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Tridirectional phase-contrast magnetic resonance velocity mapping depicts severe hemodynamic alterations in a patient with aortic dissection type Stanford B
Tridirectional phase-contrast magnetic resonance velocity mapping depicts severe hemodynamic alterations in a patient with aortic dissection type Stanford B Matthias Müller-Eschner, MD,a,b Fabian Rengier, MS,b Sasan Partovi, MS,b Roland Unterhinninghofen, PhD,c Dittmar Böckler, MD, PhD,d Sebastian Ley, MD,b and Hendrik von Tengg-Kobligk, MD,a,b Heidelberg and Karlsruhe, Germany This report describes flow patterns derived by three-dimensional (3D) three-directional velocity-encoded cine (VEC) magnetic resonance imaging (MRI), in a patient with chronic Stanford type B aortic dissection. Acquired 3D VEC MRI data illustrated an acceleration of blood flow through the primary entry toward the vessel wall of the false lumen, leading to disturbed intraluminal flow. Furthermore, accelerated blood flow was observed in the partially compressed true lumen. 3D VEC MRI data may be helpful to guide physicians for a more comprehensive preoperative and postoperative assessment of complex aortic pathologies. ( J Vasc Surg 2011;54:559-62.)
A relatively high incidence of increasing aortic diameter and the potential risk for aortic rupture in Stanford type B dissections require careful follow-up with noninvasive imaging.1,2 Currently, there is a search for advanced imaging techniques in the follow-up of patients who have survived the acute stage of aortic dissection to allow for prediction of diameter increase. Three-dimensional (3D) three-directional velocity-encoded cine (VEC) magnetic resonance imaging (MRI), also referred to as 3D VEC MRI, is a method that extends the technique of phase-contrast flow measurement by vectorial velocity-encoding; that is, by encoding in all three spatial directions in a volumetric data set. 3D VEC MRI enables visualization and interpretation of pathophysiologic hemodynamics in the vessels of the brain, neck, thorax, abdomen, and peripheral arteries.3-6 Velocity and direction of blood flow can be interpreted in From the German Cancer Research Center (DKFZ), Heidelberga; the Department of Diagnostic and Interventional Radiology, Heidelberg University Hospital, Heidelbergb; the Karlsruhe Institute of Technology (KIT), Karlsruhec; and the Department of Vascular Surgery, Heidelberg University Hospital, Heidelberg.d The research leading to these results has received funding from the European Community’s Seventh Framework Programme (FP7/2007-2013) under grant agreement No. 224495 (euHeart project). Fabian Rengier received a grant from the German Research Foundation (DFG) within the “Research training group 1126: Intelligent Surgery - Development of new computer-based methods for the future workplace in surgery.” Competition of interest: none. Video clips for this article may be found online at www.jvascsurg.org. Reprint requests: Hendrik von Tengg-Kobligk, MD, Department of Diagnostic and Interventional Radiology, University Hospital, Heidelberg Im Neuenheimer Feld 110, 69120 Heidelberg, Germany (e-mail: hendrik. [email protected]). The editors and reviewers of this article have no relevant financial relationships to disclose per the JVS policy that requires reviewers to decline review of any manuscript for which they may have a competition of interest. 0741-5214/$36.00 Copyright © 2011 by the Society for Vascular Surgery. doi:10.1016/j.jvs.2011.02.017
Fig 1. A and B, Postprocessing of aortic computed tomography angiography image by 3-dimensional volume rendering gives a good morphologic overview of the true and false lumen. C and D, Centerline analysis allows the depiction of the primary entry, located approximately 1.5 cm distal to the left subclavian artery.
vector field and streamline visualization.5 Apart from an acquisition time of approximately 20 minutes, no further effort is necessary to acquire data for complex interpretation of 3D hemodynamics because it can easily be added to the standard MR aortic protocol. Pathophysiologic find559
560 Müller-Eschner et al
JOURNAL OF VASCULAR SURGERY August 2011
Fig 2. Streamline visualization shows (A) parasagittal view of blood flow in the true and false lumen and (B) a double-oblique view of blood flow in the false lumen distal to the primary entry (color-coding according to absolute local velocity in cm/s).
