Abstract: Energy metabolism is fundamental for life. It encompasses the utilization of carbohydrates, lipids, and proteins for internal processes, while aberrant energy metabolism is implicated in many diseases. In the present study, using three-dimensional (3D) printing from polycarbonate via fused deposition modeling, we propose a multi-nuclear radiofrequency (RF) coil design with integrated¹H birdcage and interchangeable X-nuclei (²H,¹³C,²³Na, and³¹P) single-loop coils for magnetic resonance imaging (MRI)/magnetic resonance spectroscopy (MRS). The single-loop coil for each nucleus attaches to an arc bracket that slides unrestrictedly along the birdcage coil inner surface, enabling convenient switching among various nuclei and animal handling. Compared to a commercial¹H birdcage coil, the proposed¹H birdcage coil exhibited superior signal-excitation homogeneity and imaging signal-to-noise ratio (SNR). For X-nuclei study, prominent peaks in spectroscopy for phantom solutions showed excellent SNR, and the static and dynamic peaks of in vivo spectroscopy validated the efficacy of the coil design in structural imaging and energy metabolism detection simultaneously.

一种用于多核磁共振成像及波谱的鸟笼线圈与可更换单环线圈的一体化设计

[1]AbdurrachimD,NabbenM,HoerrV,et al.,2017.Diabeticdb/db mice do not develop heart failure upon pressure overload: a longitudinal in vivo PET, MRI, and MRS study on cardiac metabolic, structural, and functional adaptations.Cardiovasc Res,113(10):1148-1160.

[2]AlfonsettiM,SotgiuA,AlecciM,2010.Design and testing of a 1.5 Tesla double-tuned (¹H/³¹P) RF surface coil with intrinsic geometric isolation.Measurement,43(9):1266-1276.

[3]Al-MosalemOA,El-AnsaryA,AttasO,et al.,2009.Metabolic biomarkers related to energy metabolism in Saudi autistic children.Clin Biochem,42(10-11):949-957.

[4]AugathM,HeilerP,KirschS,et al.,2009.In vivo³⁹K,²³Na and¹H MR imaging using a triple resonant RF coil setup.J Magn Reson,200(1):134-136.

[5]BatsiosG,TaglangC,TranM,et al.,2022.Deuterium metabolic imaging reports on TERT expression and early response to therapy in cancer.Clin Cancer Res,28(16):3526-3536.

[6]BeyoğluD,ImbeaudS,MaurhoferO,et al.,2013.Tissue metabolomics of hepatocellular carcinoma: tumor energy metabolism and the role of transcriptomic classification.Hepatology,58(1):229-238.

[7]CaniPD,DelzenneNM,2009.The role of the gut microbiota in energy metabolism and metabolic disease.Curr Pharm Des,15(13):1546-1558.

[8]CherrySR,JonesT,KarpJS,et al.,2018.Total-body PET: maximizing sensitivity to create new opportunities for clinical research and patient care.J Nucl Med,59(1):3-12.

[9]ChoiCH,HaY,VeeraiahP,et al.,2016.Design and implementation of a simple multinuclear MRI system for ultra high-field imaging of animals.J Magn Reson,273:28-32.

[10]ChoiCH,HongSM,HaY,et al.,2017.Design and construction of a novel¹H/¹⁹F double-tuned coil system using PIN-diode switches at 9.4T.J Magn Reson,279:11-15.

[11]ChoiCH,HongSM,FelderJ,et al.,2020.The state-of-the-art and emerging design approaches of double-tuned RF coils for X-nuclei, brain MR imaging and spectroscopy: a review.Magn Reson Imaging,72:103-116.

[12]DeelchandDK,ShestovAA,KoskiDM,et al.,2009.Acetate transport and utilization in the rat brain.J Neurochem,109(Suppl 1):46-54.

[13]de FeyterHM,de GraafRA,2021.Deuterium metabolic imaging ‒ Back to the future. J Magn Reson,326:106932.

