle of
TE D
insonation dependency (7).
ioUS in spine lesion surgery is used from 1978 when Reid described the first case of cervical astrocytoma resected under ioUS guidance. Over the years, numerous reports on ioUS (B-mode and Doppler) in spine surgery were published, also
EP
encompassing the use of CEUS in spine tumours (6). In spinal vascular malformations, such as SDAVFs CEUS has never been described. In this case we used our standard protocol for CEUS spinal examination.
AC C
In vascular malformations such as SDAVFs, CEUS permits to study the angioarchitecture and blood flow features with great spatial and temporal resolution without the limitations of artifacts onset and angle of insonation dependency thus facilitating surgical maneuvers and physiology understanding as demonstrated in this case.
CONFLICT OF INTEREST: None.
ACKNOWLEDGEMENT The research leading to these results has received funding from the European Union Seventh Framework Programme FP7/2007–2013 under grant agreement n. 602 923.
ACCEPTED MANUSCRIPT REFERENCES
6.
7.
RI PT
SC
5.
M AN U
4.
TE D
3.
EP
2.
Kim LJ, Spetzler RF: Classification and surgical management of spinal arteriovenous lesions: arteriovenous fistulae and arteriovenous malformations. Neurosurgery 59:S195-201; discussion S193-113, 2006. Marcus J, Schwarz J, Singh IP, Sigounas D, Knopman J, Gobin YP, Patsalides A: Spinal dural arteriovenous fistulas: a review. Curr Atheroscler Rep 15:335, 2013. Orru E, Sorte DE, Gregg L, Wolinsky JP, Jallo GI, Bydon A, Tamargo RJ, Gailloud P: Intraoperative spinal digital subtraction angiography: indications, technique, safety, and clinical impact. 2016. Prada F, Del Bene M, Mattei L, Lodigiani L, DeBeni S, Kolev V, Vetrano I, Solbiati L, Sakas G, DiMeco F: Preoperative magnetic resonance and intraoperative ultrasound fusion imaging for real-time neuronavigation in brain tumor surgery. Ultraschall Med 36:174-186, 2015. Sanborn MR, Crowley RW, Uschold T, Park MS, Albuquerque FC, McDougall CG: Spinal dural arteriovenous fistulas: how, when, and why. Neurosurgery 61 Suppl 1:6-11, 2014. Vetrano IG, Prada F, Nataloni IF, Bene MD, Dimeco F, Valentini LG: Discrete or diffuse intramedullary tumor? Contrast-enhanced intraoperative ultrasound in a case of intramedullary cervicothoracic hemangioblastomas mimicking a diffuse infiltrative glioma: technical note and case report. Neurosurg Focus 39:E17, 2015. Yamamoto. S, Kim. P: Spinal Arteriovenous Fistulas and Arteriovenous Malformations – Complicated Vasculature and Surgical Imaging. In: Tjoumakaris SI, ed. Arteriovenous Fistulas - Diagnosis and Management; 2013.
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1.
ACCEPTED MANUSCRIPT FIGURES AND CAPTIONS
Figure 1) SDAVF pre- and post-operative imaging. A) antero-posterior and B) latero-lateral pre-operative digital subtraction angiography, SDAVF is supported by the right D6 intercostal artery. C) Pre-operative sagittal T1 gadolinium MRI, note the enhancement of the spinal cord from D8 to the conus consequence of capillary
RI PT
engorgement. D) Coronal and E) sagittal CT angiography (Dyna-CT), the SDAVF is clearly demarcated together with the dilated coronal plexus. F) Post-operative digital subtraction angiography, injecting the contrast medium in the right D6 intercostal
SC
artery, the fistula is no more visible.
Figure 2) intra-operative microscopic views. On the left pre-ligation appearance: it is clearly visible the arterialized vein (arrow head) between the inner dura and the
M AN U
peri-medullary plexus (*). The spinal cord (S) is dislocated and covered by an engorged serpiginous venous plexus. On the right panel the arterialized vein (arrow head) has been divided, showing the underlying D6 root (arrow-head). The perimedullary plexus appears less congested than before.
