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EURO-8508; No. of Pages 4 European Journal of Obstetrics & Gynecology and Reproductive Biology xxx (2014) xxx–xxx
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Finding the most accurate method to measure head circumference for fetal weight estimation Ulrike Schmidt a, Dunja Temerinac a,b, Katharina Bildstein b, Benjamin Tuschy a, Jade Mayer a, Marc Su¨tterlin a,b, Jo¨rn Siemer c, Sven Kehl a,d,* a
Department of Obstetrics and Gynecology, University Medical Centre Mannheim, Heidelberg University, Mannheim, Germany Department of Obstetrics and Gynecology, Stadtklinik Frankenthal, Frankenthal, Germany c Department of Obstetrics and Gynecology, Klinikum Pforzheim, Pforzheim, Germany d Department of Obstetrics and Gynecology, Erlangen University Hospital, Erlangen, Germany b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 14 December 2013 Received in revised form 4 March 2014 Accepted 31 March 2014
Objective: Accurate measurement of fetal head biometry is important for fetal weight estimation (FWE) and is therefore an important prognostic parameter for neonatal morbidity and mortality and a valuable tool for determining the further obstetric management. Measurement of the head circumference (HC) in particular is employed in many commonly used weight equations. The aim of the present study was to find the most accurate method to measure head circumference for fetal weight estimation. Study design: This prospective study included 481 term pregnancies. Inclusion criteria were a singleton pregnancy and ultrasound examination with complete fetal biometric parameters within 3 days of delivery, and an absence of structural or chromosomal malformations. Different methods were used for ultrasound measurement of the HC (ellipse-traced, ellipse-calculated, and circle-calculated). As a reference method, HC was also determined using a measuring tape immediately after birth. FWE was carried out with Hadlock formulas, including either HC or biparietal diameter (BPD), and differences were compared using percentage error (PE), absolute percentage error (APE), limits of agreement (LOA), and cumulative distribution. Results: The ellipse-traced method showed the best results for FWE among all of the ultrasound methods assessed. It had the lowest median APE and the narrowest LOA. With regard to the cumulative distribution, it included the largest number of cases at a discrepancy level of 10%. The accuracy of BPD was similar to that of the ellipse-traced method when it was used instead of HC for weight estimation. Conclusion: Differences between the three techniques for calculating HC were small but significant. For clinical use, the ellipse-traced method should be recommended. However, when BPD is used instead of HC for FWE, the accuracy is similar to that of the ellipse-traced method. The BPD might therefore be a good alternative to head measurements in estimating fetal weight. ß 2014 Elsevier Ireland Ltd. All rights reserved.
Keywords: Head circumference Biparietal diameter Measurement Ultrasound Fetal weight estimation
Introduction Accurate fetal weight estimation (FWE) is an important prognostic parameter for neonatal morbidity and mortality and is a valuable tool for determining the further obstetric management [1]. Fetal biometry using ultrasound has therefore become part of
* Corresponding author at: Department of Obstetrics and Gynecology, University Medical Centre Mannheim, Heidelberg University, Theodor-Kutzer-Ufer 1-3, 68167 Mannheim, Germany. Tel.: +49 621 383 3447/+49 17660025334; fax: +49 621 383 5074. E-mail address: [email protected] (S. Kehl).
routine practice in obstetrics. Standard fetal biometry measurements – such as abdominal circumference (AC), femur length (FL), biparietal diameter (BPD), and head circumference (HC) – are used in many formulas. However, the accuracy of these formulas appears to be generally poor [2], and accurate head measurement of the fetus is essential [3]. There is general agreement on the sonographic plane at which HC and BPD should be measured: it is the transverse section at the level at which the continuous midline echo is broken by the cavity of the septum pellucidum in the anterior third [4]. However, ways of calculating the HC have not been standardized, and it can be done with different methods. The aims of the present study were to compare different methods of calculating head circumference and to determine the most accurate one for FWE.
http://dx.doi.org/10.1016/j.ejogrb.2014.03.047 0301-2115/ß 2014 Elsevier Ireland Ltd. All rights reserved.
