doi:10.1016/S0301-5629(03)00061-9

● Original Contribution

THE ASSESSMENT OF NORMAL FETAL LIVER VOLUME BYTHREE-DIMENSIONAL ULTRASOUND

CHIUNG-HSIN CHANG,* CHEN-HSIANG YU,* FONG-MING CHANG,* HUEI-CHEN KO† and

HSI-YAO CHEN‡

*Department of Obstetrics and Gynecology and†Research Institute of Behavior Medicine, National Cheng KungUniversity Medical College, Tainan, Taiwan; and‡Department of Obstetrics and Gynecology, National Taiwan

University Medical College, Taipei, Taiwan

(Received 8 November 2002;revised 20 January 2003; in final form 12 February 2003)

Abstract—Liver volume (LIVV) is very important in determining the status of fetal growth. However, to measurehuman fetal LIVV in utero precisely and noninvasively is not an easy task. With the recent advancement ofthree-dimensional (3-D) ultrasound (US), the limitation in assessing fetal LIVV by 2-D US can be overcome. Thepurpose of this study was to establish a normal reference chart of fetal LIVV for clinical use. A prospective andcross-sectional study using 3-D US was undertaken to assess the fetal LIVV in normal pregnancy. In total, 226singleton fetuses ranging between 20 and 40 weeks of gestation and fitting the criteria of normal pregnancies wereenrolled in this study. Our results showed that fetal LIVV is highly correlated with the gestational age (GA).Furthermore, using GA as the independent variable and fetal LIVV as the dependent variable, the best-fitregression equation was LIVV (mL) � �398.26� 46.199�GA � 1.7567� GA2 � 0.0236� GA3 (r � 0.97,n� 226, p < 0.0001), with SD of LIVV (mL) � 1.2533� (0.77956� 0.17267� GA). These common indexes offetal biometry, such as biparietal diameter (BPD), occipitofrontal diameter (OFD), head circumference (HCi),abdominal circumference (ACi), femur length (FL), and estimated fetal weight (EFW), were all highly correlatedwith fetal LIVV (all p < 0.0001). In conclusion, our data of fetal LIVV assessed by 3-D US can serve as a usefulreference in evaluating fetal growth status during normal gestation. (E-mail: fchang@mail.ncku.edu.tw)© 2003 World Federation for Ultrasound in Medicine & Biology.

Key Words: Three-dimensional ultrasound, Fetus, Liver volume.

INTRODUCTION

It is crucial to assess the fetal organ volumes accuratelyin the evaluation of fetal growth. In the past decades, 2-Dultrasound (US) was the most commonly used methodfor the measurement of fetal organ dimensions. Livervolume (LIVV) is very useful in determining the statusof fetal growth (Birnholz 1990; Evans et al. 1983; Murao1991; Murao et al. 1987, 1989, 1990; Neiger 1992;Roberts et al. 1989, 1994). It is well-documented thatfetuses with macrosomia or growth restriction are rele-vant to the change of LIVV (Birnholz 1990; Evans et al.1983; Neiger 1992; Roberts et al. 1994). At first, numer-ous studies had used abdominal circumference (ACi) toassess fetal LIVV indirectly with conventional 2-D US.Later, Gross et al. (1982) and Vintzileos et al. (1985)

used the diameter of the fetal liver with 2-D US to assessits size, and some following studies had confirmed itsclinical use (Murao l991; Murao et al. 1987, 1989, 1990;Roberts et al. 1989, 1994; Vintzileos et al. 1986). How-ever, these studies are indirect assessments of the fetalLIVV.

