Magnetic resonance angiography of collateral vessel growth in a rabbit femoral artery ligation model

Lussanet, Quido G. de; Golde, Jolanda C. G. van; Beets-Tan, Regina; Haan, Michiel W. de; Zaar, Daniëlle V. J.; Post, Mark J.; Huijberts, M. S. P.; Schaper, Nicolaas C.; Engelshoven, Jos M. A. van; Backes, Walter H.

doi:10.1002/nbm.1003

Cited by 20 publications

(22 citation statements)

References 15 publications

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“…The fact that these pathways are the first to provide casting material to the distal vasculature suggests that they are the pathways of least resistance and represent the dominant or primary collaterals. These are the vessels that others have concluded are primarily responsible for distal limb perfusion (22,56). This is similar to the clinical situation as the major collaterals in the lower extremity are identified as preexisting named arteries (23, 29 -31, 57).…”

Section: Discussionsupporting

confidence: 60%

“…The largest of the preexisting vessels are typically those that become the dominant collaterals (35,45,51). Combined anatomic and modeling studies have predicted that hindlimb flow subsequent to femoral artery occlusion is primarily determined by these collaterals (22,56). This is consistent with studies of segmental resistances that demonstrated that compensation in the collateral vessels is of significantly greater hemodynamic importance than adaptations in the distal microvasculature (43,71,75).…”

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confidence: 56%

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Suppressed hindlimb perfusion in Rac2^−/− and Nox2^−/− mice does not result from impaired collateral growth

Distasi

Case

Ziegler

et al. 2009

American Journal of Physiology-Heart and Circulatory Physiology

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arteriogenesis; hindlimb ischemia; necrosis; regeneration; NADPH oxidase 2 IN THE PERIPHERAL CIRCULATION, the dilation and enlargement of preexisting vessels that form collateral pathways subsequent to arterial occlusion are the primary vascular compensations that preserve tissue viability and maintain function. These vessels dilate within seconds (25,39,45,70) and undergo expansion for weeks (20,25,45,69). In various species, the preexisting vessels are the size of the smallest arteries, and they enlarge ϳ100% (14,20,35,45,56). Available clinical studies have indicated that subsequent to arterial occlusion in the peripheral circulation, the primary vessels that enlarge as collaterals are preexisting arteries (4,29,57). The largest of the preexisting vessels are typically those that become the dominant collaterals (35,45,51). Combined anatomic and modeling studies have predicted that hindlimb flow subsequent to femoral artery occlusion is primarily determined by these collaterals (22,56). This is consistent with studies of segmental resistances that demonstrated that compensation in the collateral vessels is of significantly greater hemodynamic importance than adaptations in the distal microvasculature (43,71,75). Nevertheless, few studies investigating the mechanisms of vascular compensation subsequent to arterial occlusion in mice have specifically identified and studied these preexisting vessels that form the primary collateral pathways. Such investigations are needed because angiogenesis and collateral growth are initiated by different stimuli, and differences exist in the molecules and mechanisms that mediate these important processes (7, 11).Leukocytes, especially lymphocytes (63, 74) and macrophages (2,33,37), have been shown to have an important role in vascular compensation to hindlimb ischemia. Recent studies by Tojo et al. (66) and Urao et al. (72) have established that NADPH oxidase 2 (Nox2)-derived ROS from bone marrowderived cells (BMDCs) have an important role in neovascularization in the ischemic mouse hindlimb. The initial report (66) concluded from microsphere data that collateral growth was impaired, but did not specifically identify collateral bypass vessels or measure their diameters.To investigate the hypothesis that Nox2-derived NAD(P)H oxidase mediates primary collateral growth subsequent to arterial occlusion, the present study used Rac2-null (Rac2 Ϫ/Ϫ ) and Nox2-null (Nox2 Ϫ/Ϫ ) mice and a novel method of identifying primary hindlimb collaterals. Rac2 is expressed primarily, if not exclusively, in hematopoietic cells (38, 52) and binds to and activates Nox2-containing NAD(P)H oxidase (24,40). In addition, leukocytes from Rac2 Ϫ/Ϫ and Nox2 Ϫ/Ϫ mice have impaired function related to reduced ROS production (47,66,72). We present a method to identify the dominant or primary collateral that should be the major collateral supplying flow to

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Section: Discussionsupporting

confidence: 60%

supporting

confidence: 56%

Suppressed hindlimb perfusion in Rac2^−/− and Nox2^−/− mice does not result from impaired collateral growth

Distasi

Case

Ziegler

et al. 2009

American Journal of Physiology-Heart and Circulatory Physiology

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“…We introduced the technique of serially obtained in vivo angiograms (27). Both number and lumen of collaterals were increased directly after ligation up to 21 days after ligation in control rabbits, but this process was significantly impaired in diabetic rabbits.…”

