Three-dimensional flow-independent peripheral angiography

Three-Dimensional Flow-Independent Perip her a1 Angiograp hy Jean H. Brittain, Eric W. Olcott, Andrzej Szuba, Garry E. Gold, Graham A. Wright, Pablo Irarrazaval, Dwight G. Nishimura

A magnetization-prepared sequence, T,-Prep-IR, exploits T,, T,, and chemical shift differences to suppress background tissues relative to arterial blood. The resulting flow-independent angiograms depict vessels with any orientation and flow velocity. No extrinsic contrast agent is required. Muscle is the dciminant source of background signal in normal volunteers. However, long-T, deep venous blood and nonvascular fluids such as edema also contribute background signal in some patients. Three sets of imaging parameters are described to address patient-specific contrast requirements. A rapid, spiral-based, three-dimensional readout is utilized to generate high-resolution angiograms of the lower extremities. Comparisons with x-ray angiography and two-dimensional time-of-flight angiography indicate that this flow-independent technique has unique capabilities to accurately depict stenoses and to visualize slow flow and in-plane vessels. Key words: peripheral angiography; flow-independent angiog- ralphy; magnetic resonance angiography; magnetic resonance imaging.

1NTRODUCTlON

Symptomatic lower extremity ischemia due to peripheral vascular disease is a major cause of disability in the United States. Its clinical manifestations range from clau- dication to rest pain, tissue loss, and gangrene (1). Ap- proximately 100,000 patients undergo surgical bypass grafting for lower extremity occlusive disease each year. In addition, approximately 50,000 patients are treated by percutaneous transluminal angioplasty (PTA) and 1C~O,ooO suffer amputation annually (2).

While x-ray angiography has historically provided the information necessary for surgical planning ( 3 , 4), this

MRM 38:343-354 (1997) From the Magnetic Resonance Systems Research Laboratory, Department of Electrical Engineering, Department of Radiology (E.W.O., G.E.G.), De- paitment of Cardiovascular Medicine (A.S.), Stanford University, Stanford, California; the Department of Radiology (E.W.O.), Veterans Affairs Palo Alto Health Care System, Palo Alto, California; the Department of Medical Bio- physics and Sunnybrook Health Science Centre (G.A.W.), University of Toronto, Toronto, Ontario, Canada; and the Department of Electrical Engi- neering (P.I.), Universidad Catolica. Santiago, Chile. Adsdress correspondence to: Jean H. Brittain, Ph.D., 120 Durand Building, Deoartment of Electrical Engineering, Stanford, CA 94305-9510. Received December 12, 1997; revised June 16, 1997; accepted June 16, 1997. This work was supported by NIH NS 29434, NIH HL 39297, NSF BCS 9058556, NIH HL 47448, and GE Medical Systems; and the Medical Re- search Council of Canada (to G.A.W.). 1997 ISMRM Young Investigators' Moore Award Winner 0740-3194/97 $3.00 Copyright 0 1997 by Williams & Wilkins All rights of reproduction in any form reserved.

technique can fail to depict clinically significant run-off vessels (5). In addition, it is an invasive procedure re- quiring arterial puncture and catheterization. Although serious complications are rare, procedural risks to the patient include bleeding, allergic reaction, infection, and inadvertent embolization (6). The recent development of surgical bypass procedures extending to the infrapopli- teal and even pedal arteries is now placing ever greater demands on this diagnostic tool (7, 8).

A variety of magnetic resonance (MR) techniques have been explored as noninvasive alternatives to x-ray peripheral angiography (see for example refs. 9-20). To date, the majority of these studies have employed two- dimensional time-of-flight (2D TOF) methods (9, 12-20). While results have been promising, TOF techniques can have difficulty visualizing in-plane and retrograde flow (14, 18, 19) since they rely on the inflow of unsaturated spins for contrast and typically employ a downstream venous saturation pulse. They can also suffer significant artifacts due to pulsatility in ungated studies (18, 20).

We have developed a new flow-independent method of angiography. As the name suggests, flow-independent angiography (FIA) does not rely on flow for contrast. It is therefore able to depict vessels with any orientation and flow properties. This includes the regions of slow, in- plane, and retrograde flow often found in patients with peripheral vascular disease that can be challenging for flow-based techniques. FIA accomplishes this without the administration of an extrinsic contrast agent by ex- ploiting the intrinsic MR properties of blood (TI, T,, and chemic:al shift) to separate arteries from surrounding tissues (21).

Contrast requirements vary among patients. There are four potential sources of background signal that must be suppressed relative to arterial blood to generate a flow- independent angiogram: muscle, veins, fat, and nonvascular fluids. The final category includes both synovial fluid and a long-T, fluid seen in some patients that we refer to as edema. T2 weighting can be used to suppress both muscle and veins relative to arterial blood. Chemi- cal shift differences can be used to separate blood from fat and TI weighting can be used to suppress nonvascular fluids relative to arterial blood. All of our results utilize a spectrally selective imaging excitation to excite the signal from water while rejecting fat. Therefore, lipids need not be considered in the selection of imaging parameters.

FIA was first implemented as a spin-echo sequence with a 2DFT projective readout (21). A long TE (-200

343

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ms) suppressed muscle and veins relative to arterial blood and a spectrally selective pulse rejected fat. An- other FIA technique combined a T,-weighted magnetization-prepared sequence (T,-Prep) with a spatial-spectral excitation and a two-dimensional spiral readout (22). Compared with the spin-echo implementation, T,-Prep offers greater flexibility in excitation and readout. For example, multi-dimensional or clustered excitations can be easily incorporated.

We have developed a new magnetization-prepared FIA method, T,-Prep-IR, that combines T2-Prep with an inversion recovery period. The contrast generated by this technique is extremely flexible and can be tailored to address patient-specific contrast requirements.

