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Fat-Referenced MRI: Quanitaive MRI for Tissue Characterizaion and Volume Measurement
Linköping University, Department of Biomedical Engineering, Division of Biomedical Engineering. Linköping University, Faculty of Science & Engineering. Linköping University, Center for Medical Image Science and Visualization (CMIV).
2018 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The amount and distribution of adipose and lean tissues has been shown to be predictive of mortality and morbidity in metabolic disease. Traditionally these risks are assessed by anthropometric measurements based on weight, length, girths or the body mass index (BMI). These measurements are predictive of risks on a population level, where a too low or a too high BMI indicates an increased risk of both mortality and morbidity. However, today a large part of the world’s population belongs to a group with an elevated risk according to BMI, many of which will live long and healthy lives. Thus, better instruments are needed to properly direct health-care resources to those who need it the most.

Medical imaging method can go beyond anthropometrics. Tomographic modalities, such as magnetic resonance imaging (MRI), can measure how we have stored fat in and around organs. These measurements can eventually lead to better individual risk predictions. For instance, a tendency to store fat as visceral adipose tissue (VAT) is associated with an increased risk of diabetes type 2, cardio-vascular disease, liver disease and certain types of cancer. Furthermore, liver fat is associated with liver disease, diabetes type 2. Brown adipose tissue (BAT), is another emerging component of body-composition analysis. While the normal white adipose tissue stores fat, BAT burns energy to produce heat. This unique property makes BAT highly interesting, from a metabolic point of view.

Magnetic resonance imaging can both accurately and safely measure internal adipose tissue compartments, and the fat infiltration of organs. Which is why MRI is often considered the reference method for non-invasive body-composition analysis. The two major challenges of MRI based body-composition analysis are, the between-scanner reproducibility and a cost-effective analysis of the images. This thesis presents a complete implementation of fat-referenced MRI, a technique that produces quantitative images that can increase both inter-scanner and automation of the image analysis.

With MRI, it is possible to construct images where water and fat are separated into paired images. In these images, it easy to depict adipose tissue and lean tissue structures. This thesis takes water-fat MRI one step further, by introducing a quantitative framework called fat-referenced MRI. By calibrating the image using the subjects' own adipose tissue (paper II), the otherwise non-quantitative fat images are made quantitative. In these fat-referenced images it is possible to directly measure the amount of adipose tissue in different compartments. This quantitative property makes image analysis easy and accurate, as lean and adipose tissues can be separated on a sub-voxel level. Fat-referenced MRI further allows the quantification and characterization of BAT.

This thesis work starts by formulating a method to produce water-fat images (paper I) based on two gradient recall images, i.e.\ 2-point Dixon images (2PD). It furthers shows that fat-referenced 2PD images can be corrected for T2*, making the 2PD body-composition measurements comparable with confounder-corrected Dixon measurements (paper III}).

Both the water-fat separation method and fat image calibration are applied to BAT imaging. The methodology is first evaluated in an animal model, where it is shown that it can detect both BAT browning and volume increase following cold acclimatization (paper IV). It is then applied to postmortem imaging, were it is used to locate interscapular BAT in human infants (paper V). Subsequent analysis of biopsies, taken based on the MRI images, showed that the interscapular BAT was of a type not previously believed to exist in humans. In the last study, fat-referenced MRI is applied to BAT imaging of adults. As BAT structures are difficult to locate in many adults, the methodology was also extended with a multi-atlas segmentation methods (paper VI).

In summary, this thesis shows that fat-referenced MRI is a quantitative method that can be used for body-composition analysis. It also shows that fat-referenced MRI can produce quantitative high-resolution images, a necessity for many BAT applications.