Fig 3. Vector field visualization shows (A) sagittal view of blood flow in the true and false lumen and (B) a parasagittal view of blood flow in the true and false lumen of the descending aorta (color-coding according to absolute local velocity in cm/s).
ings by 3D VEC MRI in a patient with chronic aortic Stanford type B dissection are presented. CASE REPORT A 67-year-old man was admitted to the Department of Vascular Surgery with a diagnosed aortic dissection in 2001 when the maximum aortic diameter was 4.0 cm. Although follow-up examinations revealed a slow progression of aortic diameter up to 4.9 cm in 2007, the aortic diameter remained constant during further follow-up. The primary entry tear was located approximately 1.5 cm distal to the ostium of the left subclavian artery, corresponding to Stanford type B aortic dissection. Aside from medically treated hypertension, the patient had no further comorbidities. On the
basis of the initial computed tomography (CT) scan and the slow progression of aortic diameter, as well as the absence of symptoms, best medical treatment (candesartan, bisoprolol, and amlodipine) was favored over endovascular therapy. Volume-rendered CT images (Fig 1, A and B) and multiplanar reformations (Fig 1, C and D) allowed for a detailed morphologic assessment of the aortic pathology. However, no physiologic information for the hemodynamic variables could be derived. Therefore, after local Investigational Review Board approval, 3D VEC MRI was acquired in 2009 in addition to standard morphologic MRI to visualize and analyze blood flow patterns and thus to detect hemodynamically relevant changes in the true and false lumen.
JOURNAL OF VASCULAR SURGERY Volume 54, Number 2
These data were acquired by a 1.5-T clinical MR scanner (Magnetom Avanto; Siemens Medical Solutions, Erlangen, Germany) using the following parameters: spatial resolution, 1.5 ⫻ 1.5 ⫻ 2.1 mm3; velocity sensitivity, 150 cm/s along all three encoding directions; flip angle, 30°; and echo/repetition time, 4.05/61.20 ms. Retrospective electrocardiographic gating was used to synchronize the measurement with the cardiac motion (30 frames/ cardiac cycle were reconstructed). The in-house developed software Mediframe5 was used for postprocessing to visualize and analyze streamlines and vector fields. Streamlines colored by velocity showed an acceleration of blood flow entering the false lumen through the primary entry (Fig 2, A). Vector field visualization revealed a vortex formation at the aortic bulb, representing a normal finding that was also observable in healthy volunteers6-9 (Fig 3, A; Video 1, online only). Within the false lumen, a proximal vortex formation deriving from the flow jet through the primary entry toward the vessel wall of the false lumen was visualized (Fig 2, B; Video 2, online only). Multidirectional vectors with low velocities depicted disturbed blood flow within the enlarged false lumen, leading to narrowing and partial collapse of the true lumen and resulting in high unidirectional velocities (Fig 3, Video 1, online only).
DISCUSSION Noninvasive MR-based flow visualization and quantification are possible by phase-contrast, imaging only the flowing spins within the bloodstream. Standard imaging protocols can be complimented by 3D VEC MRI acquiring three-directional velocity vectors over time (4D acquisition) without the need for additional contrast medium. Understanding hemodynamics and interpreting their meaning in aortic dissection is particularly challenging. Pathophysiologic blood flow in other pathologies, such as aortic and intracranial aneurysms,10-12 a thrombosed aortic arch,3 and a sclerotic aortic valve4 and their associated pathologic blood flow, were previously described using tridirectional flow imaging. The idea is that 3D VEC MRI may be helpful to guide physicians for the pre- and postoperative assessment of aortic pathologies with complex blood flow or vascular shunts, atherosclerotic plaques, and cardiovascular anomalies.3-6 Geometrically triggered changes in blood flow characteristics, such as those shown in the true and false lumen, might be a useful additional clinical marker to evaluate