In normal volunteers, muscle is the dominant source of background signal. Imaging parameters can be selected to null the signal from muscle while maximizing the signal- to-noise ratio (SNR) efficiency of arterial blood (SNR/ ,TR). In some patients, long-T, deep venous blood and nonvascular fluids have been identified as additional sources of background signal. We have therefore modified our parameter selection criteria and identified two additional sets of imaging parameters. The first suppresses long-T, deep venous blood as well as muscle and the second suppresses muscle, long-T, deep venous blood, and nonvascular fluids. While these parameter sets produce additional contrast in some patients, they suff’er a loss of arterial blood signal relative to the parameters that suppress only muscle.

T,,-Prep-IR can be combined with virtually any readout strai egy. The projective imaging methods that have been incorporated with other FIA sequences rapidly acquire images covering large fields-of-view (FOV). However, their diagnostic ability is limited by the overlap of multiple vessels and by the presence of non-arterial long-T, species that can obscure the vessels of interest in the projective format (23). Traditional three-dimensional (3D] acquisitions require prohibitively long scan times to cover the required FOV with the desired resolution. In- stead, we have selected a spiral-based 3D readout method that acquires high-resolution images in clinically feasible scan times (24).

In this paper, we will first describe the T,-Prep-IR sequence and the three sets of imaging parameters. We will then demonstrate the effectiveness of this technique in generating high-resolution, high-contrast, 3D peripheral angiograms and present comparisons to x-ray angiography and 2D TOF.

METHOD

T,-F’rep Sequence

The T,-Prep sequence (22) is illustrated in Fig. 1. It was designed to generate T,-weighted magnetization from the entire volume and to store this prepared magnetization along the +z axis. Historically, B, and B, inhomogeneities have posed significant challenges for T,-weighted magnetization-prepared sequences (25-27). T,-Prep was designed to be robust in the presence of such nonunifor- mities (22). Multiple composite refocusing pulses (28) sepa.rated by an interval t180 are weighted in an MLEV pattern (29, 30), and a composite [-go;] “tip-up’’ pulse

GZ

Rf

Th

MLEV-Weighted Spoiler Composite 180’s

90 r--A-, -90

Sequence Imaging

+t180+

u !I u e TE *

FIG. 1. Magnetization-prepared, T,-weighted sequence (T,-Prep) shown with four composite refocusing pulses weighted in an MLEV pattern. T,-Prep stores the T,-weighted magnetization from the entire volume along the +z axis. With a long TE (-200 ms), T,-Prep generates sufficient blood-to-muscle contrast for a flow- independent angiogram. However, the late TE also reduces blood SNR.

(270: [-360:]) (31) is utilized. Flow-sensitivity is also minimized since the entire sequence is spatially nonselective. With a long echo-time (TE - 200 ms), the T,-Prep sequence yields sufficient blood-to-muscle and arterial- to-venous blood contrast for a flow-independent angiogram. However, the late TE also reduces arterial blood SNR.

T,-Prep-IR Sequence

As the name suggests, T,-Prep-IR combines a T,-Prep sequence with an inversion recovery period. This exten- sion provides added flexibility in parameter selection. For example, when muscle is the dominant source of background signal, a moderate TE in the T,-Prep portion of the sequence can be combined with an inversion recovery interval to achieve both an increase in arterial blood SNR and an improvement in muscle suppression as compared with a late-echo T,-Prep sequence alone.

Traditional inversion recovery sequences allow nulling of a particular T, species. However, blood and muscle share similar TI values. To compensate, the T,- Prep-IR technique begins with a moderate-TE T,-Prep sequence. The generated T, contrast suppresses muscle relative to arterial blood, differentiating the magnitude of their longitudinal components. The inversion recovery portion then nulls the already reduced muscle signal.

A simplified diagram of the T,-Prep-IR sequence is illustrated in Fig. 2. A wide bandwidth, hyperbolic se- cant inversion (32) is placed immediately before the initial 90; excitation of T,-Prep. As a result of this inversion, the composite 1-90;] pulse stores the T,-weighted magnetinmation along the -2 axis rather than the +z axis and the robustness of the T,-Prep sequence is preserved. The acquisition portion of the sequence is then delayed an interval TI from the [ -go0] pulse.

Rapid Three-Dimensional Acquisition

The acqu.isition of 3D data is beneficial in MRA because it allows retrospective examination of computed projections at arbitrary view angles. It also allows image seg-

3 0 Flow-Independent Peripheral Angiography

T2 Prep

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IR Image 0 0 . Image

mentation and therefore improved separation of structures. For example, maximum intensity projections (MIP) can be computed from a specified volume of interest.

To ensure adequate SNR in our high-resolution images, we utilize a relatively long TR (-800 ms) with the T,- Prtlp-IR sequence. The scan time resulting from a traditional 3D acquisition using such a TR would be prohib- itive. Instead, we implemented a rapid, non-Cartesian 3D acquisition using a spherical-stack-of-spirals k-space trajectory (24). As shown in Fig. 3, this trajectory phase encodes between planes of interleaved spirals that are clipped to a sphere in k-space. Compared with a 3DFT trajectory, the spherical stack-of-spirals dramatically reduces the number of excitations required to achieve the same FOV and spatial resolution. For example, a 3DFT tralectory requires 32,768 excitations to image a 16 X 16 X 8 cm3 volume with 0.625 mm isotropic resolution. The spherical stack-of-spirals requires only 4,880 excitations, a factor of seven reduction.

