Skip to main content
Top
Published in: Neuroradiology 11/2023

Open Access 22-09-2023 | Advanced Neuroimaging

Impact of cannabis use on brain metabolism using 31P and 1H magnetic resonance spectroscopy

Authors: Maximilian Fenzl, Martin Backens, Silviu Bodea, Miriam Wittemann, Florian Werler, Jule Brielmaier, Robert Christian Wolf, Wolfgang Reith

Published in: Neuroradiology | Issue 11/2023

Login to get access

Abstract

Purpose

This prospective cross-sectional study investigated the influence of regular cannabis use on brain metabolism in young cannabis users by using combined proton and phosphorus magnetic resonance spectroscopy.

Methods

The study was performed in 45 young cannabis users aged 18–30, who had been using cannabis on a regular basis over a period of at least 2 years and in 47 age-matched controls. We acquired 31P MRS data in different brain regions at 3T with a double-resonant 1H/31P head coil, anatomic images, and 1H MRS data with a standard 20-channel 1H head coil. Absolute concentration values of proton metabolites were obtained via calibration from tissue water as an internal reference, whereas a standard solution of 75 mmol/l KH2PO4 was used as an external reference for the calibration of phosphorus signals.

Results

We found an overall but not statistically significant lower concentration level of several proton and phosphorus metabolites in cannabis users compared to non-users. In particular, energy-related phosphates such as adenosine triphosphate (ATP) and inorganic phosphate (Pi) were reduced in all regions under investigation. Phosphocreatine (PCr) showed lowered values mainly in the left basal ganglia and the left frontal white matter.

