E-ISSN: 1305-3612
Proton density fat fraction: magnetic resonance imaging applications beyond the liver
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Modality-Based (US, CT, MRI, PET-CT) Imaging – Review
VOLUME: 28 ISSUE: 1
P: 83 - 91
January 2022

Proton density fat fraction: magnetic resonance imaging applications beyond the liver

Diagn Interv Radiol 2022;28(1):83-91
Ilkay S. Idilman
A. Elcin Yildiz
Ali Devrim Karaosmanoglu
Mustafa N. Ozmen
Deniz Akata
Musturay Karcaaltincaba
1. Department of Radiology, Hacettepe University School of Medicine, Ankara, Turkey
No information available.
No information available
Received Date: 07.08.2021
Accepted Date: 26.11.2021
Online Date: 05.01.2022
Publish Date: 05.01.2022
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ABSTRACT

Magnetic resonance imaging-proton density fat fraction (MRI-PDFF) is an emerging quantitative imaging biomarker that accurately measures the fat fraction of tissue by correcting factors influencing magnetic resonance signal intensity. Beyond fat quantification, it also measures R2* which is a direct measure of iron concentration. The utilization of MRI-PDFF in liver diseases is well established. In the present review, we focused on applications of MRI-PDFF in different body areas including pancreas, bone, muscle, spleen, testis, visceral, and subcutaneous adipose tissue. Future studies can enable tracking of quantitative fat fraction changes in different organs simultaneously, which can be critical in understanding fat metabolism.

Keywords:

Main points

• Pancreas MRI-PDFF is shown to be related to various metabolic, inflammatory, and neoplastic iseases.

• B one marrow MRI-PDFF allows quantification of fatty replacement which is related to loss of bone mass.

• B one marrow MRI-PDFF determination can allow differentiation of benign fractures from malignancy-associated ones.

• Muscle MRI-PDFF can be used for the determination of muscle strength and also muscle involvement in neuromuscular diseases.

Proton density fat fraction (PDFF) derived by chemical-shift encoded magnetic resonance imaging (CSE-MRI) which is also known as magnetic resonance imaging-proton density fat fraction (MRI-PDFF) is a chemical shift-based water and fat separation technique that addresses the factors influencing magnetic resonance signal intensity in the quantitative assessment of fat.1-3 MRI-PDFF provides accurate spectral modeling of fat and gives the ratio of the density of mobile protons from triglycerides and the total density of protons from mobile triglycerides and mobile water that reflects the concentration of mobile triglycerides within the tissue.3 The technique allows assessment of the tissue in a short time with quantification of fat by drawing a region of interest (ROI) on the generated fat fraction maps. Iron content can also be evaluated by R2* maps obtained simultaneously with this technique. The accuracy of MRI-PDFF in quantification of hepatic fat is demonstrated in comparative studies with magnetic resonance spectroscopy1-3 and liver biopsy.4-6 It has also been shown to be an effective tool in the follow-up evaluation of patients with nonalcoholic fatty liver disease (NAFlD).7, 8 MRI-PDFF is also accepted as a useful biomarker to assess treatment response in the setting of early phase clinical trials in nonalcoholic steatohepatitis.9 It has been shown to be feasible to evaluate fat accumulation in different tissues with MRI-PDFF.10-14 In this review article, we focused on recent applications of MRI-PDFF beyond the liver including pancreas, bone marrow, muscle, spleen, testis, visceral, and subcutaneous adipose tissue.

Pancreas

The presence of fat in the pancreatic tissue has been recognized with pathology specimens and imaging modalities for decades. It was shown that MRI-PDFF is feasible in the assessment of pancreatic fat with a moderate and significant correlation with histopathologic pancreatic lipomatosis grade.10 As a result of the assessment of the whole pancreas with this technique, fat fractions among different regions of the pancreas were also evaluated. Kühn et al.15 observed statistically significantly different fat fractions in the pancreatic head, body, and tail with the higher fat fraction in the pancreatic body in the general population. However, other studies failed to observe such a difference in these regions.11, 16 As a result of the variability of pancreatic fat fraction according to the positions of the ROI, Kato et al.17 offered a 3D evaluation of pancreatic fat, which measures pancreatic fat in each slice with a freehand ROI. However, it is hard to delineate the contours of the pancreas especially in patients with atrophy or a high degree of pancreatic steatosis and interdigitating peripancreatic fat may cause potential sampling errors.