the severity of the disease and improve the assessment of its potential risk for progression, including analysis of wall shear stress.13 The 4D method presented offers a more individual and comprehensive assessment of vascular alterations than those acquired by standard morphologic and 2D functional imaging. As shown by the supplied images and videos, vortical flow in the false lumen might be a contributing factor for chronic expansion of the false lumen leading to further compression of the true lumen. This, in turn, might result in further accelerated blood flow through the compressed true lumen, with a potential impact on the distal descending aorta. Current ongoing studies are aiming to prove whether 3D VEC MRI is able to identify certain
Müller-Eschner et al 561
hemodynamic patterns that will help to improve risk stratification of patients with type B aortic dissection. In addition, postoperative blood flow imaging may help to assess hemodynamics within reconstructed vascular geometries and its relevance for potential development of anastomotic aneurysm. Shorter acquisition times, semiautomatic postprocessing, and an improved signal- and contrast-to-noise ratio by intravenous contrast media14 are technical improvements that may help to establish this technique in clinical settings. CONCLUSIONS 3D VEC MRI is able to visualize hemodynamic patterns in a patient with chronic aortic dissection. In the near future, this may help to improve risk stratification for false lumen enlargement or even rupture. REFERENCES 1. Kunishige H, Myojin K, Ishibashi Y, Ishii K, Kawasaki M, Oka J. Predictors of surgical indications for acute type B aortic dissection based on enlargement of aortic diameter during the chronic phase. Jpn J Thorac Cardiovasc Surg 2006;54:477-82. 2. Blount KJ, Hagspiel KD. Aortic diameter, true lumen, and false lumen growth rates in chronic type B aortic dissection. AJR Am J Roentgenol 2009;192:W222-9. 3. Frydrychowicz A, Weigang E, Harloff A, Beyersdorf F, Hennig J, Langer M, et al. Images in cardiovascular medicine. Time-resolved 3-dimensional magnetic resonance velocity mapping at 3 T reveals drastic changes in flow patterns in a partially thrombosed aortic arch. Circulation 2006;113:e460-1. 4. Markl M, Harloff A, Foll D, Langer M, Hennig J, Frydrychowicz A. Sclerotic aortic valve: flow-sensitive 4-dimensional magnetic resonance imaging reveals 3 distinct flow-pattern changes. Circulation 2007;116: e336-7. 5. Unterhinninghofen R, Ley S, Ley-Zaporozhan J, von Tengg-Kobligk H, Bock M, Kauczor HU, et al. Concepts for visualization of multidirectional phase-contrast MRI of the heart and large thoracic vessels. Acad Radiol 2008;15:361-9. 6. Kilner PJ, Yang GZ, Mohiaddin RH, Firmin DN, Longmore DB. Helical and retrograde secondary flow patterns in the aortic arch studied by three-directional magnetic resonance velocity mapping. Circulation 1993;88:2235-47. 7. Morbiducci U, Ponzini R, Rizzo G, Cadioli M, Esposito A, Montevecchi FM, et al. Mechanistic insight into the physiological relevance of helical blood flow in the human aorta: an in vivo study. Biomech Models Mechanobiol 2010 Published online [doi: 10.1007/ s10237-010-0238-2]. 8. Markl M, Draney MT, Hope MD, Levin JM, Chan FP, Alley MT, et al. Time-resolved 3-dimensional velocity mapping in the thoracic aorta: visualization of 3-directional blood flow patterns in healthy volunteers and patients. J Comput Assist Tomogr 2004;28:459-68. 9. Clough RE, Schaeffter T, UribeS, Modarai B, Taylor PR, Waltham M. 4D Imaging of type B aortic dissection using real time selfrespiratory gated cardiovascular magnetic resonance imaging. Proceedings of Annual Meeting of the European Society for Vascular Surgery. 2009. p. 111. 10. Weigang E, Kari FA, Beyersdorf F, Luehr M, Etz CD, Frydrychowicz A, et al. Flow-sensitive four-dimensional magnetic resonance imaging: flow patterns in ascending aortic aneurysms. Eur J Cardiothorac Surg 2008;34:11-6. 11. Hope TA, Markl M, Wigstrom L, Alley MT, Miller DC, Herfkens RJ. Comparison of flow patterns in ascending aortic aneurysms and volunteers using four-dimensional magnetic resonance velocity mapping. J Magn Reson Img 2007;26:1471-9.