Section: Discussionmentioning

confidence: 99%

“…The rabbit ischemic hind limb model has been used extensively in arteriogenesis research. In recent years, we have adapted this model to study collateral artery growth longitudinally in the same animal (27). The aim of the present study was to investigate the effect of experimental diabetes on both the acute and remodeling phases of collateral development in the ischemia hind limb model and the role of monocyte chemotaxis.…”

mentioning

confidence: 99%

Impaired Collateral Recruitment and Outward Remodeling in Experimental Diabetes

et al. 2008

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OBJECTIVE-In this study, the effect of chronic hyperglycemia on acute ligation-induced collateral vasodilation, on monocyte chemotaxis, and on structural outward remodeling of collaterals was investigated.RESEARCH DESIGN AND METHODS-Femoral artery ligation was performed 8 weeks after alloxan or saline treatment in New Zealand White rabbits. Angiography was performed directly, 1 and 3 weeks after ligation. These angiographic recordings were used to quantify number of collaterals, lumen, and blood volume index. Reactive hyperemia response was tested by intramuscular laser Doppler measurements. Subsequently, blood was sampled from the aorta for monocyte chemotaxis.RESULTS-Ligation resulted in markedly lower acute collateral vasodilation in diabetic compared with control rabbits. Also, hyperemic vasodilatory response to local ischemia was impaired in diabetic rabbits. This difference persisted at 1 and 3 weeks after ligation, with a lower number of visible collaterals. In addition, the collateral lumen was markedly lower in diabetic rabbits after the maturation phase. Likewise, a reduced blood volume index in the region of growing collaterals was observed in diabetic animals. The monocyte migration toward vascular endothelial growth factor-A and monocyte chemotactic protein-1 was strongly reduced in diabetic rabbits.CONCLUSIONS-This study demonstrates that chronic hyperglycemia negatively affects the different phases of arteriogenesis: 1) impaired shear induced vasodilatation; 2) impaired outward collateral growth, reflected in the number of collaterals and blood volume index; and 3) inhibition of monocyte chemotaxis. Impairments were most evident in the acute phase of arteriogenesis. Therapies aimed at restoring acute collateral recruitment, such as vasodilators, may be of interest to improve collateral function in diabetes.

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“…The development of collateral arteries can be monitored non-invasively by serial MR angiography (MRA) (22)(23)(24)(25)(26)(27).…”

Section: Introductionmentioning

confidence: 99%

Dynamic contrast‐enhanced MRI of muscle perfusion combined with MR angiography of collateral artery growth in a femoral artery ligation model

Lussanet¹,

Golde²,

Beets‐Tan³

et al. 2007

NMR in Biomedicine

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To assess the use of MRI for evaluating changes in muscle blood flow and number of collateral arteries, serial dynamic contrast-enhanced MRI (DCE-MRI) was combined with high-spatial-resolution contrast-enhanced MR angiography (MRA) in a peripheral ischemia model. The combined MRI (DCE-MRI and MRA) protocol was performed serially in 15 male rabbits at 2 h (day 0(+)), 7 days, and 21 days after femoral artery ligation. In the anterior tibial and soleus muscle, changes in resting muscle blood flow determined as the endothelial transfer coefficient (K(trans)) and arterial inflow delay from DCE-MRI and changes in the number of sub-millimeter sized collateral arteries as scored with MRA were measured. Directly after ligation, K(trans) in the anterior tibial muscle was reduced to 23% of that in the control limb, then recovered to 81% on day 7, and to 85 % on day 21. K(trans) in the soleus muscle recovered from a reduction to 63% on day 0(+), to 85% on day 7, and to 90% on day 21. The number of collaterals around the ligated femoral artery increased from 1.1 on day 0(+) to 4.2 on day 7, and 6.0 on day 21 in the ligated limb only. Combined DCE-MRI and MRA allows non-invasive serial monitoring of changes in muscle blood flow and growth of sub-millimeter sized collateral arteries in a rabbit femoral artery ligation model.

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Magnetic resonance angiography of collateral vessel growth in a rabbit femoral artery ligation model

Cited by 20 publications

References 15 publications

Suppressed hindlimb perfusion in Rac2^−/− and Nox2^−/− mice does not result from impaired collateral growth

Suppressed hindlimb perfusion in Rac2^−/− and Nox2^−/− mice does not result from impaired collateral growth

Impaired Collateral Recruitment and Outward Remodeling in Experimental Diabetes

Dynamic contrast‐enhanced MRI of muscle perfusion combined with MR angiography of collateral artery growth in a femoral artery ligation model

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Magnetic resonance angiography of collateral vessel growth in a rabbit femoral artery ligation model

Cited by 20 publications

References 15 publications

Suppressed hindlimb perfusion in Rac2−/− and Nox2−/− mice does not result from impaired collateral growth

Suppressed hindlimb perfusion in Rac2−/− and Nox2−/− mice does not result from impaired collateral growth

Impaired Collateral Recruitment and Outward Remodeling in Experimental Diabetes

Dynamic contrast‐enhanced MRI of muscle perfusion combined with MR angiography of collateral artery growth in a femoral artery ligation model

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Suppressed hindlimb perfusion in Rac2^−/− and Nox2^−/− mice does not result from impaired collateral growth

Suppressed hindlimb perfusion in Rac2^−/− and Nox2^−/− mice does not result from impaired collateral growth