The impact of body position and exercise on the measurement of liver Young’s modulus by real-time shear wave elastography

Abstract

BACKGROUND:

In the past ten years, liver biopsies have been used as a method to accurately diagnose the stage of fibrosis.

OBJECTIVE:

This study aimed to evaluate whether body position and exercise affect the measurement of liver Young’s modulus of healthy volunteers by real-time shear wave elastography (RT-SWE).

Methods:

RT-SWE was used to measure liver Young’s modulus in the supine and left lateral positions of 70 healthy volunteers at rest and measure the liver Young’s modulus in the lying position before exercise, and at zero, five, and ten minutes of rest after exercise.

RESULTS:

The liver Young’s modulus in the left lateral position was significantly higher than in the supine position ( $P<$ 0.05), and the measured value in the supine position was more stable than the left lateral position. The liver Young’s modulus measured at zero minutes after exercise was significantly higher than that measured before exercise ( $P<$ 0.05). The liver Young’s modulus measured at five minutes after exercise was significantly higher than that measured at zero minutes after exercise ( $P<$ 0.05) and was not statistically different from the measured value before exercise ( $P>$ 0.05). The liver Young’s modulus measured at ten minutes after exercise was significantly higher from that measured at zero minutes after exercise ( $P<$ 0.05) and was not statistically different from the measured value at five minutes after exercise ( $P>$ 0.05).

CONCLUSION:

Body position and exercise have a significant impact on the measurement of liver Young’s modulus. It is recommended that the examinees take a supine position during the measurement, and measurement should be conducted at least ten minutes after exercise.

Keywords

Real-time shear wave elastography position exercise liver Young’s modulus liver stiffness

1. Introduction

In the past ten years, liver biopsies have been used as a method to accurately diagnose the stage of fibrosis. However, it is an invasive examination with many adverse reactions, such as patient discomfort, bleeding, and even death [1], and sampling errors and observer factors may also lead to misdiagnosis [2]. Due to the limitations of these factors, people are eager to seek a safer, more reliable, and noninvasive method to assess the degree of liver fibrosis in patients with chronic liver disease.

As a new type of noninvasive inspection technology, ultrasound elastography technology is developed according to the different tissue stiffness and has received extensive clinical attention in recent years. There are three main types of shear wave elastography techniques currently used to detect liver stiffness in clinical practice. These are transient elastography (TE), acoustic radiation force impulse (ARFI), and real-time shear wave elastography (RT-SWE) technology. In RT-SWE technology, related control technologies are applied to emit acoustic pulse radiation force to the tissue to generate transverse shear waves in the tissue. The transverse shear wave velocity (SWV) in the tissue is detected and then converted into a Young’s modulus value using the formula for evaluating the stiffness of the tissue [3]. Tissues with different stiffness will present different values of SWV, and SWV measured by RT-SWE technology is positively correlated with Young’s modulus. Therefore, the Young’s modulus can be used to express the stiffness value of the tissue. RT-SWE is different from TE and ARFI, in which the operator can select the measured area on a clear two-dimensional image, effectively exclude pipeline structures such as blood vessels, and perform elasticity detection in parts of the image [4]. In this way, the measurement result is more objective and accurate, making up for the shortcomings of the operator’s subjective scoring and manual pressure error.

The RT-SWE technology has been confirmed by many researchers to reflect liver stiffness, compared with liver biopsy fibrosis staging, and the results of the two have high consistency [5, 6, 7]. However, different researchers have different diagnostic thresholds for liver stiffness [8, 9, 10, 11, 12], and the existence of other contributing factors, such as the patient’s gender, age, diet, and cholestasis, will also affect the accuracy of liver stiffness determination.

Based on the above studies, more and more scholars are paying attention to the influencing factors of liver stiffness. Some studies [13, 14, 15] revealed that the patient’s position and age would affect the liver elasticity. There are still few studies worldwide on whether it will affect the elasticity of the liver before and after exercise. Gersak et al. [16] conducted a study on seven volunteers, and the results revealed that liver elasticity changed before and after exercise. Due to the small number of sample cases, and the fact that Chinese scholars have not done research on this influencing factor, this study chose to explain the two factors of body position and exercise separately. The study observed the influence of body position and exercise on liver elasticity of healthy adults and determined a more accurate method for measuring the stiffness value, in order to provide a basis for the standardized application of SWE technology in the future.

2. Materials and methods

2.1 Subjects

A group of 79 young, healthy, female volunteers who had undergone physical examination in our hospital from June 2019 to November 2019, were enrolled in this study. One patient had a narrow intercostal space, which was small and thin. After full exposure of the intercostal space, the images were affected by the ribs, and the images were unclear. One patient had a thicker subcutaneous fat layer. The thickness of the subcutaneous fat layer of the right chest wall was greater than 20 mm, and the image displayed was unclear. Seven patients had abnormal heart rate response after exercise. Their highest heart rate after exercise was [HRmax $=$ 220-age (years), and the target heart rate after exercise needed to be $\geqslant$ HRmax $\times$ 60% to meet the standard. These patients were excluded. This left a total of 70 patients who were included in the analysis. The age of the patients ranged from 25–34 years, with an average age of 29.03 $\pm$ 2.12 years. Body mass index (BMI) was 17.39–23.63 kg/m ${}^{2}$ , and the average was 20.43 $\pm$ 1.36 kg/m ${}^{2}$ . Heart rate after exercise was 114–143 beats/min, and the average rate was 123.16 $\pm$ 6.87 beats/min. The enrolled volunteers had no history of liver, kidney, or cardiovascular disease. Imaging abnormalities and biochemical blood examinations indicated no abnormalities in liver function.

The study was conducted in accordance with the Declaration of Helsinki (as was revised in 2013). The study was approved by Ethics Committee of the Hebei General Hospital. Written informed consent was obtained from all participants.

3. Instruments and methods

3.1 Instruments

The instrument adopted was the Supersonic Imagine Aixplorer fully digital color Doppler ultrasound diagnostic apparatus produced in France. The probe was SC6-1, and the frequency was 1–6 MHz. The instrument was equipped with SWE technology.

3.2 Inspection methods

The patients were in a fasting state, lifting their arms. First, a two-dimensional ultrasound examination was performed using the abdominal conditions set by the instrument. The probe was placed on the right mid-axillary line of the subject to avoid interference from ribs and lung gas. A color Doppler ultrasound machine was used, avoiding the structure of large blood vessels, and the appropriate measurement site was selected. After selecting the elastography mode, the examinees were asked to hold their breath. The depth was set at 3–4 cm. After waiting for 3–4 seconds, the image was fixed, then the quantitative analysis system (Q, B0X) was used to measure the elasticity value. The effective measurement region of interest (ROI) diameter was approximately 15 mm, and the unit was kPa.

Measurement of the basal heart rate at rest: The examinees were in the supine position and the left lateral position, and the same part of the liver was selected to measure the Young’s modulus. The examinees then did physical exercises of the same intensity. All examinees climbed the stairs in the same building. Each floor has 28 steps, each step is 13 cm high, and the examinees went up and down eight floors. The total length of the journey was 13 cm $\times$ 28 $\times$ 8 $\times$ 2. Their heart rate was measured immediately after the exercise. The Young’s modulus of the liver was measured immediately after exercise, and at five minutes and ten minutes after exercise. The Young’s modulus of the liver was measured at the same site. Measurement was taken three times, and the average values of the measured data were calculated. All the obtained elastic images were stored. The color of the image from red to blue indicates that the tissue is gradually softening. The larger the measured value, the harder the tissue in the area. Success criteria for elastography images: It is considered a success when the color of the elastic images filled more than half the area of the sampling frame and the color distribution was relatively uniform (see Fig. 1).

Table 1
Results of mean value, minimum value, and maximum value of Young’s modulus of liver in different body positions and inter-group comparison (kPa)

	Horizontal position (Mean $\pm$ SD)	Left lateral position (Mean $\pm$ SD)	$t$
Emean	4.78 $\pm$ 0.70	5.84 $\pm$ 1.06	$-$ 9.03
Emin	3.92 $\pm$ 0.87	4.64 $\pm$ 1.11	$-$ 5.25
Emax	5.83 $\pm$ 0.91	7.23 $\pm$ 1.32	$-$ 8.90

Figure 1.

Success criteria for elastography images.

4. Statistics analysis

Data were analyzed using statistical software SPSS20.0. Normally distributed measurement data were expressed as mean $\pm$ standard deviation (x $\pm$ SD), and non-normally distributed measurement data were expressed as the median and interquartile range (M, Q). The Young’s modulus values of the liver before and after changes in different positions of the same patient were compared. If the differences were normally distributed, they were compared using a paired t-test. If the differences were not normally distributed, they were compared using a Wilcoxon rank-sum test. For the same patient, the Young’s modulus values of the liver in the supine position measured before exercise and at zero minutes, five minutes, and ten minutes after exercise, were compared. For the comparison between any two groups, if the differences were normally distributed, a paired t-test was adopted. If the differences were not normally distributed, a Wilcoxon rank-sum test was used. $P<$ 0.05 was considered statistically significant.

5. Results

5.1 Comparison of liver Young’s modulus in different positions

The average value of liver Young’s modulus was 4.78 $\pm$ 0.70 kPa in the supine position, and 5.84 $\pm$ 1.06 kPa in the left lateral position. The liver Young’s modulus in the left lateral position was significantly higher than that in the supine position, and the difference was statistically significant ( $P<$ 0.05). The dispersion on Young’s modulus between the supine position and the left lateral position was small, and the data were relatively stable (Table 1, Fig. 2).

Table 2
Results of liver Young’s modulus before exercise, immediately after exercise, 5 min after exercise, and 10min after exercise (kPa)

	Before exercise Mean $\pm$ SD/(M, Q)	Immediately after exercise Mean $\pm$ SD/(M, Q)	5 min after exercise Mean $\pm$ SD/(M, Q)	10 min after exercise Mean $\pm$ SD/(M, Q)
Emean	4.78 $\pm$ 0.70	6.03 $\pm$ 1.12	4.77 $\pm$ 0.88	4.72 $\pm$ 0.66
Emin	3.92 $\pm$ 0.87	(4.60,1.05)	3.93 $\pm$ 0.83	3.72 $\pm$ 0.70
Emax	5.83 $\pm$ 0.91	(7.20,1.39)	5.70 $\pm$ 1.15	(5.70,0.93)

Figure 2.

Measured results of liver Young’s modulus in different positions (kPa, $n=$ 70): The data are presented in the form of boxplots, the length of the box indicates the interquartile range, the middle horizontal line indicates the median, both ends indicate the maximum and minimum markers after removing outliers. * Indicates a $P$ value $<$ 0.05 compared with supine position.

5.2 Comparison of liver Young’s modulus before and after exercise

The average values of liver Young’s modulus in the supine position were 4.78 $\pm$ 0.70 kPa, 6.03 $\pm$ 1.12 kPa, 4.77 $\pm$ 0.88 kPa, and 4.72 $\pm$ 0.66 kPa respectively, before exercise, at zero, five, and ten minutes after exercise (Table 2, Fig. 3). The liver Young’s modulus measured at zero minutes after exercise was significantly higher than that measured before exercise ( $P<$ 0.05). The liver Young’s modulus measured at five minutes after exercise was significantly lower than that measured at zero minutes after exercise ( $P<$ 0.05) and was not statistically different from the measured value before exercise ( $P>$ 0.05). The liver Young’s modulus measured at ten minutes after exercise was significantly lower than that measured at zero minutes after exercise ( $P<$ 0.05) and was not statistically different from the measured value before exercise and at five minutes after exercise ( $P>$ 0.05) (Tables 3 and 4).

Table 3
The Young’s modulus before and immediately after exercise, 5 min before and after exercise, and 10 min before and after exercise were compared in pairs

	Before and immediately after exercise			5 min before and after exercise			10 min before and after exercise
	Emean	Emin	Emax	Emean	Emin	Emax	Emean	Emin	Emax
$p$ -value	0.00	0.00	0.00	0.95	0.66	0.06	0.09	0.02	0.03

Table 4

The Young’s modulus was compared between immediately after exercise and 5 min after exercise, immediately after exercise and 10 min after exercise, and 5 min after exercise and 10 min after exercise

	Immediately after exercise and 5 min after exercise			Immediately after exercise and 10 min after exercise			5 min after exercise and 10 min after exercise
	Emean	Emin	Emax	Emean	Emin	Emax	Emean	Emin	Emax
$p$ -value	0.00	0.00	0.00	0.00	0.00	0.00	0.53	0.00	0.85

Figure 3.

Results of liver Young’s modulus measured before exercise, at 0, 5 and 10 minutes after exercise (kPa, $n=$ 70): The data are presented in the form of box diagram, the length of the box indicates the interquartile range, the middle horizontal line indicates the median, both ends indicate the maximum and minimum markers after removing outliers. * Indicates a $P$ value $<$ 0.05 compared with before exercise, # indicates a $P$ value $<$ 0.05 compared with 0 minute after exercise, indicates a P value $<$ 0.05 compared with at 5 minutes after exercise.