1'0 augment the scan time reduction achieved by our choice of k-space trajectory, we acquire multiple spiral interleaves after each contrast-preparation period as shown in Fig. 2. The spiral interleaves are ordered cen- trically (33) to minimize artifacts generated by signal vaIiations between acquisitions. In addition, a sequence of increasing flip angles, 0, through ON, is used to minimize these signal variations (34). The values for 0, through are computed from Om,, = ON assuming no TI recovery during interval TS, the time required for a single imaging excitation and acquisition as shown in Fig. 2. In some cases, the desired Omax is greater than 90'. Sirice selective excitation pulses with flip angles greater than goo are difficult to design, we instead place a nonselective adiabatic inversion immediately before the train of excitations as shown in Fig. 2. In this case, the increasing series of flip angles is computed with

3D ..* 3D Read Read

FIG. 2. A simplified diagram of t h e T,-Prep-IR flow-independent sequence. T,-Prep-IR combines a T,-Prep sequence (shown with two refocusing pulses) with an inversion recovery period. The sequence begins with an adiabatic inversion pulse. A 90" excitation is then followed by a train of equally separated composite refocusing pulses. At the echo of the final refocusing pulse, the T,-weighted magnetization is stored along the -z axis by a composite [-go"] pulse. The first imaging excitation is then delayed an interval TI. To reduce scan time, multiple spiral interleaves are acquired each TR. An increasing series of flip angles, 6, - 6, is used to minimize signal variations. If the desired 6, is greater than go", a nonselective adiabatic inversion is placed immediately before the train of excitations and 6,,,,,, , = 180" - 6,. This adiabatic inversion is shown with a dotted line, since it is only used if e, :> 900.

FIG. 3. The spherical-stack-of-spirals k-space trajectory is shown on the left. This trajectory phase encodes between planes of interleaved spirals. It is clipped to a sphere in k-space to minimize scan time while maintaining isotropic resolution. On t h e right, a single plane from t h e stack is illustrated with one spiral interleaf.

Oactual m3x = 180" - O,,,. The conditional nature of this adiabatjc inversion is indicated by the dotted line in Fig. 2.

When N interleaves are acquired in each TR, SNR is decreased by approximately 1/ ,N and image contrast is altered to some extent since only one excitation can occur ai the point of optimal contrast. The latter effect is mitigated, however, by the centric ordering of thc: acquisitions.

Acquisition Parameters

The 3D T,-Prep-IR sequence was implemented on a 1.5 T GE Sigria with shielded gradients where the maximuni gradient amplitude was 10 mT/m and maximum gradient slew rate was 20 mT/m/ms. A spectrally selective imaging excitation was used to excite only water and a trans- mit/receive extremity coil was used for FOV restriction. The overall interval for the imaging excitation and acquisition, 'TS, was approximately 40 ms. Each spiral interleaf acquired 14.3 ms of data. Peak specific absorption ratio (SAR) was approximately 3 W/kg for a TR of 800 ms. Acquisitions were ungated to minimize TR-to- TR variations. Scanning was typically preceded by a linear-term shimming procedure.

PARAMETER SELECTION

Seven parameters are necessary to describe a specific implementation of the T,-Prep-IR sequence: spatial resolution, t180, TE, TI, TR, N, and Om,,. The choice of resolution affects the amount of partial-volume averag- ing, the degree to which small structures can be resolved, and scan time. The choice of TE and refocusing interval, t180, determines the amount of venous suppression. The selection of TE, TI, TR, N , and Om,, affects the degree of background suppression, arterial blood SNR, and scan time.

We found that increased resolution improves the depiction of stenoses and the visualization of small vessels in our flow-independent angiograms of the distal lower extremity. We routinely acquire 3D volumes with either 1.25 X 1.25 X 1.25 mm3 resolution or 0.625 X 0.625 X

346 Brittain et al.

1.25 mm3 resolution. Maximum resolution is limited by arterial blood SNR and scan time constraints.

The degree of venous suppression is affected by the choice of TE and by the T, of the venous blood. The T, of blood decreases with decreasing oxygen saturation (%O,) (35-37). In addition, the T, of blood decreases as t180 increases. Most of this decrease occurs as t180 is increased from 1 to about 40 ms, and the effect is accen- tuated as S O , decreases (21). To maximize arterial-to- venous blood contrast, a longer t180 is preferable, but little additional contrast is gained by increasing t180 beyond 40 ms. As a result, we typically use two refocusing pulses with t180 = TEl2 if TE is less than approximately 100 ms. If TE is greater than 100 ms, we utilize four refocusing pulses with t180 = TE/4. This maximizes the signal difference between arterial and venous blood while maintaining the sequence's designed compensation for errors in B, and B, homogeneity. Sensitivity to flow through local B, inhomogeneities is also minimized (22).

Deep veins are typically well suppressed in our 3D angiograms of healthy volunteers. However, superficial veins often yield a greater signal. This is consistent with MF. measurements of venous blood T, that have shown increased T, in superficial veins, such as the saphenous vein, relative to deep veins, such as the femoral vein (23). Fortunately, superficial calf structures do not limit the clinical usefulness of our studies. As illustrated in Fig. 4, the 3D volume can easily be limited to include only the central structures of interest.

We have also observed increased deep venous signal in some patients with peripheral vascular disease relative to healthy volunteers. These deep veins are typically well suppressed in flow-independent images of normals. Again, this observation is consistent with T, measurements that found the average T2 of blood in the femoral vein increased in patients with ischemic rest pain as cornpared with normal volunteers (23). Due to the prox- imity of these deep vessels to the arteries of interest, suppression of long-T, deep venous blood was identified as one of two important challenges specific to the clinical application of our flow-independent technique.

The second clinical challenge stems from nonvascular fluids. These include synovial fluid and a source of signal observed within the soft tissues of some patients that we refer to as edema. Due to their long-T, nature, these fluids reduced blood-to-background contrast and in some cases impaired visualization of the vessels of interest. The observed pockets of synovial fluid were sharply defined and confined to joints. They could generally be displaced from the vessels of interest through display rotation of the 3D data set or could be eliminated entirely through segmentation of the 3D volume. The edema, however, appeared as ill-defined to well-defined regions of high signal intensity within the soft tissues. In some patients, the edema was superficial and could easily be excluded from the processed 3D volume using the meihod illustrated in Fig. 4. In other patients the edema was distributed diffusely throughout the leg, yielding globally increased background signal.

