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Volume 99(5), April 1997, pp 1237-1247

A CT Scan Technique for Quantitative Volumetric Assessment of the Mandible after Distraction Osteogenesis [Articles] Roth, Douglas A. M.D.; Gosain, Arun K. M.D.; McCarthy, Joseph G. M.D.; Stracher, Michael A. M.D.; Lefton, Daniel R. M.D.; Grayson, Barry H. M.D. New York and Brooklyn, N.Y., and Milwaukee, Wisc. From the Institute of Reconstructive Plastic Surgery and the Neuroradiology Division of the Department of Radiology at the New York University School of Medicine, the Department of Plastic and Reconstructive Surgery at the Medical College of Wisconsin, and the SUNY Downstate Medical Center. Institute of Reconstructive Plastic Surgery; New York University Medical Center; 560 First Avenue; New York, N.Y. 10016 Received for publication January 19, 1996; revised April 17, 1996. Presented in part at the 64th Annual Scientific Meeting of the American Society of Plastic and Reconstructive Surgeons, in Montreal, Canada, on October 9, 1995.

Abstract Distraction osteogenesis has become an accepted method of treatment for patients requiring reconstruction of hypoplastic mandibles. We present a quantitative analysis of volumetric changes after distraction osteogenesis in a series of 10 patients. Group I (n = 5 patients, 3 unilateral craniofacial microsomia, 1 Goldenhaar syndrome, and 1 bilateral craniofacial microsomia) underwent unilateral distraction of the mandible. Group II (n = 5 patients, 1 Nager syndrome, 1 bilateral craniofacial [Illegible Text] 1 developmental micrognathia, and 2 Treacher [Illegible Text] syndrome) underwent bilateral distraction of the mandible. Predistraction and postdistraction axial and three-dimensional computed tomographic (CT) scans were digitized and transferred to a computer for analysis with image-processing software to determine the changes in volume of the mandible and bony regenerate. The CT-derived volume method was validated by scanning three dry cadaver mandible specimens and comparing the volume data with those derived from a waterdisplacement method. The difference between the two methods was less than 5 percent. The mean distracted length, as recorded from the calibrated device, was 22.6 mm in the 10 patients. In the unilateral distraction group, the mean increase in hemimandibular bone volume was 2.8 cc, with a mean percentage increase of 27 percent in the distracted hemimandible. In the bilaterally distracted patients, the mean increase in total mandibular volume was 7.9 cc, with a mean percentage increase in bone volume of 25 percent. This study represents the first attempt to quantify the increase in bone volume resulting from distraction osteogenesis. Quantitative volumetric analysis of CT scans is an accurate method to measure the amount of bone regenerate in patients undergoing distraction osteogenesis of the mandible or the extremities. The concept and utility of quantifying the volumetric changes in bone following distraction osteogenesis may become more important as multiplanar devices are developed and used in other areas of the craniofacial skeleton.

Craniofacial abnormalities such as unilateral craniofacial microsomia, developmental micrognathia, and Treacher Collins syndrome include both unilateral and bilateral mandibular

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deficiencies. These patients traditionally have undergone complex surgical reconstructions involving soft- and hard-tissue transfers. Bone lengthening or distraction osteogenesis, as originally reported by Codivilla 1 and further refined by Ilizarov 2 for the correction of deformities in the extremities, was applied successfully to the canine mandible by several groups.3-5 Following our laboratory studies, distraction osteogenesis was used successfully for gradual lengthening of the human mandible.6 The benefits of using distraction osteogenesis for length discrepancies in the upper and lower extremities have been well documented.7 Recent studies have reported the qualitative improvement in facial symmetry and appearance,6 as well as the correction of airway obstruction 8;

however, a review of the literature reveals that there has been no quantitative assessment of

the bony regenerate formed by distraction osteogenesis. Several authors have used computed tomographic (CT) scans of the craniofacial skeleton with and without image-analysis software programs to determine intraorbital and intracranial volumes.9-12 This method of CT-derived volume determination also has been used to quantify changes after cranial vault remodeling in patients with various craniosynostoses.13-18 The purpose of this study was to determine if the CT-derived volume method was applicable and accurate for determining mandibular volume and, if so, to quantify the changes in bone volume following distraction osteogenesis of the human mandible.