Please cite this article in press as: Schmidt U, et al. Finding the most accurate method to measure head circumference for fetal weight estimation. Eur J Obstet Gynecol (2014), http://dx.doi.org/10.1016/j.ejogrb.2014.03.047
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Material and methods A prospective multicenter study was conducted between March and December 2011 at the Perinatal Center at the University Medical Centre Mannheim, Mannheim, Germany, the Department of Obstetrics and Gynecology, Stadtklinik Frankenthal, Frankenthal, Germany, and the Department of Obstetrics and Gynecology, Ludmillenstift Hospital, Meppen, Germany. Pregnant women with singleton pregnancies and a fetus in cephalic presentation at term (259 days of gestation) were recruited consecutively by the physicians in the labour. Oral informed consent was obtained. The ultrasound examination with complete biometric parameters – BPD, occipitofrontal diameter (OFD), HC, AC and FL – was carried by a total of seven different examiners. When onset of labour was excluded, the women left the hospital and measurement was repeated during the next admission, if the last assessment of fetal biometry was not undertaken within the last three days. Each fetus was included only once. Pregnancies with structural or chromosomal malformations, as well as intrauterine fetal deaths, were excluded. The gestational age was defined by the measurement of crown-rump length in the first trimester [5,6]. For all measurements, a Samsung Medison SonoAce R7 (Sonoace Ltd., Marl, Germany) was used with standard techniques [3,7]. Three different methods were used to calculate the sonographic HC. First (in the ellipse-calculated method), the BPD is measured at the largest distance from the outer edges of the skull at the level of the cavity of the septum pellucidum [8]. Measurements of the OFD are done in the same plane, between the outer edge of the frontal bone and the outer edge of the occiput. The following formula is used to estimate the HC from the measurements of the OFD and BPD: HC = p H [(BPD2 + OFD2)/2]. Kurmanavicius et al. have described this method (the ellipse-calculated method) in detail previously [3]. The second method (the ellipse-traced method) involves measuring the HC by placing an ellipse around the outer edge of the fetal skull. The ultrasound machine automatically determines the longest (DL) and shortest diameter (DS). The distances measured are then inserted into the above-mentioned formula for the ellipse-calculated method. In the third method (the circle-calculated method), the same BPD and OFD measurements from the ellipse-calculated method are used in a different equation for calculating the HC: p [(ATD + APAD)/2] [7]. As a reference value for the sonographic measurements, together with the birth weight, HC was also measured in the neonates within 1 hour after delivery. The measuring tape was placed along the maximum horizontal plane, along the occipital prominence at the back, above the ears, and directly above the eyebrows at the front. The postnatal HC measurement is very reliable, with extremely high correlation coefficients for both intraobserver (0.999) and interobserver (0.979) measurements [9,10]. Fetal weight estimation with the four different methods of HC calculation (ellipse-traced, ellipse-calculated, circle-calculated, and postpartal) was done using the Hadlock formula (HC, AC, FL) [11]. In previous studies, our group and others have shown that the Hadlock formulas are among the most accurate weight equations for term fetuses, and they have therefore been adopted as the clinical standards in our institutions [2,12–14]. In addition to HC, FWE was also determined with another Hadlock formula, using the BPD instead (BPD, AC, FL) [11]. In contrast to our BPD and HC measurements, the measuring track was set between the outer and the inner edge of the skull bone in the original publication of Hadlock. The accuracy of the estimated fetal weight (EFW) was assessed by calculating the percentage error (PE; (EFW BW)/BW 100)
and the absolute percentage error (APE; jEFW BWj/BW 100). The mean PEs for all the equations were compared with zero using the t-test at a significance level of 5% in order to assess whether any significant systematic bias had occurred. A variance test for the PE values was performed using the Pitman method [15,16]. At a significance level of 5% and with a sample size of more than 400, R values greater than 0.098 were significant. For APE values, differences between the various techniques were compared using Wilcoxon’s test at a significance level of 5%. The limits of agreement (LOA) method described by Bland and Altmann [17] was also used. The overall mean difference between the derived fetal weight and BW refers to the extent of systematic error, whereas the LOA refers to random error. The 95% LOA indicates what difference between the real BW and the EFW can be expected, and what tendency (to underestimate or to overestimate) is commonly found. Percentages of fetal weight estimations falling within discrepancy levels of 10% of the actual BW were also calculated for each technique. Differences between the postpartal measurements and the sonographic equations were compared using McNemar’s test. P values 0.05 were considered to be significant. The Statistical Package for the Social Sciences (SPSS), version 15.0.1 (2006; SPSS, Inc., Chicago, Illinois, USA) was used for statistical evaluation. Results A total of 458 women was included in this study. The median maternal age was 30, ranging from 18 to 46 years. The gestational age ranged from 37 weeks to 42 weeks, with a median gestational age of 39 weeks 5 days. The median gravidity was 2 (range from 1 to 8) and the parity including the delivery in this study 1 [1–7]. The period between ultrasound measurement and delivery was 1 day, ranging from 0 to 3. The median birth weight was 3380 g (2160– 4785). The postpartal HC measurements ranged from 312 mm to 402 mm, with a median of 350 mm. There were 13 newborns with a birth weight below 2500 g and 28 with 4000 g or more. The results of the different ultrasound measurements for HC and BPD are shown in Table 1. When the Hadlock formulas were used to estimate fetal weight, all of the methods for the HC significantly underestimated fetal weight. It was only when the BPD was used that no systematic error was found in the PE (Table 2). As an indicator of random error, the SD of the reference method (postpartal HC) was compared with all of the other methods; the variance test only showed a significant difference with the BPD formula in this case (Table 2). The APEs are shown as median values and ranges in Table 2. The lowest median APE was found for the ellipse-traced method. In comparison with the reference method, only the circle-calculated measurements were significantly larger. Table 3 illustrates the limits of agreement between the fetal weight estimates and true birth weight. FWE calculated with the postpartal HC measurements demonstrated the narrowest LOA. The BPD method showed the smallest tendency to either overestimate or underestimate fetal weight. Table 1 Head circumferences, either calculated using the three different ultrasound methods or measured after birth, and sonographic biparietal diameter of the head (BPD) (in mm). Median (range) BPD Ellipse-traced Ellipse-calculated Circle-calculated Postpartal
95.1 338.0 329.9 328.5 350.0
(81.5 to 113.1) (288.7 to 394.4) (290.9 to 386.5) (290.6 to 384.1) (312.0 to 402.0)
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Table 2 Mean values for percentage error (PE) in fetal weight estimation with Hadlock formulas, using different methods to measure head circumference (HC) or using the biparietal parameter (BPD), were compared to zero using the t-test. P values 0.05 were considered significant. Correlated variance tests of the PE between the postpartal measurement (reference method) and the ultrasound methods were performed using the Pitman method. R values >0.098 were considered significant. Absolute percentage errors (APE) were also compared between the neonatal HC and the ultrasound measurements using Wilcoxon’s test. P values 0.05 were considered significant. PE Mean (SD) BPD Ellipse-traced Ellipse-calculated Circle-calculated Postpartal
0.41 1.87 3.56 3.91 1.05
(9.52) (9.17) (9.24) (9.16) (9.19)
APE
Mean P value
Variance R value
Median (range)
P value
0.356 0.001 0.001 0.001 0.015
0.105 0.003 0.016 0.009 –
6.60 6.49 7.05 7.11 6.91
0.340 0.601 0.011 0.008 –
(0.00–32.57) (0.01–27.40) (0.01–27.82) (0.05–27.40) (0.02–28.41)
SD, standard deviation.