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12. Hope TA, Hope MD, Purcell DD, von Morze C, Vigneron DB, Alley MT, et al. Evaluation of intracranial stenoses and aneurysms with accelerated 4D flow. Magn Reson Img 2010;28:41-6. 13. Frydrychowicz A, Stalder AF, Russe MF, Bock J, Bauer S, Harloff A, et al. Three-dimensional analysis of segmental wall shear stress in the aorta by flow-sensitive four-dimensional-MRI. J Magn Reson Img 2009;30:77-84. 14. Bock J, Frydrychowicz A, Stalder AF, Bley TA, Burkhardt H, Hennig J, et al. 4D phase contrast MRI at 3 T: effect of standard and blood-pool
JOURNAL OF VASCULAR SURGERY August 2011
contrast agents on SNR, PC-MRA, and blood flow visualization. Magn Reson Med 2010;63:330-8.
Submitted Aug 18, 2010; accepted Feb 6, 2011.
Video clips for this article may be found online at www.jvascsurg.org.
A relatively high incidence of increasing aortic diameter and the potential risk for aortic rupture in Stanford type B dissections require careful follow-up with noninvasive imaging.1,2 Currently, there is a search for advanced imaging techniques in the follow-up of patients who have survived the acute stage of aortic dissection to allow for prediction of diameter increase. Three-dimensional (3D) three-directional velocity-encoded cine (VEC) magnetic resonance imaging (MRI), also referred to as 3D VEC MRI, is a method that extends the technique of phase-contrast flow measurement by vectorial velocity-encoding; that is, by encoding in all three spatial directions in a volumetric data set. 3D VEC MRI enables visualization and interpretation of pathophysiologic hemodynamics in the vessels of the brain, neck, thorax, abdomen, and peripheral arteries.3-6 Velocity and direction of blood flow can be interpreted in From the German Cancer Research Center (DKFZ), Heidelberga; the Department of Diagnostic and Interventional Radiology, Heidelberg University Hospital, Heidelbergb; the Karlsruhe Institute of Technology (KIT), Karlsruhec; and the Department of Vascular Surgery, Heidelberg University Hospital, Heidelberg.d The research leading to these results has received funding from the European Community’s Seventh Framework Programme (FP7/2007-2013) under grant agreement No. 224495 (euHeart project). Fabian Rengier received a grant from the German Research Foundation (DFG) within the “Research training group 1126: Intelligent Surgery - Development of new computer-based methods for the future workplace in surgery.” Competition of interest: none. Video clips for this article may be found online at www.jvascsurg.org. Reprint requests: Hendrik von Tengg-Kobligk, MD, Department of Diagnostic and Interventional Radiology, University Hospital, Heidelberg Im Neuenheimer Feld 110, 69120 Heidelberg, Germany (e-mail: hendrik. [email protected]). The editors and reviewers of this article have no relevant financial relationships to disclose per the JVS policy that requires reviewers to decline review of any manuscript for which they may have a competition of interest. 0741-5214/$36.00 Copyright © 2011 by the Society for Vascular Surgery. doi:10.1016/j.jvs.2011.02.017
Fig 1. A and B, Postprocessing of aortic computed tomography angiography image by 3-dimensional volume rendering gives a good morphologic overview of the true and false lumen. C and D, Centerline analysis allows the depiction of the primary entry, located approximately 1.5 cm distal to the left subclavian artery.
vector field and streamline visualization.5 Apart from an acquisition time of approximately 20 minutes, no further effort is necessary to acquire data for complex interpretation of 3D hemodynamics because it can easily be added to the standard MR aortic protocol. Pathophysiologic find559
560 Müller-Eschner et al
JOURNAL OF VASCULAR SURGERY August 2011
Fig 2. Streamline visualization shows (A) parasagittal view of blood flow in the true and false lumen and (B) a double-oblique view of blood flow in the false lumen distal to the primary entry (color-coding according to absolute local velocity in cm/s).
Fig 3. Vector field visualization shows (A) sagittal view of blood flow in the true and false lumen and (B) a parasagittal view of blood flow in the true and false lumen of the descending aorta (color-coding according to absolute local velocity in cm/s).