Pancreatic fat was evaluated with MRIPDFF in various metabolic, inflammatory, and neoplastic diseases. The metabolic diseases were initially studied and research focused on metabolic associations such as NAFlD, insulin resistance, and diabetes mellitus.11, 16, 18-24 Patel et al.16 evaluated ectopic fat deposition in the pancreas and observed that MRI-determined pancreatic fat correlates with histology-determined liver steatosis grade in patients with NAFlD. In this study, researchers also observed higher pancreatic fat in patients with a NAFlD activity score higher than 5 and with no fibrosis according to the liver biopsy.16 Idilman et al.11 also observed slightly higher pancreatic fat in patients with hepatic steatosis and nonalcoholic steatohepatitis with no statistical significance. Several studies demonstrated a correlation between hepatic and pancreatic MRI-PDFF in patients with chronic liver disease19 and NAFlD18, 20, 21 in contrast with just one study, whose results can be explained by the limited patient number.11

In another study by Patel et al.,20 it was shown that patients with a higher homeostatic model assessment of insulin resistance (HOMA-IR) had higher pancreatic and liver fat (Figure 1). Idilman et al.11 also evaluated pancreatic fat in a population of NAFlD and observed higher pancreatic fat in patients with diabetes mellitus. Sarma et al.21 demonstrated increased liver and pancreas fat and adipose tissue in patients with type 2 diabetes mellitus. In contrast with these studies, Kühn et al.15 compared pancreatic fat with MRI-PDFF in individuals with normal glucose tolerance, prediabetes and type 2 diabetes mellitus and observed no statistically significant differences in subgroups. There are also some studies evaluating pancreatic fat with MRI-PDFF in the pediatric and adult populations.22, 23 Trout et al.22 observed significant correlations between pancreatic fat and patient weight, body mass index (bMI) z-score, the absolute fat area in each location of abdominal fat stores, and with midline abdominal fat thickness. In this study, the pancreatic fat fraction was not found to be a predictive factor for diabetes status.22 However, a recent study that evaluated Chinese adolescents with obesity and NAFlD showed that liver and pancreas MRI-PDFF were both independent predictors for beta-cell dysfunction and metabolic syndrome.23 They also showed an association between fatty pancreas and insulin resistance.23 These results may be due to temporal changes during different stages of metabolic diseases.

There are also heterogeneous studies evaluating the relationship between pancreatic fat and different tissues and diseases as well as temporal changes. A decrease in pancreatic MRI-PDFF in accordance with the reduction in liver fat with weight loss in obese patients was observed.24 Singh et al.25 evaluated individuals after acute pancreatitis and observed that higher pancreatic fat depots are associated with the development of diabetes after acute pancreatitis. In another study, the authors evaluated the association between plasma metabolomics profile and liver MRI-PDFF, pancreas MRIPDFF, and visceral adipose tissue (vAT) volume and found that two metabolites (one lysine-derivate and the bile acid conjugate taurodeoxycholate) were positively associated with pancreas PDFF which shows a possible different pathway leading to fat accumulation in the pancreas as opposed to liver and vAT26 (Table 1). Idilman et al.18 also demonstrated significant but weak correlations among pancreas PDFF and vAT and bMI, but no correlation was observed between pancreas PDFF and subcutaneous adipose tissue (SAT). Oguz et al.27 evaluated pancreas PDFF in lean polycystic ovarian syndrome (PCOS) patients in comparison with healthy age and bMI matched women and observed a higher liver PDFF in the PCOS group with no difference in terms of pancreas PDFF. Despite conflicting results, a recent meta-analysis demonstrated that the presence of fatty pancreas is associated with a significantly increased risk of arterial hypertension, diabetes mellitus, and metabolic syndrome.28 In this study, a normal pancreatic fat cutoff point of 6.2% was also suggested.28

Kühn et al.15 observed that pancreatic PDFF showed a positive association with age and bMI and a negative association with serum lipase activity (P < .001). In accordance with this study, Kromrey et al.29 observed significantly higher pancreatic fat content in subjects with impaired pancreatic exocrine function in comparison to subjects with normal function. They also observed an inverse correlation between pancreatic fat and fecal elastase levels. boga et al.30 evaluated 97 NAFlD patients and observed that increasing pancreatic steatosis is associated with a higher frequency of pancreatic exocrine insufficiency. Tahtaci et al.31 also demonstrated a lower fecal elastase level in patients with pancreatic steatosis. Interestingly, Fukui et al.32 observed that the pancreatic cancer patients had higher MRIPDFF and histologic pancreatic fat fraction and in multivariate analysis, pancreas MRIPDFF was found to be the sole independent risk factor for pancreatic cancer. These results suggest that there are complex relationships between pancreatic fat and metabolic, inflammatory, and neoplastic diseases which should comprehensively be evaluated with further studies.