Figure 3) Pre-ligation CEUS scan of D6 dorsal SDAVF acquired before dural
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opening (left - axial scan; right - sagittal scan). These images demonstrate the intact dura mater (D), and the location of the arterialized vein (AV) that ends in the dilated peri-medullary plexus (P). The spinal cord (S) CEUS signal is stronger than in physiological condition because of intra-medullary capillary congestion and
EP
augmented flow. The medulla is displaced against the vertebral body (VB) Figure 4) Post-ligation CEUS scan of D6 dorsal SDAVF (left - axial scan; right -
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sagittal scan). The arterialized vein is no more visible. The formerly dilated perimedullary plexus (P) now is less congested and less visible in CEUS. The spinal cord (S) CEUS signal is still visible but less the before and more similar to physiological aspect. The spinal cord is no more displaced against the vertebral body (VB)
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ACCEPTED MANUSCRIPT
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ACCEPTED MANUSCRIPT • •
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• •
CEUS permits to study SDAVF site, architecture and blood flow both prior and after ligation The post-ligation scan demonstrates the restitution of a physiological blood flow CEUS is not affected by specific limitations of ioDSA and fluorescence CEUS is a valuable tool in SDAVF surgery that might be integrated with other imaging modalities
ACCEPTED MANUSCRIPT
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CEUS: contrast enhanced ultrasound DSA: digital subtraction angiography ICG: indocyanine green videoangiography ioDSA: intra-operative digital subtraction angiography ioUS: intra-operative ultrasound MB: microbubbles MRI: magnetic resonance imaging SDAVF: spinal dural arteriovenous fistula SVM: spinal vascular malformation
RI PT
Abbreviations list:
S1878-8750(17)30058-X
DOI:
10.1016/j.wneu.2017.01.045
Reference:
WNEU 5142
To appear in:
World Neurosurgery
Received Date: 6 November 2016 Revised Date:
7 January 2017
Accepted Date: 10 January 2017
Please cite this article as: Prada F, Del Bene M, Faragò G, DiMeco F, Spinal Dural Arteriovenous Fistula: Is There A Role For Intra-operative Contrast Enhanced Ultrasound?, World Neurosurgery (2017), doi: 10.1016/j.wneu.2017.01.045. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Spinal Dural Arteriovenous Fistula: Is There A Role For Intra-operative Contrast Enhanced Ultrasound?
Francesco Prada MD1, Massimiliano Del Bene MD1, Giuseppe Faragò2, Francesco
RI PT
DiMeco MD1,3
1 Department of Neurosurgery, Fondazione IRCCS Istituto Neurologico C. Besta, Milan;
2 Department of Neuroradiology, Fondazione IRCCS Istituto Neurologico C. Besta,
SC
Milan;
3 Department of Neurological Surgery, Johns Hopkins Medical School, Baltimore,
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M AN U
Maryland
Corresponding Author: Francesco Prada, MD.
Department of Neurosurgery, Fondazione IRCCS Istituto Neurologico “C. Besta”, Milan, Italy Via Celoria n.11, 20133, Milan, Italy Phone +39 02 23942421 Mobile +39 3394269011 Fax +39 02 5990 2239 e-mail: [email protected]
ACCEPTED MANUSCRIPT ABSTRACT Background Intra-operative imaging during surgical ligation of a spinal dural arteriovenous fistula (SDAVF) is usually based on fluorescence angiography, intra-operative ultrasound with Doppler modality and intra-operative digital subtraction angiography.
ultrasound (CEUS) during surgical management of SDAVF.
RI PT
The aim of our work was to explore the potential role of contrast enhanced
SDAVF main features in CEUS prior to treatment are described together with their modifications after surgical ligation
SC
Case Description
CEUS was performed using harmonic imaging with a second generation ultrasound contrast agent (SonoVue) in a case of right D6 spinal dorsal arterio-venous fistula.
M AN U
An initial CEUS scan demonstrated the location of the arterialized vein draining in the dilated peri-medullary plexus together with an augmented enhancement of the spinal cord because of intra-medullary capillary congestion and augmented flow. The post-ligation scan demonstrated the interruption of the arterialized vein together with normal blood flow restoration in spinal cord and in peri-medullary plexus.