Place, publisher, year, edition, pages
Linköping: Linköping University Electronic Press, 2018. , p. 85
Series
Linköping Studies in Science and Technology. Dissertations, ISSN 0345-7524 ; 1910
Keywords [en]
MRI, water-fat separation, quantitative MRI
National Category
Medical Image Processing
Identifiers
URN: urn:nbn:se:liu:diva-145316DOI: 10.3384/diss.diva-145316ISBN: 9789176853511 (print)OAI: oai:DiVA.org:liu-145316DiVA, id: diva2:1184927
Public defence
2018-03-21, Grantisalen, Campus US, Linköping, 09:15 (English)
Opponent
Supervisors
Note

DiVA-länken var felaktig i den tryckta versionen. Den är ändrad i den elektroniska versionen.

Available from: 2018-02-27 Created: 2018-02-22 Last updated: 2018-02-28Bibliographically approved
List of papers
1. Robust Water Fat Separated Dual-Echo MRI by Phase-Sensitive Reconstruction
Open this publication in new window or tab >>Robust Water Fat Separated Dual-Echo MRI by Phase-Sensitive Reconstruction
2017 (English)In: Magnetic Resonance in Medicine, ISSN 0740-3194, E-ISSN 1522-2594, Vol. 78, no 3, p. 1208-1216Article in journal (Refereed) Published
Abstract [en]

Purpose: To develop and evaluate a robust water-fat separation method for T1-weighted symmetric two-point Dixon data.

Methods: A method for water-fat separation by phase unwrapping of the opposite-phase images by phase-sensitive reconstruction (PSR) is introduced. PSR consists of three steps; 1, identification of clusters of tissue voxels; 2, unwrapping of the phase in each cluster by solving Poisson’s equation; 3, find the correct sign of each unwrapped opposite-phase cluster, so that the water-fat images are assigned the correct identities. The robustness was evaluated by counting the number of water-fat swap artifacts in a total of 733 image volumes. The method was also compared to commercial software.

Results: In the water-fat separated image volumes, the PSR method failed to unwrap the phase of one cluster and misclassified 10. One swap was observed in areas affected by motion and was constricted to the affected area. Twenty swaps were observed surrounding susceptibility artifacts, none of which spread outside the artifact affected regions. The PSR method had fewer swaps when compared to commercial software.

Conclusion: The PSR method can robustly produce water-fat separated whole-body images based on symmetric two-echo spoiled gradient echo images, under both ideal conditions and in the presence of common artifacts.

Place, publisher, year, edition, pages
Wiley-Blackwell, 2017
Keywords
Dixon Imaging; Phase correction; Segmentation; Water-fat separation; Whole-body imaging
National Category
Medical Image Processing Radiology, Nuclear Medicine and Medical Imaging
Identifiers
urn:nbn:se:liu:diva-131134 (URN)10.1002/mrm.26488 (DOI)000407855700040 ()27775180 (PubMedID)
Available from: 2016-09-12 Created: 2016-09-12 Last updated: 2018-02-22
2. MANA - Multi scale adaptive normalized averaging
Open this publication in new window or tab >>MANA - Multi scale adaptive normalized averaging
2011 (English)In: 2011 IEEE International Symposium on Biomedical Imaging: From Nano to Macro, IEEE conference proceedings, 2011, p. 361-364Conference paper, Published paper (Refereed)
Abstract [en]

It is possible to correct intensity inhomogeneity in fat–water Magnetic Resonance Imaging (MRI) by estimating a bias field based on the observed intensities of voxels classified as the pure adipose tissue. The same procedure can also be used to quantify fat volume and its distribution which opens up for new medical applications. The bias field estimation method has to be robust since pure fat voxels are irregularly located and the density varies greatly within and between image volumes. This paper introduces Multi scale Adaptive Normalized Average (MANA) that solves this problem bybasing the estimate on a scale space of weighted averages. By usingthe local certainty of the data MANA preserves details where the local data certainty is high and provides realistic values in sparse areas.