With regard to postpartal HC measurements, 74.2% of the fetal weight estimates fell within 10% of the actual weight at birth (Table 4). This was significantly higher than when the ellipsecalculated or circle-calculated methods were used. No significant differences were observed between the ellipse-traced method (73.4%) and the BPD formula (71.4%).
Comments Fetal head measurements provide indispensable data for weight estimation with the majority of the weight equations commonly used [12,18]. The present study compared three different ultrasound methods for calculating the fetal HC. The results were compared with postpartal HC measurements and with a weight formula including BPD instead of HC. The results of the study show that the ellipse-traced method is preferable for FWE. The ellipse-traced method had the lowest median APE of all the methods investigated and included the largest number of cases at a discrepancy level of 10% among the ultrasound methods. When the BPD was used instead of HC, the accuracy of FWE was similar to that of the ellipse-traced method. BPD might therefore be an appropriate alternative, especially in cases in which the HC is difficult to measure due to poor ultrasound conditions. Since there were fetuses in breech position included – a dolichocephalic head shape might influence the BPD – this has to be confirmed in further investigations. In a study by Melamed et al. [19], ultrasound estimates of fetal HC were compared with measurements taken postnatally with a measuring tape. The ultrasound HC was measured as an ellipse around the perimeter of the fetal skull, within 3 days before delivery. A total of 3008 pregnancies were examined. The study showed significant underestimation with ultrasound HC measurements in comparison with the postnatally measured HC. The type of fetal presentation did not affect the ultrasound measurement error, but the difference increased with gestational age. Male sex and delivery by vacuum extraction had an influence on reduced ultrasound accuracy. In a published letter, Wegrzyn et al. [20] noted that the influence of gestational age may be due to larger babies, as a result of increased subcutaneous tissue. The error also depended on the mode of delivery; it was smallest for cesarean Table 3 Limits of agreement between fetal weight estimated using the Hadlock formula (HC, AC, FL or BPD, AC, FL) and birth weight (in g) in the study group (n = 458). Head measurement Biparietal diameter Ellipse-traced Ellipse-calculated Circle-calculated Postpartal
Mean (SD) 2 74 131 143 26
(316) (308) (311) (309) (307)
95% limits of agreement 617 678 741 749 576
to to to to to
621 530 479 463 628
sections and increased for vaginal deliveries and vacuum extractions. Wegrzyn based these findings on the influence of subcutaneous tissue edema on neonatal HC. However, FWE was not one of the objectives in their study. Fetal sex and mode of delivery were not taken into account in the present study, and it may be assumed that these did not make any difference in relation to the issue currently being investigated. Head circumference also plays an important role in other areas apart from fetal weight estimation. In cases of congenital diaphragmatic hernia, the lung-to-head ratio (LHR) is an important prognostic parameter for neonatal outcome [21] and accurate HC measurement is therefore essential in these fetuses. Fetal growth restriction is another issue in which accurate HC measurement is needed. Campbell et al. described the impact of the fetal head-toabdomen ratio on the assessment of fetal growth restriction and demonstrated that the HC–AC ratio is an important tool for distinguishing between symmetrical and asymmetrical growth restriction [4]. To what extent the results of this study can be transferred in these situations is unclear since these examinations are undertaken in earlier weeks of gestation. Detecting macrosomic fetuses is an important obstetric issue in relation to increased perinatal morbidity. The neonatal records for newborns with a BW of at least 4000 g were reviewed in a study by Oral et al. [22]. In comparison with the control group, the macrosomic infants were at increased risk for birth trauma and asphyxia. These data once again demonstrate the importance of accurate weight estimation. In a recent study, Larson et al. [23] investigated the association between HC and shoulder dystocia. The results showed that infants with a smaller mean HC were more likely to suffer from shoulder dystocia than infants of similar size who did not have asymmetric macrosomia. In macrosomic fetuses, AC is increased and this influences fetal weight estimation in the first place. Ellipse-traced measurement of fetal AC also seems to be method of choice [24]. The present study only identified small differences between the methods evaluated. However, since all of the methods are likely to be equally time-consuming, the ellipse-traced technique can still be recommended. Table 4 Percentages (%) of fetal weight estimates falling within a discrepancy level of 10% of the actual birth weight using either three different sonographic methods to calculate the head circumference (HC), or the biparietal parameter (BPD). Postpartal HC measurements were compared with the ultrasound methods using McNemar’s test. P values 0.05 were considered significant. Head measurement