With the advent of three-dimensional (3-D) US, itbecomes an easy and noninvasive approach to obtain anypossible planes and views whenever the targeted-scanned 3-D volume is obtained (Kuo et al. 1992; Lee etal. 1994; Merz et al. 1995). Moreover, precise quantita-tive measurement of fetal organ dimensions becomespossible when the 3-D volume is retrieved (Lee et al.1994; Merz et al. 1995; Chang et al. 1997a). Since ourfirst report of primary application of 3-D US in obstetrics(Kuo et al. 1992), we have published a series of fetalorgan volume assessment using 3-D US, including fetalliver, heart, cerebellum, renal, upper arm and adrenalgland volume, from early second trimester to third tri-mester, and obtained more accurate results than when

Address correspondence to: Dr. Fong-Ming Chang, Departmentof Obstetrics and Gynecology, National Cheng Kung University Med-ical College and Hospital, 138 Victory Road, Tainan, Taiwan. E-mail:fchang@mail.ncku.edu.tw

Ultrasound in Med. & Biol., Vol. 29, No. 8, pp. 1123–1129, 2003Copyright © 2003 World Federation for Ultrasound in Medicine & Biology

Printed in the USA. All rights reserved0301-5629/03/$–see front matter

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using 2-D US (Chang et al. 1997a, 1997b, 1997c; 2000a,b; Liang et al. 1997; Yu et al. 2000; Chang et al. 2002a,b). In addition, fetal weight prediction has also beenreported by several studies using quantitative 3-D US(Chang et al. 1997c; Song et al. 2000; Schild et al. 2000;Lee et al. 2001). In 1997, we first tried to assess the fetalLIVV in normal gestation using 3-D US (Chang et al.1997b). However, due to the limitation of the narrow 3-Dscanner we used previously, we could only measure thefetal LIVV ranging from 20 to 31 weeks of gestation(Chang et al. 1997b). To date, in addition to our previousstudy (Chang et al. 1997b), there were two studies in-vestigating the measurements of fetal LIVV by 3-D US(Laudy et al. 1998; Kuno et al. 2002). First, Laudy andcolleagues measured 34 healthy fetuses ranging from 19to 39 weeks of gestation to calculate the normal fetalLIVV in a Dutch population (Laudy et al. 1998). Second,Kuno and coworkers chose 14 healthy fetuses and 10small-for-gestational fetuses for the fetal LIVV assess-ment in a Japanese population (Kuno et al. 2002). Thenumbers of fetuses in these two studies may be too smallto represent the normal fetal LIVV. Therefore, in thepresent study, we attempted to use a larger 3-D scannerin constructing a reference centiles of normal fetal LIVVduring normal gestation for clinical application, and alsoto compare our results with previous reports in differentpopulations.

MATERIALS AND METHODS

PatientsThe inclusion criteria for the patients in this study

were the following: 1. patients with defined last men-strual period (LMP) and confirmed by a dating US ex-amination in early pregnancy, either by crown-rumplength (CRL) or biparietal diameter (BPD); 2. singletonpregnancies with gestational age (GA) ranging from 20to 40 weeks; 3. normal pregnancies without maternal orfetal complications; and 4. the US examination of eachfetus being selected only once in this series (a cross-sectional study). The setting was at the Ultrasound Unitof the Department of Obstetrics and Gynecology, Na-tional Cheng Kung University Hospital. All the fetusesscanned in this study were followed to delivery to ensurethat they were born healthy. The Institutional ReviewBoard of National Cheng Kung University Hospital ap-proved this study and, before ultrasonic scanning, all thepregnant women gave their informed consent.

3-D ultrasound scanningThe 3-D US equipment (Voluson 530D, Kretztech-

nik, Zipf, Austria), with a 3.0- to 5.0-MHz transabdom-inal mechanical transducer (S-VAW 3 to 5, sweepingangle ranges: 30° to 90°), was used for fetal liver scan-

ning. The details of 3-D US in scanning and assessingfetal LIVV had been previously described elsewhere(Chang et al. 1997b). Briefly, a high-resolution, real-time2-D US scanner scanned the plane of fetal liver. Whenthe fetus was at rest and there was no fetal respiratorymovement, the traditional plane for measuring fetal ACiwas identified by using the high-resolution real-time 2-DUS. The landmark of the fetal ACi plane is the umbilicalportion of the left portal vein deep in the liver, or thebifurcation of the main portal vein into the right and leftbranches, with the fetal stomach as the secondary land-mark (Hadlock 1990; Jeanty and Romero 1984). Then,we turned on the 3-D transabdominal Voluson mechan-ical transducer to measure the fetal LIVV with the nor-mal velocity mode (which swept 90° automaticallywithin 4 s) when the fetus was at rest. The data set wasfurther saved into the built-in computer or in the laserdisks for further retrieval and processing, such as volumedetermination or 3-D-image reconstruction (Merz et al.1995).