ings by 3D VEC MRI in a patient with chronic aortic Stanford type B dissection are presented. CASE REPORT A 67-year-old man was admitted to the Department of Vascular Surgery with a diagnosed aortic dissection in 2001 when the maximum aortic diameter was 4.0 cm. Although follow-up examinations revealed a slow progression of aortic diameter up to 4.9 cm in 2007, the aortic diameter remained constant during further follow-up. The primary entry tear was located approximately 1.5 cm distal to the ostium of the left subclavian artery, corresponding to Stanford type B aortic dissection. Aside from medically treated hypertension, the patient had no further comorbidities. On the
basis of the initial computed tomography (CT) scan and the slow progression of aortic diameter, as well as the absence of symptoms, best medical treatment (candesartan, bisoprolol, and amlodipine) was favored over endovascular therapy. Volume-rendered CT images (Fig 1, A and B) and multiplanar reformations (Fig 1, C and D) allowed for a detailed morphologic assessment of the aortic pathology. However, no physiologic information for the hemodynamic variables could be derived. Therefore, after local Investigational Review Board approval, 3D VEC MRI was acquired in 2009 in addition to standard morphologic MRI to visualize and analyze blood flow patterns and thus to detect hemodynamically relevant changes in the true and false lumen.
JOURNAL OF VASCULAR SURGERY Volume 54, Number 2
These data were acquired by a 1.5-T clinical MR scanner (Magnetom Avanto; Siemens Medical Solutions, Erlangen, Germany) using the following parameters: spatial resolution, 1.5 ⫻ 1.5 ⫻ 2.1 mm3; velocity sensitivity, 150 cm/s along all three encoding directions; flip angle, 30°; and echo/repetition time, 4.05/61.20 ms. Retrospective electrocardiographic gating was used to synchronize the measurement with the cardiac motion (30 frames/ cardiac cycle were reconstructed). The in-house developed software Mediframe5 was used for postprocessing to visualize and analyze streamlines and vector fields. Streamlines colored by velocity showed an acceleration of blood flow entering the false lumen through the primary entry (Fig 2, A). Vector field visualization revealed a vortex formation at the aortic bulb, representing a normal finding that was also observable in healthy volunteers6-9 (Fig 3, A; Video 1, online only). Within the false lumen, a proximal vortex formation deriving from the flow jet through the primary entry toward the vessel wall of the false lumen was visualized (Fig 2, B; Video 2, online only). Multidirectional vectors with low velocities depicted disturbed blood flow within the enlarged false lumen, leading to narrowing and partial collapse of the true lumen and resulting in high unidirectional velocities (Fig 3, Video 1, online only).
DISCUSSION Noninvasive MR-based flow visualization and quantification are possible by phase-contrast, imaging only the flowing spins within the bloodstream. Standard imaging protocols can be complimented by 3D VEC MRI acquiring three-directional velocity vectors over time (4D acquisition) without the need for additional contrast medium. Understanding hemodynamics and interpreting their meaning in aortic dissection is particularly challenging. Pathophysiologic blood flow in other pathologies, such as aortic and intracranial aneurysms,10-12 a thrombosed aortic arch,3 and a sclerotic aortic valve4 and their associated pathologic blood flow, were previously described using tridirectional flow imaging. The idea is that 3D VEC MRI may be helpful to guide physicians for the pre- and postoperative assessment of aortic pathologies with complex blood flow or vascular shunts, atherosclerotic plaques, and cardiovascular anomalies.3-6 Geometrically triggered changes in blood flow characteristics, such as those shown in the true and false lumen, might be a useful additional clinical marker to evaluate the severity of the disease and improve the assessment of its potential risk for progression, including analysis of wall shear stress.13 The 4D method presented offers a more individual and comprehensive assessment of vascular alterations than those acquired by standard morphologic and 2D functional imaging. As shown by the supplied images and videos, vortical flow in the false lumen might be a contributing factor for chronic expansion of the false lumen leading to further compression of the true lumen. This, in turn, might result in further accelerated blood flow through the compressed true lumen, with a potential impact on the distal descending aorta. Current ongoing studies are aiming to prove whether 3D VEC MRI is able to identify certain