TE D
Conclusions
CEUS allowed both pre- and post-ligation real-time visualization of site of the fistula and blood flow changes occurring in the spinal cord and peri-medullary plexus. In our opinion CEUS is definitely a valuable tool in SDAVF surgery, that encompass
EP
limitations of Doppler imaging and that might be integrated with other imaging
AC C
modalities such as fluorescence.
Keywords Spinal dural arteriovenous fistula, Contrast enhanced ultrasound, vascular malformation, intra-operative ultrasound, surgical ligation.
ACCEPTED MANUSCRIPT INTRODUCTION Spinal dural arteriovenous fistulas (SDAVFs) represent the most common spinal vascular malformation (SVMs) accounting for 70% of the cases (2). Numerous classifications exist for SVMs, consequently the definition for SDAVFs may appear confusing. In this article we will focus on intradural dorsal spinal arteriovenous fistulas as defined by Spetzler and colleagues, in the past defined as Type I spinal
RI PT
arteriovenous fistulas in Di Chiro classification or Type III in Borden classification.
Typically these malformations are characterized by a pathological connection between a dural branch of a radicular artery and the coronal venous plexus, usually in the dural sleeve of the nerve root (Figure 1 and 2). This shunt allows high pressure
SC
arterial flow within the venous compartment, thus inducing coronal plexus congestion and capillary spinal cord hypertension related to increased resistance to medullary venous outflow with consequent myelopathy (1).
M AN U
Common presentation encompasses gait instability, numbness and paresthesias having a stepwise deterioration: up to 50% of the patients has a severe disability after 3 years from the diagnosis. Latter stages involve limb paralysis, pain, bowel, bladder and sexual dysfunction.
Diagnosis is based on imaging findings in magnetic resonance imaging (MRI) and digital subtraction angiography (DSA) (5).
TE D
Treatment resides in obliteration of the arterialized vein at and it can be achieved with endovascular technique or with open surgery. In the latter cases identification of the target vessel is mandatory: intra-operative imaging is usually based on fluorescence angiography, intra-operative ultrasound (ioUS) with Doppler modality
EP
and intra-operative DSA (7).
We report for the first time the use of intra-operative contrast enhanced ultrasound (CEUS) in SDAVF surgery, presenting its principals features prior treatment and the
AC C
modifications after surgical ligation. CASE DESCRIPTION
We present the case of a 72-year-old man who suffered from worsening paraparesis, lower limbs hypo-aesthesia, gait instability and incontinence in the 3 years before admission in our Institution. An MRI demonstrated a T2 hyperintensity of the spinal cord between T3 and the conus, associated to peri-medullary flow-void compatible with SDAVF. A DSA confirmed the presence of a D6 right spinal dorsal arterio-venous fistula (Figure 1). After spinal level identification, surgery was performed through a posterior approach with D5-D6 laminectomy (Figure 2). In order to identify the correct point to open the
ACCEPTED MANUSCRIPT dura we performed a trans-dural US scan with Doppler to evaluate perimedullary flow. We then performed CEUS as described in other papers from our group (4, 6), visualizing the arterialized vein with inverted flow bridging from the right D6 radicular dural sleeve to the congested and distended peri-medullary plexus. The dura was then opened and spinal cord appeared covered and dislocated by the engorged coronal venous plexus in continuity to the arterialized D6 right radicular vein (Figure
RI PT
2). A new scan was performed with CEUS in order to confirm pre-ligation blood flow dynamics. The arterialized bridging vein was highlighted by CEUS: in particular the direction of the microbubbles (MB) was evident, showing the inverted flow from the radicular sleeve toward the perimedullary coronal plexus. The plexus appeared
SC
engorged and dilated, characterized by chaotic high flow of MB. CEUS signal of the spinal cord seemed increased if compared to physiological conditions. This was probably due to the inverted high blood flow from the coronal plexus to the
M AN U
intramedullary capillaries that were consequently enlarged (Figure 3).
