Age- and sex-related variations of normal spleen T1rho and the more stable liver T1rho to spleen T1rho ratio

Abstract

Purpose

We aim to evaluate the potential age- and sex-related variations of normative values of spleen T1rho.

Materials and Methods

Two T1rho sequences were used, with one based on fast spin echo sequence (FSE) and the other based on gradient echo sequence (GRE). Spleen and liver FSE T1rho values were measured in 52 healthy volunteers (36 females, 16 males), and spleen and liver GRE T1rho values were measured in 14 healthy volunteers (6 females, 8 males).

Results

For FSE data, an age-related decreasing trend of spleen T1rho was noted for both females and males. This trend was consistent with female liver T1rho values, while such a trend was not noted for male liver T1rho. Females had a higher T1rho than males, both for the spleen (92.8 vs 77.3 ms, p<0.0001) and for the liver (44.2 vs. 38.9 ms, p<0.0001, FSE data). The spleen T1rho value was approximately double the liver T1rho value. The spleen T1rho and liver T1rho were positively correlated, both for FSE data (r=0.611) and GRE data (r=0.541). When the spleen T1rho was used to normalize the liver T1rho, the ratio of T1rho_liver/T1rho_spleen largely removed the sex and age effect. The spleen T1rho in menstrual phase women was 10.7% lower (p=0.012) than that of non-menstrual phase women, while the liver T1rho in menstrual phase women was 3.8% lower than that of non-menstrual phase women.

Conclusion

Since women in the menstrual phase tend to have lower body iron, the fact that both liver T1rho and spleen T1rho are shorter among women in the menstrual phase than women in the non-menstrual phase indicates that liver and spleen T1rho physiological variations may not be dominantly affected by the iron content of the tissue. If a pathology has only affected the liver while the spleen is normal, there is a possibility the ratio T1rho_liver/T1rho_spleen may offer better characterization of liver pathologies.

Key Points

• There is an age-related decreasing trend of spleen T1rho.

• Females have a higher spleen T1rho than males.

• The spleen T1rho value is approximately double the liver T1rho value.

• Spleen T1rho and liver T1rho are positively correlated.

Citation Format

• Wáng YXJ, Yu W-L, Deng M. Age- and sex-related variations of normal spleen T1rho and the more stable liver T1rho to spleen T1rho ratio. Fortschr Röntgenstr 2024; DOI 10.1055/a-2428-7409

 

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Zusammenfassung

Zweck

Unser Ziel ist es, mögliche alters- und geschlechtsbedingte Variationen der normativen Werte von Milz-T1rho zu bewerten.

Materialien und Methoden

Es wurden zwei T1rho-Sequenzen verwendet, von denen eine auf einer schnellen Spin-Echo-Sequenz (FSE) und die andere auf einer Gradienten-Echo-Sequenz (GRE) basierte. Milz- und Leber-FSE-T1rho wurden bei 52 gesunden Freiwilligen (36 Frauen, 16 Männer) und Milz- und Leber-GRE-T1rho bei 14 gesunden Freiwilligen (6 Frauen, 8 Männer) gemessen.

Ergebnisse

Bei den FSE-Daten wurde sowohl bei Frauen als auch bei Männern ein altersbedingter abnehmender Trend des Milz-T1rho festgestellt. Dieser Trend stimmte mit dem Leber-T1rho bei Frauen überein, während ein solcher Trend bei der Leber von Männern nicht festgestellt wurde. Frauen hatten einen höheren T1rho als Männer, sowohl für die Milz (92,8 vs. 77,3 ms, p<0,0001) als auch für die Leber (44,2 vs. 38,9 ms, p<0,0001, FSE-Daten). Der T1rho-Wert der Milz war etwa doppelt so hoch wie der T1rho-Wert der Leber. Milz-T1rho und Leber-T1rho korrelierten positiv, sowohl für FSE-Daten (r=0,611) als auch für GRE-Daten (r=0,541). Wenn Milz-T1rho zur Normalisierung von Leber-T1rho verwendet wurde, beseitigte das Verhältnis von T1rho_liver/T1rho_spleen den Geschlechts- und Alterseffekt weitgehend. Der Milz-T1rho von Frauen in der Menstruationsphase war 10,7% niedriger (p = 0,012) als der von Frauen in der Nicht-Menstruationsphase; während der Menstruationsphase war der Leber-T1rho bei Frauen um 3,8% niedriger als bei Frauen außerhalb der Menstruationsphase.

