{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,17]],"date-time":"2026-07-17T02:33:26Z","timestamp":1784255606388,"version":"3.55.0"},"reference-count":35,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2025,5,13]],"date-time":"2025-05-13T00:00:00Z","timestamp":1747094400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2025,5,13]],"date-time":"2025-05-13T00:00:00Z","timestamp":1747094400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100003107","name":"Bundesministerium f\u00fcr Gesundheit","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100003107","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100014690","name":"Ministerium f\u00fcr Kultur und Wissenschaft des Landes Nordrhein-Westfalen","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100014690","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002347","name":"Bundesministerium f\u00fcr Bildung und Forschung","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100002347","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100031584","name":"German Center for Diabetes Research","doi-asserted-by":"crossref","id":[{"id":"10.13039\/100031584","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100018693","name":"HORIZON EUROPE Framework Programme","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100018693","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100021371","name":"Schmutzler Stiftung","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100021371","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Eur Radiol Exp"],"abstract":"<jats:title>Abstract<\/jats:title>\n          <jats:sec>\n            <jats:title>Background<\/jats:title>\n            <jats:p>\n              <jats:sup>31<\/jats:sup>P-magnetic resonance spectroscopy (MRS) saturation transfer (ST) allows for noninvasive investigation of liver energy metabolism by assessing flux rates of adenosine triphosphate (ATP) synthesis. However, this technique has rarely been applied at clinical field strengths because of long examination times and contamination from muscle tissue. Our aim was to establish a new method to robustly assess ATP synthesis using a clinical scanner.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Methods<\/jats:title>\n            <jats:p>A prospective single-center study was performed (January 2023\u2013August 2024) within the German Diabetes Study. We established a suitable <jats:sup>31<\/jats:sup>P-MRS ST protocol, tested it <jats:italic>in vitro<\/jats:italic> and <jats:italic>in vivo<\/jats:italic> and assessed its reproducibility. We assessed the hepatic apparent spin-lattice relaxation time of inorganic phosphate (<jats:inline-formula>\n                <jats:alternatives>\n                  <jats:tex-math>$${T}_{1,{Pi}}^{{\\prime} }$$<\/jats:tex-math>\n                  <mml:math xmlns:mml=\"http:\/\/www.w3.org\/1998\/Math\/MathML\">\n                    <mml:msubsup>\n                      <mml:mrow>\n                        <mml:mi>T<\/mml:mi>\n                      <\/mml:mrow>\n                      <mml:mrow>\n                        <mml:mn>1<\/mml:mn>\n                        <mml:mo>,<\/mml:mo>\n                        <mml:mi>P<\/mml:mi>\n                        <mml:mi>i<\/mml:mi>\n                      <\/mml:mrow>\n                      <mml:mrow>\n                        <mml:mo>\u2032<\/mml:mo>\n                      <\/mml:mrow>\n                    <\/mml:msubsup>\n                  <\/mml:math>\n                <\/jats:alternatives>\n              <\/jats:inline-formula>), equilibrium forward rate constant (<jats:inline-formula>\n                <jats:alternatives>\n                  <jats:tex-math>$${k}_{f}$$<\/jats:tex-math>\n                  <mml:math xmlns:mml=\"http:\/\/www.w3.org\/1998\/Math\/MathML\">\n                    <mml:msub>\n                      <mml:mrow>\n                        <mml:mi>k<\/mml:mi>\n                      <\/mml:mrow>\n                      <mml:mrow>\n                        <mml:mi>f<\/mml:mi>\n                      <\/mml:mrow>\n                    <\/mml:msub>\n                  <\/mml:math>\n                <\/jats:alternatives>\n              <\/jats:inline-formula>), and forward ATP synthesis rate (<jats:inline-formula>\n                <jats:alternatives>\n                  <jats:tex-math>$${F}_{{ATP}}$$<\/jats:tex-math>\n                  <mml:math xmlns:mml=\"http:\/\/www.w3.org\/1998\/Math\/MathML\">\n                    <mml:msub>\n                      <mml:mrow>\n                        <mml:mi>F<\/mml:mi>\n                      <\/mml:mrow>\n                      <mml:mrow>\n                        <mml:mi>A<\/mml:mi>\n                        <mml:mi>T<\/mml:mi>\n                        <mml:mi>P<\/mml:mi>\n                      <\/mml:mrow>\n                    <\/mml:msub>\n                  <\/mml:math>\n                <\/jats:alternatives>\n              <\/jats:inline-formula>) in nine control volunteers (CON) (six females) and eight patients (five females) with type 1 diabetes (T1D) and compared differences by ANOVA.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Results<\/jats:title>\n            <jats:p>Reproducibility assessment in nine CON, aged 27\u2009\u00b1\u20094 years (mean\u2009\u00b1\u2009standard deviation), yielded coefficients of variation for repeated measurements of 7.1% and 21.3% for <jats:inline-formula>\n                <jats:alternatives>\n                  <jats:tex-math>$${T}_{1,{Pi}}^{{\\prime} }$$<\/jats:tex-math>\n                  <mml:math xmlns:mml=\"http:\/\/www.w3.org\/1998\/Math\/MathML\">\n                    <mml:msubsup>\n                      <mml:mrow>\n                        <mml:mi>T<\/mml:mi>\n                      <\/mml:mrow>\n                      <mml:mrow>\n                        <mml:mn>1<\/mml:mn>\n                        <mml:mo>,<\/mml:mo>\n                        <mml:mi>P<\/mml:mi>\n                        <mml:mi>i<\/mml:mi>\n                      <\/mml:mrow>\n                      <mml:mrow>\n                        <mml:mo>\u2032<\/mml:mo>\n                      <\/mml:mrow>\n                    <\/mml:msubsup>\n                  <\/mml:math>\n                <\/jats:alternatives>\n              <\/jats:inline-formula> and <jats:inline-formula>\n                <jats:alternatives>\n                  <jats:tex-math>$${k}_{f}$$<\/jats:tex-math>\n                  <mml:math xmlns:mml=\"http:\/\/www.w3.org\/1998\/Math\/MathML\">\n                    <mml:msub>\n                      <mml:mrow>\n                        <mml:mi>k<\/mml:mi>\n                      <\/mml:mrow>\n                      <mml:mrow>\n                        <mml:mi>f<\/mml:mi>\n                      <\/mml:mrow>\n                    <\/mml:msub>\n                  <\/mml:math>\n                <\/jats:alternatives>\n              <\/jats:inline-formula>, respectively. Group comparison revealed higher hepatic <jats:inline-formula>\n                <jats:alternatives>\n                  <jats:tex-math>$${k}_{f}$$<\/jats:tex-math>\n                  <mml:math xmlns:mml=\"http:\/\/www.w3.org\/1998\/Math\/MathML\">\n                    <mml:msub>\n                      <mml:mrow>\n                        <mml:mi>k<\/mml:mi>\n                      <\/mml:mrow>\n                      <mml:mrow>\n                        <mml:mi>f<\/mml:mi>\n                      <\/mml:mrow>\n                    <\/mml:msub>\n                  <\/mml:math>\n                <\/jats:alternatives>\n              <\/jats:inline-formula> (0.34\u2009\u00b1\u20090.03\u2009s<jats:sup>-1<\/jats:sup>\n              <jats:italic>versus<\/jats:italic> 0.16\u2009\u00b1\u20090.03\u2009s<jats:sup>-1<\/jats:sup>; <jats:italic>p<\/jats:italic>\u2009=\u20090.001) and <jats:inline-formula>\n                <jats:alternatives>\n                  <jats:tex-math>$${F}_{{ATP}}$$<\/jats:tex-math>\n                  <mml:math xmlns:mml=\"http:\/\/www.w3.org\/1998\/Math\/MathML\">\n                    <mml:msub>\n                      <mml:mrow>\n                        <mml:mi>F<\/mml:mi>\n                      <\/mml:mrow>\n                      <mml:mrow>\n                        <mml:mi>A<\/mml:mi>\n                        <mml:mi>T<\/mml:mi>\n                        <mml:mi>P<\/mml:mi>\n                      <\/mml:mrow>\n                    <\/mml:msub>\n                  <\/mml:math>\n                <\/jats:alternatives>\n              <\/jats:inline-formula> (35.3\u2009\u00b1\u20093.5\u2009mM\/min <jats:italic>versus<\/jats:italic> 16.4\u2009\u00b1\u20093.5\u2009mM\/min; <jats:italic>p<\/jats:italic>\u2009=\u20090.002) in CON than in T1D, aged 42\u2009\u00b1\u200915 years, respectively.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Conclusion<\/jats:title>\n            <jats:p>This <jats:sup>31<\/jats:sup>P-MRS ST method allowed for robust assessment of hepatic ATP synthesis at clinical field strength and was sensitive enough to detect differences between CON and T1D volunteers.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Relevance statement<\/jats:title>\n            <jats:p>Noninvasive methods to investigate hepatic energy metabolism are urgently needed to evaluate liver health while preventing unnecessary biopsies. For broad clinical applicability, the robustness shown by the proposed method at clinical field strength is crucial.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Trial registration<\/jats:title>\n            <jats:p>ClinicalTrials.gov: NCT01055093\u2014Prospective study on diabetes mellitus and its complications in newly diagnosed adult patients (GDC), NCT01055093, Registered: 01\/22\/2010, <jats:ext-link xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" xlink:href=\"https:\/\/clinicaltrials.gov\/study\/NCT01055093?term=NCT01055093&amp;rank=1#study-overview\" ext-link-type=\"uri\">https:\/\/clinicaltrials.gov\/study\/NCT01055093?term=NCT01055093&amp;rank=1#study-overview<\/jats:ext-link>.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Key Points<\/jats:title>\n            <jats:p>\n              <jats:list list-type=\"bullet\">\n                <jats:list-item>\n                  <jats:p>The proposed magnetic resonance spectroscopy method calculates hepatic ATP synthesis rates at clinical field strength.<\/jats:p>\n                <\/jats:list-item>\n                <jats:list-item>\n                  <jats:p>The protocol shows acceptable reproducibility and spectra without contamination from muscle.<\/jats:p>\n                <\/jats:list-item>\n                <jats:list-item>\n                  <jats:p>The method can detect differences between participants with type 1 diabetes and controls.