Bone marrow

MRI-PDFF has also been used for the evaluation of the bone marrow.12-14,33,34 It is known that bone marrow fat increases with age presumably as a result of fatty bone marrow replacement with loss of bone mass of the vertebrae.35 The ratio of adipocytic to hematopoietic/stromal tissue is shown to be higher in osteoporotic bone in comparison with normal controls.36 Studies evaluating lumbar vertebral MRI-PDFF in comparison with bone mineral densitometry (bMD) examination observed a statistically significant negative correlation between MRI-PDFF and bMD with higher MRI-PDFF in patients with osteopenia or osteoporosis.12-14 Ergen et al.13 also proposed a cutoff value of 39.2% for differentiation of osteoporotic and/or osteopenic groups from the healthy population. guo et al.33 evaluated the role of MRI-PDFF in combination with quantitative susceptibility mapping (QSM), which is increased with osteopenia and osteoporosis, and proposed a combination of QSM and MRI-PDFF for the assessment of postmenopausal osteoporosis. Martel et al.34 reported a reliable assessment of proximal femur bone marrow adipose tissue quantity and composition with MRI-PDFF and validated with magnetic resonance spectroscopy. baum et al.37 evaluated the age-related changes in bone marrow with MRI-PDFF and observed an accelerated fatty conversion of bone marrow in females, which is more evident after menopause (Figure 2). There are also studies evaluating bone marrow fat with MRI-PDFF in patients with known or suspected NAFlD.11, 38 It was demonstrated that there is also a close correlation between vertebral MRI-PDFF and age in NAFlD patients with slightly higher vertebral body MRI-PDFF in patients with type 2 diabetes mellitus.11 Yu et al.38 demonstrated a positive correlation between hepatic and lumbar MRI-PDFF in children with known or suspected NAFLD.

The differences in fat composition during specific treatments were also evaluated with MRI-PDFF by researchers.34, 39, 40 Carmona et al.39 demonstrated increased bone marrow MRI-PDFF in accordance with decreasing peripheral blood cell counts in patients receiving highly myelotoxic treatments for different malignancies. Martel et al.34 showed altered bone marrow fat metabolism in the proximal femur by MRI-PDFF in patients using glucocorticoids. Dieckmeyer et al.40 evaluated patients with breast cancer receiving combined aromatase inhibitor and bisphosphonate therapy and observed significantly increased PDFF after 12 months of treatment in comparison to patients receiving isolated aromatase inhibitor. These findings are promising to quantify temporal changes in MRI-PDFF of specific patient populations whose treatment efficacy monitoring is essential.

The role of MRI-PDFF was also evaluated in bone lesions, including both focal and inflammatory. bray et al.41 evaluated patients with sacroiliitis and observed that MRI-PDFF values were significantly lower in areas of edema compared to normal bone marrow. Increased MRI-PDFF values were observed in fat metaplasia areas of patients with known or suspected sacroiliitis.41, 42 Schmeel et al.43 evaluated a total of 66 patients and observed that MRI-PDFF of non-neoplastic vertebral lesions is significantly higher than that of malignant lesions. In this study, they proposed a cutoff value of 6.4% to differentiate between benign and malignant lesions.43 Kwack et al.44 evaluated 126 patients with focal vertebral bone marrow lesions and observed statistically significantly lower MRI-PDFF values in metastasis and proposed a cutoff value of 9% for differentiation of metastasis from other benign lesions (Figure 3). Jung et al.45 evaluated the role of MRI-PDFF in differentiating vertebral metastases from focal hematopoietic marrow depositions and observed improved diagnostic performance. lee et al.46 evaluated the role of MRI-PDFF in differentiating bone metastases from Schmorl nodes and observed that metastases have lower fat fraction and fat fraction ratios than Schmorl nodes. Perez-lopez et al.47 evaluated bone metastases of prostate cancer and observed significantly lower fat fractions in bone metastasis in comparison with non-metastatic bone (Table 2). In this study, they also observed a significantly lower fat fraction in bone biopsies contain- ing tumor in contrast with biopsies not con- taining tumor. Quantitative PDFF measure- ment of fat fraction in bone metastases may allow assessment of treatment response in prostate cancer patients.47