Conclusion

The results suggest that the increased risk of functional brain disorders observed in long-term cannabis users could be caused by an impairment of the energy metabolism of the brain, but this needs to be verified in future studies.
Appendix
Available only for authorised users
Literature
1.
go back to reference (UNODC) UNOoDaC (2018) World drugs report. United Nations Publications, Vienna (UNODC) UNOoDaC (2018) World drugs report. United Nations Publications, Vienna
11.
go back to reference Pope HG Jr, Yurgelun-Todd D (1996) The residual cognitive effects of heavy marijuana use in college students. Jama 275(7):521–527 CrossRefPubMed Pope HG Jr, Yurgelun-Todd D (1996) The residual cognitive effects of heavy marijuana use in college students. Jama 275(7):521–527 CrossRefPubMed
27.
go back to reference Iotti S, Malucelli E (2008) In vivo assessment of Mg2+ in human brain and skeletal muscle by 31P-MRS. Magnes Res 21(3):157–162 PubMed Iotti S, Malucelli E (2008) In vivo assessment of Mg2+ in human brain and skeletal muscle by 31P-MRS. Magnes Res 21(3):157–162 PubMed
30.
go back to reference Von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP (2007) The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Ann Intern Med 147(8):573–577 CrossRef Von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP (2007) The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Ann Intern Med 147(8):573–577 CrossRef
31.
go back to reference Provencher SW (1993) Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med 30(6):672–679 CrossRefPubMed Provencher SW (1993) Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med 30(6):672–679 CrossRefPubMed
32.
go back to reference Ernst T, Kreis R, Ross B (1993) Absolute quantitation of water and metabolites in the human brain. I. Compartments and water. J Magn Reson Ser B 102(1):1–8 CrossRef Ernst T, Kreis R, Ross B (1993) Absolute quantitation of water and metabolites in the human brain. I. Compartments and water. J Magn Reson Ser B 102(1):1–8 CrossRef
33.
go back to reference Mills T, Ortendahl D, Hylton N, Crooks L, Carlson J, Kaufman L (1987) Partial flip angle MR imaging. Radiology 162(2):531–539 CrossRefPubMed Mills T, Ortendahl D, Hylton N, Crooks L, Carlson J, Kaufman L (1987) Partial flip angle MR imaging. Radiology 162(2):531–539 CrossRefPubMed
34.
go back to reference Wansapura JP, Holland SK, Dunn RS, Ball WS Jr (1999) NMR relaxation times in the human brain at 3.0 tesla. Journal of Magnetic Resonance Imaging: An Official Journal of the International Society for. Magn Reson Med 9(4):531–538 Wansapura JP, Holland SK, Dunn RS, Ball WS Jr (1999) NMR relaxation times in the human brain at 3.0 tesla. Journal of Magnetic Resonance Imaging: An Official Journal of the International Society for. Magn Reson Med 9(4):531–538
35.
go back to reference Mlynárik V, Gruber S, Moser E (2001) Proton T 1 and T 2 relaxation times of human brain metabolites at 3 tesla. NMR Biomed 14(5):325–331 CrossRefPubMed Mlynárik V, Gruber S, Moser E (2001) Proton T 1 and T 2 relaxation times of human brain metabolites at 3 tesla. NMR Biomed 14(5):325–331 CrossRefPubMed
36.
go back to reference Ethofer T, Mader I, Seeger U, Helms G, Erb M, Grodd W et al (2003) Comparison of longitudinal metabolite relaxation times in different regions of the human brain at 1.5 and 3 tesla. Magn Reson Med 50(6):1296–1301 CrossRefPubMed Ethofer T, Mader I, Seeger U, Helms G, Erb M, Grodd W et al (2003) Comparison of longitudinal metabolite relaxation times in different regions of the human brain at 1.5 and 3 tesla. Magn Reson Med 50(6):1296–1301 CrossRefPubMed
37.
go back to reference Träber F, Block W, Lamerichs R, Gieseke J, Schild HH (2004) 1H metabolite relaxation times at 3.0 tesla: measurements of T1 and T2 values in normal brain and determination of regional differences in transverse relaxation. J Magn Reson Imaging 19(5):537–545 CrossRefPubMed Träber F, Block W, Lamerichs R, Gieseke J, Schild HH (2004) 1H metabolite relaxation times at 3.0 tesla: measurements of T1 and T2 values in normal brain and determination of regional differences in transverse relaxation. J Magn Reson Imaging 19(5):537–545 CrossRefPubMed