In addition, the results showed that the dispersion degree of the measured values at zero minutes of rest was larger than that before exercise, and the results measured were not stable. The Young’s modulus at five minutes after exercise returned to the baseline level before exercise; however, the dispersion of data was larger than that at ten minutes after exercise. The results were not as stable as those taken ten minutes after exercise.

6. Discussion

Accurate assessment of the severity of fibrosis and reliable diagnosis of liver cirrhosis is extremely important. It is important to find a safe, acceptable, and noninvasive examination method for patients to evaluate the degree of liver fibrosis [17, 18]. A related study has confirmed that elastography, a noninvasive technique, has been widely used in detecting problems in the liver, breast, musculoskeletal system, and thyroid nodules [19]. Although there has been research into elastography and it is easy to operate, there are also many influencing factors, so further studies are needed to determine the effectiveness of this method [20].

More and more scholars worldwide are paying attention to its influencing factors. Some studies have confirmed that obesity, gender, hormone levels can affect liver stiffness [21, 22, 23, 24, 25, 26, 27, 28]. Goertz et al. [29] used ARFI to measure the effect of different breathing movements on liver elasticity. The results revealed that there was no significant difference in liver elasticity among deep inspiration, deep exhalation, and Valsalva maneuvers. The elastic value of the liver is also affected by different measurement depth. An et al. [30] selected 121 male volunteers to measure liver elasticity at different depths by SWE. The results revealed that with the increase in measurement depth, the elastic value of the liver would increase. This is consistent with the research conducted by Zheng et al. [31]. Many scholars have also studied the influence factor of position. Goertz et al. [29] measured the liver elasticity of 30 healthy adults in different body positions (standing position and supine position). The results revealed that the value measured in the standing position was higher than that in the supine position. Huang [26] and Han et al. [13] revealed that the elasticity of the liver in the left lateral position was higher than that in the horizontal position. However, some scholars [15] concluded that body position did not affect liver stiffness, and there was no significant difference in the value measured by SWV between supine and left lateral positions.

In view of the above affecting factors, in this study, other factors such as the young age of the women (age 25–34), a BMI of 17.39–23.63 kg/m ${}^{2}$ , breath-holding states, and depth maintained at 3–4 cm, were maintained at a high degree of consistency, while under the same measurement conditions, whether the change of body position would affect the elastic value of the liver was studied. The results revealed that the average value of liver Young’s modulus in a left lateral position was higher than that in a supine position, and the difference was statistically significant ( $P<$ 0.05). This is consistent with the studies conducted by Huang [26] and Han et al. [13]. The specific reason remains unknown. It is considered that in the left lateral position, the liver is affected by gravity, and the stiffness of tissue under the traction of ligament increases to a certain extent, resulting in the increase of elastic measurement value [13]. The results of this study also revealed that the average measured value in the supine position was more stable than that in the left lateral position. It is suggested that it may be affected by the ribs, and the acoustic window of intercostal space in the left lateral position is unstable. Therefore, the present study suggests that when measuring the stiffness of the liver, the examinees should take the supine position, and the intercostal space should be fully exposed. Thus, the measurement results will be more accurate.

In addition, a study revealed that the changes in liver blood flow also had a significant effect on liver stiffness. It has been confirmed by some scholars [9, 27] that dietary factors increase liver stiffness, so it is recommended that examination should be carried out in a fasting state or at least four hours after fasting. Researchers believe that this may be related to liver hemodynamics. The increase of liver stiffness caused by severe decompensated heart failure is also related to the change of liver blood flow [32]. Exercise is another important cause of liver blood flow change. During and shortly after strenuous exercise, visceral and liver blood flow decreases significantly [33]. Due to sympathetic nerve activity, blood flow will decrease by more than 50% of the baseline value [34].

