doi:10.1016/j.ultrasmedbio.2003.08.012

● Original Contribution

PRENATAL ASSESSMENT OF NORMAL FETAL HUMERUS VOLUME BYTHREE-DIMENSIONAL ULTRASOUND

CHIUNG-HSIN CHANG,* CHEN-HSIANG YU,* HUEI-CHEN KO,† FONG-MING CHANG* andHSI-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 17 April 2003;revised 7 August 2003; in final form 14 August 2003)

Abstract—Because fetal humerus dysplasia is associated with a variety of congenital syndromes, prenatalassessment of the fetal humerus growth is very important. The fetal humerus volume is one of the indexes inevaluating the humerus growth, but it has never been studied by 3-D ultrasound (US)in utero. To establish anormal reference chart of the fetal humerus volume for clinical use, we undertook a prospective and cross-sectional study using 3-D US to assess the fetal humerus volume in normal pregnancy. A total of 216 singletonfetuses that ranged between 20 and 40 weeks of gestation and fit the criteria of normal pregnancies were includedin this study. Our results showed that the fetal humerus volume is highly correlated with the gestational age (GA).Using GA as the independent variable and the humerus volume as the dependent variable, the best-fit regressionequation was humerus volume (mL)� 0.0044GA2 � 0.0841GA� 0.6874 (r� 0.97,n � 216,p < 0.0001). Forclinical use, a chart of normal growth centiles of the fetal humerus volume was then established based on thisequation. In addition, the common indexes of fetal biometry, such as biparietal diameter, occipitofrontaldiameter, head circumference, abdominal circumference, femur length and estimated fetal weight, were all highlycorrelated with the humerus volume (all p < 0.0001). In conclusion, our data of the fetal humerus volumeassessed by 3-D US can serve as a useful reference in evaluating the fetal humerus growth during normalgestation. (E-mail: fchang@mail.ncku.edu.tw) © 2003 World Federation for Ultrasound in Medicine & Biology.

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

INTRODUCTION

Prenatal assessment of the fetal humerus growth is veryimportant because fetal humerus dysplasia is associatedwith a variety of congenital syndromes (Benacerraf et al.1987, 1991; LaFollette et al. 1989). During the pastdecades, 2-D ultrasound (US) was the most commonlyused tool for the measurement of the fetal humeruslength (HL). In addition to the HL, the fetal humerusvolume is one of the useful indexes in evaluating hu-merus growth. Although the humerus possesses a uniqueshape, the humerus volume cannot be directly assessedby 2-D US in utero precisely.

With the advent of 3-D US, accurate measurementof the fetal organ dimensions becomes possible when the3-D volume is retrieved (Chang FM et al. 1997a; Lee et

al. 1994; Merz et al. 1995). Since our first report ofprimary application of 3-D US in obstetrics (Kuo et al.1992), we have published a series of papers on fetalorgan volumetry using 3-D US, including the liver, heart,cerebellum, kidney, upper arm, adrenal gland, thigh andlung volume, and we obtained more accurate results thanwith 2-D US (Chang CH et al. 2000a, 2000b, 2002a,2002b, 2003a, 2003b, 2003c; Chang FM et al. 1997a,1997b, 1997c; Liang et al. 1997; Yu et al. 2000). To date,no reports on the fetal humerus volume assessed by 3-DUS in normal gestation were available. We undertookthis study with three main aims. First, we attempted toassess the correlation between the fetal humerus volumeand gestational age (GA) using 3-D US. Second, we triedto evaluate the relevance between the fetal humerusvolume and the common indexes of the fetal biometry;such as biparietal diameter (BPD), occipitofrontal diam-eter (OFD), head circumference (HCi), abdominal cir-cumference (ACi), femur length (FL) and estimated fetalweight (EFW) using 3-D US. And, third, we would like

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. 12, pp. 1675–1680, 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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to construct reference centiles of the fetal humerus vol-ume using 3-D US during normal gestation for clinicalapplication.

MATERIALS AND METHODS

PatientsWomen who attended the prenatal clinic and were

referred for a US examination for fetal biometry wereincluded. The enrolled criteria for patients in this studywere as follows: 1. patients with defined last menstrualperiod and confirmed by US dating in early pregnancy,either by crown-rump length (CRL) or BPD; 2. singletonpregnancies with GA ranging from 20 to 40 weeks; 3.normal pregnancies with neither maternal nor fetal com-plications; and 4. the US examination of each fetus inthis study was a mixture of cross-sectional and serialmeasurements. All the fetuses scanned in this study hadfollow-up to delivery to ensure that they were bornnormal. The setting was the Ultrasound Unit of theDepartment of Obstetrics and Gynecology, NationalCheng Kung University Hospital. This study was ap-proved by the Institutional Review Board of NationalCheng Kung University Hospital, and all the pregnantwomen gave their informed consent before ultrasonicscanning.