Fortunately, T,-Prep-IR is a flexible source of contrast. We have selected three sets of parameters to address the

C

FIG. 4. 3D J2-Prep-IR angiogram of popliteal artery trifurcation of a normal volunteer. A s shown in (c), 3 D information allows MlPs to be limited to the central structures of interest. Data set was acquired with T2-Prep-IR parameters selected to suppress muscle: T€/TI/TR = 80/46/800 ms, NIC),,, = 5/125", resolution = 0.625 X 0.625 x 1.25 mm3, scan time = 13 min. (a) Axial image from the 30 data set at the level of the horizontal line in (b). Circle designates target region for limited MIP shown in (c). Arrow indi- cates orientation of MlPs shown in (b) and (c). (b) MIP through full 3 D volume. (c) MIP through targeted volume shown in (a).

interpat ient variability in deep-venous T, and edema. The firsi set is designed to suppress only muscle relative to arterjal blood. The second suppresses muscle and long-T, veins, and the third suppresses muscle, long-T, veins, and edema. We will first discuss a model for the

3 Ll Flo w-In depen den t Periph era1 Angiography

0.4

347

.

T2-Prep 0.6 I

Arterial Blood

Muscle

-. 0.4

2 -. 0.2

e

-0.4 I

IR

20 40 7 a (ms) a Muscle

-0.2

FIG. 5. Steady-state \Mx,,\ and Mz are plotted for the T,-Prep and IR segments of the T,-Prep-IR sequence, respectively. Figure assumes TR = 800 ms, N = 1, and 6 = 90". Rernaining parameters of TE = 84 rns and TI = 40 ms were selected to null the signal from muscle while maximizing the signal of arterial blood. The T,-Prep portion of the sequence allows the signal of muscle to decay relative to that of arterial blood. The T,-weighted magnetization is then stored along the -z axis and the imaging sequence is delayed an interval TI until the signal from muscle has nulled.

stl-ady-state signal produced by the T,-Prep-IR sequence and then describe the three sets of parameters.

Steady-State Signal

The T,-Prep-IR sequence yields a mixture of T, and T, contrast. If we assume ideal pulses with zero transverse signal before the 6 imaging excitations and the initial 90" excitation of T,-Prep, the steady-state signal resulting from a T,-Prep-IR sequence with N = 1 is:

M,(1 - E, - E,E2 + E,E,)sin 6

1 + E,E, cos 0 M,, = ~ [11

where

If N > 1, we must also consider the time interval, TS, required for a single imaging excitation and acquisition as shown in Fig. 2. In this case, the steady-state magnetization resulting from 6, of a T,-Prep-IR sequence with N excitations is:

w.here

Background Signal: Muscle

The contrast produced by the T,-Prep-IR sequence is per- haps most easily understood when parameters are selected to null the signal from muscle while maximizing the signal from arterial blood. This is appropriate when muscle is the dominant source of background signal in our flow-independent angiograms. For clarity, we will first develop the case of a single acquisition after each contrast preparation, N = 1, with steady-state signal given by Eq. [I I .

For a given TR, there are a variety of (TE, TI) c,ombina- tions that will null the signal from muscle. The steady-state

signal produced by one such combination assuming TR = 800 ms and 6 = 90" is shown in Fig. 5. In this figure we have plotted lMx,, and M, for the T,-Prep and IR segments, respectively. Note that the T,-Prep interval allows the signal from muscle to decay relative to that of arterial blood. At time TE = 84 ms, the prepared TL contrast is stored along the - z axis. The imaging excitation is then delayed an interval TI = 40 ms until the signal from muscle has nulled. Since we have implemented T,-Prep-IR with a 3D acquisition, our analysis assumes that blood lingers within the region of interest (ROI). Any inflow enhancement that does occur will improve blood-to-muscle contrast beyond what is pre- dicted. Our analysis assumes the following relaxation time constants: T, = 800 ms (21), T, musr le = 35 nis

220 ms (35, 38).

- (21), artcrial blood = loo0 ( 3 8 ) 1 and T L x t v i i ~ t l blood -

Figure 6 compares the ability of the T,-Prep and

-0.4, . , , . , , , , , , -0.4 . , , . , , , , , Q

52% Gain in S N R

.- X Q T2 Prep E n , . - I , I . . .

m o.2 1 52y0 Gain i n SNR

E .k I I I

-. . 0 0.02 0.04 0.06 0.08 0.1

Muscle Signal

FIG. 6. Maximum blood signal achievable for a given level of muscle signal is plotted for T,-Prep and T,-Prep-IR techniques. Plot assumes TR = 800 ms and 6 = 90". At typical points of operation (T,-Prep: TE = 200 ms; T,-Prep-IR: TE = 84 ms, TI = 40 ms), T,-Prep-IR yields 52% greater blood SNR than T,-Prep as well as improved muscle suppression. Note that the blood signal generated by T,-Prep-IR is consistently higher than that generated by J,-Prep alone.

348 Brittain et al.

' 500 1000 1500 2000 2500 3000 TR (ms)

a 130, . I

500 1000 1500 2000 2500 3000 TR (ms)

b

I 500 1000 1500 2000 2500 3000

9 0 ' .