After this evaluation, the arterialized vein was coagulated and divided close to the dura, while a post-ligation CEUS control was performed (Figure 2). CEUS demonstrated the interruption of the arterialized vein together with normal blood flow restoration in peri-medullary plexus that appeared no more congested. CEUS signal of the spinal cord at the level of the fistula revealed the restitution of normal signal,
TE D
without inverted flow in the capillary district (Figure 4).
The post-operative period was uneventful and the patient demonstrated a prompt relief from the symptoms.
EP
DISCUSSION
In this case of SDAVF CEUS permitted to visualize the site of the fistula prior dural opening, to understand the pathophysiology of this condition and the modification of
AC C
blood flow dynamics that take place after fistula disconnection. Before ligation, blood freely flows from the fistula in the radicular dural sleeve through the arterialized radicular vein (characterized by inverted high flow) towards the perimedullary plexus. The latter presents chaotic high velocity flow that pour out in medullary capillary (Figure 3). This flow dynamics might explain the medullary edema seen as T2 hyperintensity or T1 gadolinium enhancement in MRI, that is consequence of the inverted flow and subsequent capillary increased pressure with interstitial fluid extravasation (Figure 1).
After ligation, the reduction of spinal cord contrast
enhancement in CEUS demonstrates that the medullary capillaries regain physiological pressure and flow, therefore permitting the correct fluid balance in the medullary interstitial space (Figure 4)
ACCEPTED MANUSCRIPT Regarding the surgical procedure itself CEUS permits to find the fistula with great accuracy, then allowing a targeted opening of the dura mater and safe identification of the fistula position (Figure 1). Other intra-operative imaging modalities applicable in SVMs are intra-operative DSA (IODSA), indocyanine green videoangiography (ICG), intra-operative Doppler ultrasound.
RI PT
IODSA is an extremely valuable tool capable to highlight the SVM angio-architecture also outside the operative field and demonstrated high sensitivity for flow dynamics changes and lesion localization. On the other hand it is an invasive procedure that uses radiation and a demanding technique that requires experience and specific
SC
operating room (3).
ICG is less invasive and time consuming if compared to IODSA, is able to identify the SVM, to confirm the exclusion of the fistula and through specific analysis can lead to
M AN U
a quantitative assessment of flow dynamics. A major drawback of ICG, as for the other fluorescence techniques, is the need to expose the area of interest in order to value the fluorescence, thus the vessels not already exposed are not evaluable. Microdoppler and more recently Doppler ultrasound have been proposed in order to study flow dynamics changes after ligation and lesion location. It must be underlined that Doppler imaging is negatively influenced by artifacts onset and angle of
TE D
insonation dependency (7).
ioUS in spine lesion surgery is used from 1978 when Reid described the first case of cervical astrocytoma resected under ioUS guidance. Over the years, numerous reports on ioUS (B-mode and Doppler) in spine surgery were published, also
EP
encompassing the use of CEUS in spine tumours (6). In spinal vascular malformations, such as SDAVFs CEUS has never been described. In this case we used our standard protocol for CEUS spinal examination.
AC C
In vascular malformations such as SDAVFs, CEUS permits to study the angioarchitecture and blood flow features with great spatial and temporal resolution without the limitations of artifacts onset and angle of insonation dependency thus facilitating surgical maneuvers and physiology understanding as demonstrated in this case.
CONFLICT OF INTEREST: None.
ACKNOWLEDGEMENT The research leading to these results has received funding from the European Union Seventh Framework Programme FP7/2007–2013 under grant agreement n. 602 923.
ACCEPTED MANUSCRIPT REFERENCES
6.
7.
RI PT
SC
5.
M AN U
4.
TE D
3.
EP
2.
