Changes in Liver Shear Wave Elastography of Preterm Infants during Hospitalization

Abstract

Objective

Liver evaluation is essential in preterm infants because of exposure to hepatotoxic drugs, the effects of parenteral nutrition, and their organ immaturity. The clinical significance of shear wave elastography (SWE) which measures tissue elasticity, is unclear in preterm infants. For SWE application to liver evaluation in preterm infants, we examined the postnatal course and factors associated with changes.

Study Design

We prospectively measured liver SWE values every other week in 37 preterm infants born at 23 to 35 weeks gestation and 12 term infants born after 36 weeks gestation.

Results

The median early postnatal liver SWE value was 1.22 (interquartile range, 1.19–1.26) m/s. The correlations of liver SWE values with gestational age and birth weight were r = −0.18 (p = 0.23) and r = −0.21 (p = 0.157), respectively. The median liver SWE values from birth to 36 to 38 postmenopausal weeks were 1.22 (1.17–1.24) m/s at <28 weeks gestation (n = 9), 1.21 (1.18–1.25) m/s at 28 to 29 weeks gestation (n = 11), 1.24 (1.21–1.28) m/s at 30 to 31 weeks gestation (n = 8), and 1.21 (1.20–1.24) m/s at ≥32 weeks gestation (n = 9). There was no change over time in any gestational age group (p = 0.158). The median liver SWE values were 1.22 (1.17–1.25) m/s (n = 10) and 1.22 (1.19–1.25) m/s (n = 27) for small- and appropriate-for-gestational-age infants, respectively (p = 0.93). The correlations of abnormally high serum concentrations of direct bilirubin (>1.0 mg/dL) and alanine aminotransferase (>12 IU/L) with liver SWE values were r = 0.37 (p = 0.041) and r = 0.21 (p = 0.35), respectively.

Conclusion

Liver SWE values may be useful for the evaluation of liver damage with cholestasis in preterm infants because they remain constant regardless of gestational age and birth weight and do not change over time or with a deviation of body size.

Key Points

• Liver SWE was prospectively performed in preterm infants.

• Liver SWE was constant until term regardless of gestational age or birth weight.

• Liver SWE values of preterm infants ranged from 1.2 to 1.3 m/s.

• For preterm infants, elevation of liver SWE values reflected cholestasis.

• Liver SWE may become the new standard for liver evaluation in preterm infants.

 

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Keywords

acoustic radiation force impulse imaging - preterm infant - cholestasis - liver stiffness - small for gestational age

Ultrasonic elastography is a noninvasive technique used to measure tissue elasticity. It provides quantitative estimates of the elasticity of various tissues. Shear wave elastography (SWE), a specific technique within ultrasonic elastography, measures tissue elasticity according to the velocity of shear waves generated by ultrasonic push pulses.[1] [2] 2-D SWE is reportedly superior to other types of elastography for the evaluation of liver stiffness because it can theoretically obtain quantitative information on tissue elasticity in real time without being affected by target size, and it can simultaneously display color mapping of tissue stiffness to ensure the accuracy of the measurements.[3] Compared with liver biopsy, measurement of tissue elasticity by liver SWE is becoming popular in adult medicine as a noninvasive and more comprehensive method for evaluating fibrosis and stiffness of the whole liver.[3]

Preterm infants, particularly very low-birth-weight infants, often develop intestinal failure-related liver disease and parenteral nutrition-associated liver disease. These conditions are due to long-term enteral nutrition failure following intestinal diseases such as necrotizing enterocolitis.[4] [5] Preterm infants, especially those who are small for gestational age (SGA), have a high incidence of cholestasis due to low protein metabolism and utilization, which in turn increases the risk of parenteral nutrition-associated liver disease.[6] [7] [8] The only available quantitative method for evaluating liver damage and cholestasis in preterm infants is through blood testing, such as measurement of hepatobiliary enzymes. However, blood tests are highly invasive and thus difficult to repeat in the short term. B-mode ultrasound evaluation based on liver brightness is a noninvasive method but it is not quantitative.[9] Additionally, it may be inaccurate in very low-birth-weight infants with potential renal insufficiency because abnormal kidney luminescence can affect the quality of the control.[10] [11]

In the present study, therefore, we focused on liver SWE, which can be used to quantitatively evaluate liver stiffness. Liver stiffness is considered an effective prognostic factor for liver disease in adults.[12] Liver SWE, which can be used to noninvasively evaluate tissue elasticity, is thought to be suitable for evaluating liver stiffness over time in preterm infants with small body size and unstable general condition. However, only one report to date has described the use of liver SWE for evaluation of preterm infants,[13] and no standard values for preterm infants have been established. These factors make it difficult to utilize this method in clinical practice.

We performed repeated liver SWE in preterm infants from the early postnatal period to evaluate changes that occur with gestational age, birth weight, and the postnatal time course and examine the validity of liver SWE for evaluating liver stiffness in preterm infants.

Materials and Methods

Study Design and Study Population

We prospectively measured liver 2-D SWE in 37 preterm infants born before 36 weeks of gestation and 12 term infants admitted to the neonatal intensive care unit of Kanagawa Children's Medical Center from April 2022 to March 2023. Infants with multiple malformations or chromosomal diseases were excluded. The preterm group was classified into infants with a gestational age of <28, 28–29, 30–31, and ≥32 weeks. All infants underwent measurement of the serum direct bilirubin and alanine aminotransferase (ALT) concentrations at the time of liver SWE.

 

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2D Shear Wave Elastography

We performed liver 2-D SWE in the neonatal intensive care unit. Measurements were made by a neonatologist with 10 years of experience in neonatal imaging and 12 months of experience in 2-D liver SWE (T.K.) using a 5-1 MHz convex probe (EPIQ Elite ElastQ; Phillips, Amsterdam, Netherlands). After a 2-hour fast, the infants were placed in the supine or prone position without sedation, and measurements were taken through the right intercostal or subcostal arch approach. The upper edge of the shear wave box was placed 10 to 20 mm from the liver capsule in the right lobe of the liver, avoiding the shadows produced by the hepatic vessels and ribs, and a 10-mm circular region of interest was placed where the confidence map showed a confidence level of ≥80%. To ensure the reliability of the measured values, we adopted values as stable only when the median/interquartile range (IQR) of the measurements in the region of interest was <15%. Measurements were expressed in velocity (m/s), and the median value of the measurements within the region of interest was used for analysis. Five to 10 data values were obtained for each measurement, and the mean value was calculated. We started measurements within 2 weeks after birth and repeated them at 2- to 3-week intervals thereafter until discharge from the hospital or until 40 postmenopausal weeks.

We examined the relationship of the time course of liver SWE values with the weeks of gestation and birth weight. We also examined the relationship between the serum ALT and direct bilirubin concentrations and liver SWE values. We compared liver SWE values between the SGA group and the appropriate for gestational age (AGA) group. In accordance with the infant physical development research report by the Ministry of Health, Labor and Welfare of Japan in 2001, SGA was defined as both height and weight at birth falling below the 10th percentile.

 

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Statistical Analysis

Data are presented as median and IQR. Spearman's correlation coefficients were used to identify relationships within and between different outcome measures. Differences in median values between two groups and among more than two groups were compared using the Wilcoxon signed-rank test or Mann–Whitney U-test and the Friedman test or Kruskal–Wallis test, respectively. Statistical analysis was performed using SPSS 29.0 software (IBM Corp., Armonk, NY), and p-values of <0.05 were considered statistically significant.

 

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Results

Patients' Characteristics

We enrolled 37 (18 boys, 19 girls) preterm infants and 12 (7 boys, 5 girls) term infants. Preterm infants were measured four times (IQR, 3–5) starting at day 1 (IQR, 1–4), and term infants were measured at day 0 (IQR, 0–1).

No deaths occurred, but three infants developed severe gastrointestinal disorders requiring parenteral nutrition for >4 weeks ([Table 1]).

Table 1 Characteristics of the populations studied

Gestational age at birth	<28 weeks (N = 9)	28–29 weeks (N = 11)	30–31 weeks (N = 8)	32–35 weeks (N = 9)	>35 weeks (N = 12)
Total measurement (times)	6 (5–7)	4 (4–5)	3 (3–4)	1 (1–2)	1 (1–1)
Birth weight (g)	678 (582–963)	1,221 (1,093–1,246)	1,100 (1,018–1,226)	2,128 (1,874–2,321)	2,557 (2,420–2,931)
Direct bilirubin (mg/dL)	1.3 (0.8–1.7)	1.2 (0.8–1.7)	1.3 (1.0–1.3)	0.9 (0.8–1.1)	0.9 (0.7–1.1)
Alanine aminotransferase (IU/L)	5 (3–6)	5 (3–5)	6 (3–6)	7 (6–9)	8 (7–11)
Small for gestational age	3 (33)	1 (9)	4 (50)	2 (22)	2 (17)
Multiple gestations	0 (0)	4 (36)	6 (75)	0 (0)	2 (17)
Male	3 (33)	5 (45)	3 (38)	7 (78)	7 (58)
Respiratory distress syndrome	9 (100)	11 (100)	6 (75)	0 (0)	0 (0)
Total parenteral nutrition >4 weeks	2 (22)	0 (0)	1 (13)	0 (0)	0 (0)
Levothyroxine supplementation for hypothyroidism	1 (11)	0 (0)	0 (0)	1 (11)	0 (0)

Values are expressed as either median (interquartile range) or n (%).