3-D ultrasoundThe 3-D US equipment (Voluson 530D MT, Kretz,

Zipf, Austria), with a 3.0- to 5.0-MHz transabdominaltransducer (S-VAW 3 to 5), was used for the fetal hu-merus scanning. The details of 3-D US in scanning andassessing the fetal organ volumetries has been describedpreviously (Chang CH et al. 2000b). In brief, a high-resolution, real-time 2-D US scanner scanned the tradi-tional plane of the fetal humerus initially. Then, weturned on the 3-D transabdominal transducer to measurethe fetal humerus volume with the normal velocity mode(which swept 90° automatically within 4 s) when thefetus was at rest.

Figure. 1 showed the stepwise measurements of thefetal humerus volume by 3-D US, described as follows.At first, we used the traditional plane of the humerus formeasuring the humerus length on the first screen (upperleft panel) and rotated this plane to make the humerus ina horizontal position. Then, we fixed this plane as thebasis and moved the cursor along the axis of the humerusfrom one end of the diaphysis to the other end, slice byslice every 3 mm. The corresponding transaxial planewas simultaneously illustrated on the second screen (up-per right panel), and the dot cursor was marked along theoutline of the humerus. The dotted area in the upper-rightpanel was measured, as was the thickness of each sliceby a built-in computer as we proceeded along the axis of

the humerus. Meanwhile, the image of the third planewas displayed (lower left panel), and the movement ofthe measured plane was displayed simultaneously (lowerright panel). The integration of the fetal humerus volumewas calculated by the 3-D US automatically when thecursor was moved forward and the area was enclosed.

A complete assessment of the humerus volume usu-ally took 10 to 15 min. The built-in 3-D view softwareallowed the 3-D volume to display simultaneously inthree perpendicular orthogonal planes on the monitor.The data set was further saved into the built-in computeror on the laser disks for further retrieval and processing,such as volume determination or 3-D image reconstruc-tion.

The fetal biometryTo observe the correlation of the fetal humerus

volume with the common fetal growth parameters, wefurther measured the fetal BPD, OFD, HCi, ACi and FLaccording to the methods described in previous reports(Chang CH et al. 1996, 1997, 1998; Chitty et al. 1994a,1994b, 1994c). Estimated fetal weight (EFW) was alsocalculated from the weight-predicting equation, com-posed of BPD, ACi and FL derived from a Taiwanesepopulation (Hsieh et al. 1987).

StatisticsAll the data of the fetal humerus volume measure-

ments were put into an IBM-compatible personal com-puter (PC) for final analysis. We used the SPSS-PCstatistical package (Chicago, IL) to perform statisticalcalculation. Linear regression analysis and correlationanalysis were calculated to test the relationship betweenthe independent and dependent variables. Polynomial

Fig. 1. Stepwise measurements of the fetal humerus volume by3-D US.

1676 Ultrasound in Medicine and Biology Volume 29, Number 12, 2003

regression analysis was calculated from the first order tothe fourth order to find the best-fit equations. To obtainthe predicted values of the humerus volume using GA asthe independent variable (Chitty et al. 1994a, 1994b,1994c), we further generated a table from the best-fitequation. A p value of less than 0.05 was consideredstatistically significant.

RESULTS

A total of 216 cases were included for final analysis.The mean and SD of the observed values of the humerusvolume per 2 weeks are listed in Table 1. The humerusvolume per every 2 weeks was significantly larger thanthose of the previous 2 weeks. Using GA as the inde-pendent variable and the fetal humerus volume as thedependent variable, the best-fit equation of the fetalhumerus volume is a second-order polynomial regressionequation: humerus volume (mL) � 0.0044GA2 �0.0841GA � 0.6874 (r � 0.97, n � 216, p � 0.0001),with SD of the humerus volume (mL) � 1.2533(�0.24734 � 0.01422GA).

Table 2 lists the predicted values of the normalgrowth centiles of the fetal humerus volume; these val-ues were calculated and established by this equation. Inaddition, the scattergram, best-fit equation, r and p valuesof the fetal humerus volume vs. GA are demonstrated inFig. 2.

Table 3 shows the correlations between the fetalhumerus volume and the common fetal growth parame-ters. The correlation coefficients between the fetal hu-merus volume and the common fetal growth parametersare all highly significant (all p � 0.0001). In addition, the

scattergrams of the fetal humerus volume vs. BPD andFL are also illustrated in Fig. 3a and b.

In this study, all the measurements of the fetal hu-merus volume were undertaken by one operator (C-H.Chang), and no interobserver error needs to be consid-ered. As demonstrated in Fig. 4, our result show that thecorrelation coefficient of intraobserver errors was highlysignificant (r � 0.99, n � 30, p � 0.0001).