38.
go back to reference Lu H, Nagae-Poetscher LM, Golay X, Lin D, Pomper M, Van Zijl PC (2005) Routine clinical brain MRI sequences for use at 3.0 tesla. Journal of Magnetic Resonance Imaging: An Official Journal of the International Society for. Magn Reson Med 22(1):13–22 Lu H, Nagae-Poetscher LM, Golay X, Lin D, Pomper M, Van Zijl PC (2005) Routine clinical brain MRI sequences for use at 3.0 tesla. Journal of Magnetic Resonance Imaging: An Official Journal of the International Society for. Magn Reson Med 22(1):13–22
39.
go back to reference Stanisz GJ, Odrobina EE, Pun J, Escaravage M, Graham SJ, Bronskill MJ et al (2005) T1, T2 relaxation and magnetization transfer in tissue at 3T. Magn Reson Med 54(3):507–512 CrossRefPubMed Stanisz GJ, Odrobina EE, Pun J, Escaravage M, Graham SJ, Bronskill MJ et al (2005) T1, T2 relaxation and magnetization transfer in tissue at 3T. Magn Reson Med 54(3):507–512 CrossRefPubMed
40.
go back to reference Choi C, Coupland NJ, Bhardwaj PP, Kalra S, Casault CA, Reid K et al (2006) T2 measurement and quantification of glutamate in human brain in vivo. Magn Reson Med 56(5):971–977 CrossRefPubMed Choi C, Coupland NJ, Bhardwaj PP, Kalra S, Casault CA, Reid K et al (2006) T2 measurement and quantification of glutamate in human brain in vivo. Magn Reson Med 56(5):971–977 CrossRefPubMed
41.
go back to reference Tsai SY, Posse S, Lin YR, Ko CW, Otazo R, Chung HW et al (2007) Fast mapping of the T2 relaxation time of cerebral metabolites using proton echo-planar spectroscopic imaging (PEPSI). Magn Reson Med 57(5):859–865 CrossRefPubMed Tsai SY, Posse S, Lin YR, Ko CW, Otazo R, Chung HW et al (2007) Fast mapping of the T2 relaxation time of cerebral metabolites using proton echo-planar spectroscopic imaging (PEPSI). Magn Reson Med 57(5):859–865 CrossRefPubMed
42.
go back to reference Zaaraoui W, Fleysher L, Fleysher R, Liu S, Soher BJ, Gonen O (2007) Human brain-structure resolved T2 relaxation times of proton metabolites at 3 tesla. Magn Reson Med 57(6):983–989 CrossRefPubMed Zaaraoui W, Fleysher L, Fleysher R, Liu S, Soher BJ, Gonen O (2007) Human brain-structure resolved T2 relaxation times of proton metabolites at 3 tesla. Magn Reson Med 57(6):983–989 CrossRefPubMed
43.
go back to reference Li Y, Srinivasan R, Ratiney H, Lu Y, Chang SM, Nelson SJ (2008) Comparison of T1 and T2 metabolite relaxation times in glioma and normal brain at 3T. J Magn Reson Imaging 28(2):342–350 CrossRefPubMedPubMedCentral Li Y, Srinivasan R, Ratiney H, Lu Y, Chang SM, Nelson SJ (2008) Comparison of T1 and T2 metabolite relaxation times in glioma and normal brain at 3T. J Magn Reson Imaging 28(2):342–350 CrossRefPubMedPubMedCentral
44.
go back to reference Kirov II, Liu S, Fleysher R, Fleysher L, Babb JS, Herbert J et al (2010) Brain metabolite proton T2 mapping at 3.0 T in relapsing-remitting multiple sclerosis. Radiology. 254(3):858–866 CrossRefPubMedPubMedCentral Kirov II, Liu S, Fleysher R, Fleysher L, Babb JS, Herbert J et al (2010) Brain metabolite proton T2 mapping at 3.0 T in relapsing-remitting multiple sclerosis. Radiology. 254(3):858–866 CrossRefPubMedPubMedCentral
45.
go back to reference Ganji SK, Banerjee A, Patel AM, Zhao YD, Dimitrov IE, Browning JD et al (2012) T2 measurement of J-coupled metabolites in the human brain at 3T. NMR Biomed 25(4):523–529 CrossRefPubMed Ganji SK, Banerjee A, Patel AM, Zhao YD, Dimitrov IE, Browning JD et al (2012) T2 measurement of J-coupled metabolites in the human brain at 3T. NMR Biomed 25(4):523–529 CrossRefPubMed
46.
go back to reference Bojorquez JZ, Bricq S, Acquitter C, Brunotte F, Walker PM, Lalande A (2017) What are normal relaxation times of tissues at 3 T? Magn Reson Imaging 35:69–80 CrossRefPubMed Bojorquez JZ, Bricq S, Acquitter C, Brunotte F, Walker PM, Lalande A (2017) What are normal relaxation times of tissues at 3 T? Magn Reson Imaging 35:69–80 CrossRefPubMed
47.
go back to reference Wyss PO, Bianchini C, Scheidegger M, Giapitzakis IA, Hock A, Fuchs A et al (2018) In vivo estimation of transverse relaxation time constant (T2) of 17 human brain metabolites at 3T. Magn Reson Med 80(2):452–461 CrossRefPubMed Wyss PO, Bianchini C, Scheidegger M, Giapitzakis IA, Hock A, Fuchs A et al (2018) In vivo estimation of transverse relaxation time constant (T2) of 17 human brain metabolites at 3T. Magn Reson Med 80(2):452–461 CrossRefPubMed
49.
go back to reference Michaelis T, Merboldt K, Bruhn H, Hänicke W, Frahm J (1993) Absolute concentrations of metabolites in the adult human brain in vivo: quantification of localized proton MR spectra. Radiology 187(1):219–227 CrossRefPubMed Michaelis T, Merboldt K, Bruhn H, Hänicke W, Frahm J (1993) Absolute concentrations of metabolites in the adult human brain in vivo: quantification of localized proton MR spectra. Radiology 187(1):219–227 CrossRefPubMed
50.
go back to reference Smith S, Martin P, Davies J, Edwards R, Stevens A (1990) The assessment of treatment response in non-Hodgkin's lymphoma by image guided 31 P magnetic resonance spectroscopy. Br J Cancer 61(3):485–490 CrossRefPubMedPubMedCentral Smith S, Martin P, Davies J, Edwards R, Stevens A (1990) The assessment of treatment response in non-Hodgkin's lymphoma by image guided 31 P magnetic resonance spectroscopy. Br J Cancer 61(3):485–490 CrossRefPubMedPubMedCentral
51.
go back to reference Rata M, Giles SL, deSouza NM, Leach MO, Payne GS (2014) Comparison of three reference methods for the measurement of intracellular pH using 31P MRS in healthy volunteers and patients with lymphoma. NMR Biomed 27(2):158–162 CrossRefPubMed Rata M, Giles SL, deSouza NM, Leach MO, Payne GS (2014) Comparison of three reference methods for the measurement of intracellular pH using 31P MRS in healthy volunteers and patients with lymphoma. NMR Biomed 27(2):158–162 CrossRefPubMed
52.
go back to reference Lanza IR, Bhagra S, Nair KS, Port JD (2011) Measurement of human skeletal muscle oxidative capacity by 31P-MR spectroscopy: a cross-validation with in vitro measurements. J Magn Reson Imaging 34(5):1143–1150 CrossRefPubMedPubMedCentral Lanza IR, Bhagra S, Nair KS, Port JD (2011) Measurement of human skeletal muscle oxidative capacity by 31P-MR spectroscopy: a cross-validation with in vitro measurements. J Magn Reson Imaging 34(5):1143–1150 CrossRefPubMedPubMedCentral
54.
go back to reference Newman SD, Cheng H, Schnakenberg Martin A, Dydak U, Dharmadhikari S, Hetrick W et al (2019) An investigation of neurochemical changes in chronic cannabis users. Front Hum Neurosci 13:318 CrossRefPubMedPubMedCentral Newman SD, Cheng H, Schnakenberg Martin A, Dydak U, Dharmadhikari S, Hetrick W et al (2019) An investigation of neurochemical changes in chronic cannabis users. Front Hum Neurosci 13:318 CrossRefPubMedPubMedCentral
56.
go back to reference Cupo L, Plitman E, Guma E, Chakravarty MM (2021) A systematic review of neuroimaging and acute cannabis exposure in age-of-risk for psychosis. Transl Psychiatry 11(1):217 CrossRefPubMedPubMedCentral Cupo L, Plitman E, Guma E, Chakravarty MM (2021) A systematic review of neuroimaging and acute cannabis exposure in age-of-risk for psychosis. Transl Psychiatry 11(1):217 CrossRefPubMedPubMedCentral
57.
go back to reference Pretzsch CM, Freyberg J, Voinescu B, Lythgoe D, Horder J, Mendez MA et al (2019) Effects of cannabidiol on brain excitation and inhibition systems; a randomised placebo-controlled single dose trial during magnetic resonance spectroscopy in adults with and without autism spectrum disorder. Neuropsychopharmacology. 44(8):1398–1405 CrossRefPubMedPubMedCentral Pretzsch CM, Freyberg J, Voinescu B, Lythgoe D, Horder J, Mendez MA et al (2019) Effects of cannabidiol on brain excitation and inhibition systems; a randomised placebo-controlled single dose trial during magnetic resonance spectroscopy in adults with and without autism spectrum disorder. Neuropsychopharmacology. 44(8):1398–1405 CrossRefPubMedPubMedCentral