<\/jats:p>\n                <\/jats:list-item>\n              <\/jats:list>\n            <\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Graphical Abstract<\/jats:title>\n          <\/jats:sec>","DOI":"10.1186\/s41747-025-00588-9","type":"journal-article","created":{"date-parts":[[2025,5,13]],"date-time":"2025-05-13T19:04:44Z","timestamp":1747163084000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["31P-MRS saturation transfer for assessing human hepatic ATP synthesis at clinical field strength"],"prefix":"10.1186","volume":"9","author":[{"given":"Marc","family":"Jonuscheit","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Benedict","family":"Korzekwa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael","family":"Sch\u00e4r","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Julian","family":"Mevenkamp","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stefan","family":"Wierichs","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pavel","family":"Bobrov","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Theresia","family":"Sarabhai","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sabine","family":"Kahl","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael","family":"Roden","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7795-584X","authenticated-orcid":false,"given":"Vera B.","family":"Schrauwen-Hinderling","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2025,5,13]]},"reference":[{"key":"588_CR1","doi-asserted-by":"publisher","first-page":"415","DOI":"10.1016\/j.jhep.2022.09.020","volume":"78","author":"B Fromenty","year":"2023","unstructured":"Fromenty B, Roden M (2023) Mitochondrial alterations in fatty liver diseases. J Hepatol 78:415\u2013429. https:\/\/doi.org\/10.1016\/j.jhep.2022.09.020","journal-title":"J Hepatol"},{"key":"588_CR2","doi-asserted-by":"publisher","first-page":"739","DOI":"10.1016\/j.cmet.2015.04.004","volume":"21","author":"C Koliaki","year":"2015","unstructured":"Koliaki C, Szendroedi J, Kaul K et al (2015) Adaptation of hepatic mitochondrial function in humans with non-alcoholic fatty liver is lost in steatohepatitis. Cell Metab 21:739\u2013746. https:\/\/doi.org\/10.1016\/j.cmet.2015.04.004","journal-title":"Cell Metab"},{"key":"588_CR3","doi-asserted-by":"publisher","first-page":"497","DOI":"10.1056\/NEJMoa2309000","volume":"390","author":"SA Harrison","year":"2024","unstructured":"Harrison SA, Bedossa P, Guy CD et al (2024) A phase 3, randomized, controlled trial of Resmetirom in NASH with liver fibrosis. N Engl J Med 390:497\u2013509. https:\/\/doi.org\/10.1056\/NEJMoa2309000","journal-title":"N Engl J Med"},{"key":"588_CR4","doi-asserted-by":"publisher","first-page":"928","DOI":"10.2337\/dc21-1758","volume":"45","author":"S Gancheva","year":"2022","unstructured":"Gancheva S, Kahl S, Pesta D et al (2022) Impaired hepatic mitochondrial capacity in nonalcoholic steatohepatitis associated with type 2 diabetes. Diabetes Care 45:928\u2013937. https:\/\/doi.org\/10.2337\/dc21-1758","journal-title":"Diabetes Care"},{"key":"588_CR5","doi-asserted-by":"publisher","first-page":"367","DOI":"10.1259\/0007-1285-60-712-367","volume":"60","author":"RD Oberhaensli","year":"1987","unstructured":"Oberhaensli RD, Galloway GJ, Hilton-Jones D et al (1987) The study of human organs by phosphorus-31 topical magnetic resonance spectroscopy. Br J Radiol 60:367\u2013373. https:\/\/doi.org\/10.1259\/0007-1285-60-712-367","journal-title":"Br J Radiol"},{"key":"588_CR6","doi-asserted-by":"publisher","first-page":"17","DOI":"10.1002\/nbm.1940030103","volume":"3","author":"DJ Meyerhoff","year":"1990","unstructured":"Meyerhoff DJ, Karczmar GS, Matson GB et al (1990) Non-invasive quantitation of human liver metabolites using image-guided 31P magnetic resonance spectroscopy. NMR Biomed 3:17\u201322. https:\/\/doi.org\/10.1002\/nbm.1940030103","journal-title":"NMR