Materials and Methods In order to validate the accuracy of the CT-derived volume determination technique, several human and canine cadaver mandible specimens were subjected to CT scanning with the identical protocol as pediatric craniofacial patients. The cadaver specimens underwent standard craniofacial CT scans consisting of 3-mm axial cuts. The same specimens were taken to the laboratory for volume determination by a water-displacement technique. The technique for measuring the volume of the cadaver mandibles by water displacement was as follows: (1) The dry mandibles were first weighed (Mettler Balance Company). (2) Then they were covered with a thin layer of heated paraffin wax to occlude all porous surfaces and reweighed. The difference in weight corresponded to the amount of paraffin wax added. With the known density of this paraffin (Tissue Processing Medium Type 9, Stephen Scientific Company, Riverdale, N.J.), the added volume of paraffin was determined. (3) The paraffin-covered mandibles were placed in graduated cylinders to determine volume by measuring water displacement. (4) The volume of the mandible specimen itself was determined by subtracting the volume of the extra paraffin wax from the volume of the paraffin-covered mandible. This water-displacement volume method was repeated three times for each specimen. The volume study of distracted mandibles consisted of 10 patients divided into two equal groups (group I: unilateral; group II: bilateral) who had undergone distraction osteogenesis of the mandible to correct severe deficiencies in size and shape. Following distraction osteogenesis, the mandible was left in fixation with the external device for an average of 8 weeks to allow complete ossification. Each patient was evaluated before and after distraction of the mandible with standardized medical-quality photographs, conventional anteroposterior and lateral cephalograms, and dental casts. Each patient also was evaluated with a GE 9800 computed tomographic scanner (GE Medical Systems, 3000 North Granview, Waukesha, Wisc.). Preoperative and postdistraction CT scans were obtained to define the deformity, determine feasibility of surgery, plan the site of osteotomy, evaluate the outcome of treatment, and help plan any secondary treatment, if

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necessary. Nine patients were scanned an average of 28 days after removal of the distraction apparatus, and 1 patient was scanned 26 months after removal. All CT scans were obtained through a standard protocol consisting of[Illegible Text] contiguous axial images taken from the hyoid bone to the cranial vertex with the patient in a supine position. In the typical scan, the mandible consisted of 22 to 25 slices from menton to condyle. The CT scanner was set up with a 15-cm-diameter scan circle with a 512 × 512 pixel reconstruction matrix yielding a voxel size (volume element) of 0.27 mm3. Three-dimensional surface reconstructions from the CT scans were used for preoperative planning and for qualitative assessment of the mandibular distraction results. For CT-derived volume determination, hard copies of the CT scans (bone windows only) were digitized at 1024 × 1024 pixels to 8 bits of gray scale with a Lumisys laser film digitizer (Advanced Video Products, Westford, Mass.) and transferred to a Macintosh Centris 610 computer (Apple Computer Corporation, Cupertino, Calif.). Each slice was analyzed by means of image-analysis software.19 The level and window of each slice were set optimally by the computer in a standard fashion on all studies to allow precise delineation between bony cortex and soft tissue. An optimal threshold for the bone-soft-tissue interface was determined and set for consistent use throughout each study Under direction of the operator, the program automatically outlined the bony contours of the mandible on the basis of this threshold.20 Figure 1

illustrates the technique of outlining the specific contours of the mandible in different

axial cuts. The area within the contour can be determined precisely by calibrating the imageanalysis program with the 5-cm scale reproduced on every hard-copy axial image. For the five unilateral distraction patients in group I, the mandible was divided by means of two landmarks: On the digitized CT scans, a line was constructed between the central incisors and the genial tubercle on the alveolar surface (Fig. 2). Mandibular volume was computed by first applying Green's theorem to each contour on serial contiguous slices to obtain area(cm2) within the contour, then muliplying by the slice width (0.3 cm) to obtain the volume contribution of each slice, and finally, summing over all slices pertaining to the mandible for mandibular bone volume:Equation

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Fig. 1. Outlining the contour of the mandible on serial axial slices progressing in a cephalad direction along the rami of the mandible. Note in the upper left scout panel the 22 to 25 slices through the mandible.