Kim LJ, Spetzler RF: Classification and surgical management of spinal arteriovenous lesions: arteriovenous fistulae and arteriovenous malformations. Neurosurgery 59:S195-201; discussion S193-113, 2006. Marcus J, Schwarz J, Singh IP, Sigounas D, Knopman J, Gobin YP, Patsalides A: Spinal dural arteriovenous fistulas: a review. Curr Atheroscler Rep 15:335, 2013. Orru E, Sorte DE, Gregg L, Wolinsky JP, Jallo GI, Bydon A, Tamargo RJ, Gailloud P: Intraoperative spinal digital subtraction angiography: indications, technique, safety, and clinical impact. 2016. Prada F, Del Bene M, Mattei L, Lodigiani L, DeBeni S, Kolev V, Vetrano I, Solbiati L, Sakas G, DiMeco F: Preoperative magnetic resonance and intraoperative ultrasound fusion imaging for real-time neuronavigation in brain tumor surgery. Ultraschall Med 36:174-186, 2015. Sanborn MR, Crowley RW, Uschold T, Park MS, Albuquerque FC, McDougall CG: Spinal dural arteriovenous fistulas: how, when, and why. Neurosurgery 61 Suppl 1:6-11, 2014. Vetrano IG, Prada F, Nataloni IF, Bene MD, Dimeco F, Valentini LG: Discrete or diffuse intramedullary tumor? Contrast-enhanced intraoperative ultrasound in a case of intramedullary cervicothoracic hemangioblastomas mimicking a diffuse infiltrative glioma: technical note and case report. Neurosurg Focus 39:E17, 2015. Yamamoto. S, Kim. P: Spinal Arteriovenous Fistulas and Arteriovenous Malformations – Complicated Vasculature and Surgical Imaging. In: Tjoumakaris SI, ed. Arteriovenous Fistulas - Diagnosis and Management; 2013.
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1.
ACCEPTED MANUSCRIPT FIGURES AND CAPTIONS
Figure 1) SDAVF pre- and post-operative imaging. A) antero-posterior and B) latero-lateral pre-operative digital subtraction angiography, SDAVF is supported by the right D6 intercostal artery. C) Pre-operative sagittal T1 gadolinium MRI, note the enhancement of the spinal cord from D8 to the conus consequence of capillary
RI PT
engorgement. D) Coronal and E) sagittal CT angiography (Dyna-CT), the SDAVF is clearly demarcated together with the dilated coronal plexus. F) Post-operative digital subtraction angiography, injecting the contrast medium in the right D6 intercostal
SC
artery, the fistula is no more visible.
Figure 2) intra-operative microscopic views. On the left pre-ligation appearance: it is clearly visible the arterialized vein (arrow head) between the inner dura and the
M AN U
peri-medullary plexus (*). The spinal cord (S) is dislocated and covered by an engorged serpiginous venous plexus. On the right panel the arterialized vein (arrow head) has been divided, showing the underlying D6 root (arrow-head). The perimedullary plexus appears less congested than before.
Figure 3) Pre-ligation CEUS scan of D6 dorsal SDAVF acquired before dural
TE D
opening (left - axial scan; right - sagittal scan). These images demonstrate the intact dura mater (D), and the location of the arterialized vein (AV) that ends in the dilated peri-medullary plexus (P). The spinal cord (S) CEUS signal is stronger than in physiological condition because of intra-medullary capillary congestion and
EP
augmented flow. The medulla is displaced against the vertebral body (VB) Figure 4) Post-ligation CEUS scan of D6 dorsal SDAVF (left - axial scan; right -
AC C
sagittal scan). The arterialized vein is no more visible. The formerly dilated perimedullary plexus (P) now is less congested and less visible in CEUS. The spinal cord (S) CEUS signal is still visible but less the before and more similar to physiological aspect. The spinal cord is no more displaced against the vertebral body (VB)
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ACCEPTED MANUSCRIPT • •
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CEUS permits to study SDAVF site, architecture and blood flow both prior and after ligation The post-ligation scan demonstrates the restitution of a physiological blood flow CEUS is not affected by specific limitations of ioDSA and fluorescence CEUS is a valuable tool in SDAVF surgery that might be integrated with other imaging modalities
ACCEPTED MANUSCRIPT
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CEUS: contrast enhanced ultrasound DSA: digital subtraction angiography ICG: indocyanine green videoangiography ioDSA: intra-operative digital subtraction angiography ioUS: intra-operative ultrasound MB: microbubbles MRI: magnetic resonance imaging SDAVF: spinal dural arteriovenous fistula SVM: spinal vascular malformation
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Abbreviations list: