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The purpose of this work was to develop a novel method to disentangle the intra- and extracellular components of the total sodium concentration (TSC) in breast cancer from a combination of proton (1H) and sodium (23Na ) magnetic resonance imaging (MRI) measurements. To do so, TSC is expressed as function of the intracellular sodium concentration (CIC), extracellular volume fraction (ECV), and the water fraction (WF) based on a three-compartment model of the tissue. TSC is measured from 23Na MRI, ECV is calculated from baseline and post-contrast 1H T1 maps, while WF is measured with a 1H chemical shift technique. CIC is then extrapolated from the model. Proof-of-concept was demonstrated in three healthy subjects and two patients with triple-negative breast cancer. In both patients, TSC was two to threefold higher in the tumor than in normal tissue. This alteration mainly resulted from increased CIC (~30 mM), which was ~130% greater than in healthy conditions (10–15 mM) while the ECV was within the expected range of physiological values (0.2–0.25). Multinuclear MRI shows promise for disentangling CIC and ECV by taking advantage of complementary 1H and 23Na measurements.

Introduction

Breast cancer is the most commonly diagnosed type of cancer among women worldwide. Breast imaging is an essential tool in breast cancer screening and diagnosis. Mammography is the preferred imaging methodology used to detect breast cancer at an early stage. Other imaging techniques, such as ultrasound (US) and magnetic resonance imaging (MRI), are often used to supplement mammography. Annual screening breast MRI is recommended in addition to mammography in high-risk patients (e.g., patients with a family history of breast cancer, BRCA gene mutation, or history of chest radiation). Breast MRI also helps evaluate the extent of the disease, the response to neoadjuvant chemotherapy (NACT), and the integrity of silicone implants. Dynamic contrast-enhanced (DCE) MRI is the backbone of any breast MRI protocol due to its high sensitivity for detecting breast cancer, providing rich morphological, tissue vascularity, and pharmacokinetic information. Additionally, diffusion-weighted imaging (DWI) provides information on tissue organization at the microscopic level. However, all these markers are surrogates for the underlying metabolic activity. Advances in high and ultra-high field MRI have spurred renewed interest in X-nuclei (non-hydrogen) MRI applications in breast cancer. Unlike standard proton (1H) MRI, X-nuclei MRI can provide functional information by probing ions involved in metabolic processes at the cellular level. This added metabolic information could complement the morphological data offered by standard MRI.

Sodium (23Na) MRI non-invasively and directly probes sodium ions, which play a key role in regulating osmotic pressure and ionic homeostasis at the cellular level. Studies have shown that total sodium concentration (TSC) is significantly higher in malignant breast lesions compared to benign lesions and healthy fibroglandular tissue. Further, TSC is inversely correlated with the apparent diffusion coefficient measured with diffusion MRI, with low values typically indicating high cellularity and malignancy. While TSC can be quantified with 23Na MRI, it is influenced by two main factors that confound its physiological interpretation: (1) the intracellular sodium concentration (CIC), governed by the sodium-potassium pump, and (2) the extracellular volume (ECV) fraction, which can vary with cellular swelling, death, or edema. An increase in TSC could result from an increase in CIC or an increase in ECV while maintaining a constant extracellular sodium concentration, or a combination of both. Therefore, CIC and ECV could be more specific indicators of cell viability, inflammation, or fluid content compared to TSC alone. Unfortunately, the intrinsic low signal-to-noise ratio (SNR) of 23Na MRI, along with uncertain relaxation properties of intra- and extracellular sodium, complicates the disentanglement of these two contributions.

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Efforts have been made to isolate the intracellular sodium concentration using multiple quantum filtering (MQF) or inversion recovery (IR) 23Na MRI techniques. MQF sequences use a specific pattern of radiofrequency (RF) pulses and phase cycling to separate intra- and extracellular compartments based on differences in their biexponential T2 relaxation properties. In biological tissues, the presence and evolution of multiple quantum coherences related to restricted spin motion and tissue anisotropy can be detected with MQF sequences. The main assumption in MQF is that the isolated multiple quantum coherence signal originates mainly from the intracellular compartment due to its packed arrangement of proteins and molecules that restrict sodium spin motion to a higher degree compared with the extracellular environment. MQF proponents argue that by carefully selecting the amplitudes and phases of the RF pulses, it is possible to selectively isolate the triple quantum coherence component from the total sodium signal. However, the isolated signal is only a small fraction of the total signal (approximately 10%), which is already characterized by low 23Na SNR. Moreover, the main MQF assumption remains controversial, with many studies showing contributions of the extracellular space to the signal originating from double or triple quantum coherences. Whereas MQF relies on T2, IR techniques rely on T1 contrast to separate the intra- and extracellular compartments: the intracellular space exhibits shorter T1 due to its denser environment as opposed to the extracellular space and fluids which typically have longer T1. To separate the signals, 23Na IR suppresses the fluid component, which can be subtracted from a distinct measurement of the total signal to obtain an intracellular weighted contribution. Similarly to MQF, the assumption of different T1 between intra- and extracellular space based on the differences in the two environments is inaccurate and IR methods can only offer an "intracellular weighted" signal rather than isolating the absolute intracellular signal. Other technical drawbacks include a long, power-demanding inversion pulse that can be sensitive to B0 and B1 inhomogeneity, along with a priori knowledge of fluid T1. Moreover, like MQF, IR utilizes only 23Na measurements, which are inherently noisy.

In this study, we eliminate the need to rely on carefully calibrated RF pulses, subtle differences in relaxation times, and undiversified low-SNR 23Na data. We propose a pipeline that takes advantage of a combination of 1H and 23Na MRI measurements to enable CIC and ECV quantification in breast cancer. We used a three-compartment tissue model to describe the TSC in terms of components that can be measured by either 1H or 23Na MRI measurements. According to the model, an imaging voxel comprises two main compartments: water and fat. The water compartment can moreover be decomposed in the intracellular and the extracellular spaces. Each compartment is characterized by its own sodium concentration and volume fraction (CIC and ICV, CEC and ECV, Cfat and Vfat respectively for the intracellular, extracellular, and fat compartments). Summing ICV and ECV gives the water fraction (WF). While the TSC is only accessible with 23Na MRI, the ECV and the WF are morphological features that can be measured via 1H MRI. By extracting ECV using contrast uptake information and WF from a chemical shift technique, we are able to determine CIC. Specifically, TSC was related to 23Na MRI signal intensity using images from a multi-compartment calibration phantom with known sodium concentrations and relaxation times. ECV was measured from the ratio of the 1H T1 change due to contrast uptake in the breast related to 1H T1 change in a reference tissue. This method has been largely investigated in cardiac MRI to assess myocardial infarction and fibrosis. While in cardiac applications blood is used as a reference with known volume fraction, here we chose the pectoral muscle as reference tissue due to its proximity to the breast. The WF was calculated using a four-point Dixon-based technique. Once all other quantities in the model are measured, CIC can then be extracted from the model equation. The pipeline in which 1H gradient echo (GRE) images, 1H T1 maps, and 23Na images allow CIC quantification is illustrated.

The purpose of this study was to investigate the feasibility of exploiting robust, high SNR 1H MRI to resolve the intra- and extracellular components of TSC in breast cancer from complementary 1H/23Na MRI measurements at 7 T. To demonstrate proof of concept, phantom data were collected for validation and in vivo scans were carried out on three healthy female subjects and two female patients with triple-negative breast cancer (TNBC). Additional volunteers were recruited to measure TSC repeatability and 23Na relaxation times.

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