Volume measurement with 3-D ultrasoundThe data set was retrieved from the built-in com-

puter or the laser disks by the Voluson 530D scanner(Kretztechnik). As shown in Fig. 1, we used 3-D US tomeasure the fetal LIVV. We fixed the upper-left panel on

Fig. 1. Stepwise measurements of the fetal liver volume by 3-DUS. First, we chose the traditional plane of the abdominalcircumference for measuring the largest dimension of fetal liver(upper right panel). Then we fixed the plane on upper left panelas the reference and moved the cursor on the upper right panelto measure the liver area (dotted area) slice-by-slice every 3mm along the axis of the upper left panel. The computer withinthe 3-D US then integrated and calculated the fetal liver vol-ume; the area enclosed was calculated automatically as weproceeded forward step-by -step. The movement of the mea-sured plane was displayed simultaneously on the lower rightpanel, in the reverse direction. Meanwhile, the reconstructionof the image of the third plane is also displayed concurrently on

the lower left panel for reference.

1124 Ultrasound in Medicine and Biology Volume 29, Number 8, 2003

the first screen as the reference and moved the cursor onthe second screen to measure the liver area (Fig. 1, dottedarea of the upper right panel) slice-by-slice every 3 mmalong the axis of the first screen. The computer within the3-DUS scanner (Voluson 530D) then integrated and cal-culated the fetal LIVV automatically as we proceededforward step-by-step. The details are described in thelegend of Fig. 1.

Fetal biometryTo observe the correlation of fetal LIVV with other

common fetal growth parameters, we further measuredthe BPD, occipitofrontal diameter (OFD), head circum-ference (HCi), ACi and femur length (FL) according tothe methods described in previous reports (Chang et al.1996, 1997, 1998; Chitty et al. 1994a, 1994b, 1994c).Estimated fetal weight (EFW) was also calculated fromthe weight-predicting equation, composed of BPD, ACiand FL, reported by Hsieh and colleagues derived from aTaiwanese population (Hsieh et al. 1987).

ReproducibilityThe intraobserver error was determined by one of

the investigators (C-H. Chang), who repeatedly mea-sured the fetal LIVV of the same subject. The interob-server error was also determined by two of the investi-gators (C-H. Chand and F-M. Chang), who repeatedlymeasured the aforementioned parameters on the samesubject. The observers were blinded to other data whenperforming the interobserver reproducibility test.

StatisticsAll the data of fetal LIVV measurements were put

into an IBM-compatible personal computer for finalanalysis. The SPSS-PC statistical package (Chicago, IL)was used to perform statistical calculation. Linear regres-sion analysis and the correlation analysis were calculatedto test the relationship between the independent anddependent variables. Polynomial regression analysis wascalculated from the first order to the fourth order to findthe best-fit equations. A p value of less than 0.05 wasconsidered statistically significant.

RESULTS

In total, 226 patients who fit all the inclusion criteriawere enrolled for final analysis. The mean and SD of theobserved values of fetal LIVV assessed by 3-D US per 2weeks are shown in Table 1. The fetal LIVV values ofevery 2 weeks were significantly larger than those ofprevious 2 weeks. When using GA as the independentvariable and the fetal LIVV as the dependent variable,the best-fit equation of the fetal LIVV is a third-orderpolynomial regression equation: LIVV (mL) � �398.26

� 46.199 � �1.7567 � GA2 � 0.0236 � GA3(r � 0.97,n � 226, p � 0.0001), with SD of LIVV (m) � 1.2533� (0.77956 � 0.17267 � GA). In addition, the scatter-gram, best-fit equation, r and p values of fetal LIVV vs.GA are demonstrated in Fig. 2; the correlation coefficientof fetal LIVV vs. GA was highly significant (r � 0.97, p� 0.0001). The predicted values of fetal LIVV using GAas the independent variable are listed in Table 2.