Müller-Eschner et al 561
hemodynamic patterns that will help to improve risk stratification of patients with type B aortic dissection. In addition, postoperative blood flow imaging may help to assess hemodynamics within reconstructed vascular geometries and its relevance for potential development of anastomotic aneurysm. Shorter acquisition times, semiautomatic postprocessing, and an improved signal- and contrast-to-noise ratio by intravenous contrast media14 are technical improvements that may help to establish this technique in clinical settings. CONCLUSIONS 3D VEC MRI is able to visualize hemodynamic patterns in a patient with chronic aortic dissection. In the near future, this may help to improve risk stratification for false lumen enlargement or even rupture. REFERENCES 1. Kunishige H, Myojin K, Ishibashi Y, Ishii K, Kawasaki M, Oka J. Predictors of surgical indications for acute type B aortic dissection based on enlargement of aortic diameter during the chronic phase. Jpn J Thorac Cardiovasc Surg 2006;54:477-82. 2. Blount KJ, Hagspiel KD. Aortic diameter, true lumen, and false lumen growth rates in chronic type B aortic dissection. AJR Am J Roentgenol 2009;192:W222-9. 3. Frydrychowicz A, Weigang E, Harloff A, Beyersdorf F, Hennig J, Langer M, et al. Images in cardiovascular medicine. Time-resolved 3-dimensional magnetic resonance velocity mapping at 3 T reveals drastic changes in flow patterns in a partially thrombosed aortic arch. Circulation 2006;113:e460-1. 4. Markl M, Harloff A, Foll D, Langer M, Hennig J, Frydrychowicz A. Sclerotic aortic valve: flow-sensitive 4-dimensional magnetic resonance imaging reveals 3 distinct flow-pattern changes. Circulation 2007;116: e336-7. 5. Unterhinninghofen R, Ley S, Ley-Zaporozhan J, von Tengg-Kobligk H, Bock M, Kauczor HU, et al. Concepts for visualization of multidirectional phase-contrast MRI of the heart and large thoracic vessels. Acad Radiol 2008;15:361-9. 6. Kilner PJ, Yang GZ, Mohiaddin RH, Firmin DN, Longmore DB. Helical and retrograde secondary flow patterns in the aortic arch studied by three-directional magnetic resonance velocity mapping. Circulation 1993;88:2235-47. 7. Morbiducci U, Ponzini R, Rizzo G, Cadioli M, Esposito A, Montevecchi FM, et al. Mechanistic insight into the physiological relevance of helical blood flow in the human aorta: an in vivo study. Biomech Models Mechanobiol 2010 Published online [doi: 10.1007/ s10237-010-0238-2]. 8. Markl M, Draney MT, Hope MD, Levin JM, Chan FP, Alley MT, et al. Time-resolved 3-dimensional velocity mapping in the thoracic aorta: visualization of 3-directional blood flow patterns in healthy volunteers and patients. J Comput Assist Tomogr 2004;28:459-68. 9. Clough RE, Schaeffter T, UribeS, Modarai B, Taylor PR, Waltham M. 4D Imaging of type B aortic dissection using real time selfrespiratory gated cardiovascular magnetic resonance imaging. Proceedings of Annual Meeting of the European Society for Vascular Surgery. 2009. p. 111. 10. Weigang E, Kari FA, Beyersdorf F, Luehr M, Etz CD, Frydrychowicz A, et al. Flow-sensitive four-dimensional magnetic resonance imaging: flow patterns in ascending aortic aneurysms. Eur J Cardiothorac Surg 2008;34:11-6. 11. Hope TA, Markl M, Wigstrom L, Alley MT, Miller DC, Herfkens RJ. Comparison of flow patterns in ascending aortic aneurysms and volunteers using four-dimensional magnetic resonance velocity mapping. J Magn Reson Img 2007;26:1471-9.
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12. Hope TA, Hope MD, Purcell DD, von Morze C, Vigneron DB, Alley MT, et al. Evaluation of intracranial stenoses and aneurysms with accelerated 4D flow. Magn Reson Img 2010;28:41-6. 13. Frydrychowicz A, Stalder AF, Russe MF, Bock J, Bauer S, Harloff A, et al. Three-dimensional analysis of segmental wall shear stress in the aorta by flow-sensitive four-dimensional-MRI. J Magn Reson Img 2009;30:77-84. 14. Bock J, Frydrychowicz A, Stalder AF, Bley TA, Burkhardt H, Hennig J, et al. 4D phase contrast MRI at 3 T: effect of standard and blood-pool
JOURNAL OF VASCULAR SURGERY August 2011
contrast agents on SNR, PC-MRA, and blood flow visualization. Magn Reson Med 2010;63:330-8.
Submitted Aug 18, 2010; accepted Feb 6, 2011.
Video clips for this article may be found online at www.jvascsurg.org.