There are few studies at home and abroad on the changes in liver stiffness caused by exercise. Therefore, in this study, the liver stiffness of healthy examinees before and after exercise was measured to determine the effect of exercise on liver stiffness. The results revealed that the elastic value of the liver would change before and after exercise. Immediately after exercise, the measured value on liver stiffness increased compared with that before, and the measured value was not stable. The elastic value would return to the baseline level five minutes after rest; however, the variation of the average value of Young’s modulus five minutes after exercise was larger than that at ten minutes after exercise. Therefore, this study suggests that we should rest for ten minutes after exercise and then check the elastic value of the liver. Gersak et al. [16] revealed that after resting for ten minutes after exercise, the stiffness of the liver returned to the baseline level. The reason for the difference may be related to the intensity of exercise. Van Wijck [35] revealed that when the exercise time was prolonged or the environment was hot, the blood flow to the liver and viscera would decrease at a more intense rate and the time to return to the baseline level would increase. It was analyzed that in this study, the reason for the increase in liver stiffness after exercise and its recovery after rest may be related to the change of liver blood flow. The liver blood flow will increase in a short time due to the buffering effect of the hepatic artery and the reflux of the hepatic vein. After rest, liver blood flow recovers, and liver stiffness returns to the basic level, but the specific reasons still need to be further studied in depth. On the other hand, studies have revealed that cardiac and aortic pulsation transfers could also increase the measured value of elasticity of the liver. Such studies were only reported in the research of the left lobe of the liver [36]. Because this study focused on the right lobe of the liver, further study is needed to see whether it is due to the transmission of motion.

It is important to observe the influence factor of exercise in clinical applications; therefore, for patients who exert themselves on the way to their appointments, an immediate examination will affect the measurement of liver elasticity. The value is unstable, resulting in the false increase of liver stiffness. Children who might indulge in active play and exercise before their appointments may also find the measured liver stiffness value will be affected. After exercise, the breathing rate of the examinees is accelerated, and the breath-holding effect is not good. As a result, the measured elastic value is unstable, and the degree of dispersion is large. Therefore, this study revealed that it is not recommended to measure immediately after exercise. Instead, a relatively stable measured value should be obtained after at least ten minutes of rest.

Although the results of this study are satisfactory, there are some limitations: 1. The samples were taken from healthy volunteers, with no patients as controls, and the sample size was small. 2. Because it takes time to measure the elasticity, liver blood flow cannot be monitored to observe hemodynamic changes in real-time. Subsequent studies will increase the sample size and add a control group. In the future, the effect of exercise on liver blood flow in animal experiments should be studied.

7. Conclusion

This study suggests that body position and exercise can affect the measurement of liver Young’s modulus. The measured value in left lateral positions is significantly higher than that in the supine position, and the measured value is not as stable as that in the supine position. It is suggested that the supine position should be adopted in the measurement of liver Young’s modulus in the future. The liver Young’s modulus measured at zero minutes after exercise is significantly higher than that measured before exercise, and the measured values are not as stable as before exercise. The liver Young’s modulus measured at five minutes after exercise returned to the baseline level before exercise, but the measured value is not as stable as that after ten minutes of rest. Therefore, it is suggested that liver Young’s modulus should be measured at least ten minutes after exercise. The results of this study will be helpful for the standardized application of RT-SWE technology in the determination of liver Young’s modulus, providing more accurate liver stiffness value for clinical practice.

Footnotes

Acknowledgments

The authors are particularly grateful to all people who helped with this article.

Conflict of interest

The authors declare that they have no competing interests.

Funding

None to report.

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The impact of body position and exercise on the measurement of liver Young’s modulus by real-time shear wave elastography

Abstract

BACKGROUND:

OBJECTIVE:

Methods:

RESULTS:

CONCLUSION:

Keywords

1. Introduction

2. Materials and methods

2.1 Subjects

3. Instruments and methods

3.1 Instruments

3.2 Inspection methods

Table 1 Results of mean value, minimum value, and maximum value of Young’s modulus of liver in different body positions and inter-group comparison (kPa)

5. Results

5.1 Comparison of liver Young’s modulus in different positions

Table 2 Results of liver Young’s modulus before exercise, immediately after exercise, 5 min after exercise, and 10min after exercise (kPa)

Table 3 The Young’s modulus before and immediately after exercise, 5 min before and after exercise, and 10 min before and after exercise were compared in pairs

7. Conclusion

Footnotes

Acknowledgments

Conflict of interest

Funding

References

Table 1
Results of mean value, minimum value, and maximum value of Young’s modulus of liver in different body positions and inter-group comparison (kPa)

Table 2
Results of liver Young’s modulus before exercise, immediately after exercise, 5 min after exercise, and 10min after exercise (kPa)

Table 3
The Young’s modulus before and immediately after exercise, 5 min before and after exercise, and 10 min before and after exercise were compared in pairs