Muscle

The term myosteatosis, a possible con- comitant component of sarcopenia, refers to fatty infiltration of the skeletal muscle, which is caused by several factors including aging, disuse, muscle injury, and hormon- al dysfunction.48 Myosteatosis is associat- ed with loss of muscle mass and strength and increased mortality among the elder- ly.48 Several studies investigated the effect of age and sex on fat accumulation in the skeletal muscle and demonstrated that men had lower muscle MRI-PDFF values in comparison to women.49-51 There was also a significant correlation between muscle MRI-PDFF and age.51 burian et al.52 demon- strated a correlation between abdominal muscle MRI-PDFF with age in both men and women and erector spinae muscle MRI-PDFF with age in women. In this study, they also observed a statistically significant association between age and abdominal muscle MRI-PDFF after adjusting bMI in women and concluded that myosteatosis is mainly correlated with age, but not with bMI in women.52

The relationship between muscle strength and MRI-PDFF was also evaluated. Schlaeger et al.49 evaluated the relationship between the performance of erector spi-nae and psoas muscle strength with PDFF and cross-sectional area of the muscles in healthy individuals and observed that erec-tor spinae muscle MRI-PDFF is negatively correlated with relative extension and flex-ion muscle strength. It remained as the only statistically significant predictor of relative extensor strength in multivariate regression models.49 Similarly, Inhuber et al.50 observed significant correlations between thigh mus-cle MRI-PDFF and relative maximum volun-tary isometric contraction. Dieckmayer et al.53 evaluated texture features of MRI-PDFF in paraspinal muscles and observed global Kurtosis of erector spinae muscle and bMI are statistically significant predictors of ex-tension strength and global variance and skewness of psoas muscle are statistically significant predictors of flexion strength indicating that muscular function is related to muscle fat distribution. In contrast with the previous studies, Klupp et al.54 did not find a correlation between paraspinal mus-cle strength and MRI-PDFF, but they found a correlation between diffusion tensor imag-ing parameters. The muscle MRI-PDFF and strength was also evaluated in different cir-cumstances. grimm et al.55 evaluated thigh muscle area and MRI-PDFF in healthy sub-jects before and after training and observed that muscle area increases after training despite a significant decrease in muscle MRI-PDFF. Nguyen et al.56 also evaluated MRI-PDFF of quadriceps muscle before and after a mountain ultramarathon race and observed a reduction in MRI-PDFF. villagon et al.57 evaluated the changes in fat distribu-tion after fasting and observed an increase in muscle and spine bone marrow fat de-spite a decrease or no change in other re-gions of the body. Karampinos et al.58 evalu-ated supraspinatus MRI-PDFF in patients 10 years after unilateral rotator cuff repair and observed that supraspinatus MRI-PDFF cor-related significantly with goutallier scores, more severe cartilage defects of the humer-us and correlated negatively with isometric muscle strength. These studies demonstrat-ed that MRI-PDFF can be used for demon-stration of fatty infiltration of muscle as well as fat distribution in the muscle which is in-versely related to the muscle strength.

There are also studies evaluating the rela-tionship between muscle and bone marrow  fat in the literature. Sollmann et al.59 evalu-ated the relationship between paraspinal muscle and lumbar vertebrae MRI-PDFF in premenopausal and postmenopausal wom-en and observed a significant correlation among them in postmenopausal women in comparison with premenopausal women. Zhao et al.60 evaluated the relationship be-tween paraspinal muscles and lumbar ver-tebrae MRI-PDFF in both women and men and observed lower paraspinal muscle MRI-PDFF values in patients with normal bMD in contrast with patients with osteopenia and osteoporosis (Figure 2). These two stud-ies suggest a positive correlation between bone marrow and paraspinal muscle fat in patients with decreased bMD. Dieckmeyer et al.61 evaluated the bone-muscle MRI-PDFF in the thigh and hip region in healthy volunteers and observed a weak correlation between only the MRI-PDFF of the quadri-ceps muscle and greater trochanter bone marrow. burian et al.62 did not find a cor-relation between bone marrow and muscle MRI-PDFF in sacral and lumbar spine re-gions in healthy volunteers. Although these conflicting results raise suspicion regarding the use of high levels of fat infiltration as a diagnostic or therapeutic tool for osteosar-copenia, it still maintains its importance for further exploration.