TR (ms) C

500 1000 1500 2000 2500 3000 TR (ms)

d FIG. 7. When muscle is the dominant source of background signal, T,-Prep-IR parameters are selec:ted to maximize arterial blood SNR efficiency while nulling the signal from muscle. Results are shown for N = 1. (a) Maximum arterial blood SNR efficiency as a function of TR. Assumes optimal TE, TI, and 6. (b) Optimal TE and TI as a function of TR. (c) Optimal 6 as a function of TR. Optimal 6 is greater than 90" since the longitudinal component of blood is negative-valued at the point of muscle null. (d) Arterial blood SNR generated by T,-Prep-IR sequence is normalized to arterial blood S N R generated by general Ernst-angle excitation recovery sequence. 7,-Prep-IR yields approximately 50% of the SNR efficiency possible and achieves a nearly complete null of muscle signal

T,-Prep-IR sequences to suppress the signal from muscle while maintaining arterial blood signal. For a given level of muscle signal, the maximum arterial blood signal achievable with the two techniques is shown. This result once again assumes TR = 800 ms, 8 = 90°, and no inflow enhancement. Note that the blood signal achieved by T,-Prep-IR is consistently higher than that by T,-Prep alone. Typical points of operation assuming the con- strained TR and 8 art: shown for T,-Prep and T,-Prep-IR. Using the indicated parameters, T,-Prep-IR yields both improved muscle suppression and a 52% gain in arterial blood SNR.

While the contrast produced by the T,-Prep-IR sequence is not sensitive to small changes in imaging parameters, optimization techniques can be used to select appropriate families of parameters to achieve a given contrast goal and to gain an overall understanding of the T,-Prep-IR sequence. For example, when muscle is the dominant source of background signal, we select our parameters to maximize the SNR efficiency of arterial blood while nulling the signal from muscle. If N = I, our goal is to select TE, TI, TI?, and 8 to maximize IM,,II!TR for arterial blood T, and T,, where M,, is given by Eq. [I], while nulling M,, for muscle. Division by "TR normalizes the steady-state signal for differences in scan time.

The TI necessary to null a single species with known TI and T, relaxation times can be expressed as a function of TE and TR:

The 8 that maximizes M,, can also be expressed as a function of TE and TR:

As a result, when N = 1 our task is reduced to the selection of two parameters: TE and TR.

By first selecting the optimal TE for each TR of interest, we can plot the maximum arterial blood SNR efficiency as a function of TR, as shown in Fig. 7a. The optimal TE, TI, and 8 as a function of TR are illustrated in Figs. 7b and 7c. Note that the optimum TE and TI increase with increasing TR as expected. The optimal 8 is greater than 90' because blood's longitudinal magnetization is inverted at the point of muscle null. As explained previously, when the desired 8 is greater than go', we place a nonselective adiabatic inversion before the first imaging excitation as shown in Fig. 2.

(In this case, N = 1 so there is only one excitation.) The actual imaging excitation then has a flip angle of Ha,:tuai =

180' - 8. Figure 7d normalizes the results shown in Fig. 7a to a

standard excitation recovery sequence using the Ernst angle appropriate for each TR. Note that T,-Prep-IR yields approximately 50% of the signal that could be expected from a simple excitation recovery sequence. For this cost, we have achieved an image with nearly complete muscle suppression.

While examining the optimal parameters and resulting image contrast for N = 1 provides an intuitive understanding of the T,-Prep-IR sequence, scan time consider- ations preclude the acquisition of high-resolution 3D images with N = 1 and a TR greater than 1 s. The results presented in this paper were acquired with either 1.25 x 1.25 X 1.25 mm3 resolution over a 18 X 15 X 18 cm,' FOV or 0.625 :< 0.625 X 1.25 mm3 resolution over a 16 X 16 X

16 cm" FOV. These trajectories require 1434 and 4880 excitations, respectively. To maintain reasonable scan times and ensure adequate arterial blood SNR, we typically limit our TR to 800 ms and acquire either three or five excitations in each TR. This results in scan times of 6.4 and 1:3 min for the two trajectories. In our experience,

3 0 Flow-Independent Peripheral Angiography 349

the higher resolution trajectory produces superior clinical results and is therefore preferred. In addition, the optimal parameters for a fixed TR of 800 ms do not differ significantly for N = 3 and N = 5. As a result, we will limit our discussion to the selection of TE, TI, and Omax for a fixed TR = 800 ms and N = 5.

l’he steady-state signal resulting from a T,-Prep-IR sequence with N > 1 is given by Eq. [6]. The TI necessary to null a species with known T, and T, relaxation times is now a function of 8, through 8, as well as TE and TR:

TI =

Since the values for 8, through 8,-, are computed from Om,,, = erV and since TR is restricted to 800 ms as described previously, we select TE and On,, to null the signal from muscle while maximizing arterial blood SNR. (Differences in SNR efficiency for N > 1, M,, , N/, TR, are equivalent to differences in SNR when TR and N are fixed.)

l’he optimal parameters for N = 5 assuming a TR of 800 ms are TE = 80 ms, TI = 43 ms, and Om,, = 139”. However, the contrast produced by the T,-Prep-IR sequence is not sensitive to small changes in parameters. Some of the results in this paper utilize slightly different values for TI and Om,,. The value of TI can be tuned to adjust for interpatient variability in relaxation parameter:;. While this tuning achieves somewhat improved suppression of muscle, it is not necessary in routine clinical use. Even 50% variations from the “optimal”

FIG. 8. Targeted MIP of a flow-independent angiogram of the foot of 81 normal volunteer. Note the fine anatomic detail depicted, with visualization of small vessels including the dorsalis pedis, lateral tarsal, lateral plantar, medial plantar, and metatarsal arteries. Data set was acquired with T,-Prep-IR parameters selected to suppress muscle: TE/TIITR = 80/15/800 ms, NIB,,, = 5/134”, resolution = 0.625 x 0.625 x 1.25 mm3. scan time = 13 min.

value of TI yield a muscle signal that is at most 10% of the arterial blood signal. If a TI other than the calculated “optimal” value is selected, it is in general better to reduce ‘TI from the optimal point rather than increase it since arterial blood signal increases with reduced TI. Due to historical reasons, some of our results were acquired with 8,,,,, values that differ from the optimal choice listed above. However, even a 15” offset from the optimal 8,,, results in only a 6% loss in arterial blood signal from that achieved using the optimal Om,,. The muscle signal is minimally affected by such a change. The critical features of this set of parameters are the moderate TE and TI to null muscle and the emax greater than 90” to maximize arterial blood SNR.