Fig. 2. For unilateral patients, the mandible was divided by a line drawn between the incisors and the genial tubercle.

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Equation 1A

Results The results of both the CT-derived and water-displacement volumes for the cadaver mandible specimens are summarized in Table I. The difference between the two methods was less than 5 percent.

TABLE I Correlation of Water-Displacement Volume and CT-Derived Volume of Cadaver Mandibles

The characteristics of the 10 patients in the study are summarized in Table II. The results of the CT-derived volume determinations for group I patients are summarized in Table III. The average increase in hemimandibular volume was 2.8 cc, with an average increase in percentage volume of 27 percent. Figure 3 illustrates an example from group I with the three-dimensional reconstructions showing the improvement in the shape and volume of the left mandibular ramus.

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TABLE II Clinical Characteristics of Group I and Group II Patients

TABLE III Results of CT-Derived Volume Measurements for Group I Unilateral Distraction Patients

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Fig. 3. Predistraction and postdistraction three-dimensional CT scan reconstructions for patient 2 in group I. This 30-month-old girl with left-sided craniofacial microsomia underwent 30 mm of mandibular distraction on the left side. The increase in bone volume was 20.5 percent. Note the pin holes from the distraction device in the left side of the mandible in the postdistraction CT. Note the increase in the vertical dimension of the affected ramus and the increased projection of the pogonion.

The results of the volume analyses for group II are summarized in Table IV. The average increase in total mandibular bone volume was 7.9 cc, with an average percentage increase of 25 percent from the predistraction bone volume. Figures 4 and 5 represent examples of bilateral mandibular distraction illustrating the improvements in ramus height and pogonion projection along with the mandibular volume determinations.

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TABLE IV Results of CT-Derived Volume for Group II Bilateral Distraction Osteogenesis Patients

Fig. 4. Predistraction and postdistraction three-dimensional CT scan reconstructions for patient 8

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in group II. This 3-year-old boy with developmental micrognathia underwent bilateral distraction osteogenesis (29 mm on right, 28 mm on left). The increase in bone volume was 30 percent. Note the increase in vertical height of the rami and the counterclockwise rotation of the mandible (right profile views).

Fig. 5. Predistraction and postdistraction three-dimensional CT scan reconstructions for patient 10 in group II. This 3-year-old boy with Nager syndrome underwent 21 mm of distraction osteogenesis bilaterally. The increase in bone volume was 32.4 percent. Note the increase in projection of the pogonion and the body of the mandible with less increase in vertical height of the ramus (see Fig. 4). The anterior occlusal relationships are significantly improved.

To determine the average increase in mandibular volume per increment of linear distraction (from the distraction device), the unilateral and bilateral distraction patients were combined. The 5 bilateral patients were analyzed as having 10 unilaterally distracted mandibles and were grouped with the 5 unilateral patients to give a total of 15 distracted hemimandibles. The volume

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of a hemimandible was determined as described under Materials and Methods. The mean predistraction hemimandibular volume was 14.7 ± 4.9 cc, and the mean postdistraction hemimandibular volume was 18.3 ± 5.6 cc. The increase in mandibular volume following distraction was statistically significant according to Student's paired t test(p < 0.001). The average increase in mandibular volume per increment of linear distraction was 0.16 cc/mm (n = 15), and the average percent increase in mandibular volume was 1.15 percent/mm of distraction (Table V).