Biomed"},{"key":"588_CR7","doi-asserted-by":"publisher","first-page":"1079","DOI":"10.1002\/hep.23093","volume":"50","author":"J Szendroedi","year":"2009","unstructured":"Szendroedi J, Chmelik M, Schmid AI et al (2009) Abnormal hepatic energy homeostasis in type 2 diabetes. Hepatology 50:1079\u20131086. https:\/\/doi.org\/10.1002\/hep.23093","journal-title":"Hepatology"},{"key":"588_CR8","doi-asserted-by":"publisher","first-page":"1849","DOI":"10.2337\/db16-0162","volume":"65","author":"S Gancheva","year":"2016","unstructured":"Gancheva S, Bierwagen A, Kaul K et al (2016) Variants in genes controlling oxidative metabolism contribute to lower hepatic ATP independent of liver fat content in type 1 diabetes. Diabetes 65:1849\u20131857. https:\/\/doi.org\/10.2337\/db16-0162","journal-title":"Diabetes"},{"key":"588_CR9","doi-asserted-by":"publisher","first-page":"2892","DOI":"10.1063\/1.1734121","volume":"39","author":"S Fors\u00e9n","year":"1963","unstructured":"Fors\u00e9n S, Hoffman RA (1963) Study of moderately rapid chemical exchange reactions by means of nuclear magnetic double resonance. J Chem Phys 39:2892\u20132901. https:\/\/doi.org\/10.1063\/1.1734121","journal-title":"J Chem Phys"},{"key":"588_CR10","doi-asserted-by":"publisher","first-page":"e14005","DOI":"10.1111\/acel.14005","volume":"22","author":"EJ Fear","year":"2023","unstructured":"Fear EJ, Torkelsen FH, Zamboni E et al (2023) Use of 31P magnetisation transfer magnetic resonance spectroscopy to measure ATP changes after 670\u2009nm transcranial photobiomodulation in older adults. Aging Cell 22:e14005. https:\/\/doi.org\/10.1111\/acel.14005","journal-title":"Aging Cell"},{"key":"588_CR11","doi-asserted-by":"publisher","first-page":"22","DOI":"10.1002\/mrm.26663","volume":"79","author":"C Chen","year":"2018","unstructured":"Chen C, Stephenson MC, Peters A et al (2018) 31P magnetization transfer magnetic resonance spectroscopy: assessing the activation induced change in cerebral ATP metabolic rates at 3\u2009T. Magn Reson Med 79:22\u201330. https:\/\/doi.org\/10.1002\/mrm.26663","journal-title":"Magn Reson Med"},{"key":"588_CR12","doi-asserted-by":"publisher","first-page":"745","DOI":"10.1016\/j.ejrad.2011.09.024","volume":"82","author":"L Valkovi\u010d","year":"2013","unstructured":"Valkovi\u010d L, Chmel\u00edk M, Just Kukurova I et al (2013) Time-resolved phosphorous magnetization transfer of the human calf muscle at 3\u2009T and 7\u2009T: a feasibility study. Eur J Radiol 82:745\u2013751. https:\/\/doi.org\/10.1016\/j.ejrad.2011.09.024","journal-title":"Eur J Radiol"},{"key":"588_CR13","doi-asserted-by":"publisher","first-page":"898","DOI":"10.1002\/mrm.23095","volume":"67","author":"AI Schmid","year":"2012","unstructured":"Schmid AI, Schrauwen-Hinderling VB, Andreas M et al (2012) Comparison of measuring energy metabolism by different 31P-magnetic resonance spectroscopy techniques in resting, ischemic, and exercising muscle. Magn Reson Med 67:898\u2013905. https:\/\/doi.org\/10.1002\/mrm.23095","journal-title":"Magn Reson Med"},{"key":"588_CR14","doi-asserted-by":"publisher","first-page":"188","DOI":"10.1002\/nbm.3242","volume":"28","author":"T Buehler","year":"2015","unstructured":"Buehler T, Kreis R, Boesch C (2015) Comparison of 31P saturation and inversion magnetization transfer in human liver and skeletal muscle using a clinical MR system and surface coils. NMR Biomed 28:188\u2013199. https:\/\/doi.org\/10.1002\/nbm.3242","journal-title":"NMR Biomed"},{"key":"588_CR15","doi-asserted-by":"publisher","first-page":"437","DOI":"10.1002\/nbm.1207","volume":"21","author":"AI Schmid","year":"2008","unstructured":"Schmid AI, Chmel\u00edk M, Szendroedi J et al (2008) Quantitative ATP synthesis in human liver measured by localized 31P spectroscopy using the magnetization transfer experiment. NMR Biomed 21:437\u2013443. https:\/\/doi.org\/10.1002\/nbm.1207","journal-title":"NMR Biomed"},{"key":"588_CR16","doi-asserted-by":"publisher","first-page":"1509","DOI":"10.1002\/mrm.25058","volume":"72","author":"L Valkovi\u010d","year":"2014","unstructured":"Valkovi\u010d L, Bogner W, Gajdo\u0161\u00edk M et al (2014) One-dimensional image-selected in vivo spectroscopy localized phosphorus saturation transfer at 7T. Magn Reson Med 72:1509\u20131515. https:\/\/doi.org\/10.1002\/mrm.25058","journal-title":"Magn Reson Med"},{"key":"588_CR17","doi-asserted-by":"publisher","first-page":"e989","DOI":"10.1210\/clinem\/dgad206","volume":"108","author":"P Fellinger","year":"2023","unstructured":"Fellinger P, Beiglb\u00f6ck H, Semmler G et al (2023) Increased GH\/IGF-I axis activity relates to lower hepatic lipids and phosphor metabolism. J Clin Endocrinol Metab 108:e989\u2013e997. https:\/\/doi.org\/10.1210\/clinem\/dgad206","journal-title":"J Clin Endocrinol Metab"},{"key":"588_CR18","doi-asserted-by":"publisher","first-page":"e134638","DOI":"10.1172\/jci.insight.134638","volume":"5","author":"P Fellinger","year":"2020","unstructured":"Fellinger P, Wolf P, Pfleger L et al (2020) Increased ATP synthesis might counteract hepatic lipid accumulation in acromegaly. JCI Insight 5:e134638. https:\/\/doi.org\/10.1172\/jci.insight.134638","journal-title":"JCI Insight"},{"key":"588_CR19","doi-asserted-by":"publisher","first-page":"1544","DOI":"10.1111\/liv.13451","volume":"37","author":"S Traussnigg","year":"2017","unstructured":"Traussnigg S, Kienbacher C, Gajdo\u0161\u00edk M et al (2017) Ultra-high-field magnetic resonance spectroscopy in non-alcoholic fatty liver disease: novel mechanistic and diagnostic insights of energy metabolism in non-alcoholic steatohepatitis and advanced fibrosis. Liver Int 37:1544\u20131553. https:\/\/doi.org\/10.1111\/liv.13451","journal-title":"Liver Int"},{"key":"588_CR20","doi-asserted-by":"publisher","first-page":"1602","DOI":"10.1007\/s00330-014-3141-x","volume":"24","author":"L Valkovi\u010d","year":"2014","unstructured":"Valkovi\u010d L, Gajdo\u0161\u00edk M, Traussnigg S et al (2014) Application of localized \u00b3\u00b9P MRS saturation transfer at 7\u2009T for measurement of ATP metabolism in the liver: reproducibility and initial clinical application in patients with non-alcoholic fatty liver disease. Eur Radiol 24:1602\u20131609. https:\/\/doi.org\/10.1007\/s00330-014-3141-x","journal-title":"Eur Radiol"},{"key":"588_CR21","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-019-39362-4","volume":"9","author":"P Wolf","year":"2019","unstructured":"Wolf P, Fellinger P, Pfleger L et al (2019) Reduced hepatocellular lipid accumulation and energy metabolism in patients with long standing type 1 diabetes mellitus. Sci Rep 9:2576. https:\/\/doi.org\/10.1038\/s41598-019-39362-4","journal-title":"Sci Rep"},{"key":"588_CR22","doi-asserted-by":"publisher","first-page":"1493","DOI":"10.1002\/mrm.22347","volume":"63","author":"M Sch\u00e4r","year":"2010","unstructured":"Sch\u00e4r M, El-Sharkawy A-MM, Weiss RG et al (2010) Triple repetition time saturation transfer (TRiST) 31P spectroscopy for measuring human creatine kinase reaction kinetics. Magn Reson Med 63:1493\u20131501. https:\/\/doi.org\/10.1002\/mrm.22347","journal-title":"Magn Reson Med"},{"key":"588_CR23","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1186\/s12933-016-0374-9","volume":"15","author":"J Szendroedi","year":"2016","unstructured":"Szendroedi J, Saxena A, Weber KS et al (2016) Cohort profile: the German Diabetes Study (GDS). Cardiovasc Diabetol 15:59. https:\/\/doi.org\/10.1186\/s12933-016-0374-9","journal-title":"Cardiovasc Diabetol"},{"key":"588_CR24","doi-asserted-by":"publisher","first-page":"e5120","DOI":"10.1002\/nbm.5120","volume":"37","author":"M Jonuscheit","year":"2024","unstructured":"Jonuscheit M, Wierichs S, Rothe M et al (2024) Reproducibility of absolute quantification of adenosine triphosphate and inorganic phosphate in the liver with localized 31P\u2010magnetic resonance spectroscopy at 3\u2010T using different coils. NMR Biomed 37:e5120. https:\/\/doi.org\/10.1002\/nbm.5120","journal-title":"NMR Biomed"},{"key":"588_CR25","doi-asserted-by":"publisher","first-page":"433","DOI":"10.1016\/0022-2364(78)90003-3","volume":"29","author":"GA Morris","year":"1978","unstructured":"Morris GA, Freeman R (1978) Selective excitation in Fourier transform nuclear magnetic resonance. J Magn Reson 29:433\u2013462. https:\/\/doi.org\/10.1016\/0022-2364(78)90003-3","journal-title":"J Magn Reson"},{"key":"588_CR26","doi-asserted-by":"publisher","first-page":"799","DOI":"10.1002\/mrm.20024","volume":"51","author":"M Sch\u00e4r","year":"2004","unstructured":"Sch\u00e4r M, Kozerke S, Fischer SE et al (2004) Cardiac SSFP imaging at 3 tesla. Magn Reson Med 51:799\u2013806. https:\/\/doi.org\/10.1002\/mrm.20024","journal-title":"Magn Reson Med"},{"key":"588_CR27","doi-asserted-by":"publisher","first-page":"283","DOI":"10.1016\/0022-2364(86)90031-4","volume":"66","author":"R Ordidge","year":"1986","unstructured":"Ordidge R, Connelly A, Lohman J (1986) Image-selected in vivo spectroscopy (ISIS). A new technique for spatially selective NMR spectroscopy. J Magn Reson 66:283\u2013294. https:\/\/doi.org\/10.1016\/0022-2364(86)90031-4","journal-title":"J Magn Reson"},{"key":"588_CR28","doi-asserted-by":"publisher","first-page":"e4484","DOI":"10.1002\/nbm.4484","volume":"34","author":"A Lin","year":"2021","unstructured":"Lin A, Andronesi O, Bogner W et al (2021) Minimum reporting standards for in vivo magnetic resonance spectroscopy (MRSinMRS): experts\u2019 consensus recommendations. NMR Biomed 34:e4484. https:\/\/doi.org\/10.1002\/nbm.4484","journal-title":"NMR Biomed"},{"key":"588_CR29","doi-asserted-by":"publisher","first-page":"e4347","DOI":"10.1002\/nbm.4347","volume":"34","author":"R Kreis","year":"2020","unstructured":"Kreis R, Boer V, Choi I-Y et al (2020) Terminology and concepts for the characterization of in vivo MR spectroscopy methods and MR spectra: background and experts\u2019 consensus recommendations. NMR Biomed 34:e4347. https:\/\/doi.org\/10.1002\/nbm.4347","journal-title":"NMR Biomed"},{"key":"588_CR30","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-020-15684-0","volume":"11","author":"KHM Roumans","year":"2020","unstructured":"Roumans KHM, Lindeboom L, Veeraiah P et al (2020) Hepatic saturated fatty acid fraction is associated with de novo lipogenesis and hepatic insulin resistance. Nat Commun 11:1891. https:\/\/doi.org\/10.1038\/s41467-020-15684-0","journal-title":"Nat Commun"},{"key":"588_CR31","doi-asserted-by":"publisher","first-page":"716","DOI":"10.1016\/j.mri.2012.01.005","volume":"30","author":"F Du","year":"2012","unstructured":"Du F, Zhang Y, Chen W (2012) Relayed magnetization transfer from nuclear Overhauser effect and chemical exchange observed by in vivo \u00b3\u00b9P MRS in rat brain. Magn Reson Imaging 30:716\u2013721. https:\/\/doi.org\/10.1016\/j.mri.2012.01.005","journal-title":"Magn Reson Imaging"},{"key":"588_CR32","doi-asserted-by":"publisher","first-page":"448","DOI":"10.2337\/dc10-1076","volume":"34","author":"AI Schmid","year":"2011","unstructured":"Schmid AI, Szendroedi J, Chmelik M et al (2011) Liver ATP synthesis is lower and relates to insulin sensitivity in patients with type 2 diabetes. Diabetes Care 34:448\u2013453. https:\/\/doi.org\/10.2337\/dc10-1076","journal-title":"Diabetes Care"},{"key":"588_CR33","doi-asserted-by":"publisher","unstructured":"Kemp GJ (2008) The interpretation of abnormal 31P magnetic resonance saturation transfer measurements of Pi\/ATP exchange in insulin-resistant skeletal muscle. Am J Physiol Endocrinol Metab 294:E640\u2013E642; author reply E643\u2013 E644. https:\/\/doi.org\/10.1152\/ajpendo.00797.2007","DOI":"10.1152\/ajpendo.00797.2007"},{"key":"588_CR34","doi-asserted-by":"publisher","first-page":"C12","DOI":"10.1152\/ajpcell.00100.2011","volume":"301","author":"RS Balaban","year":"2011","unstructured":"Balaban RS, Koretsky AP (2011) Interpretation of \u00b3\u00b9P NMR saturation transfer experiments: what you can\u2019t see might confuse you. Focus on \u201cStandard magnetic resonance-based measurements of the Pi\u2192ATP rate do not index the rate of oxidative phosphorylation in cardiac and skeletal muscles\u201d. Am J Physiol Cell Physiol 301:C12\u2013C15. https:\/\/doi.org\/10.1152\/ajpcell.00100.2011","journal-title":"Am J Physiol Cell Physiol"},{"key":"588_CR35","doi-asserted-by":"publisher","first-page":"193","DOI":"10.1016\/j.ab.2017.01.018","volume":"529","author":"L Valkovi\u010d","year":"2017","unstructured":"Valkovi\u010d L, Chmel\u00edk M, Kr\u0161\u0161\u00e1k M (2017) In-vivo 31P-MRS of skeletal muscle and liver: a way for non-invasive assessment of their metabolism. Anal Biochem 529:193\u2013215. https:\/\/doi.org\/10.1016\/j.ab.2017.01.018","journal-title":"Anal Biochem"}],"container-title":["European Radiology Experimental"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s41747-025-00588-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s41747-025-00588-9\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s41747-025-00588-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,5,13]],"date-time":"2025-05-13T19:04:45Z","timestamp":1747163085000},"score":1,"resource":{"primary":{"URL":"https:\/\/eurradiolexp.springeropen.com\/articles\/10.1186\/s41747-025-00588-9"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,5,13]]},"references-count":35,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2025,12]]}},"alternative-id":["588"],"URL":"https:\/\/doi.org\/10.1186\/s41747-025-00588-9","relation":{},"ISSN":["2509-9280"],"issn-type":[{"value":"2509-9280","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,5,13]]},"assertion":[{"value":"22 January 2025","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"14 April 2025","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"13 May 2025","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"Institutional Review Board approval was obtained. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional committee (Medical Faculty, Heinrich Heine University, D\u00fcsseldorf; ref#4508) and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"All participants provided written informed consent.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors of this manuscript declare relationships with the following companies. MR received fees consulting, lecturing or serving on advisory boards from Astra Zeneca, Boehringer-Ingelheim, Echosens, Eli Lilly, Madrigal, Merck-MSD, and Novo Nordisk and has performed investigator-initiated research with support from Boehringer-Ingelheim, Novo Nordisk, and Nutricia\/Danone to the German Diabetes Center (DDZ). The other authors declare that they have no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"51"}}