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The Proceedings of the American Thoracic Society 2:528-532 (2005)
© 2005 The American Thoracic Society

Hyperpolarized 3-Helium Magnetic Resonance Imaging to Probe Lung Function

Edwin J. R. van Beek and Jim M. Wild

Department of Radiology, Carver College of Medicine, University of Iowa, Iowa City, Iowa; and Academic Unit of Radiology, University of Sheffield, Sheffield, United Kingdom

Correspondence and requests for reprints should be addressed to Edwin J. R. van Beek, M.D., Ph.D., Department of Radiology, Carver College of Medicine, University of Iowa, JPP 3895, 200 Hawkins Drive, Iowa City, IA 52242-1077. E-mail: edwin-vanbeek{at}uiowa.edu

ABSTRACT

Understanding pulmonary pathophysiology has increasing implications for imaging modalities. Although it was sufficient to perform high-resolution computed tomography in the past, the impetus now is on providing quantitative and functional lung data. Magnetic resonance imaging, which was traditionally difficult to perform in the lungs, has developed into a promising technology. One of the main areas of interest is the use of hyperpolarized noble gases, such as 3-He and 129-Xe, which enable high-definition lung imaging that includes information on lung microstructure. It is possible to obtain three-dimensional information on essential pulmonary processes, such as ventilation, oxygen uptake, and spirometry, which offers new insight into lung pathophysiology. This article focuses on the novel aspects of hyperpolarized 3-He magnetic resonance imaging.

Key Words: hyperpolarized 3-helium • imaging • magnetic resonance imaging • lung function

Lung imaging is increasingly developing from morphology into the acquisition of functional information. One of the main reasons to focus on magnetic resonance imaging (MRI) is its capability of obtaining information without the need for ionizing radiation. In addition, MRI has greatly enhanced speed of image acquisition compared with computed tomography (CT) and lung scintigraphy, the main modalities that compete in the area of lung imaging. Early lung images using traditional proton MRI methodology were of a lower quality than those obtained in other parts of the body; this is largely due to the low density of water molecules in lung tissue and the inhomogeneous magnetic field inside the thorax. With the advent of new imaging sequences and the use of exogenous contrast, the modality is starting to develop. Hyperpolarized noble gases were recognized to be of potential interest in the 1990s, and the technology has made its entry from animals into human research (1–9). Thus, hyperpolarized 3-helium (3-He) MRI has been recognized as one of the areas of interest. This article discusses several techniques that have shown encouraging results. More recently, the drive from technique development has been shifting toward quantitative and regional information of lung function, which will assist in more detailed understanding of pulmonary pathophysiology, the earlier diagnosis of lung diseases, and the potential effects of therapeutic intervention.

Although this article focuses on 3-He, MRI of other hyperpolarized nuclei, such as 129-xenon, which were explored in the early years (1–4), are being reevaluated for clinical potential (10, 11). The development of improved polarization methods will undoubtedly influence the choice of gas in the future (12). The use of 3-He has advanced most in the diagnostic testing in humans due to its higher polarization levels, higher signal-to-noise ratio, lack of anesthetic properties, and insolubility (3-He remains in the airways and does not transfer across the lung membranes into the blood) (13). Hyperpolarization of 3-He with optical pumping leads to a greatly enhanced signal when compared with signal produced by thermal polarization (Zeeman polarization) at standard temperatures and field strengths used in clinical MRI. Thus, even with relatively small amounts of gas being administered into the lungs, the signal obtained is capable of producing striking images (14).

REQUIREMENTS FOR 3-He MRI

A standard (proton) MRI system is not capable of producing images after hyperpolarized 3-He inhalation. The system needs to be adapted using a dedicated radiofrequency (RF) amplifier and transmit/receive RF coils tuned to the Larmor frequency of He (48 MHz at 1.5 T). Several types of RF coils, varying from solid birdcage models to flexible wrap-around models, have been tested (6, 8, 9, 14–17).

Imaging of protons exploits the polarization provided by the Zeeman effect in a strong magnetic field, and this polarization can be renewed after RF pulsing, thus allowing images to build up over time. For hyperpolarized 3-He, the optical pumped polarization is typically five orders of magnitude bigger than the Zeeman polarization. Hence, this renewable contribution to the overall signal is negligible. Instead, the polarization providing image contrast can be used only once and is depleted by the action of the RF pulses and through T1-relaxation. This requires careful consideration in data acquisition protocols, which are focused mainly on maintaining signal as long as possible. Furthermore, oxygen has a paramagnetic effect that destroys the polarization of 3-He. Finally, 3-He is a highly diffusive gas, which results in measurable signal loss during the image acquisition. Novel MR sequences have been developed to work within these constraints.

Gas can be polarized on site or using a central production facility, and successful transportation of hyperpolarized 3-He gas has been achieved using air–road courier delivery (17, 18). Once the gas arrives in the MRI room, delivery to the patient most often takes place through inhalation from a Tedlar plastic bag. More sophisticated systems, with options of standardization, have been developed with computer-driven, respirator-assisted delivery via positive-pressure masks.

Safe delivery of hyperpolarized 3-He gas has been demonstrated using both methods in various institutions in Europe and in the United States (19–21). It seems that an anoxic gas mixture of 300 ml 3-He with 700 ml N2 can be delivered safely to a wide range of patients with lung diseases, resulting in only minor adverse events in less than 10% of patients. The presented data and the authors' experience are now in excess of 2,000 deliveries, with an age range of 5 to 80 yr. The computer-driven gas delivery system has the advantage of a bolus delivery within a normal breath of room air and has been equally safe, with the added capability of gas recycling through a closed delivery/recapture system.

TECHNIQUES USING HYPERPOLARIZED 3-He MRI

Spin density measurements after inhalation of 3-He gas is an effective means of demonstrating distribution of the gas through the airspaces. The assumption is that any area with signal is a reflection of ventilated lung.

The images are typically acquired after full inspiration (total lung capacity) during a single breath-hold of approximately 20 s. Several sequences have been used at 1.5 T, including two-dimensional–fast, low-angle single shot (22); steady-state free precession (23); echo planar imaging (24); single-shot, fast-spin echo (25); and, most recently, three-dimensional (3D) gradient echo (26). Various adaptations have been tried to further enhance signal-to-noise ratio, including k-space filtering and variable flip angles (27), but these have not entered clinical applications. The most recent method, 3D gradient echo, results in the entire volume of the lungs being imaged, and 15 to 20 slices can be displayed in any plane at a voxel size (spatial resolution) of approximately 4 x 4 x 2 mm (Figure 1) (26). Although this resolution does not match CT, it is considerably better than lung scintigraphy.



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  		Figure 1. Image acquired from a healthy normal individual using a three-dimensional (3D) imaging sequence. The spatial resolution is exemplified by the surface-rendered volume of the 3D data. The surface contours of the ribs and tracheal rings are visible, as is a peripheral ventilation defect in the posterior left lung (arrow). Reprinted with permission from Reference 26.

 
Ventilation defects are easily seen, but quantifying them has been more problematic. Initial attempts have tried to assess the number and size of defects and their morphologic appearance. Volume measurements have been attempted, but reproducibility between breaths is a factor. More recently, a subtraction method using proton MRI as a template from which hyperpolarized 3-He MRI–ventilated areas are deducted has been developed (28). This yields ventilated lung as a percentage of overall chest cavity volume, and this method seems reproducible.

Using the high diffusivity of 3-He gas, it is feasible to determine the distance of diffusion over a short period (29–32). In a restricted structure, such as the lungs, the length scales of the space in which these atoms can move through Brownian motion become limited. Hence, the apparent diffusion coefficient (ADC), which we can measure through MRI, can be extrapolated as a means of establishing small airspace size. Gradient echo-pulse sequences have been used that collect two or more images at each position with different diffusion weighting gradients. Atoms that move freely, such as gas atoms in enlarged airways and airspaces, experience more dephasing due to the action of these gradients than those in confined spaces. By taking the ratio of these two images, we can spatially map the ADC and identify areas of increased ADC corresponding to emphysematous airway enlargement. Tagging of the motion of atoms has also been successfully performed (33), and studies have demonstrated excellent correlation between ADC and lung diseases (30–32) and positional and gravitational effects (34). One of the main drawbacks of the technique is that ADC can be obtained only in ventilated lung areas.