To investigate the correlation between fetal LIVVand other common fetal growth parameters, the scatter-grams of fetal LIVV vs. BPD, OFD, HCi, ACi, FL andEFW are also illustrated in Fig. 3a to f. The best-fitequations for fetal LIVV vs. BPD, HCi, and FL were thethird-order polynomial equations (Fig. 3a, c and e) andthe correlation coefficients were all highly significant (p� 0.0001). The best-fit equations for fetal LIVV vs. OFD

Table 1. Observed values of fetal liver volume per every 2weeks of gestation by 3-D US

GA (week) Sample size

Liver volume (mL)

Mean SD p

20 9 11.73 1.39 –21–22 22 16.51 5.62 0.00123–24 15 24.67 6.35 0.00025–26 15 30.62 8.18 0.03527–28 24 32.23 8.95 0.56929–30 27 41.22 9.87 0.00131–32 22 51.32 9.54 0.00133–34 28 65.93 6.10 0.00035–36 25 81.36 6.34 0.00037–38 24 110.18 10.07 0.00039–40 15 131.59 16.71 0.000Total 226 – – –

GA � gestational age; p � values between the mean values of every2 weeks and those of previous 2 weeks examined by Student’s t-test;most were significantly different.

Fig. 2. The scattergram, best-fit equation, r, and p values offetal liver volume vs. gestational age (GA).

Fetal liver volume by 3-D ultrasound ● C-H. CHANG et al. 1125

and ACi were the second-order polynomial equations(Fig. 3b and d) and the correlation coefficients were alsohighly significant (p � 0.0001). The equation betweenfetal LIVV vs. EFW (Fig. 3f) was a simple linear regres-sion equation, and the correlation coefficient was highlysignificant (p � 0.0001).

The reproducibility data for determining the intraob-server and interobserver errors of the fetal LIVV are alsodemonstrated in Fig. 4a and b. Our data showed that thecorrelation coefficients of intraobserver and interob-server errors were both highly significant (r � 0.99, p �0.0001).

Comparison with the previous literature of fetalLIVV is listed in Table 3. When comparing with theprevious results in different populations (Laudy et al.1998; Kuno et al. 2002), our fetal LIVV data in theseseries are different from theirs. In general, our values offetal LIVV are closer to those of Japanese values than tothose of the Dutch values. For example, at 21 weeks ofgestation, the difference of fetal LIVV between theDutch and our series was 67%; in contrast, the differenceof fetal LIVV between the Japanese and our series was8%. At 40 weeks of gestation, the difference of fetalLIVV between the difference of fetal LIVV between theDutch and our series was 19%; however, the differenceof fetal LIVV between the Japanese and our series wasonly 1%.

DISCUSSION

Using 2-D US for precise assessment of fetal organvolumes has to depend upon the assumption that fetal

organs observe an ideal geometric shape, which may beerroneous, especially when the shape of fetal organ isirregular (e.g., fetal liver). With the advent of 3-D US, aseries of precise quantitative measurements of fetal or-gan volumes was published, including heart volume(Chang et al. 1997a), liver volume (Chang et al. 1997b;Laudy et al. 1998; Kuno et al. 2002), lung volume (Leeet al. 1996; Pohls and Rempen 1998), brain volume(Endres and Cohen 2001), cerebellar volume (Chang etal. 2000b), renal volume (Yu et al. 2000), upper armvolume (Chang et al. 2002a) and adrenal volume (Changet al. 2002b). In this series, we further confirmed thefeasibility of 3-D US in the assessment of fetal LIVV inutero.

In this study, the reproducibility data for determin-ing the intraobserver and interobserver errors of the fetalLIVV showed that the correlation coefficients of intraob-server and interobserver errors were both highly signif-icant (r � 0.99, p � 0.0001). The high reproducibilityfurther validates the potential of 3-D US in clinicalpractice.

In addition, the correlation between fetal LIVV andother common fetal growth parameters (e.g., BPD, OFD,HCi, ACi, FL and EFW) and the correlation coefficientswere all shown to be highly significant (p � 0.0001). Ourobservation implies that the fetal liver growth is closelyrelevant to the other growth indexes and to fetal weight,as well.

When comparing this study with the previous liter-ature on fetal LIVV, the fetal LIVV data in these seriesare different from theirs (Laudy et al. 1998; Kuno et al.