The studies also evaluated the role of MRI-PDFF in the assessment of fatty re-placement in muscles in neuromuscular dis-eases such as Pompe disease and facio-sca-pulo-humeral dystrophy.63-66 Horvath et al.63 observed severe tongue and axial muscle group fat involvement with MRI-PDFF in patients with late-onset Pompe disease (lOPD) and proposed that whole-body MRI provides more detailed data than physical examination. Khan et al.64 showed muscle strength and functional testing in patients with lOPD are correlated with MRI-PDFF and supposed that MRI-PDFF can be used for assessment of the severity of muscle dis-ease and follow-up. Fernandez et al.65 evaluated muscle fat infiltration with MRI-PDFF in children with infantile Pompe disease (IPD) and pediatric lOPD and observed that patients with IPD had higher PDFF values in comparison with lOPD patients despite younger age in IPD population. leporq et al.66 evaluated seven patients with fa-cio-scapulo-humeral dystrophy and higher fatty infiltration was observed in muscles despite a normal appearance of the muscle. Stouge et al.67 evaluated patients with dia-betes with and without diabetic polyneuropathy in comparison with healthy con-trols and demonstrated higher fat fraction in lower extremity muscles in patients with diabetic polyneuropathy. MRI-PDFF allows demonstration and quantification of fatty replacement in muscles in neuromuscular diseases which may be helpful in both diag-nosis and evaluation of treatment response (Figure 4).

The effects of hormonal disorders on myosteatosis with MRI-PDFF were also eval-uated by several researchers. Sollman et al.59 observed significantly higher paraspinal muscle PDFF in patients with postmeno-pausal women compared to premenopausal women. Kiefer et al.68 evaluated ab-dominal muscle MRI-PDFF in patients with prediabetes and diabetes as well as healthy controls and observed statistically higher MRI-PDFF in patients with prediabetes and diabetes in contrast with healthy controls. Oguz et al.27 evaluated patients with the lean PCOS and observed lower paraspinal muscle and lumbar MRI-PDFF values in the patient population compared to healthy in-dividuals.

Miscellaneous

There are also different studies evalu-ating the usage of MRI-PDFF in different organs and tissues. Franz et al.69 evaluated supraclavicular and gluteal region adipose tissue MRI-PDFF and observed a close cor-relation with vAT-SAT volume and moderate correlation with liver MRI-PDFF. Hong et al.70 evaluated the role of MRI-PDFF in the assessment of spleen fat in comparison with magnetic resonance spectroscopy and observed poor agreement between two methods with higher fat fraction values with MRI-PDFF which can be artifactual. Idilman et al.71 evaluated R2* values of the spleen in patients with transfusion-related iron overload and observed no correlation with R2* values of liver, pancreas, renal cortex, and vertebral bone marrow with MRIPDFF. However, in this study, they demonstrated positive correlations between liver R2* and pancreas-renal cortex R2* as well as pancreas R2* and renal cortex R2*. Idilman et al.11 evaluated the relationship between renal cortex and sinus MRI-PDFF with liver, pancreas and vertebra MRI-PDFF and observed a correlation between renal sinus PDFF and pancreas PDFF. In another study, Notohamiprodjo et al.72 demonstrated renal sinus fat volume is higher in prediabetic and diabetic subjects and also associated with vAT. guo et al.73 evaluated testis and epididy-

mis fat fraction with MRI-PDFF in different age groups and observed increased fat deposition with age and a reduction of fat fraction after ejaculation. li et al.74 evaluated the utility of testicular fat deposition in determining and monitoring testicular infertility and demonstrated that testicular fat deposition determined by MRI-PDFF is more specific than testicular volume for diagnosis of male infertility and suggested that it can also be used for monitoring infertility.

Conclusion

MRI-PDFF can be used for demonstration and quantification of fat in various organs and tissues as well as liver, which may show the effect of both in several diseases. Pancreas MRI-PDFF is shown to be related to various metabolic, inflammatory, and neoplastic diseases. bone marrow MRI-PDFF allows quantification of fatty replacement which is related to loss of bone mass. It is also useful for the differentiation of benign fractures from malignancy-associated ones. Muscle MRI-PDFF can be used for the determination of muscle strength and also muscle involvement in neuromuscular diseases. we believe that further studies will expand the utilization of MRI-PDFF in various organs and tissues and will help the understanding of fat metabolism.

Conflict of interest disclosure

The authors declared no conflicts of interest.

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