Dynamic ventilation imaging enables the visualization of gas flow into the lungs during a single respiratory cycle through the application of ultrafast pulse sequences. The technique has been refined from standard proton sequences to radial (35) and spiral acquisition techniques (36, 37), which enable a temporal resolution of approximately 5 ms/frame with a sliding window reconstruction. This technique can determine gas inflow based on signal change, enabling quantification of regional gas flow during a respiratory cycle. Recent studies have shown good correlation between this methodology and pulmonary function testing (38–40). Furthermore, because it optimizes flip angles, it becomes feasible to assess central airway diameter changes during the respiratory cycle (41).

The paramagnetic effect of oxygen results in a predictable (calculable) decrease in signal due to polarization loss. It allows for calculation of oxygen uptake from the airways into the pulmonary blood within lung regions. The method has been developed from a multiple-breath to a single-breath 3D technique (42–45). Because oxygen uptake is dependent on coexisting pulmonary perfusion, the oxygen-dependent signal changes lead to a regional V·A/Q· map (43, 45) and allow for indirect estimation of pulmonary perfusion (46).

APPLICATIONS IN A CLINICAL SETTING

There is increasing evidence that hyperpolarized 3-He MRI offers a uniquely different approach to lung imaging, offering a combination of functional and morphologic information that was previously not achievable. The results in approximately 1,000 subjects worldwide have been reported by researchers studying this technology in a range of physiologic conditions and lung diseases, including asthma, cystic fibrosis, emphysema, smoking-related lung diseases (including lung cancer), lung transplant patients, and animal models of pulmonary embolism. Advantages include the lack of ionizing radiation (allowing repeated studies in normal and young subjects), the noninvasive nature, and the apparent safety.

In healthy individuals, there is homogeneous distribution of 3-He gas throughout the airspaces (9, 14, 16). Small ventilation defects may be visible, particularly in dependent lung regions (47). Gravity- and positional-dependent distribution of gas and changes in airway size on the basis of ADC have been demonstrated (34). The dynamic imaging in normal volunteers reveals a homogeneous gas in- and outflow (see movie at http://www.shef.ac.uk/dcss/medical/radiology/research/chestimg/psd1.html), whereas oxygen-uptake maps demonstrate homogeneous distribution.

Studies comparing healthy nonsmokers with healthy smokers have revealed that there is an increase in mean ADC and heterogeneity (Figure 2 [p. 510]). These findings predate spirometry decline to pathologic levels, suggesting that the technique is much more sensitive at detecting early smoking-related emphysema. Direct correlations have been found between the extent of ventilation defects, smoking history, and lung function tests (once they become abnormal) (30–32). Quantification of ventilated lung volumes using a proton–3-He subtraction technique demonstrated a significant correlation with plethysmography (28).

Patients with varying severity of emphysema have been studied using ventilation distribution and ADC maps (9, 14, 16, 21, 30–32). Correlations were seen between these parameters and spirometry. A disadvantage of ADC maps is that they can be calculated only for ventilated lung regions, but, despite this drawback, the ADC maps show impressive changes based on airspace size enlargement and heterogeneity of ADC with increasing emphysema based on spirometry data and symptoms of patients (30–32). Similar to healthy volunteers, gravity- and posture-dependent effects on ADC can be visualized (34), and these may affect patient well-being and improved understanding of pathophysiology.

Dynamic gas flow imaging has demonstrated ventilation defects and flow patterns compatible with delayed in- and outflow (air trapping) in patients with emphysema (as well as other lung diseases; see movie at http://www.shef.ac.uk/dcss/medical/radiology/research/chestimg/psd1.html) (35, 37, 38). This could be quantified using various methods, giving access to regional spirometry with the potential to further classify the disease and assess treatment response (38–40). Medical, interventional bronchoscopic, and surgical lung volume reduction surgery are interesting areas to study further in this population because conventional methods (e.g., spirometry and CT) are virtually incapable of demonstrating subtle changes or regional dependence.