BPD Ellipse-traced Ellipse-calculated Circle-calculated Postpartal
10% %
P value
71.4 73.4 67.5 66.8 74.2
0.143 0.754 0.005 0.003 –
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Postpartal HC measurement was used as a reference method in this study. It provided the highest level of accuracy for FWE in comparison with the ultrasound methods. It can therefore be assumed that there are still difficulties with regard to accuracy in measuring and calculating the real HC. Especially in the late weeks of gestation, fetal head measurement on ultrasound can be difficult, as there is less amniotic fluid and poorer demarcation from other tissues. Another problem may be that the fetal head lies deep in the pelvic inlet, making it difficult to replicate the correct ultrasound plane. The results of this study are only applicable in mature fetuses, and differences between the HC calculations may not be apparent in preterm fetuses. Conclusion Measurement of the head circumference is an important parameter for fetal weight estimation. On the basis of this study’s results, use of the ellipse-traced method can be recommended for calculating the head circumference in term fetuses. Its superiority is based on the fact that at term pregnancy it is very difficult to demarcate endpoints where to put calipers for measurement, as outer borders of frontal and occipital bones are very poorly defined due to the shadow from the bones of the cranial vault that are proximal to the transducer. Ellipse-traced method helps to measure head circumference as it assumes ellipsoidal shape of the skull at this cross-section. However, when the biparietal diameter is used instead of head circumference for weight estimation, the accuracy is similar to that with the ellipse-traced method. The BPD may therefore be a good alternative for head measurements in fetal weight estimation.
[6]
[7]
[8]
[9]
[10]
[11]
[12]
[13]
[14]
[15] [16]
[17]
[18]
Condensation
[19]
Ellipse-traced method can be recommended for calculating the head circumference in term fetuses.
[20]
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Parameter Z Geburtshilfe Perinatol 1991;195(4):163–71 (PubMed PMID: 1950060). Gardosi J, Geirsson RT. Routine ultrasound is the method of choice for dating pregnancy. Br J Obstet Gynaecol 1998;105(9):933–6 (PubMed PMID: 9763041. Epub 1998/10/08.eng). Kurmanavicius J, Wright EM, Royston P, Zimmermann R, Huch R, Huch A, et al. Fetal ultrasound biometry: 2. Abdomen and femur length reference values. Br J Obstet Gynaecol 1999;106(2):136–43 (PubMed PMID: 10426679). Campbell S. An improved method of fetal cephalometry by ultrasound. J Obstet Gynaecol Br Commonwealth 1968;75(5):568–76 (PubMed PMID: 5754625. Epub 1968/05/01.eng). Bartram JL, Rigby AS, Baxter PS. The ‘‘Lasso-o’’ tape: stretchability and observer variability in head circumference measurement. Arch Dis Child 2005;90(8):820–1 (PubMed PMID: 16040879. Pubmed Central PMCID: 1720542). Group WHOMGRS. Reliability of anthropometric measurements in the WHO multicentre growth reference study. Acta Paediatr 2006;450(Suppl.):38–46 (PubMed PMID: 16817677). Hadlock FP, Harrist RB, Sharman RS, Deter RL, Park SK. Estimation of fetal weight with the use of head, body, and femur measurements—a prospective study. Am J Obstet Gynecol 1985;151(3):333–7 (PubMed PMID: 3881966). Siemer J, Egger N, Hart N, Meurer B, Muller A, Dathe O, et al. Fetal weight estimation by ultrasound: comparison of 11 different formulae and examiners with differing skill levels. Ultraschall Med 2008;29(2):159–64 (PubMed PMID: 17602369. Epub 2007/07/03.eng). Siemer J, Peter W, Zollver H, Hart N, Muller A, Meurer B, et al. How good is fetal weight estimation using volumetric methods? Ultraschall Med 2008;29(4):377–82 (PubMed PMID: 18484061. Epub 2008/05/17.eng). Siemer J, Wolf T, Hart N, Schrauder M, Meurer B, Goecker T, et al. Increased accuracy of fetal weight estimation with a gender-specific weight formula. Fetal Diagn Ther 2008;24(4):321–6 (PubMed PMID: 18836268. Epub 2008/10/ 07.eng). Pitman EJG. A note on normal correlation. Biometrika 1939;31:9–12. Snedecor GW, Cochran WG. Comparison of two correlated variances in paired samples. In: Statistical methods8th ed. Ames, IA: Iowa State University Press; 1989. p. 192–3. Bland JM, Altman DG. Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1986;1(8476):307–10 (PubMed PMID: 2868172). Dudley NJ, Chapman E. The importance of quality management in fetal measurement. Ultrasound Obstet Gynecol 2002;19(2):190–6 (PubMed PMID: 11876814. Epub 2002/03/06.eng). Melamed N, Yogev Y, Danon D, Mashiach R, Meizner I, Ben-Haroush A. Sonographic estimation of fetal head circumference: how accurate are we? Ultrasound Obstet Gynecol 2011;37(1):65–71 (PubMed PMID: 20661958. Epub 2010/07/28.eng). Wegrzyn P, Borowski D, Bomba-Opon D, Wielgos M. Accuracy of sonographic estimation of fetal head circumference. Ultrasound Obstet Gynecol: Off J Int Soc Ultrasound Obstet Gynecol 2011;37(6):743 (author reply-4. PubMed PMID: 21618316. Epub 2011/05/28.eng). Aspelund G, Fisher JC, Simpson LL, Stolar CJ. Prenatal lung-head ratio: threshold to predict outcome for congenital diaphragmatic hernia. J Matern-Fetal Neonatal Med: Off J Eur Assoc Perinat Med Fed Asia Oceania Perinat Soc Int Soc Perinat Obstet 2012;25(7):1011–6 (PubMed PMID: 21815746. Epub 2011/08/ 06.eng). Oral E, Cagdas A, Gezer A, Kaleli S, Aydinli K, Ocer F. Perinatal and maternal outcomes of fetal macrosomia. Eur J Obstet Gynecol Reprod Biol 2001;99(2):167–71 (PubMed PMID: 11788165. Epub 2002/01/15.eng). Larson A, Mandelbaum DE. Association of head circumference and shoulder dystocia 329 in macrosomic neonates. Mater Child Health J 2013;17(3):501–4 (PubMed PMID: 22492227, 330. Epub 2012/04/12.eng). Kehl S, Zaiss I, Freiburg F, Speierer A, Sutterlin M, Siemer J. Comparison of different sonographic methods to determine fetal abdominal circumference. Fetal Diagn Ther 2010;28(4):201–6 (PubMed PMID: 20881366. Epub 2010/10/ 01.eng).
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Contents lists available at ScienceDirect
European Journal of Obstetrics & Gynecology and Reproductive Biology journal homepage: www.elsevier.com/locate/ejogrb
Finding the most accurate method to measure head circumference for fetal weight estimation Ulrike Schmidt a, Dunja Temerinac a,b, Katharina Bildstein b, Benjamin Tuschy a, Jade Mayer a, Marc Su¨tterlin a,b, Jo¨rn Siemer c, Sven Kehl a,d,* a
Department of Obstetrics and Gynecology, University Medical Centre Mannheim, Heidelberg University, Mannheim, Germany Department of Obstetrics and Gynecology, Stadtklinik Frankenthal, Frankenthal, Germany c Department of Obstetrics and Gynecology, Klinikum Pforzheim, Pforzheim, Germany d Department of Obstetrics and Gynecology, Erlangen University Hospital, Erlangen, Germany b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 14 December 2013 Received in revised form 4 March 2014 Accepted 31 March 2014
Objective: Accurate measurement of fetal head biometry is important for fetal weight estimation (FWE) and is therefore an important prognostic parameter for neonatal morbidity and mortality and a valuable tool for determining the further obstetric management. Measurement of the head circumference (HC) in particular is employed in many commonly used weight equations. The aim of the present study was to find the most accurate method to measure head circumference for fetal weight estimation. Study design: This prospective study included 481 term pregnancies. Inclusion criteria were a singleton pregnancy and ultrasound examination with complete fetal biometric parameters within 3 days of delivery, and an absence of structural or chromosomal malformations. Different methods were used for ultrasound measurement of the HC (ellipse-traced, ellipse-calculated, and circle-calculated). As a reference method, HC was also determined using a measuring tape immediately after birth. FWE was carried out with Hadlock formulas, including either HC or biparietal diameter (BPD), and differences were compared using percentage error (PE), absolute percentage error (APE), limits of agreement (LOA), and cumulative distribution. Results: The ellipse-traced method showed the best results for FWE among all of the ultrasound methods assessed. It had the lowest median APE and the narrowest LOA. With regard to the cumulative distribution, it included the largest number of cases at a discrepancy level of 10%. The accuracy of BPD was similar to that of the ellipse-traced method when it was used instead of HC for weight estimation. Conclusion: Differences between the three techniques for calculating HC were small but significant. For clinical use, the ellipse-traced method should be recommended. However, when BPD is used instead of HC for FWE, the accuracy is similar to that of the ellipse-traced method. The BPD might therefore be a good alternative to head measurements in estimating fetal weight. ß 2014 Elsevier Ireland Ltd. All rights reserved.