Place, publisher, year, edition, pages
IEEE conference proceedings, 2011
Series
International Symposium on Biomedical Imaging. Proceedings, ISSN 1945-7928
National Category
Medical Laboratory and Measurements Technologies Computer Vision and Robotics (Autonomous Systems) Radiology, Nuclear Medicine and Medical Imaging
Identifiers
urn:nbn:se:liu:diva-67848 (URN)10.1109/ISBI.2011.5872424 (DOI)000298849400083 ()978-1-4244-4128-0 (ISBN)
Conference
IEEE International Symposium on Biomedical Imaging: From Nano to Macro, Chicago, IL, USA, March 30 2011-April 2 2011
Available from: 2011-04-29 Created: 2011-04-29 Last updated: 2018-02-22
3. Characterization of Brown Adipose Tissue by water-fat separated Magnetic Resonance Imaging
Open this publication in new window or tab >>Characterization of Brown Adipose Tissue by water-fat separated Magnetic Resonance Imaging
Show others...
2015 (English)In: Journal of Magnetic Resonance Imaging, ISSN 1053-1807, E-ISSN 1522-2586, Vol. 42, no 6, p. 1639-1645Article in journal (Refereed) Published
Abstract [en]

Purpose: To evaluate the possibility of quantifying brown adipose tissue (BAT) volume and fat concentration with a high resolution, long TE, dual-echo Dixon imaging protocol.

Materials and methods: A 0.42 mm isotropic resolution water-fat separated MRI protocol was implemented by utilizing the second opposite-phase echo and third in-phase echo. Fat images were calibrated with regard to the intensity of nearby white adipose tissue (WAT) to form relative fat content (RFC) images. To evaluate the ability to measure BAT volume and RFC contrast dynamics, rats were divided into two groups that were kept at 4° or 22° C for five days. The rats were then scanned in a 70 cm bore 3.0 T MRI scanner and a human dual energy CT. Interscapular, paraaortal and perirenal BAT (i/pa/pr-BAT) depots as well as WAT and muscle were segmented in the MRI and CT images. Biopsies were collected from the identified BAT depots.

Results: The biopsies confirmed that the three depots identified with the RFC images consisted of BAT. There was a significant linear correlation (p <0.001) between the measured RFC and the Hounsfield units from DECT. Significantly lower iBAT RFC (p = 0.0064) and significantly larger iBAT and prBAT volumes (p=0.0017) were observed in the cold stimulated rats.

Conclusions: The calibrated Dixon images with RFC scaling can depict BAT and be used to measure differences in volume, and fat concentration, induced by cold stimulation. The high correlation between RFC and HU suggests that the fat concentration is the main RFC image contrast mechanism.

Place, publisher, year, edition, pages
John Wiley & Sons, 2015
Keywords
Brown Adipose Tissue; BAT; Fat Water MRI
National Category
Medical Image Processing Radiology, Nuclear Medicine and Medical Imaging
Identifiers
urn:nbn:se:liu:diva-116931 (URN)10.1002/jmri.24931 (DOI)000368258100020 ()
Funder
Knowledge Foundation, 2011.0059
Available from: 2015-04-09 Created: 2015-04-09 Last updated: 2018-02-22
4. Evidence for two types of brown adipose tissue in humans
Open this publication in new window or tab >>Evidence for two types of brown adipose tissue in humans
Show others...
2013 (English)In: Nature Medicine, ISSN 1078-8956, E-ISSN 1546-170X, Vol. 19, no 5, p. 631-634Article in journal (Refereed) Published
Abstract [en]

The previously observed supraclavicular depot of brown adipose tissue (BAT) in adult humans was commonly believed to be the equivalent of the interscapular thermogenic organ of small mammals. This view was recently disputed on the basis of the demonstration that this depot consists of beige (also called brite) brown adipocytes, a newly identified type of brown adipocyte that is distinct from the classical brown adipocytes that make up the interscapular thermogenic organs of other mammals. A combination of high-resolution imaging techniques and histological and biochemical analyses showed evidence for an anatomically distinguishable interscapular BAT (iBAT) depot in human infants that consists of classical brown adipocytes, a cell type that has so far not been shown to exist in humans. On the basis of these findings, we conclude that infants, similarly to rodents, have the bona fide iBAT thermogenic organ consisting of classical brown adipocytes that is essential for the survival of small mammals in a cold environment.