Figure 4 illustrates the popliteal artery trifurcation of a healthy volunteer acquired with parameters selected to null the signal from muscle while maximizing the arterial blood signal. Note the excellent blood-to-muscle contrast. Figure 8 was acquired with similar parameters. This image of the foot of a healthy volunteer demonstrates the ability of our flow-independent technique to depict fine anatomic detail.

Background Signals: Muscle and Long-T, Deep Venous Blood

In some patients, the T, of deep venous blood is increased relative to that of healthy volunteers. This increase jn T, results in incomplete suppression of the deep veins in flow-independent images acquired with the T,-Prep-IR parameters described in the previous section. We have therefore selected a set of parameters that suppresses both long-T, deep venous blood and muscle relative to arterial blood.

Venous blood in patients has an average T, of approximately 120 ms (23) and a T, of 1 s (38). If we utilize the guideline for maximizing contrast in a spin-echo exper- iment (21), we find that the optimal TE to maximize arterial-to-venous blood contrast is 160 ms. This is dou- ble the TE of 80 ms used when muscle is the dominant source of background signal. Using this new TE and the restricted TR of 800 ms, we can select TI and Omax to null the signal from muscle while maximizing the SNR of arterial blood as before. When N = 5, assuming a TE of 160 ms and a TR of 800 ms, the selected parameters are TI = 5 ins (minimum achievable), and Om,, = 135”. The minimum achievable TI is determined by the duration of the spoiler played after the composite [ -go0] pulse as shown in Fig. 1. Once again, the contrast produced is not sensitive to small changes in the selected parameters.

As illustrated in Fig. 9, the increased TE of 160 ms provides improved venous suppression compared with the previously described TE of 80 ms. It also provides additional muscle suppression. In fact, only the minimum achievable TI of 5 ms is necessary to null the signal from muscle. As a result, the performance of a T,-Prep-IK sequence with the parameters described above does not differ significantly from a T,-Prep sequence with TE = 160 ms, TR = 800 ms, Omax = 4 5 O , and N = 5. For consistency, we typically utilize the T,-Prep-IR alterna- tive since the T,-Prep-IR sequence is superior to T,-Prep alone when parameters are chosen to address the other two contrast goals (to suppress muscle or to suppress

350 Brittain et al.

Background Signals: Muscle, Long-T, Deep Venous Blood, and Edema

Initial patient studies revealed two challenges to the clinical application of our flow-independent technique: long-T2 deep venous blood and nonvascular fluids such as edema. We have demonseated that an increased TE of 160 ms provides improved suppression of long-T, deep venous blood. However, without additional compensation, this increase in TE yields an increased ratio of edema signal to arterial blood signal.

To simultaneously address the challenges of nonvascular fluids and long-T, deep venous blood, we again altered our parameter selection crite- a b

FIG. 9. Targeted MIPS generated from 3D T,-Prep-IR angiograms of the popliteal artery trifurcation rion. described in the pre- of a patient with a stenosis (curved arrows) in the popliteal artery. The straight arrows indicate vious section, arterial-to-ve- improved suppression of popliteal vein signal achieved with increased T€. (a) 7;-Prep-lR param- nous blood contrast is eters selected to suppress muscle: T€/TI/TR = 80/25/800 ms, N/@,,,, = 3/125", resolution = optimized with a TE of 160 1.25 x 1.25 x 1.25 mm3, scan time = 6.4 min. (b) T2-Prep-IR parameters selected to suppress ms. This increased TE also muscle and long-T, veins: Tf/TI/TR = 160/5/800 ms, N/f?,,, = 3/125", resolution = 1.25 X 1.25 X provides ample muscle sup-

pression. To suppress nonvas- 1.25 mm3, scan time = 6.4 min.

cular fluids as well, we select muscle, long-T, venous blood, and edema). The critical TI and Omax to maximize arterial-to-fluids contrast, (lMbl features of this set of T,-Prep-IR parameters are the long - (MA), assuming a TE of 160 ms, a TR of 800 ms, and N = TE of 160 ms to suppress long-T, deep venous blood and 5, where IM,, and ]MA represent the magnitude of the the Omax of greater than 90' to maximize arterial blood steady-state signal from arterial blood and nonvascular SNR. fluids, respectively.

a b

The TI of edema is reported to be inhomogeneous but rang- ing up to 4 s (39) with T,s reported up to 700 ms (23). Sy- novial fluid has a T, of 500 ms (23) with TI on the order of 2.5 to 3 s. For our analysis we assume T, = 2 s and T, = 700 ms for nonvascular fluids. This is the longest T, and shortest T, expected and would therefore be the most difficult to suppress relative to arterial blood with the T,- Prep-IR technique. The resulting optimal parameters assuming N = 5, TE = 160 ms, and TR = 800 ms are TI = 5 ms (minimum achievable) and em, = 33". Because the longitudinal

FIG. 10. Targeted MIPS generated from 3D T,-Prep-IR angiograms of the popliteal artery trifurca- magnetization from blood and tion of a patient with long-T, veins and edema. Note the resulting improvement in contrast between nonvascular fluids is inverted at arterial blood and background achieved with a Omax of less than 90". (a) T,-Prep-IR parameters

selected to suppress muscle and long-T, veins: TETTIITR = 160/5/800 rns, N/OmaX = 5/125", the end Of the T2-Prep-1K inter- resolution = 0.625 x 0.625 x 1.25 mm3, scan time = 13 min. (b) T,-Prep-IR parameters selected val, the selected %,, of less to suppress muscle. long-T, veins, and edema: Tf/TI/TR = 160/5/800 ms, N/8,, = 5/57", than 90" suppresses long-TI resolution = 0.625 x 0.625 x 1.25 mm3, scan time = 13 min. materials such as nonvascular