Keywords: Head circumference Biparietal diameter Measurement Ultrasound Fetal weight estimation
Introduction Accurate fetal weight estimation (FWE) is an important prognostic parameter for neonatal morbidity and mortality and is a valuable tool for determining the further obstetric management [1]. Fetal biometry using ultrasound has therefore become part of
* Corresponding author at: Department of Obstetrics and Gynecology, University Medical Centre Mannheim, Heidelberg University, Theodor-Kutzer-Ufer 1-3, 68167 Mannheim, Germany. Tel.: +49 621 383 3447/+49 17660025334; fax: +49 621 383 5074. E-mail address: [email protected] (S. Kehl).
routine practice in obstetrics. Standard fetal biometry measurements – such as abdominal circumference (AC), femur length (FL), biparietal diameter (BPD), and head circumference (HC) – are used in many formulas. However, the accuracy of these formulas appears to be generally poor [2], and accurate head measurement of the fetus is essential [3]. There is general agreement on the sonographic plane at which HC and BPD should be measured: it is the transverse section at the level at which the continuous midline echo is broken by the cavity of the septum pellucidum in the anterior third [4]. However, ways of calculating the HC have not been standardized, and it can be done with different methods. The aims of the present study were to compare different methods of calculating head circumference and to determine the most accurate one for FWE.
http://dx.doi.org/10.1016/j.ejogrb.2014.03.047 0301-2115/ß 2014 Elsevier Ireland Ltd. All rights reserved.
Please cite this article in press as: Schmidt U, et al. Finding the most accurate method to measure head circumference for fetal weight estimation. Eur J Obstet Gynecol (2014), http://dx.doi.org/10.1016/j.ejogrb.2014.03.047
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Material and methods A prospective multicenter study was conducted between March and December 2011 at the Perinatal Center at the University Medical Centre Mannheim, Mannheim, Germany, the Department of Obstetrics and Gynecology, Stadtklinik Frankenthal, Frankenthal, Germany, and the Department of Obstetrics and Gynecology, Ludmillenstift Hospital, Meppen, Germany. Pregnant women with singleton pregnancies and a fetus in cephalic presentation at term (259 days of gestation) were recruited consecutively by the physicians in the labour. Oral informed consent was obtained. The ultrasound examination with complete biometric parameters – BPD, occipitofrontal diameter (OFD), HC, AC and FL – was carried by a total of seven different examiners. When onset of labour was excluded, the women left the hospital and measurement was repeated during the next admission, if the last assessment of fetal biometry was not undertaken within the last three days. Each fetus was included only once. Pregnancies with structural or chromosomal malformations, as well as intrauterine fetal deaths, were excluded. The gestational age was defined by the measurement of crown-rump length in the first trimester [5,6]. For all measurements, a Samsung Medison SonoAce R7 (Sonoace Ltd., Marl, Germany) was used with standard techniques [3,7]. Three different methods were used to calculate the sonographic HC. First (in the ellipse-calculated method), the BPD is measured at the largest distance from the outer edges of the skull at the level of the cavity of the septum pellucidum [8]. Measurements of the OFD are done in the same plane, between the outer edge of the frontal bone and the outer edge of the occiput. The following formula is used to estimate the HC from the measurements of the OFD and BPD: HC = p H [(BPD2 + OFD2)/2]. Kurmanavicius et al. have described this method (the ellipse-calculated method) in detail previously [3]. The second method (the ellipse-traced method) involves measuring the HC by placing an ellipse around the outer edge of the fetal skull. The ultrasound machine automatically determines the longest (DL) and shortest diameter (DS). The distances measured are then inserted into the above-mentioned formula for the ellipse-calculated method. In the third method (the circle-calculated method), the same BPD and OFD measurements from the ellipse-calculated method are used in a different equation for calculating the HC: p [(ATD + APAD)/2] [7]. As a reference value for the sonographic measurements, together with the birth weight, HC was also measured in the neonates within 1 hour after delivery. The measuring tape was placed along the maximum horizontal plane, along the occipital prominence at the back, above the ears, and directly above the eyebrows at the front. The postnatal HC measurement is very reliable, with extremely high correlation coefficients for both intraobserver (0.999) and interobserver (0.979) measurements [9,10]. Fetal weight estimation with the four different methods of HC calculation (ellipse-traced, ellipse-calculated, circle-calculated, and postpartal) was done using the Hadlock formula (HC, AC, FL) [11]. In previous studies, our group and others have shown that the Hadlock formulas are among the most accurate weight equations for term fetuses, and they have therefore been adopted as the clinical standards in our institutions [2,12–14]. In addition to HC, FWE was also determined with another Hadlock formula, using the BPD instead (BPD, AC, FL) [11]. In contrast to our BPD and HC measurements, the measuring track was set between the outer and the inner edge of the skull bone in the original publication of Hadlock. The accuracy of the estimated fetal weight (EFW) was assessed by calculating the percentage error (PE; (EFW BW)/BW 100)