[14]de FeyterHM,BeharKL,CorbinZA,et al.,2018.Deuterium metabolic imaging (DMI) for MRI-based 3D mapping of metabolism in vivo.Sci Adv,4(8):eaat7314.

[15]EliaM,CummingsJH,2007.Physiological aspects of energy metabolism and gastrointestinal effects of carbohydrates.Eur J Clin Nutr,61:S40-S74.

[16]FerreiraIL,ResendeR,FerreiroE,et al.,2010.Multiple defects in energy metabolism in Alzheimers disease.Curr Drug Targets,11(10):1193-1206.

[17]GareisD,NeubergerT,BehrVC,et al.,2006.Transmit-receive coil-arrays at17.6T, configurations for 1H, 23Na, and 31P MRI.Concepts Magn Reson Part B Magn Reson Eng,29B(1):20-27.

[18]GruetterR,AdrianyG,ChoiIY,et al.,2003.Localizedin vivo ¹³C NMR spectroscopy of the brain.NMR Biomed,16(6-7):313-338.

[19]HaY,ChoiCH,ShahNJ,2018.Development and implementation of a PIN-diode controlled, quadrature-enhanced, double-tuned RF coil for sodium MRI.IEEE Trans Med Imaging,37(7):1626-1631.

[20]HernandezD,2021.Design of a coplanar interlayer gapped microstrips arrangement for multi-nuclei (¹H,¹⁹F,³¹P, and²³Na) applications in 7T MRI.Appl Sci,11(3):957.

[21]HertzL,DienelGA,2002.Energy metabolism in the brain.Int Rev Neurobiol,51:1-102, IN1-IN4.

[22]HorchRA,WilkensK,GochbergDF,et al.,2010.RF coil considerations for short-T₂ MRI.Magn Reson Med,64(6):1652-1657.

[23]ImamuraH,NhatKPH,TogawaH,et al.,2009.Visualization of ATP levels inside single living cells with fluorescence resonance energy transfer-based genetically encoded indicators.Proc Natl Acad Sci USA,106(37):15651-15656.

[24]JamesJR,GaoY,SoonVC,et al.,2010.Controlled radio-frequency hyperthermia using an MR scanner and simultaneous monitoring of temperature and therapy response by¹H,²³Na and³¹P magnetic resonance spectroscopy in subcutaneously implanted 9L-gliosarcoma.Int J Hyperthermia,26(1):79-90.

[25]KempGJ,MeyerspeerM,MoserE,2007.Absolute quantification of phosphorus metabolite concentrations in human musclein vivo by³¹P MRS: a quantitative review.NMR Biomed,20(6):555-565.

[26]LongCP,AntoniewiczMR,2019.High-resolution¹³C metabolic flux analysis.Nat Protoc,14(10):2856-2877.

[27]LopaschukGD,KarwiQG,TianR,et al.,2021.Cardiac energy metabolism in heart failure.Circ Res,128(10):1487-1513.

[28]LuM,ZhuXH,ZhangY,et al.,2017.Quantitative assessment of brain glucose metabolic rates using in vivo deuterium magnetic resonance spectroscopy.J Cereb Blood Flow Metab,37(11):3518-3530.

[29]MagistrettiPJ,AllamanI,2015.A cellular perspective on brain energy metabolism and functional imaging.Neuron,86(4):883-901.

[30]MedhurstL,ShahnazF,RamnarineN,et al.,2016.Measurement of phosphates in soft drinks: a general chemistry experiment using NMR. In: Soulsby D, Anna LJ, Wallner AS (Eds.),NMR Spectroscopy in the Undergraduate Curriculum:First Year and Organic Chemistry Courses Volume2.ACS Publications,Washington, p.31-37.

[31]MergenthalerP,LindauerU,DienelGA,et al.,2013.Sugar for the brain: the role of glucose in physiological and pathological brain function.Trends Neurosci,36(10):587-597.

