Wall Shear Stress in the Feeding Native Conduit Arteries of Superficial Arteriovenous Malformations of the Lower Face is a Reliable Marker of Disease Progression

Abstract

Purpose To assess the prognostic value of the wall shear stress (WSS) measured in the feeding native arteries upstream from facial superficial arteriovenous malformations (sAVMs). Reliable prognostic criteria are needed to distinguish progressive from stable sAVMs and thus support the indication for an aggressive or a conservative management to avoid severe facial disfigurement.

Materials and Methods We prospectively included 25 patients with untreated facial sAVMs, 15 patients with surgically resected sAVMs and 15 controls. All had undergone Doppler ultrasound examination (DUS) with measurements of inner diameters, blood flow velocities, computation of blood flow and WSS of the feeding arteries. Based on the absence or presence of progression in clinical and imaging examinations 6 months after, we discriminated untreated patients as stable or progressive.

Results WSS in the ipsilateral external carotid artery was higher in progressive compared to stable sAVMs (15.8 ± 3.3dynes/cm² vs. 9.6 ± 2.0dynes/cm², mean±SD, p < 0.0001) with a cut-off of 11.5dynes/cm² (sensitivity: 92 %, specificity: 92 %, AUC: 0.955, [95 %CI: 0.789–0.998], p = 0.0001). WSS in the ipsilateral facial artery was also higher in progressive compared to stable sAVMs (50.7 ± 14.5dynes/cm² vs. 25.2 ± 7.1dynes/cm², p < 0.0001) with a cut-off of 34.0dynes/cm² (sensitivity: 100 %, specificity: 92 %, AUC: 0.974, [95 %CI: 0.819–1.000], p = 0.0001). The hemodynamic data of operated patients were not different from those of the control group.

Conclusion WSS measured in the feeding arteries of an sAVM may be a simple reliable criterion to distinguish stable from progressive sAVMs. This value should be considered to guide the therapeutic strategy as well as the long-term follow-up of patients with facial sAVMs.

Zusammenfassung

Ziel Beurteilung des prognostischen Wertes der Wandschubspannung (WSS), gemessen in den zuführenden nativen Arterien stromaufwärts von oberflächlichen arteriovenösen Fehlbildungen des Gesichts (sAVMs). Um progressive von stabilen sAVMs zu unterscheiden sind verlässliche prognostische Kriterien erforderlich, die bei der Indikation für eine aggressive oder konservative Behandlung hilfreich sind, um schwere Gesichtsdeformierungen zu vermeiden.

Material und Methoden Prospektiv wurden 25 Patienten mit unbehandelten sAVMs im Gesicht, 15 Patienten mit chirurgisch-resezierten sAVMs und 15 Kontrollpatienten eingeschlossen. Alle hatten eine Doppler-Ultraschalluntersuchung (DUS) mit Bestimmungen der Innendurchmesser, Blutflussgeschwindigkeiten, Berechnung des Blutflusses und der WSS der zuführenden Arterien. Aufgrund des Fehlens oder Auftretens einer Progression bei den klinischen und bildgebenden Untersuchungen nach 6 Monaten unterschieden wir unbehandelte Patienten als stabil oder progressiv.

Ergebnisse WSS in der ipsilateralen A. carotis externa war bei progressiven sAVMs im Vergleich zu stabilen sAVMs höher (15,8 ± 3,3 dyn/cm² vs. 9,6 ± 2,0 dyn/cm², Mittelwert±SD, p < 0,0001) mit einem Cut-off von 11,5 dyn/cm² (Sensitivität: 92 %, Spezifität: 92 %, AUC: 0,955, [95 %CI: 0,789–0,998], p = 0,0001). WSS in der ipsilateralen A. facialis war ebenfalls höher bei den progressiven im Vergleich zu den stabilen sAVMs (50,7 ± 14,5 dyn/cm² vs. 25,2 ± 7,1 dyn/cm², p < 0,0001) mit einem Cut-off von 34,0 dyn/cm² (Sensitivität: 100 %, Spezifität: 92 %, AUC: 0,974, [95 %CI: 0,819–1,000], p = 0,0001). Die hämodynamischen Daten operierter Patienten unterschieden sich nicht von denen der Kontrollgruppe.

Schlussfolgerung WSS, gemessen in den zuführenden Arterien eines sAVM, kann ein einfache zuverlässiges Kriterium sein, um stabile von progressiven sAVMs zu unterscheiden. Dieser Wert sollte als Richtschnur für die therapeutische Strategie sowie für die langfristige Nachsorge von Patienten mit sAVM im Gesicht angesehen werden.