TABLE V Results of Mandibular Volume for Group I (Unilateral) and Group II(Bilateral) Considered as Hemimandibles for Determining Volume Increase per Millimeter of Distraction

Discussion CT scans have been used for quantitative volume measurements of the cranial vault by several authors.9-17,21 In addition, these techniques have been validated previously by comparison with water displacement by many of the same investigators.14,15,22 Posnick et al.16 termed the CT-derived volume measurements of intracranial volume indirect volume measurements and compared them with direct (water-displacement) volume measurements; they found an average difference of 3.7 percent in a validation study consisting of five cadaver skulls. We performed a validation study of the mandibular volume method and found an average difference of 4.2 percent when compared with water displacement. Volumetric determinations in craniofacial surgery have been employed previously to estimate intracranial and intraorbital volumes. In 1955, Mackinnon 23 made direct measurement of intracranial volume in 52 dry adult skulls by [Illegible Text] the skulls with lead shot. Although there was a relationship between the measured volume of the dry skulls and their glabellaopisthocranion lengths, estimation of intracranial volume by the single dry skull measurement produced an error of up to 17 percent with respect to the measured dry skull volume. In 1956, Mackinnon et al.24 determined a formula for the optimal estimate of cranial capacity based on a series of linear measurements recorded from anteroposterior and lateral skull radiographs. This formula was accurate to within 6.2 percent of the measured intracranial volume. Based on this

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calculation, numerous authors have made clinical measurements of intracranial volume in normal pediatric populations.25-31 Radiographically derived measurements of intracranial volume have been made in French, British, American, East Indian, and West Indian children. Of these studies, only Lichtenberg's 25 data provide statistics on the mean and standard deviation of the intracranial volume in children grouped by age and sex. For this reason, statistical analyses of intracranial volume in pediatric populations have relied on Lichtenberg's normative data.9,13,15 Comparisons of the various studies of intracranial volume in normal pediatric populations show considerable variability from one study to another. The variation in the results and volumetric data also may be due to differences in radiographic technique and the resulting error in the measurements used to calculate intracranial volume, which are derived from plain roentgenograms. This error could have been avoided had a ruler been placed on the patient, allowing measurements from radiographs to be converted to real measurements.24 Another shortcoming of roentgenographic techniques for determinations of intracranial volume is their reliance on skull symmetry. Because of cranial vault asymmetry, these techniques are not valid in determining intracranial volume in the craniofacial synostoses.29 CT-derived volumetric calculations are therefore necessary in patients with skull asymmetry due to cranial synostosis.15 CT-derived soft-tissue volumes were first determined by Koehler et al.32 The technique was further refined by Brieman et al.33 in calculating organ volumes in cadaver specimens to within 5 percent of the volume measured by water-displacement techniques. Keller et al.20 described a technique for automatic outlining of regions of the CT scan based on CT density. Bite et al.10 utilized a technique of automatic outlining of regions from CT scans using a software package in order to estimate orbital volumes in patients with enophthalmos. In this method, 1.5-mm orbital slices were obtained, and intraorbital volume was determined by counting the number of voxels, or measures of a unit of volume, on each slice. However, it was difficult to determine the accuracy of the method, since the paper on the methodology of their technique was unpublished at the time of their report. In addition, there has been technical difficulty in automated outlining of the ventral surface of the orbit, especially toward the orbital rim.11 Manson et al.34 avoided these shortcomings by calculating intraorbital volume in enophthalmos from hand-traced images obtained from thin CT slices. The intraorbital volumes estimated from CT scans were correlated with volumes determined from direct measurement. By analyzing intraorbital volume of both bone and soft-tissue structures in enophthalmos, the preceding studies concluded that an increase in the bony intraorbital volume is the major component of posttraumatic enophthalmos. Dufresne et al.14 used a software package for automatic contour tracing to determine intracranial volume and intraventricular volume following cranial vault remodeling. While an accurate assessment of the relative change in volume following cranial vault remodeling could be obtained in this study, the absolute volumes were not correlated with real skull volumes. Gooskens et al.35 used a hand-tracing technique to determine intracranial volume in 60 children. While they attempted to provide a CT-derived database for intracranial volume in children, the weaknesses of the study included a lack of correlation between obtained volumes and actual skull volumes and an inconsistent technique in obtaining the CT scans among different patients. Gault et al.9,13 traced the intracranial area by hand from actual CT scan slices to determine intracranial volume with accurate correlation with measured dry skull volumes. Posnick et al.16 showed that automated contour tracing with a software package also had satisfactory correlation with dry skull volumes. A recent study in our laboratory has shown that in normal skulls without significant asymmetry, there is an accurate correlation among the CT-derived volume, the roentgenographically derived volume, and the measured skull volume at autopsy.15