Schlussfolgerung

Da Frauen in der Menstruationsphase tendenziell weniger Eisen im Körper haben, deutet die Tatsache, dass sowohl Leber-T1rho als auch Milz-T1rho bei Frauen in der Menstruationsphase kürzer sind als bei Frauen in der Nicht-Menstruationsphase, darauf hin, dass die physiologischen Variationen von Leber- und Milz-T1rho möglicherweise nicht hauptsächlich durch den Eisengehalt des Gewebes beeinflusst werden. Wenn eine Pathologie nur die Leber betrifft, während die Milz normal ist, besteht die Möglichkeit, dass das Verhältnis T1rho_liver/T1rho_spleen eine bessere Charakterisierung von Leberpathologien ermöglicht.

Kernaussagen

• Es gibt einen altersbedingten abnehmenden Trend des Milz-T1rho.

• Frauen haben einen höheren Milz-T1rho-Wert als Männer.

• Der T1rho-Wert der Milz ist etwa doppelt so hoch wie der T1rho-Wert der Leber.

• Milz-T1rho und Leber-T1rho-Werte korrelieren positiv.

 

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Keywords

liver - spleen - magnetic resonance imaging - T1rho - aging - menstrual cycle

Introduction

T1rho (T1ρ) has been shown to be sensitive to the interactions between water molecules and macromolecules, including collagen. Allkemper et al. [1] reported that the liver T1rho value was significantly associated with the Child-Pugh staging of the patients. Hector et al. [2] reported T1rho values were significantly higher in the cortex of fibrotic renal allografts than in functional kidney allografts. The cortical T1rho value significantly correlated with Masson’s trichrome-stained fractions. In another study, Hector et al. [3] reported that spleen T1rho showed a significant correlation with portal pressure and clinically significant portal hypertension. It was suggested that the elevation in T1rho in the spleen with increased portal hypertension severity may reflect the deposition of collagen associated with fibrogenesis.

In liver fibrosis evaluation, pre-clinical studies reported that liver T1rho quantification allows excellent separation between normal liver and early-stage liver fibrosis [4] [5]. However, the application of T1rho for real-world detection early-stage liver fibrosis in human patients has been less successful [6]. Under experimental settings, the same batch of animals with the same age and animals raised under the same environment with the same diet would show fewer inter-subject variations. However, even among healthy human livers, liver physiology has variations related to age and sex which in turn are affected by variations in iron/fat deposition and perfusion changes [7] [8]. Moreover, which factors contribute to liver T1rho variation has not been fully elucidated [9]. In this study, we aim to evaluate potential age- and sex-related variations in normative spleen T1rho values.

 

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Materials and methods

This healthy volunteer study was conducted with the approval of the institutional ethics committee, and informed consent was obtained. Two T1rho sequences were used, with one based on gradient echo sequence (GRE) with multiple breath-hold acquisitions [10], and the other was based on fast spin echo sequence (FSE) with a single breath-hold acquisition [11].

For the FSE sequence, 96 healthy volunteers were recruited from the local community. Single-breath-hold black blood FSE T1rho acquisition was conducted using a Philips Achieva TX 3.0 T scanner equipped with a dual transmitter (Philips Healthcare, Best, the Netherlands). The combination of double inversion recovery and 2D fast FSE was used to achieve the black blood effect. The parameters for MR imaging included: TR/TE 2,000/20 msec, in-plane resolution 1.5 mm × 1.5 mm, slice thickness 7 mm, SENSE acceleration factor 2, half scan factor (partial Fourier) 0.6, number of signal averaging 1, delay time for SPAIR (SPectral Attenuated Inversion Recovery) 250 msec, delay time for double inversion recovery 650 msec, spin-lock frequency 500Hz. T1rho images with six spin lock times of 0, 10, 20, 25, 35, 50 msec were acquired, with a single breath-hold of 12 seconds for data acquisition. Six axial slices were acquired for each examination.

For the GRE sequence, 28 health subjects were recruited. Multi-breath-hold GRE T1rho acquisition without suppression of the blood signal was conducted using a 3T clinical scanner (Achieva, Philips Healthcare, Best, The Netherlands). For T1rho measurement, a rotary echo spin-lock pulse was implemented in a 2D fast GRE sequence. The spin-lock frequency was set to 500 Hz and spin-lock times of 1 ms, 10 ms, 20 ms, 30 ms, 40 ms, and 50 ms were used for T1rho mapping. TE and TR were 1.16 ms and 2.3 ms, respectively. The voxel size was 1.50×1.50×7.00 mm³. The flip angle was 40 degrees, the number of signal averages was 2, and the SENSE acceleration factor was 1.5. Six axial slices were acquired for each examination. The data were acquired with one image of one spin-lock time during one breath-hold.

Both the FSE acquisition and the GRE acquisition were initially aimed to cover the center of the liver, sufficient coverage of the spleen to allow T1rho measurement of the spleen was available in 52 FSE cases (36/62 for females, 16/34 for males) and 14 GRE cases (6/7 for females, 8/8 for males), respectively. The summed spleen region of interest (ROI) area was on average 4067 cm²/case (standard deviation: 4167 cm²). All images were processed using Matlab (Mathworks, Natick, MA, USA). T1rho maps were computed using a mono-exponential decay model, as described by the following equation: M (TSL) = A · exp (- TSL/T1 rho), where A is a constant scaling factor and TSL is the time of spin-lock. A non-linear least square fit with the Levenberg-Marquardt algorithm was applied. Maps of coefficient of determination (R²) were also generated for the evaluation of goodness of fit. Only T1rho values for pixels associated with R²>0.80 were included in the subsequent ROI placement and T1rho analysis to eliminate the unreliable poorly fitted T1rho values due to artifacts. The mean value within the ROI for the spleen was obtained. Liver T1rho has been shown to have high scan-rescan reproducibility with right scan setups [10] [11]. Liver 1rho values have been previously reported [10] [11], and we re-used the previously reported values for cases with spleen values analyzed in the current study. For the spleen FSE T1rho, the scan-rescan reproducibility in two separate sessions ICC (intraclass correlation coefficient) was 0.902 with the 9 cases (5 males, and 4 females) available for evaluation.

Statistical analysis was performed using GraphPad Prism (GraphPad Software, San Diego, CA, USA). Comparisons between groups were tested by Mann–Whitney U test, Wilcoxon signed rank test, or Wilcoxon matched-pairs signed rank test as appropriate. The significances of correlation were tested with Pearson correlation. A p-value of less than 0.05 was considered statistically significant.

 

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Results

The study participants’ demographics and T1rho results are shown in [Table 1], and [Fig. 1], [Fig. 2], [Fig. 3], [Fig. 4], [Fig. 5].

Table 1 Physiological spleen T1rho sex- and age-related variations.

Subjects	Spleen T1rho ms§	Slope	r	Pslope
#: years in mean and range. §: median (range), 95% confidence internal (CI). slope: slope related to age, r: Pearson r
FSE imaging, both sexes, age#: 37.3 (18–80)	87.72 (67.14–105.1), 95%CI: 84.46–90.21	–0.3513	–0.4872	0.0002*
FSE imaging, females (n=36), age: 35.6(18–75)	92.78 (67.92–105.1), 95%CI: 88.08–93.92	–0.2675	–0.4317	0.0086*
FSE imaging, males (n=16), age: 41.1 (24–80)	77.26 (67.14–97.25), 95%CI: 74.22–83.99	–0.3396	–0.5515	0.0268*
GRE imaging, both sexes, age: 28.6 (20–44)	72.52 (57.48–91.87), 95%CI: 67.27–80.44
GER imaging, females (n=6), age: 27.3 (24–30)	70.12 (57.48–91.87), 95%CI: 58.30–83.91
GRE imaging, males (n=8), age: 29.5 (20–44)	75.04 (61.56–88.94), 95%CI: 66.61–85.23

Fig. 1 a–f An illustrative case of upper abdominal imaging shows T1rho images [spin lock time (TSL), a: 0 ms, b: 10 ms, c: 20 ms, d: 25 ms, e: 35 ms, f: 50 ms] and T1rho map (g, without region of interest drawn, f: a region of interest drawn on the spleen). Note the higher signal of the spleen relative to that of the liver.

Fig. 2 a–h Sex- and age-related variations of normal spleen and liver T1rho values. Data are from the same group of subjects (n=36 for females and n=16 for males) with FSE acquisition. In d and h, the bar denotes the median value.

Fig. 3 a–d Correlation of liver T1rho value and spleen T1rho value (a: FSE imaging, b: GRE imaging), and higher spleen T1rho for FSE values than for GRE T1rho values (c: females’ data, d: males’ data) when the ages of the study subjects were approximately similar.

Fig. 4 a–e Ratio of liver T1rho to spleen T1rho for males (M) and females (F). Fast spin echo (FSE) in a, b, c, and d, both FSE and gradient echo (GRE) data in e. a: males’ and females’ data together. b: females’ data. c: males’ data. M: males, F: females. M, F in e: males and females.

Fig. 5 a–d Menstrual cycle-related variations in spleen T1rho and liver T1rho. a and b (bar denotes median values) are data used in this study’s analysis. c (mean ± standard deviation) included all the liver T1rho data from the earlier report [11], with 26 women scanned in the non-menstrual phase (mean age: 29.4 years) and 11 women scanned in the menstrual phase (mean age: 25.4 years). d: Five female’s liver T1rho values were scanned twice, one being in the menstrual phase and the other being in the second half of the non-menstrual phase (data from the earlier report [11]).

For FSE data, an age-related decreasing trend of spleen T1rho was noted for both females and males ([Fig. 2]). This trend was consistent with liver T1rho for females, while such a trend was not apparent for males’ liver T1rho. Overall, females also had a higher T1rho than males, both for the spleen (92.8 vs 77.3 ms, p<0.0001) and for the liver (44.2 vs. 38.9 ms, p<0.0001).

Spleen T1rho and liver T1rho were positively correlated, both for FSE data (r=0.611, p<0.0001) and GRE data (r=0.541, p=0.046, [Fig. 3]). When the ages of the study subjects are approximately similarly matched, spleen T1rho was higher for FSE values than for GRE T1rho values, with a median of 93.2 ms vs. 70.1 ms for females [n= 25 cases for FSE data (mean age: 26.4 yrs), and n=6 cases for GRE data (mean age: 27.3 years), p=0.001] and a median of 83.2 ms vs. 75.1 ms for males [n= 8 cases for FSE data (mean age: 33.5 yrs), and n=8 cases for GRE (mean age: 29.5 yrs), p=0.44]. When grouping females’ and males’ data together, the spleen FSE T1rho was 21.2% higher than the GRE value (89.5±10.2 ms vs. 73.9 ±11.4 ms, p<0.001).

When spleen T1rho was used to normalize liver T1rho, the ratio of T1rho_liver/T1rho_spleen largely removed the sex and age effect ([Fig. 4]). There was no statistically significant age-related trend for the T1rho_liver/T1rho_spleen ratio when females’ and males’ data were grouped together ([Fig. 4]a), and for the T1rho_liver/T1rho_spleen ratio of females’ data ([Fig. 4]b). The T1rho_liver/T1rho_spleen ratio of males’ data showed a weak increasing trend ([Fig. 4]c, p=0.032). There was also no difference in FSE ratio T1rho_liver/T1rho_spleen between females and males ([Fig. 4]d, GRE data not compared for males vs. females due to limited sample size and the mean age was very young for GRE data). Ratio T1rho_liver/T1rho_spleen was larger for GRE data than for FSE data ([Fig. 4]e, p<0.0001).

Among pre-menopausal females, the menstrual cycle of 23 female participants was recorded. 18 cases were in the non-menstrual phase (mean age: 28.1 years) and 5 cases were in the menstrual phase (mean age: 24.1 years). The spleen T1rho among women in the menstrual phase was 10.7% shorter (95.9ms vs. 85.6ms, p=0.012) than that of women not in the non-menstrual phase ([Fig. 5]a), while the liver T1rho among women in the menstrual phase was 3.8% shorter than that of women in the non-menstrual phase ([Fig. 5]b).

 

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Discussion

The T1rho relaxation time is correlated to the T2 relaxation time. At 3.0 Tesla, the T2 relaxation times of the liver and the spleen are estimated to be around 42 ms and 61 ms, respectively. In the current study, the spleen T1rho value (median= 89.1 ms for females, median= 77.3 ms for males) was accordingly much higher than the liver T1rho value (median=44.1 ms for females, median=38.9 ms for males, FSE data). These results are approximately consistent with the earlier study of Hectors et al. [2] [3]. This study demonstrates that older subjects are associated with a shorter T1rho value, and the same as the liver, male spleens have a shorter T1rho than female spleens. Liver T1rho and spleen T1rho were positively correlated, and this correlation was consistent with both the FSE sequence and the GRE sequence. More interestingly, when the spleen T1rho was used to normalize the liver T1ho, then age- and sex-related effects on liver T1rho were largely removed. This observation can potentially have important clinical relevance. It can be anticipated that the ratio T1rho_liver/T1rho_spleen may offer better characterization of liver pathologies when the pathology has only affected the liver while the spleen is normal. Though many systemic diseases have both liver and spleen involvement [3], early pathologies tend to involve only the liver. One point of note is that, for males, a statistically significant trend of reduction of spleen T1rho along with increasing age was noted for the spleen (p=0.027) but not for the liver (p=0.47). This led to the ratio T1rho_liver/T1rho_spleen having an increasing trend following increased age. More studies are needed to clarify this ratio trend. In the current study, the sample size for male livers was n=16. In our earlier report, the sample size for male livers was n=34, and p was 0.617, still no age-related trend was noted for the liver T1rho [11].

The results of this study may also help to clarify the liver/spleen T1rho MR relaxometry mechanism. An age-related increase in iron deposition in the spleen and in the liver has been well documented [8] [12]. Due to women’s menstruation and pregnancy, iron deposition in the liver and spleen is lower in adult pre-menopausal women than in age-matched adult men. In women, iron deposition in the liver and spleen substantially increases after menopause. Iron can shorten T1rho relaxation time [13]. It is tempting to suggest that organ iron concentration differences may explain why male spleens had a shorter T1rho than female spleens. However, we argued that it is likely that the spleen age-related T1rho change is not dominantly caused by spleen iron concentration variation [9]. In this study, the median spleen T1rho in women in the menstrual phase was 10.7% lower than that of women in the non-menstrual phase (p=0.01), and the median liver T1rho in women in the menstrual phase was 3.8% lower than that of women in the non-menstrual phase in the current analysis (p>0.05). These two observations suggest that factors affecting biochemical tissue composition detectable by T1rho may have a greater impact on the spleen than on the liver ([Fig. 2]c, [Fig. 2]g, [Fig. 5]). [Fig. 5]c shows liver data from our earlier report including 26 females in the non-menstrual phase and 11 females in the menstrual phase, with p=0.064, which is close to being statistically significant. [Fig. 5]d shows five women who underwent MRI both in the non-menstrual phase and the menstrual phase, with four of them having a lower live T1rho in the menstrual phase. It has been observed that women in the menstrual phase tend to have lower body iron [14]. Though, in theory, lower spleen iron will lead to a longer T1rho, in our studies, both the liver T1rho and spleen T1rho were shorter, rather than longer, among women in the menstrual phase than in women in the non-menstrual phase. Fat deposition in the liver has been shown to shorten T1rho [5]. However, fatty spleen is uncommon under physiological conditions. Our previous analysis suggests that 10% additional liver fat contributes to shortening of the liver T1rho by 1.55 ms [5]. We do not expect the spleen T1rho variation to be largely affected by spleen fat variations.

Among healthy young women, there are large variations in liver T1rho, for which we do not yet have a satisfactory explanation [11], though we suspect this could be partially related to hormonal variations. It is possible that there are sufficient age- and sex-related macromolecular biochemical differences among healthy human subjects which contribute to the liver and spleen T1rho variations. The liver undergoes “brown atrophy” with old age [15]. Mild fibrosis is a hallmark of the aging of various organs, which reflects increased deposition of the extracellular matrix. Naturally, subclinical diseases in apparently normal persons, smoking habits, nutritional differences, and other factors may also contribute to the variability in the liver and spleen aging process.

This study also showed the ratio T1rho_liver/T1rho_spleen may vary according to different T1rho acquisition sequences and is higher with GRE acquisition than with FSE acquisition. While further exploration of the NMR physics mechanism is beyond the scope of this study, further inter-study comparison should take into account this phenomenon.

There are many limitations to this study. As noted above, we could not explore the biophysical mechanisms behind the observed variations. The image data were initially acquired with a focus on the liver, this leads to only 52 cases with FSE T1rho acquisition and 14 cases with GRE T1rho acquisition available for the analysis of the spleen. However, due to the high stability of measurement, the observed trends mostly achieved statistical significance for FSE T1rho data. Another limitation is that we do not have data for pediatric populations. Finally, we can only speculate that the ratio of liver T1rho to spleen T1rho can offer better characterization of liver pathologies when the pathology has only affected the liver while the spleen is normal, and this should be confirmed with further patient studies.

In conclusion, we describe sex- and aged-related spleen T1rho variation among healthy women and men. The spleen T1rho value is approximately double the liver T1rho value. This study demonstrates that older subjects are associated with a shorter spleen T1rho value, and male spleens show a shorter T1rho than female spleens. Liver T1rho and spleen T1rho are positively correlated. When spleen T1rho is used to normalize the liver T1ho, then age and sex-related effects of liver T1rho are largely removed.

Clinical Relevance

1. Interpreting normal spleen T1rho should consider age and gender factors.

2. The ratio of liver T1rho to spleen T1rho can potentially offer better characterization of liver pathologies when the pathology has only affected the liver while the spleen is normal.

3. Spleen T1rho physiological variations may not be dominantly affected by tissue iron content.

Data availability statement: the data that support the findings of this study are available from the corresponding authors upon reasonable request.

 

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Conflict of Interest

The authors declare that they have no conflict of interest.

Acknowledgement

We thank Dr. Weitian Chen, the Chinese University of Hong Kong, for the FSE T1rho sequence used in this study; Dr. Feng Zhao and Dr. Jing Yuan, formerly with the Chinese University of Hong Kong, currently with Zhejiang University, China and Hong Kong Sanatorium & Hospital, Hong Kong, respectively, for the supports during the GRE T1rho data acquisition. Dr. Ben-Heng Xiao, the Chinese University of Hong Kong, helped image post-processing.

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Publikationsverlauf

Eingereicht: 27. Juli 2024

Angenommen nach Revision: 23. September 2024

Artikel online veröffentlicht:
22. Oktober 2024