 

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Correlation between Liver Shear Wave Elastography Values in Early Postnatal Period and Perinatal Data

There was no correlation between the liver SWE values within 2 weeks of birth and either the gestational age or birth weight ([Fig. 1A, B]).

Fig. 1 Correlation between liver shear wave elastography (SWE) values in the early postnatal period and perinatal data. Scatter plots show the correlation between the early postnatal liver SWE values and the perinatal information. (A) Gestational age: r = −0.18 (p = 0.23). (B) Birth weight: r = −0.21 (p = 0.157).

 

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Postnatal Time Course of liver Shear Wave Elastography Values

Liver SWE values were generally constant regardless of postmenopausal weeks in each gestational age group, and there were no differences between any of the gestational age groups at each postmenopausal week ([Table 2]).

Table 2 Time course of liver shear wave elastography values

GA at birth (wk)	PMA 28 weeks	PMA 30 weeks	PMA 32 weeks	PMA ≥34 weeks	p-Value
<28 n = 9	1.16 (1.16–1.22) m/s	1.21 (1.18–1.23) m/s	1.22 (1.17–1.23) m/s	1.24 (1.21–1.26) m/s	0.175
28–29 n = 11		1.20 (1.18–1.25) m/s	1.23 (1.21–1.28) m/s	1.20 (1.17–1.23) m/s	0.33
30–31 n = 8			1.25 (1.19–1.28) m/s	1.24 (1.23–1.25) m/s	0.40
32–35 n = 9				1.21 (1.20–1.24) m/s
p-Value		0.94	0.36	0.45

Abbreviations: GA, gestational age; PMA, postmenopausal age.

The liver SWE values were generally constant in the SGA and AGA groups regardless of postmenopausal weeks, and there were no differences between the two groups at each postmenopausal week ([Table 3]).

Table 3 Time course of liver shear wave elastography values in the small and appropriate for gestational age groups

	PMA 28 weeks	PMA 30 weeks	PMA 32 weeks	PMA ≥34 weeks	p-Value
SGA n = 10	1.16 (1.15–1.19) m/s	1.23 (1.22–1.27) m/s	1.22 (1.16–1.25) m/s	1.22 (1.19–1.29) m/s	0.33
AGA n = 27	1.18 (1.16–1.22) m/s	1.19 (1.17–1.25) m/s	1.23 (1.20–1.26) m/s	1.23 (1.20–1.25) m/s	0.177
p-Value	0.91	0.35	0.68	0.90

Abbreviations: AGA, appropriate for gestational age; GA, gestational age; PMA, postmenopausal age; SGA, small for gestational age.

 

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Correlation of Liver Shear Wave Elastography Values with Serum Alanine Aminotransferase and Direct Bilirubin Concentrations

Infants in whom the serum direct bilirubin concentration was >1.0 mg/dL, defined as cholestasis[14] (n = 30), showed a correlation between the direct bilirubin concentration and liver SWE values ([Fig. 2A]). Infants in whom the serum ALT concentration was >12 IU/L, which is the upper limit of normal for preterm infants[15] (n = 22), showed no correlation between the ALT concentration and liver SWE values ([Fig. 2B]).

Fig. 2 Correlation between liver shear wave elastography values and laboratory data. Scatter plots show the correlation between the liver shear wave elastography values and the maximum serum direct bilirubin and alanine aminotransferase concentrations. (A) Maximum serum direct bilirubin concentrations of the infants in whom the serum direct bilirubin concentration was >1.0 mg/dL, defined as direct hyperbilirubinemia (n = 30): r = 0.37 (p = 0.041). (B) Maximum serum alanine aminotransferase concentrations of the infants in whom the serum alanine aminotransferase concentration was >12 IU/L, which is the upper limit of normal for preterm infants (n = 22): r = 0.21 (p = 0.35).

In addition, elevated liver SWE levels were observed in three patients with cholestasis due to persistent dependence on parenteral nutrition ([Fig. 3A–C]).

Fig. 3 Time course of liver shear wave elastography values in infants with cholestasis. (A) A boy born at 23 weeks of gestation, 450 g, underwent colostomy because of necrotizing enterocolitis at 3 weeks after birth. He required prolonged parenteral nutrition and subsequently developed intestinal failure-related liver disease. (B) A boy born at 24 weeks of gestation, 544 g, digested enteral feeding (mother's milk) well, and parenteral nutrition was terminated 2 weeks after birth. However, when feeding with milk formula was started 5 weeks after birth, he developed a gastrointestinal allergy, and parenteral nutrition was resumed. He thereafter required prolonged parenteral nutrition and subsequently developed intestinal failure-related liver disease. (C) A boy born at 30 weeks of gestation, 839 g, had poor digestion on enteral feeding; therefore, parenteral nutrition was continued until 4 weeks after birth. He developed intestinal failure-related liver disease 4 weeks after birth because of persistent indigestion associated with gastrointestinal allergy, which resolved spontaneously 6 weeks after birth. All infants were discharged from the hospital alive.