Patients with lung cancer have been studied (Figure 3), and initial work has focused on image fusion of radiotherapy planning CT with hyperpolarized 3-He MRI (48). It is suggested that the combined modality approach may change the radiation field, which could have a beneficial effect on the development of radiation pneumonitis and could give the option to increase radiation dose to the tumor by using nonfunctioning lung tissue as a window of radiation application.




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  		Figure 3. (Top) A hyperpolarized 3He magnetic resonance image (MRI) that exhibits a complete ventilation obstruction for a patient with a tumor in the upper right lobe. (Bottom) The corresponding conventional proton MRI in which the mass is evident.

 
Pediatric lung diseases have been studied, albeit largely in the young adult population. Patients with asthma have demonstrated ventilation abnormalities before and after challenge with methacholine or exercise challenge (49, 50). Furthermore, the effects of bronchodilator therapy in these patients have been studied (50). Although the studies were small, the results have been impressive, matching spirometric changes and often predating spirometry-based improvement. Patient-reported asthma severity was more difficult to correlate, which suggests that patient's subjective well-being is not necessarily correlated with objective imaging-based findings. Recently, airway diameter changes have been studied in asthma in response to challenge and therapy (41). It seems feasible to study down to fifth generation airways without too much difficulty (Figure 4). It is highly likely that this technology will be able to assist in defining pathophysiologic changes based on medical and interventional therapies.



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  		Figure 4. MRI bronchography with dynamic radial 3He MRI in a healthy volunteer. Visualization of branching to the fifth generation is possible.

 
A limited number of studies have been performed in cystic fibrosis. Several studies have assessed the disease in adults (51, 52). Early attempts have been made to quantify the disease in comparison with chest radiography, CT, and spirometry (53). Hyperpolarized 3-He MRI has shown that ventilation is preferentially reduced in the upper lobes as disease progresses. Quantification of loss of ventilation can be achieved using a proton– 3-He subtraction technique (28). Furthermore, dynamic ventilation studies have demonstrated that airflow obstruction and air trapping occurs in upper lobes and in lower lung zones, which can be quantified using regional spirometry assessment (40). Finally, some anecdotal evidence suggests that the technique can detect early bronchiolitis obliterans in these patients.

Another group of interest consists of patients who are lung transplant recipients, where host-versus-graft disease (bronchiolitis obliterans) is a main cause of concern (54, 55). Studies have shown that hyperpolarized 3-He detects the disease earlier than spirometry or high-resolution CT studies. Hence, MRI may be the technique of choice for follow-up in these patients, allowing repeated studies to determine the optimal timing and planning of lung biopsy, which remains the reference method for demonstrating pathologic evidence of bronchiolitis obliterans.

Pulmonary vascular disease may be an indication in the future. Given the potential to derive regional ventilation–perfusion ratios using oxygen-dependent signal changes, it is anticipated that this technique could be useful in planning for thromboendarterectomy and treatment planning in patients with chronic thromboembolic pulmonary hypertension. Only animal studies have been performed thus far.

CONCLUSIONS

Hyperpolarized 3-He MRI is emerging in clinical research and has shown novel ways to evaluate pathophysiologic parameters in a 3D (regional) setting. It is also capable of probing microstructural changes, which could improve the earlier diagnosis of a range of lung diseases. Based on its capability, we expect that future use of this technology (together with hyperpolarized 129-Xe MRI) will change the way in which therapy response is measured. Furthermore, it is likely that it will improve our understanding of the pathophysiology and subsequent management of lung diseases because it offers complementary information to existing imaging and physiology techniques.

FOOTNOTES

The color figure for this article is on p. 510.

Conflict of Interest Statement: Neither of the authors has a financial relationship with a commercial entity that has an interest in the subject of this manuscript.

(Received in original form July 29, 2005; accepted in final form September 13, 2005)

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