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Having established the reliability of CT-derived volumetric techniques in craniofacial surgery, we believed that these techniques could be applied to studies of mandibular distraction in order to quantitatively assess the resulting change in bone volume. Using a software package 19 for automated contour tracing from CT scans of the mandible, we again found accurate correlation between the indirect volume measurement and the actual volume as measured by a waterdisplacement technique. Prior to this study there has been no documentation of the volume of new bone created by the distracted bony regenerate. One of the problems with the study was obtaining craniofacial CT scans immediately prior to and following distraction osteogenesis. Patient 1 of the unilateral distraction group underwent predistraction CT scanning 24 months prior to the distraction procedure; the postdistraction CT scan was obtained 30 days after the removal of the device. A similar problem occurred with patient 9 in the bilateral group. For this patient, the predistraction CT scan was performed 12 months before distraction osteogenesis, whereas the postdistraction CT scan was performed 35 days after removal of the device. The relatively long interval between CT scans in these two patients brings in a potentially large contribution from normal growth of the mandible in the determination of the increase in mandibular bone volume resulting from distraction osteogenesis. In both groups of patients the increases in total and hemimandibular bone volume following distraction osteogenesis do not take into consideration the possible contribution from normal growth of the mandible that occurred in the time interval between CT scans. Volume change on the unaffected side of the unilateral distraction patients (see Table III) is the best index of growth in the absence of distraction, since there are no standards for mandibular growth in syndromic patients. The changes in bone volume on the unaffected side are markedly less than on the distracted side of the mandible. While no such control side is present in the bilateral distraction patients, in four of these patients the interval between predistraction and postdistraction CT scans was 8 months or less and therefore not of long enough duration for significant growth to have occurred. The only bilateral distraction patient in whom there was a longer interval between predistrction and postdistraction CT scans was in a female with Treacher Collins syndrome (case 9) who was 12 years and 9 months of age at the time of the initial CT scan and 14 years and 3 months of age at the time of the final CT scan. The measured change in volume during this period in the left hemimandible was 2.6 cc, or 17 percent of the initial volume, and in the right hemimandible was 1.9 cc, or 14 percent of the initial volume. The best reference data available for mandibular size in normal females between the ages of 12 and 14 years are the Michigan Moyer Standards,36 which provide normative cephalometric values at yearly intervals. By these standards, one can extrapolate a mean linear growth of the hemimandible (articulare to gonion plus gonion to pogonion) in normal controls to be 3.5 mm, or an increase of 2.8 percent from its initial dimensions. The only available data that attempt to correlate change in mandibular length with change in mandibular volume are those of the present study, in which mandibular distraction produced a mean increase in mandibular volume of 0.16 cc/mm of distraction, or an increase of 1.1 percent of initial mandibular volume per millimeter of distraction. Were this to apply to mandibular growth as well, the expected increase due to growth of the hemimandible in a normal female would be 0.56 cc (3.5 mm × 0.16 cc). These estimates of growth in a normal mandible are considerably less than the change in mandibular volume observed in the study patient. However, these comparisons must be qualified, since we have no data by which to estimate the expected change in mandibular volume due to growth alone in a female with Treacher Collins syndrome. For the unilateral distraction patients, the mandible was divided on the axial CT scan slices by

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a line drawn through the middle of the central incisors and through the genial tubercle on the alveolar surface of the mandible. By dividing the mandible in this fashion, the entire hemimandible on the affected side was analyzed for volume change following distraction. A potential problem with dividing the mandible as described is that there is still a portion of the body of the mandible that was not distracted that is included in the bone volume determination. However, to study the mandibular ramus alone in order to focus specifically on the distraction zone would have required an arbitrary point of division of the mandible approximately where the ramus meets the body and would not have been consistent from one CT scan to another or from one patient to another. In the future, the CT-derived method of bone volume determination may be more important for quantitative assessment as multiplanar distraction devices are developed and applied to other areas of the craniofacial skeleton such as the cranium and orbits. In addition, this indirect volume method can be used with magnetic resonance imaging (MRI) scans to eliminate the risks of radiation exposure. The CT-derived volume method also could be used as a research tool for analyzing collections of MRI or CT scans derived from young trauma and neurosurgery patients for volume determinations of the normal growth of the mandible and the cranium. Joseph G. McCarthy, M.D. Institute of Reconstructive Plastic Surgery; New York University Medical Center; 560 First Avenue; New York, N.Y. 10016