DISCUSSION

Because humerus dysplasia is associated with a va-riety of congenital syndromes, mild shortening of the

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

Humerus volume

GA Sample size Mean SD p

20 14 0.7387 0.114 –21–22 29 0.8672 0.074 0.00123–24 18 1.0513 0.146 0.00025–26 12 1.5986 0.053 0.00027–28 21 1.8432 0.099 0.00029–30 21 1.9810 0.165 0.00231–32 23 2.4206 0.218 0.00033–34 22 2.7963 0.128 0.00035–36 21 3.1243 0.332 0.00037–38 24 3.5046 0.535 0.00639–40 11 4.5145 0.407 0.000Total 216 – – –

Unit of humerus volume � mL; unit of GA � weeks; GA �gestational age; p values - between the mean values of every 2 weeksand those of previous 2 weeks examined by Student’s t-test; most weresignificantly different.

Table 2. Predicted values of the fetal humerus volume by3-D US

Humerus volume (mL)

GA (weeks) 10th 25th 50th 75th 90th SD

20 0.71 0.73 0.77 0.80 0.82 0.0521 0.78 0.82 0.86 0.91 0.94 0.0622 0.86 0.91 0.97 1.02 1.07 0.0823 0.95 1.01 1.08 1.15 1.21 0.1024 1.05 1.12 1.20 1.28 1.35 0.1225 1.16 1.24 1.33 1.43 1.51 0.1426 1.28 1.37 1.48 1.58 1.67 0.1527 1.41 1.51 1.62 1.74 1.84 0.1728 1.54 1.65 1.78 1.91 2.02 0.1929 1.68 1.81 1.95 2.09 2.21 0.2130 1.84 1.97 2.12 2.28 2.41 0.2231 2.00 2.15 2.31 2.47 2.62 0.2432 2.17 2.33 2.50 2.68 2.83 0.2633 2.35 2.52 2.70 2.89 3.06 0.2834 2.54 2.71 2.91 3.11 3.29 0.3035 2.73 2.92 3.13 3.35 3.54 0.3136 2.94 3.14 3.36 3.59 3.79 0.3337 3.15 3.36 3.60 3.84 4.05 0.3538 3.38 3.60 3.85 4.09 4.32 0.3739 3.61 3.84 4.10 4.36 4.59 0.3940 3.85 4.09 4.36 4.64 4.88 0.40

GA � gestational age.

Fig. 2. The scattergram, best-fit equation, r and p values of thefetal humerus volume vs. gestational age.

Fetal humerus volume by 3-D ultrasound ● C-H. CHANG et al. 1677

humerus may be indicative of a syndrome or a chromo-somal aberration (Benacerraf et al. 1987, 1991; LaFol-lette et al. 1989). Benacerraf and colleagues claimed thatmild humerus shortening (defined as humerus length(HL) � 90% of the predicted HL) is even more specificthan femur shortening in detecting trisomy 21. In addi-tion, Nyberg et al.(1990, 1993) found significant hu-merus shortening in 24% of Down syndrome fetuses.

Therefore, it is very important to make early prenataldiagnosis of humerus dysplasia and to detect relevantsyndromes; thus, it may allow prenatal counseling andappropriate management as soon as possible.

In addition to the mild shortening of the fetal HL,humerus volume is one of the useful indices in evaluat-ing fetal humerus growth. But, to date, no medical liter-ature about the fetal humerus volume has been studied.Although 2-D US is the major tool in fetal biometry, it isimpossible to assess the fetal humerus volume using 2-DUS. When using 2-D US, the volumetry of most fetalorgans has to depend upon the assumption that the fetalorgans observe an ideal geometric shape, which may beerroneous, especially for the fetal humerus. With theadvent of 3-D US, a series of precise quantitative mea-surements of the fetal organ volumes had been reported,including heart volume (Chang FM et al. 1997a), lungvolume (Chang CH et al. 2003c; Lee et al. 1996; Pohlsand Rempen 1998), liver volume (Chang CH et al.2003b; Chang FM et al. 1997b; Laudy et al. 1998), brainvolume (Endres and Cohen 2001), cerebellar volume(Chang CH et al. 2000b), renal volume (Yu et al. 2000),upper arm volume (Chang CH et al. 2002a) and thigh

Table 3. The correlation and regression equations of humerus volume vs. common fetal growth indexes

Y X Regression equations r p

Humerus volume BPD Y � 0.0651X2 � 0.2529X � 0.4067 0.92 �0.0001Humerus volume OFD Y � 0.0142X2 � 0.3026X � 1.8659 0.89 �0.0001Humerus volume HCi Y � 0.0045X2 � 0.0315X � 0.1791 0.91 �0.0001Humerus volume ACi Y � 0.001X2 � 0.1121X � 1.2751 0.92 �0.0001Humerus volume FL Y � 0.1122X2 � 0.3249X � 0.5691 0.93 �0.0001Humerus volume EFW Y � 0.0011X � 0.4091 0.92 �0.0001

Y � dependent variable; X � independent variables; r � correlation coefficient; BPD � biparietal diameter; OFD � occipitofrontal diameter; HCi� head circumference; ACi � abdominal circumference; FL � femur length; EFW � estimated fetal weight; units of humerus volume � mL; Unitsof BPD, OFD, HCi, ACi, FL - cm; units of EFW g.

Fig. 3. The scattergrams and correlations between the fetalhumerus volume and the common parameters of the fetalgrowth: (a) fetal humerus volume vs. biparietal diameter; (b)

fetal humerus volume vs. femur length.Fig. 4. The assessment of intraobserver reproducibility of the

fetal humerus volume using 3-D US.

1678 Ultrasound in Medicine and Biology Volume 29, Number 12, 2003

volume (Chang CH et al. 2003a). In the assessment ofthe fetal skeletal volume, several papers using 3-D USfor the assessment of the volume of the fetal lumbarspine and the spinal canal have been published (Schild etal. 1999, 2000; Wallny et al. 1999). However, no reportson the normal fetal humerus volume assessed by 3-D UShave been published to date. This study may be the firstseries in reporting the assessment of the fetal humerusvolume using 3-D US in normal gestation.

Qualitative 3-D US rendering reconstruction canassist in the diagnosis of skeletal dysplasias because itoffers the potential to better understand spatial relation-ships of normal and abnormal fetal anatomy than con-ventional 2-D US (Garjian et al. 2000). On the otherhand, quantitative 3-D US may provide accurate assess-ment of the fetal organ growth. In this study, we usedquantitative 3-D US to measure the fetal humerus vol-ume and obtained a highly significant correlation be-tween GA and the fetal humerus volume. In addition, thefetal humerus volume is also highly correlated with thecommon indexes of fetal biometry, such as BPD, OFD,HCi, ACi, FL and EFW (Table 3). In addition to thequalitative 3-D US by other investigators (Garjian et al.2000), our study shows that quantitative 3-D US can alsoallow direct assessment of the fetal humerus volume inassisting the prenatal diagnosis of humerus dysplasia.

For reproducibility of the fetal humerus volumeusing 3-D US, all the measurements in this study wereperformed by the same operator (C-H. Chang), and itwas not necessary to consider the interobserver error. Forthe intraobserver error in this study (Fig. 4), our resultsshowed that it was highly significant between the firstmeasurements and repeated measurements of the fetalhumerus volume by 3-D US (r � 0.99, n � 30, p �0.0001). Our study implied that using 3-D US to assessthe fetal humerus volume is clinically applicable, with ahighly significant reproducibility in repeated measure-ments.

The benefit of using humerus volume measurementby 3-D US to find fetal abnormality instead of usinghumerus length by 2-D US is still unclear. In this study,we just reported the references values of humerus vol-ume in normal gestation as a new index for furtherclinical use in prenatal diagnosis. Further studies areneeded to compare humerus length and humerus volumein detecting fetal abnormality; this is being undertakennow in our Ultrasound Unit.

3-D US has provided great advancements in assess-ing volumetry (Merz et al. 1995) and in determining thevascularization as well as blood flow of human organs in3-D (Pairleitner et al. 1999) in recent years. In fetalmedicine, we have used 3-D US in assessing a series ofthe fetal organ volumetry (Chang CH et al. 2000a,2000b, 2000c, 2002a, 2002b, 2003a, 2003b, 2003c;

Chang FM et al. 1997a, 1997b, 1997c; Liang et al. 1997;Yu et al. 2000). In addition, we have applied 3-D US indepicting the vascularization and blood flow of the fetalkidney, liver and placenta (Chang CH et al. 2003d,2003e; Yu et al. 2003). In reproductive medicine, 3-DUS has been used to assess the ovarian blood flow inpolycystic ovary syndrome, aging, in vitro fertilizationand endometriosis (Pan et al. 2002a, 2002b, 2003a,2003b; Wu et al. 2003). In gynecologic oncology, 3-DUS has been used in evaluating the tumor volume incervical cancer (Chou et al. 1997). With the variousapplications of 3-D US in clinical medicine, we believeour chart for the fetal humerus volume using 3-D US atnormal gestation can be applied as a useful clinicalreference in assessing fetal humerus 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 study was also supported in part by a grant from Prema-ture Babies Foundation and a grant from Foundation of Behavior andMaternal-Children’s Medicine. The authors are grateful to Ms. Chu-Ling Chen, Yueh-Chin Cheng and Yi-Jen Wang for their assistance.

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