3 L) Flo w-In depen den t Peripheral Angiography 351

Table 1 T,-Prep-IR Parameters Selected to Address Patient-Specific Contrast Requirements

Background Relative arterial

SuDDressed @max blood signal signals N TE TI TR

Muscle 5 80 43 800 139 1 .oo

Muscle 5 160 5 800 135 0.75 Long-T, Veins

Muscle 5 160 5 800 33 0.55 Long-T, Veins Edema

C

FIG. 11. Patient with a stenosis (arrow) at origin of the anterior titiial artery. T,-Prep-IR images vessels regardless of their orientation. Note the superior depiction of this largely in-plane stenosis using T,-Prep-IR as compared with 2D TOF. Also note the close anatomic correlation between t h e x-ray angiogram and the flow- independent result. (a) MIP of a 2D TOF angiogram acquired with (9): TEITR = 7.7/33 ms, 0 = 60", FOV = 16 x 16 cm', matrix =

256 x 128, slice thickness = 2.0 mm, scan time = 5.6 min. (b) MIP of a 3D T,-Prep-IR angiogram acquired with parameters selected to suppress muscle, long-T, veins, and edema: TETTIITR = 160/ 5h300 ms, N/@,,, = 5/57", resolution = 0.625 X 0.625 X 1.25 mm3, scan time = 13 min. (c) X-ray angiograrn.

fluids in the steady state. Al- though the selected parameters once again include a minimal TI, the T,-Prep-IR sequence is more effective than T,-Prep in providing this long- T, suppression since the T,-Prep sequence stores the magnetization along the +z axis rather than the -2

axis. The critical features of this set of T,-Prep-IR parameters are the long TE of 160 ms to suppress long-T, veins and the Om:= of less than goo to suppress long-TI nonvascular fluids.

Figure 10 compares MIPS of a patient with long-T, deep veins and diffuse edema. Images were acquired with parameters designed to suppress muscle and long-T,, deep venous blood and those designed to suppress muscle, long-T, deep venous blood, and nonvascular fluids. Note the improved contrast between arterial blood and background achieved with the decreased Om,,.

Parameter Comparison

Table 1 compares the parameters selected to suppress: muscle; muscle and long-T, veins; and muscle, long-T, veins, ;and nonvascular fluids. Optimal values are shown for N == 5 assuming a TR of 800 ms.

When muscle is the dominant source of background signal, a moderate TE can be used in conjunction with an inversion recovery interval to null the signal from muscle. However, if long-T, veins are present, we use an increased TE to maximize the arterial-to-venous blood contrast. This increased TE also provides additional muscle suppression, so a minimal TI is necessary to null the signal from muscle.

An imaging excitation flip angle, O,,,, of greater than 90" maximizes arterial blood SNR since the signal from arterial blood is inverted at the point of the first imaging excitation. However, this improvement is sacrificed when nonvascular fluids are present. In this case, a Omax of less than goo maximizes arterial-to-fluids contrast.

Arterial blood signal is reduced when parameters are selected to suppress more background tissues. As shown in Table 1, approximately 25% of the arterial blood signal is lost in suppressing muscle and long-T, veins compared with only suppressing muscle. An additional 20% is sacrificed when nonvascular fluids are also suppressed. It is therefore beneficial to select the set of parameters appropriate for a given patient before begin- ning a full 3D acquisition. We currently assess the contrast requirements of each patient by acquiring three thin-slab acquisitions with the parameters listed in Table 1. The full 3D acquisition is then completed with the parameter set that yields the maximum arterial blood SNR and adequate contrast.

CLINICAL RESULTS

To demonstrate the clinical utility of the 3D T,-Prep-IR sequence, we studied patients with known peripheral

352 Brittain et al.

a b

with Buerger’s disease acquired using 2D TOF (Fig. 13a), 3D T,-Prep-IR (Fig. 13b), and x-ray angiography (Fig. 13c). Buerger’s disease, also known as thromhoangi- itis obliterans, causes occlu- sion of small- and medium- sized arteries and veins of the extremities and is most commonly found in patients that smoke heavily. The x- ray angiogram of this patient illustrates the posterior tibial artery but fails to depict the lateral plantar, dorsalis pedis, and lateral tarsal arteries. 2D TOF fails to show any of these vessels. In contrast, 3D T,-Prep-IR illustrates the posterior tibial artery as well as the lateral plantar$ dorsa- Iis pedis* lateral and

FIG. 12. Patient with stenosis (arrows) in the tibioperoneal trunk and severely diseased anterior tibial artery that ends mid-calf. Note the fine anatomic detail in the T,-Prep-IR result and the close correlation to the x-ray angiogram. (a) Targeted MIP generated from a 3 D T,-Prep-IR angiogram acquired with parameters selected to suppress muscle and long-T, veins: T€/TI/TR = 160/33/800 ms, NIH,,,, = 3/125”, resolution = 1.25 X 1.25 X 1.25 mm3, scan time = 6.4 min. (Shown contrast- reversed for ease of comparison). (b) X-ray angiogram.

vascular disease. Each patient was studied with a variety of T,-Prep-IR parameters in an effort to develop a clinical protocol. Results were compared to x-ray angiography and, when scan time allowed, 2D TOF. Com- parison images using 2D TOF were acquired with parameters drawn from the 1995 multicenter trial conducted by Baum et al. (9): TE = 7.7 ms, TR = 33 ms (calf) or 45 ms (foot), 8 = 60°, matrix = 256 X 1 2 8 , FOV = 16 cm, slice thickness = 2.0 mm (calf) or 1.8 mm (foot). A traveling saturation band inferior to the slice was used for venous saturation as specified in the published protocol.