Table 2. Predicted values of fetal liver volume using gestational age (GA) as the independent variable

GA

Liver volume (mL)

5th 10th 25th 50th 75th 90th 95th SD

20 3.09 5.05 8.26 11.84 15.42 18.63 20.59 5.3121 6.66 8.71 12.05 15.77 19.50 22.84 24.88 5.5222 9.70 11.82 15.29 19.17 23.04 26.51 28.64 5.7423 12.34 14.54 18.14 22.16 26.18 29.79 31.99 5.9524 14.72 17.00 20.74 24.90 29.07 32.80 35.09 6.1725 16.99 19.35 23.22 27.53 31.84 35.70 38.07 6.3926 19.28 21.73 25.72 30.18 34.64 38.63 41.07 6.6027 21.74 24.27 28.39 33.00 37.60 41.73 44.25 6.8228 24.52 27.12 31.38 36.13 40.88 45.13 47.74 7.0429 27.74 30.42 34.81 39.71 44.60 48.99 51.67 7.2530 31.56 34.32 38.84 43.88 48.92 53.44 56.20 7.4731 36.11 38.95 43.60 48.79 53.98 58.63 61.47 7.6932 41.53 44.46 49.24 54.57 59.91 64.69 67.61 7.9033 47.98 50.98 55.89 61.37 66.85 71.77 74.77 8.1234 55.58 58.67 63.71 69.34 74.96 80.00 83.09 8.3335 64.49 67.65 72.83 78.60 84.37 89.54 92.71 8.5536 74.84 78.08 83.38 89.30 95.22 100.53 103.77 8.7737 86.77 90.09 95.53 101.59 107.66 113.09 116.42 8.9838 100.43 103.83 109.40 115.61 121.82 127.38 130.79 9.2039 115.95 119.44 125.13 131.49 137.85 143.54 147.03 9.4240 133.49 137.05 142.88 149.38 155.88 161.71 165.27 9.63

1126 Ultrasound in Medicine and Biology Volume 29, Number 8, 2003

2002). As listed in Table 3, it seems that our values offetal LIVV are closer to those of Japanese values than tothose of the Dutch values. The data showed that at 21weeks and 40 weeks of gestation, the difference of fetalLIVV between the Dutch and our series was 67% and19%, respectively; in contrast, at 21 weeks and 40 weeksof gestation, the difference of fetal LIVV between the

Japanese and our series was 8% and 1%, respectively.These differences might be attributed to two possiblefactors. First, the sample sizes of the previous two stud-ies (Laudy et al. 1998; Kuno et al. 2002) were too smallto reach a strong power in representing a normal popu-lation for a clinical study (34 fetuses in the Dutch studyand 14 fetuses in the Japanese study). Second, the dif-

Fig. 3. The fetal liver volume vs. the common parameters of fetal growth. Scattergram and correlation between the fetalliver volume (a) vs. BPD, (b) vs. OFD, (c) vs. head circumference, (d) vs. abdominal circumference,. (e) vs. femur

length, and (f) vs. estimated fetal weight..

Fetal liver volume by 3-D ultrasound ● C-H. CHANG et al. 1127

ference might be due to the ethnic factors in differentpopulations. In the future, an internationally collaboratedstudy for the evaluation of fetal LIVV in different pop-ulations by 3-D US is warranted.

In conclusion, in this study, we used 3-D US tomeasure the fetal LIVV and obtained a good correlationbetween GA and the fetal LIVV. Furthermore, the fetalLIVV is also highly correlated with common indexes offetal biometry (e.g., BPD, OFD, HCi, ACi, FL, andEFW). We believe that our chart of fetal LIVV at normalgestation assessed by 3-D US can be utilized as a clinicalreference for the evaluation of fetal growth.

Acknowledgments—This study was supported in part by grants to F-M.Chang and to C-H. Chang from National Science Council, Taipei,Taiwan. The authors are grateful to Ms. Wen-Chu Chen, Yueh-ChinCheng and Yi-Jen Wang for their assistance.

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n � cases number; *The data in the Laudy’s series were calculatedfrom their equation of liver volume.

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Fetal liver volume by 3-D ultrasound ● C-H. CHANG et al. 1129