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11. Vannier, M. W., and Marsh, J. A. Orbital volume measurements in enophthalmos using threedimensional CT imaging (Discussion).Plast. Reconstr. Surg. 75: 508, 1985. [Context Link] 12. Geist, C. E., Stracher, M. A., and Grove, A. S. Orbital augmentation by hydroxyapatite-based composites: A rabbit study and comparative analysis. Ophthalmic Plast. Reconstr. Surg. 7: 8, 1991. [Context Link]

13. Gault, D. T., Renier, D., Marchac, D., et al. Intracranial volume in patients with craniosynostosis. J. Craniofac. Surg. 1: 1, 1990. [Context Link] 14. Dufresne, C. R., McCarthy, J. G., Cutting, C. B., et al. Volumetric quantification of intracranial and ventricular volume following cranial vault remodeling: A preliminary report. Plast. Reconstr. Surg. 79: 24, 1987. [Context Link] 15. Gosain, A. K., McCarthy, J. G., Glatt, P., et al. A study of intracranial volume in Apert syndrome. Plast. Reconstr. Surg. 95: 284, 1995. [Context Link] 16. Posnick, J. C., Bite, U., Nakano, P., et al. Indirect intracranial volume measurements using CT scans: Clinical applications for craniosynostosis. Plast. Reconstr. Surg. 89: 34, 1992. [Context Link] 17. Posnick, J. C., Armstrong, D., and Bite, U. Metopic and sagittal synostosis: Intracranial volume measurements prior to and after cranio-orbital reshaping in childhood. Plast. Reconstr. Surg. 96: 299, 1995. Bibliographic Links Library Holdings [Context Link] 18. Posnick, J. C., Armstrong, D., and Bite, U. Crouzon and Apert syndromes: Intracranial volume measurements before and after cranio-orbital reshaping in childhood. Plast. Reconstr. Surg. 96: 539, 1995. Bibliographic Links Library Holdings [Context Link] 19. NIH Image 1.54 is a public-domain program written by Wayne Rasband at NIH, Research Services Branch, National Institute of Mental Health, Bethesda, Md. [Context Link] 20. Keller, J. M., Edwards, F. M., and Rundle, R. Automatic outlining on regions of CT scans. J. Comput. Assist. Tomogr. 5: 240, 1981. Bibliographic Links Library Holdings [Context Link] 21. Spinelli, H. M., Irizarry, D., McCarthy, J. G., et al. An analysis of extradural dead space after frontoorbital surgery.Plast. Reconstr. Surg. 93: 1372, 1994. [Context Link] 22. Disler, D. G., Marr, D. S., and Rosenthal, D. I. Accuracy of volume measurements of computed tomography and magnetic resonance imaging phantoms by three-dimensional reconstruction and preliminary clinical applications. Invest. Radiol. 29: 739, 1994. Bibliographic Links Library Holdings [Context Link]

23. Mackinnon, I. L. The relation of the capacity of the human skull to its roentgenological length. A.J.R. 74: 1026, 1955. [Context Link] 24. Mackinnon, I. L., Kennedy, J. A., and Davies, T. V. The estimation of skull capacity from roentgenological measurements.A.J.R. 76: 303, 1956. [Context Link] 25. Lichtenberg, R. Radiographie du crane de 226 enfants normaux de la naissance a 8 ans: Impressions digitiformes, capacite, angles et indices. Thesis, University of Paris, 1960. [Context Link] 26. Gordon, I. R. S. Measurement of cranial capacity in children. Br. J. Radiol. 39: 377, 1966. [Context Link] 27. Bray, P. F., Shields, W. D., Wolcott, G. J., and Madsen, J. A. Occipitofrontal head circumference: An accurate measure of intracranial volume. J. Pediatr. 75: 303, 1969. Bibliographic Links Library Holdings [Context Link]

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