Like x-ray angiography, our flow-independent sequence is capable of imaging vessels with any orientation. Figure 11 compares images acquired with 2D TOF (Fig. I la) , 3D T,-Prep-IR (Fig. lib), and x-ray (Fig. l l c ) angiography. As sholvn in the x-ray angiogram, this patient has a stenosis at the origin of the anterior tibial artery. Note the superior depiction of this largely in-plane stenosis with the flow- independent technique as compared with 2D TOF. This patient exhibited long-T, deep venous signal as well as diffuse edema. The parameters selected to suppress all three sources of background signal were clearly superior in this case as illustrated in Fig. 10.

The flow-independence of the T,-Prep-IR technique also allows robust depiction of stenoses. Figure 1 2 compares a flow-independent angiogram to an x-ray angiogram of a patient with a stenosis in the tibioperoneal trunk. Note the close anatomic correlation between the two images. Scout images revealed long- T, venous signal but minimal edema in this patient volunteer. As a result, parameters designed to suppress muscle and long-T, veins were appropriate.

Finally, our flow-independent method can image slow and in-plane flow that is challenging for conventional techniques. Figure 13 compares images of the foot of a patient

even the metatarsal arteries. Parameters designed to suppress only muscle were used

since this patient had neither edema nor long-T, venous signal.

DISCUSSION

Because its contrast mechanism is not based on flow, 3D T,-Prep-IR is capable of visualizing arteries with any orientation and flow properties. This includes arteries with in- plane, retrograde, and slow flow that can be challenging for TOF techniques. In addition, the rapid, spiral-based 3D acquisition allows images with submillimeter resolution to be obtained in clinically feasible scan times.

We have developed three sets of parameters to respond to the patient-specific contrast requirements of long-T, deep venous blood and nonvascular fluids. These three sets of parameters have been successful in generating images of the popliteal trifurcation with adequate contrast and SNR. However results in the ankle and foot have been more variable. The great saphenous and lesser saphenous veins have increased T, relative to even long-T, deep veins (23). These structures are superficial in the calf and can therefore be eliminated from the volume of interest as illustrated in Fig. 4. In the ankle and foot, however, they are closer to the arteries of interest and therefore pose more of a challenge. While the T, in these superficial veins is increased relative to deep veins, it is still differentiable from the T, of arterial blood. This suggests an approach that either selectively nulls the signal from venous blood or a technique that acquires images at several TEs and estimates TL on a pixel- by-pixel lbasis. The first approach is very similar to our current method of nulling the signal from muscle. Further study is required to evaluate the relative benefits of the two approaches.

Extrinsic contrast agents are another possible source of flow-independent contrast. In this case, arterial-to-background contrast relies on the T, shortening of the contrast

3 0 Flo w-In depen den t Periph era1 Angiograph y 353

C

FIG. 13. Foot of patient with Buerger’s disease (thromboangiitis obliterans). Only T,-Prep-IR demonstrates the dorsal and plantar pedal arterial systems. (a) MIP of 2D TOF angiogram acquired with (9): TEITR = 7.7/45 ms, 8 = 60”. FOV = 16 X 16 cm2, matrix =

256 x 128, slice thickness = 1.8 mm, scan time = 8.5 min. (b) MIP of a 3 D T,-Prep-IR angiogram acquired with parameters selected to suppress muscle: T€/TI/TR = 80/5/800 ms, N/B,,, = 5/125”, resolution = 0.625 x 0.625 x 1.25 mm3, scan time = 13 min. (c) X-ray angiogram obtained 60 s after contrast medium injection, following administration of intra-arterial vasodilator.

agent rather than any flow-related effect. Techniques ex- ploiting this change in relaxation time have produced im- pressive results in a variety of anatomic regions. Such studies are currently done in a dynamic mode (40-50), with arterial-phase images being acquired after the contrast agent

arrives in the region of interest but before venous and tissue enhancement. This restriction on imaging time imposes limits on the resolution and FOV acquired (49, 50). In addition, many of these techniques subtract precontrast and postcontrast images and are therefore susceptible to motion-related artifacts (50). Further study will determine if these challenges present significant limitations in imaging the important small vessels of the distal lower extremity and foot. If approved for routine clinical use, tho recent development of intravascular contrast agents (51) would alleviate the restriction on imaging time and allow steady- state imaging of the extrinsic contrast agent. Such a steady- state technique would produce images of both arterial and venous structures (52). This could present a significant challenge for arterial imaging in the distal lower extremity where each artery is accompanied by two venae comites that are typically of larger diameter than the artery. If T, differences between arterial and venous blood are retained in the presence of intravascular contrast agents, a modified form of the T,-Prep or T,-Prep-IR sequence could poten- tially be used to separate arteries and veins in contrast- enhanced images acquired in steady-state.

We have demonstrated the performance of T,-Prep-IR in visualizing the arteries of the lower extremity. However, different choices of T,-Prep-IR parameters and imaging sequence could adapt T,-Prep-IR for use in different anatomic regions. Potential areas include the cerebral vessels as well as the carotid, coronary, and renal arteries. Parameters could also be selected to address a myriad of venous applications. Cholangiography or perfusion studies represent additional areas of possible application. In addition, while we have implemented T,-Prep-IR with a spherical-stack-of- spirals trajectory, our flow-independent sequence could be combined with almost any readout including echo-planar, RARE, (;RASE, or segmented 2DFT or 3DFT techniques.

In summary, 3D T,-Prep-IR provides flow-independent contrast that visualizes blood regardless of vessel orientation or flow velocity. The T,-Prep-IR parameters can be selected to achieve a variety of contrast goals. Specifi- cally, they can be used to suppress the long-T, deep venous blood and nonvascular fluids identified as clinical challenges in imaging the arteries of the lower extremities. This technique’s ability to image in-plane and slow flow make it a promising clinical tool for the assessment of peripheral artery disease.

ACKNOWLEDGMENTS

The authors thank Adam B. Kerr for his development of maximum intensity projection computation software and display applications.

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Three-dimensional flow-independent peripheral angiography

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