 

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Discussion

In our study, liver SWE values within 2 weeks of birth in preterm infants remained consistent irrespective of gestational age or birth weight. Although not associated with an increase in ALT alone, the liver SWE values increased in correlation with the direct bilirubin level, and there was no difference between the SGA and AGA groups.

The fetal liver is immature and depends on the metabolic activities of the maternal liver for many functions. It acquires its own functions during the neonatal period after birth at full term.[16] [17] At 5 to 6 months of gestation, the biliary system and other structures are established, but functional maturation is gradual.[18] Thus, the level of liver stiffness is assumed to remain constant in preterm infants. This assumption aligns with the time frame following the establishment of the biliary system and other structures at approximately 5 to 6 months of gestation.

The previously reported mean liver SWE values for healthy adults vary widely from 1.07 to 1.59 m/s,[19] [20] [21] whereas those for healthy children range between 1.10 and 1.16 m/s although there is an increase throughout childhood and adolescence.[22] [23] [24] [25] [26] [27] In our study, the median liver SWE value in the early postnatal period was 1.22 m/s (IQR, 1.19–1.26 m/s), which is slightly higher than that previously reported in children. This might be explained by the fact that the liver elasticity is higher in infants than in older children because of residual intrahepatic hematopoiesis, especially during preterm birth.[28]

SWE must be performed with immobile tissues, but infants are unable to hold their breath. Hence, there is concern about the influence of body movement on the measurements in infants, who are unable to cooperate. Previous studies showed no significant difference in measurements between free breathing and respiratory arrest in children.[29] [30] Therefore, we ensured the reliability of the measurements by adopting values as stable only when the median/IQR of the measurements in the region of interest was <15%. The number of measurements required for adults is considered to be 10, but it is difficult to obtain 10 stable measurements in infants. Because previous studies revealed no significant difference between 5 and 10 measurements in children,[29] [31] and recommended that the minimum acquisition number should be 3 to 5 for 2-D SWE.[32] we set the minimum number of measurements at 5 and terminated the examination when body movements made stable measurements difficult.

Alison et al[13] examined preterm infants and found higher liver SWE values in those with than without intrauterine growth restriction. In our study, no difference was found between the SGA and AGA groups. This likely occurred because 2 of 10 (20%) infants had direct hyperbilirubinemia in the SGA group, which was a lower proportion than 7 of 18 (39%) infants in the intrauterine growth restriction group reported by Alison et al.[13]

The main limitation of this study is the small sample size, particularly for infants born before 28 weeks gestation, which led to a lower number of infants with cholestasis. Future investigations should focus on larger cohorts, especially those including extremely preterm infants with cholestasis, to enhance the statistical power and generalizability of the findings. In addition, a liver biopsy could not be performed for research purposes because of its invasive nature and the large sample required for the measurement of liver fibrosis markers. Therefore, the evaluation of serum direct bilirubin and ALT, which are commonly used in routine evaluations, was performed as a substitute. Moreover, the ultrasonographers were not completely blind to the patient's clinical presentations. However, we consider this to be of little influence because we comprehensively measured all patients during the study period and the SWE values were measured semiautomatically.

Fortunately, none of the infants developed serious liver injury or liver failure during the observation period. However, this prevented us from assessing the efficacy of liver SWE in cases of fetal liver cirrhosis.

 

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Conclusion

Liver SWE is stable and easy to perform even in preterm infants, and the measured values remain consistent until 40 postmenopausal weeks regardless of gestational age, birth weight, and deviation of body size. Liver SWE may be useful for repeated noninvasive evaluation of liver damage with cholestasis in preterm infants. Larger prospective studies are needed to validate these findings and provide more robust data.

 

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Conflict of interest

None declared.

Acknowledgments

Authors thank Angela Morben, DVM, ELS, from Edanz ( https://jp.edanz.com/ac ) for editing a draft of this manuscript.

Ethical Approval

The study was conducted in accordance with the principles contained in the Declaration of Helsinki and was approved by the institutional review board of Kanagawa Children's Medical Center (No. 144-1). All parents or guardians of the participating infants were informed of the use of the test data and the study purpose using an opt-out approach. There were no inquiries regarding the non-use of data during the posting of the opt-out option because the liver SWE images were obtained simultaneously with comprehensive ultrasound examinations of the brain, heart, and abdominal organs for biweekly health monitoring purposes.

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Publikationsverlauf

Eingereicht: 15. Oktober 2024

Angenommen: 25. November 2024

Accepted Manuscript online:
28. November 2024

Artikel online veröffentlicht:
28. Dezember 2024