58.
go back to reference Zoccatelli G, Alessandrini F, Rimondo C, Beltramello A, Serpelloni G, Ciceri EF (2020) Magnetic resonance spectroscopy in adolescent cannabis users: metabolites in the anterior cingulate cortex reflects individual differences in personality traits and can affect rehabilitation compliance. Neurol India 68(3):640 CrossRefPubMed Zoccatelli G, Alessandrini F, Rimondo C, Beltramello A, Serpelloni G, Ciceri EF (2020) Magnetic resonance spectroscopy in adolescent cannabis users: metabolites in the anterior cingulate cortex reflects individual differences in personality traits and can affect rehabilitation compliance. Neurol India 68(3):640 CrossRefPubMed
70.
go back to reference Cohen BM, Renshaw PF, Stoll AL, Wurtman RJ, Yurgelun-Todd D, Babb SM (1995) Decreased brain choline uptake in older adults. An in vivo proton magnetic resonance spectroscopy study. Jama. 274(11):902–907 CrossRefPubMed Cohen BM, Renshaw PF, Stoll AL, Wurtman RJ, Yurgelun-Todd D, Babb SM (1995) Decreased brain choline uptake in older adults. An in vivo proton magnetic resonance spectroscopy study. Jama. 274(11):902–907 CrossRefPubMed
71.
go back to reference Cosgrove KP, Mazure CM, Staley JK (2007) Evolving knowledge of sex differences in brain structure, function, and chemistry. Biol Psychiatry 62(8):847–855 CrossRefPubMedPubMedCentral Cosgrove KP, Mazure CM, Staley JK (2007) Evolving knowledge of sex differences in brain structure, function, and chemistry. Biol Psychiatry 62(8):847–855 CrossRefPubMedPubMedCentral
72.
go back to reference Baxter LR Jr, Mazziotta JC, Phelps ME, Selin CE, Guze BH, Fairbanks L (1987) Cerebral glucose metabolic rates in normal human females versus normal males. Psychiatry Res 21(3):237–245 CrossRefPubMed Baxter LR Jr, Mazziotta JC, Phelps ME, Selin CE, Guze BH, Fairbanks L (1987) Cerebral glucose metabolic rates in normal human females versus normal males. Psychiatry Res 21(3):237–245 CrossRefPubMed
73.
go back to reference Hsieh TC, Lin WY, Ding HJ, Sun SS, Wu YC, Yen KY et al (2012) Sex-and age-related differences in brain FDG metabolism of healthy adults: an SPM analysis. J Neuroimaging 22(1):21–27 CrossRefPubMed Hsieh TC, Lin WY, Ding HJ, Sun SS, Wu YC, Yen KY et al (2012) Sex-and age-related differences in brain FDG metabolism of healthy adults: an SPM analysis. J Neuroimaging 22(1):21–27 CrossRefPubMed
93.
go back to reference Herzig DA, Sullivan S, Lewis G, Corcoran R, Drake R, Evans J et al (2015) Hemispheric language asymmetry in first episode psychosis and schizotypy: the role of cannabis consumption and cognitive disorganization. Schizophr Bull 41(suppl_2):S455–SS64 CrossRefPubMed Herzig DA, Sullivan S, Lewis G, Corcoran R, Drake R, Evans J et al (2015) Hemispheric language asymmetry in first episode psychosis and schizotypy: the role of cannabis consumption and cognitive disorganization. Schizophr Bull 41(suppl_2):S455–SS64 CrossRefPubMed
98.
go back to reference Sharma P, Murthy P, Bharath MM (2012) Chemistry, metabolism, and toxicology of cannabis: clinical implications. Iran J Psychiatry 7(4):149–156 PubMedPubMedCentral Sharma P, Murthy P, Bharath MM (2012) Chemistry, metabolism, and toxicology of cannabis: clinical implications. Iran J Psychiatry 7(4):149–156 PubMedPubMedCentral
Metadata
Title
Impact of cannabis use on brain metabolism using 31P and 1H magnetic resonance spectroscopy
Authors
Maximilian Fenzl
Martin Backens
Silviu Bodea
Miriam Wittemann
Florian Werler
Jule Brielmaier
Robert Christian Wolf
Wolfgang Reith
Publication date
22-09-2023
Publisher
Springer Berlin Heidelberg
Published in
Neuroradiology / Issue 11/2023
Print ISSN: 0028-3940
Electronic ISSN: 1432-1920
DOI
https://doi.org/10.1007/s00234-023-03220-y

Other articles of this Issue 11/2023

Neuroradiology 11/2023 Go to the issue