Key words

arteriovenous malformation - blood flow volume - external carotid artery - facial artery - wall shear stress

• References

• 1 Mulligan PR, Prajapati HJ, Martin LG. et al. Vascular anomalies: classification, imaging characteristics and implications for interventional radiology treatment approaches. Br J Radiol 2014; 87: 20130392
• 2 Dubois J, Alison M. Vascular anomalies: what a radiologist needs to know. Pediatr Radiol 2010; 40: 895-905
• 3 Morgan P, Keller R, Patel K. Evidence-based management of vascular malformations. Facial Plast Surg 2016; 32: 162-176
• 4 Lee BB, Baumgartner I, Berlien HP. et al. International union of angiology. Consensus document of the international union of angiology (IUA)-2013. Current concept on the management of arterio-venous management. Int Angiol 2013; 32: 9-36
• 5 Uller W, Alomari AI, Richter GT. Arteriovenous malformations. Semin Pediatr Surg 2014; 23: 203-207
• 6 Rudic RD, Shesely EG, Maeda N. et al. Direct evidence for the importance of endothelium-derived nitric oxide in vascular remodeling. J Clin Invest 1998; 10: 731-736
• 7 Tronc F, Mallat Z, Lehoux S. et al. Role of matrix metalloproteinases in blood flow-induced arterial enlargement: interaction with NO. Arterioscler Thromb Vasc Biol 2000; 20: E120-E126
• 8 Ben DrissA, Benessiano J, Poitevin P. et al. Arterial expansive remodeling induced by high flow rates. Am J Physiol 1997; 272: H851-H858
• 9 Tronc F, Wassef M, Esposito B. et al. Role of NO in flow-induced remodeling of the rabbit common carotid artery. Arterioscler Thromb Vasc Biol 1996; 16: 1256-1262
• 10 Davies PF. Flow-mediated endothelial mechanotransduction. Physiol Rev 1995; 75: 519-560
• 11 Langille BL, O’Donnell F. Reductions in arterial diameter produced by chronic decreases in blood flow are endothelium-dependent. Science 1986; 231: 405-407
• 12 Kubis N, Checoury A, Tedgui A. et al. Adaptive common carotid arteries remodeling after unilateral internal carotid artery occlusion in adult patients. Cardiovasc Res 2001; 50: 597-602
• 13 Lehoux S, Lévy BI. Collateral artery growth: making the most of what you have. Circ Res 2006; 99: 567-569
• 14 Bonnin P, Coelho J, Pocard M. et al. Anti-TNFa therapy early improves hemodynamics in local intestinal and extraintestinal circulations in active Crohn's disease. J Crohns Colitis 2013; 7: 451-459
• 15 Collins KA, Korcarz CE, Lang RM. Use of echocardiography for the phenotypic assessment of genetically altered mice. Physiol Genomics 2003; 13: 227-239
• 16 Papaioannou TG, Stefanadis C. Vascular wall shear stress: basic principles and methods. Hell J Cardiol 2005; 46: 9-15
• 17 British Standards Institution:. Precision of Test Method (BS5497, part 1). London: BSI; 1979
• 18 Moyé L. Statistical methods for cardiovascular researchers. Circ Res 2016; 118: 439-453
• 19 Johnson VE. Revised standards for statistical evidence. Proc Natl Acad Sci USA 2013; 110: 19313-19317
• 20 Pourageaud F, De Mey JG. Vasomotor responses in chronically hyperperfused and hypoperfused rat mesenteric arteries. Am J Physiol 1998; 274: H1301-H3077
• 21 Buus CL, Pourageaud F, Fazzi GE. et al. Smooth muscle cell changes during flow-related remodeling of rat mesenteric resistance arteries. Circ Res 2001; 89: 180-186
• 22 Alaraj A, Amin-Hanjani S, Shakur SF. et al. Quantitative assessment of changes in cerebral arteriovenous malformation hemodynamics after embolization. Stroke 2015; 46: 942-947
• 23 Rossitti S, Svendsen P. Shear stress in cerebral arteries supplying arteriovenous malformations. Acta Neurochir (Wien) 1995; 137: 138-145
• 24 Oshinski JN, Curtin JL, Loth F. Mean-average wall shear stress measurements in the common carotid artery. J Cardiovasc Magn Reson 2006; 8: 717-722
• 25 Efstathopoulos EP, Patatoukas G, Pantos I. et al. Measurement of systolic and diastolic arterial wall shear stress in the ascending aorta. Phys Med 2008; 24: 196-203
• 26 Peng SL, Shih CT, Huang CW. et al. Optimized analysis of blood flow and wall shear stress in the common carotid artery of rat model by phase-contrast MRI. Sci Rep 2017; 7: 5253
• 27 Piatti F, Sturla F, Bissell MM. et al. 4D Flow Analysis of BAV-Related Fluid-Dynamic Alterations: Evidences of Wall Shear Stress Alterations in Absence of Clinically-Relevant Aortic Anatomical Remodeling. Front Physiol 2017; 26: 441
• 28 Wu SP, Ringgaard S, Oyre S. et al. Wall shear rates differ between the normal carotid, femoral, and brachial arteries: an in vivo MRI study. J Magn Reson Imaging 2004; 19: 188-193