and the absolute percentage error (APE; jEFW BWj/BW 100). The mean PEs for all the equations were compared with zero using the t-test at a significance level of 5% in order to assess whether any significant systematic bias had occurred. A variance test for the PE values was performed using the Pitman method [15,16]. At a significance level of 5% and with a sample size of more than 400, R values greater than 0.098 were significant. For APE values, differences between the various techniques were compared using Wilcoxon’s test at a significance level of 5%. The limits of agreement (LOA) method described by Bland and Altmann [17] was also used. The overall mean difference between the derived fetal weight and BW refers to the extent of systematic error, whereas the LOA refers to random error. The 95% LOA indicates what difference between the real BW and the EFW can be expected, and what tendency (to underestimate or to overestimate) is commonly found. Percentages of fetal weight estimations falling within discrepancy levels of 10% of the actual BW were also calculated for each technique. Differences between the postpartal measurements and the sonographic equations were compared using McNemar’s test. P values 0.05 were considered to be significant. The Statistical Package for the Social Sciences (SPSS), version 15.0.1 (2006; SPSS, Inc., Chicago, Illinois, USA) was used for statistical evaluation. Results A total of 458 women was included in this study. The median maternal age was 30, ranging from 18 to 46 years. The gestational age ranged from 37 weeks to 42 weeks, with a median gestational age of 39 weeks 5 days. The median gravidity was 2 (range from 1 to 8) and the parity including the delivery in this study 1 [1–7]. The period between ultrasound measurement and delivery was 1 day, ranging from 0 to 3. The median birth weight was 3380 g (2160– 4785). The postpartal HC measurements ranged from 312 mm to 402 mm, with a median of 350 mm. There were 13 newborns with a birth weight below 2500 g and 28 with 4000 g or more. The results of the different ultrasound measurements for HC and BPD are shown in Table 1. When the Hadlock formulas were used to estimate fetal weight, all of the methods for the HC significantly underestimated fetal weight. It was only when the BPD was used that no systematic error was found in the PE (Table 2). As an indicator of random error, the SD of the reference method (postpartal HC) was compared with all of the other methods; the variance test only showed a significant difference with the BPD formula in this case (Table 2). The APEs are shown as median values and ranges in Table 2. The lowest median APE was found for the ellipse-traced method. In comparison with the reference method, only the circle-calculated measurements were significantly larger. Table 3 illustrates the limits of agreement between the fetal weight estimates and true birth weight. FWE calculated with the postpartal HC measurements demonstrated the narrowest LOA. The BPD method showed the smallest tendency to either overestimate or underestimate fetal weight. Table 1 Head circumferences, either calculated using the three different ultrasound methods or measured after birth, and sonographic biparietal diameter of the head (BPD) (in mm). Median (range) BPD Ellipse-traced Ellipse-calculated Circle-calculated Postpartal
95.1 338.0 329.9 328.5 350.0
(81.5 to 113.1) (288.7 to 394.4) (290.9 to 386.5) (290.6 to 384.1) (312.0 to 402.0)
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Table 2 Mean values for percentage error (PE) in fetal weight estimation with Hadlock formulas, using different methods to measure head circumference (HC) or using the biparietal parameter (BPD), were compared to zero using the t-test. P values 0.05 were considered significant. Correlated variance tests of the PE between the postpartal measurement (reference method) and the ultrasound methods were performed using the Pitman method. R values >0.098 were considered significant. Absolute percentage errors (APE) were also compared between the neonatal HC and the ultrasound measurements using Wilcoxon’s test. P values 0.05 were considered significant. PE Mean (SD) BPD Ellipse-traced Ellipse-calculated Circle-calculated Postpartal
0.41 1.87 3.56 3.91 1.05
(9.52) (9.17) (9.24) (9.16) (9.19)
APE
Mean P value
Variance R value
Median (range)
P value
0.356 0.001 0.001 0.001 0.015
0.105 0.003 0.016 0.009 –
6.60 6.49 7.05 7.11 6.91
0.340 0.601 0.011 0.008 –
(0.00–32.57) (0.01–27.40) (0.01–27.82) (0.05–27.40) (0.02–28.41)
SD, standard deviation.
With regard to postpartal HC measurements, 74.2% of the fetal weight estimates fell within 10% of the actual weight at birth (Table 4). This was significantly higher than when the ellipsecalculated or circle-calculated methods were used. No significant differences were observed between the ellipse-traced method (73.4%) and the BPD formula (71.4%).