Place, publisher, year, edition, pages
Nature Publishing Group, 2013
Keywords
BAT, MRI
National Category
Medical Genetics Cell and Molecular Biology Medical Image Processing Radiology, Nuclear Medicine and Medical Imaging
Identifiers
urn:nbn:se:liu:diva-91307 (URN)10.1038/nm.3017 (DOI)000318583000037 ()
Funder
Knut and Alice Wallenberg Foundation, 2011.0059
Available from: 2013-04-21 Created: 2013-04-21 Last updated: 2018-02-22Bibliographically approved
5. A randomized trial of cold-exposure on energy expenditure and supraclavicular brown adipose tissue volume in humans
Open this publication in new window or tab >>A randomized trial of cold-exposure on energy expenditure and supraclavicular brown adipose tissue volume in humans
Show others...
2016 (English)In: Metabolism: Clinical and Experimental, ISSN 0026-0495, E-ISSN 1532-8600, Vol. 65, no 6, p. 926-934Article in journal (Refereed) Published
Abstract [en]

Objective

To study if repeated cold-exposure increases metabolic rate and/or brown adipose tissue (BAT) volume in humans when compared with avoiding to freeze.

Design

Randomized, open, parallel-group trial.

Methods

Healthy non-selected participants were randomized to achieve cold-exposure 1 hour/day, or to avoid any sense of feeling cold, for 6 weeks. Metabolic rate (MR) was measured by indirect calorimetry before and after acute cold-exposure with cold vests and ingestion of cold water. The BAT volumes in the supraclavicular region were measured with magnetic resonance imaging (MRI).

Results

Twenty-eight participants were recruited, 12 were allocated to controls and 16 to cold-exposure. Two participants in the cold group dropped out and one was excluded. Both the non-stimulated and the cold-stimulated MR were lowered within the group randomized to avoid cold (MR at room temperature from 1841 ± 199 kCal/24 h to 1795 ± 213 kCal/24 h, p = 0.047 cold-activated MR from 1900 ± 150 kCal/24 h to 1793 ± 215 kCal/24 h, p = 0.028). There was a trend towards increased MR at room temperature following the intervention in the cold-group (p = 0.052). The difference between MR changes by the interventions between groups was statistically significant (p = 0.008 at room temperature, p = 0.032 after cold-activation). In an on-treatment analysis after exclusion of two participants that reported ≥ 8 days without cold-exposure, supraclavicular BAT volume had increased in the cold-exposure group (from 0.0175 ± 0.015 l to 0.0216 ± 0.014 l, p = 0.049).

Conclusions

We found evidence for plasticity in metabolic rate by avoiding to freeze compared with cold-exposure in a randomized setting in non-selected humans.

Place, publisher, year, edition, pages
Elsevier, 2016
Keywords
Brown adipose tissue; Cold exposure; Magnetic resonance imaging; Metabolic rate
National Category
Pharmacology and Toxicology
Identifiers
urn:nbn:se:liu:diva-128200 (URN)10.1016/j.metabol.2016.03.012 (DOI)000376145100013 ()27173471 (PubMedID)
Funder
Knut and Alice Wallenberg Foundation
Note

Funding agencies: Linkoping University; County Council of Ostergotland (LUA-ALF), Sweden; Swedish Research Council [2013-4466, 2012-1652, 2014-2516]; Knut and Alice Wallenberg Foundation; Sahlgrenskas University Hospital (LUA-ALF); European Union grant (DIABAT) [HEALTH-F2-

Available from: 2016-05-22 Created: 2016-05-22 Last updated: 2018-03-22

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