[32]MiloneM,WongLJ,2013.Diagnosis of mitochondrial myopathies.Mol Genet Metab,110(1-2):35-41.

[33]MirkesC,ShajanG,ChadzynskiG,et al.,2016.³¹P CSI of the human brain in healthy subjects and tumor patients at 9.4 T with a three-layered multi-nuclear coil: initial results.Magn Reson Mater Phys,29(3):579-589.

[34]Moreno-SánchezR,Rodríguez-EnríquezS,Marín-HernándezA,et al.,2007.Energy metabolism in tumor cells.FEBS J,274(6):1393-1418.

[35]NehrkeK,BörnertP,2012.DREAM—a novel approach for robust, ultrafast, multisliceB₁ mapping.Magn Reson Med,68(5):1517-1526.

[36]O'DonnellME,ChenYJ,LamTI,et al.,2013.Intravenous HOE-642 reduces brain edema and Na uptake in the rat permanent middle cerebral artery occlusion model of stroke: evidence for participation of the blood‒brain barrier Na/H exchanger. J Cereb Blood Flow Metab,33(2):225-234.

[37]RenJM,SherryAD,MalloyCR,2015.³¹P-MRS of healthy human brain: ATP synthesis, metabolite concentrations, pH, andT₁ relaxation times.NMR Biomed,28(11):1455-1462.

[38]RoachPJ,2002.Glycogen and its metabolism.Curr Mol Med,2(2):101-120.

[39]RobbinsNM,SwansonRA,2014.Opposing effects of glucose on stroke and reperfusion injury: acidosis, oxidative stress, and energy metabolism.Stroke,45(6):1881-1886.

[40]RothmanDL,de GraafRA,HyderF,et al.,2019.In vivo¹³C and¹H-[¹³C] MRS studies of neuroenergetics and neurotransmitter cycling, applications to neurological and psychiatric disease and brain cancer.NMR Biomed,32(10):e4172.

[41]Scheuermann-FreestoneM,MadsenPL,MannersD,et al.,2003.Abnormal cardiac and skeletal muscle energy metabolism in patients with type 2 diabetes.Circulation,107(24):3040-3046.

[42]ShapiroEM,BorthakurA,DandoraR,et al.,2000.Sodium visibility and quantitation in intact bovine articular cartilage using high field²³Na MRI and MRS.J Magn Reson,142(1):24-31.

[43]TaglangC,BatsiosG,MukherjeeJ,et al.,2022.Deuterium magnetic resonance spectroscopy enables noninvasive metabolic imaging of tumor burden and response to therapy in low-grade gliomas.Neuro Oncol,24(7):1101-1112.

[44]ValkovičL,ChmelíkM,KrššákM,2017.In-vivo³¹P-MRS of skeletal muscle and liver: a way for non-invasive assessment of their metabolism.Anal Biochem,529:193-215.

[45]von MorzeC,EngelbachJA,BlazeyT,et al.,2021.Comparison of hyperpolarized¹³C and non-hyperpolarized deuterium MRI approaches for imaging cerebral glucose metabolism at 4.7 T.Magn Reson Med,85(4):1795-1804.

[46]WarburgO,1956.On respiratory impairment in cancer cells.Science,124(3215):269-270.

[47]WeissN,HilairePBS,ColschB,et al.,2016.Cerebrospinal fluid metabolomics highlights dysregulation of energy metabolism in overt hepatic encephalopathy.J Hepatol,65(6):1120-1130.

[48]ZhangXT,ZhangY,RoeAW,2021.Ultra-high-field MRI studies of brain structure and function in humans and nonhuman primates: a collaborative approach to precision medicine.Curr Opin Biomed Eng,20:100320.

[49]ZhangY,GaoY,FangK,et al.,2022.Proton/deuterium magnetic resonance imaging of rodents at 9.4T using birdcage coils.Bioelectromagnetics,43(1):40-46.