Comments Fetal head measurements provide indispensable data for weight estimation with the majority of the weight equations commonly used [12,18]. The present study compared three different ultrasound methods for calculating the fetal HC. The results were compared with postpartal HC measurements and with a weight formula including BPD instead of HC. The results of the study show that the ellipse-traced method is preferable for FWE. The ellipse-traced method had the lowest median APE of all the methods investigated and included the largest number of cases at a discrepancy level of 10% among the ultrasound methods. When the BPD was used instead of HC, the accuracy of FWE was similar to that of the ellipse-traced method. BPD might therefore be an appropriate alternative, especially in cases in which the HC is difficult to measure due to poor ultrasound conditions. Since there were fetuses in breech position included – a dolichocephalic head shape might influence the BPD – this has to be confirmed in further investigations. In a study by Melamed et al. [19], ultrasound estimates of fetal HC were compared with measurements taken postnatally with a measuring tape. The ultrasound HC was measured as an ellipse around the perimeter of the fetal skull, within 3 days before delivery. A total of 3008 pregnancies were examined. The study showed significant underestimation with ultrasound HC measurements in comparison with the postnatally measured HC. The type of fetal presentation did not affect the ultrasound measurement error, but the difference increased with gestational age. Male sex and delivery by vacuum extraction had an influence on reduced ultrasound accuracy. In a published letter, Wegrzyn et al. [20] noted that the influence of gestational age may be due to larger babies, as a result of increased subcutaneous tissue. The error also depended on the mode of delivery; it was smallest for cesarean Table 3 Limits of agreement between fetal weight estimated using the Hadlock formula (HC, AC, FL or BPD, AC, FL) and birth weight (in g) in the study group (n = 458). Head measurement Biparietal diameter Ellipse-traced Ellipse-calculated Circle-calculated Postpartal
Mean (SD) 2 74 131 143 26
(316) (308) (311) (309) (307)
95% limits of agreement 617 678 741 749 576
to to to to to
621 530 479 463 628
sections and increased for vaginal deliveries and vacuum extractions. Wegrzyn based these findings on the influence of subcutaneous tissue edema on neonatal HC. However, FWE was not one of the objectives in their study. Fetal sex and mode of delivery were not taken into account in the present study, and it may be assumed that these did not make any difference in relation to the issue currently being investigated. Head circumference also plays an important role in other areas apart from fetal weight estimation. In cases of congenital diaphragmatic hernia, the lung-to-head ratio (LHR) is an important prognostic parameter for neonatal outcome [21] and accurate HC measurement is therefore essential in these fetuses. Fetal growth restriction is another issue in which accurate HC measurement is needed. Campbell et al. described the impact of the fetal head-toabdomen ratio on the assessment of fetal growth restriction and demonstrated that the HC–AC ratio is an important tool for distinguishing between symmetrical and asymmetrical growth restriction [4]. To what extent the results of this study can be transferred in these situations is unclear since these examinations are undertaken in earlier weeks of gestation. Detecting macrosomic fetuses is an important obstetric issue in relation to increased perinatal morbidity. The neonatal records for newborns with a BW of at least 4000 g were reviewed in a study by Oral et al. [22]. In comparison with the control group, the macrosomic infants were at increased risk for birth trauma and asphyxia. These data once again demonstrate the importance of accurate weight estimation. In a recent study, Larson et al. [23] investigated the association between HC and shoulder dystocia. The results showed that infants with a smaller mean HC were more likely to suffer from shoulder dystocia than infants of similar size who did not have asymmetric macrosomia. In macrosomic fetuses, AC is increased and this influences fetal weight estimation in the first place. Ellipse-traced measurement of fetal AC also seems to be method of choice [24]. The present study only identified small differences between the methods evaluated. However, since all of the methods are likely to be equally time-consuming, the ellipse-traced technique can still be recommended. Table 4 Percentages (%) of fetal weight estimates falling within a discrepancy level of 10% of the actual birth weight using either three different sonographic methods to calculate the head circumference (HC), or the biparietal parameter (BPD). Postpartal HC measurements were compared with the ultrasound methods using McNemar’s test. P values 0.05 were considered significant. Head measurement
BPD Ellipse-traced Ellipse-calculated Circle-calculated Postpartal
10% %
P value
71.4 73.4 67.5 66.8 74.2
0.143 0.754 0.005 0.003 –
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Postpartal HC measurement was used as a reference method in this study. It provided the highest level of accuracy for FWE in comparison with the ultrasound methods. It can therefore be assumed that there are still difficulties with regard to accuracy in measuring and calculating the real HC. Especially in the late weeks of gestation, fetal head measurement on ultrasound can be difficult, as there is less amniotic fluid and poorer demarcation from other tissues. Another problem may be that the fetal head lies deep in the pelvic inlet, making it difficult to replicate the correct ultrasound plane. The results of this study are only applicable in mature fetuses, and differences between the HC calculations may not be apparent in preterm fetuses. Conclusion Measurement of the head circumference is an important parameter for fetal weight estimation. On the basis of this study’s results, use of the ellipse-traced method can be recommended for calculating the head circumference in term fetuses. Its superiority is based on the fact that at term pregnancy it is very difficult to demarcate endpoints where to put calipers for measurement, as outer borders of frontal and occipital bones are very poorly defined due to the shadow from the bones of the cranial vault that are proximal to the transducer. Ellipse-traced method helps to measure head circumference as it assumes ellipsoidal shape of the skull at this cross-section. However, when the biparietal diameter is used instead of head circumference for weight estimation, the accuracy is similar to that with the ellipse-traced method. The BPD may therefore be a good alternative for head measurements in fetal weight estimation.
[6]
[7]
[8]
[9]
[10]
[11]
[12]
[13]
[14]
[15] [16]
[17]
[18]
Condensation
[19]
Ellipse-traced method can be recommended for calculating the head circumference in term fetuses.
[20]
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