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Metopic synostosis: Measuring intracranial volume change following fronto-orbital advancement using three-dimensional photogrammetry
Journal of Cranio-Maxillo-Facial Surgery 43 (2015) 593e598
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Metopic synostosis: Measuring intracranial volume change following fronto-orbital advancement using three-dimensional photogrammetry €chli b, Elek Somlo a, Christian Freudlsperger a, *, Sahra Steinmacher a, Heidi Ba a a Jürgen Hoffmann , Michael Engel a b
Department of Oral and Maxillofacial Surgery, University Hospital Heidelberg, Heidelberg, Germany Department of Neurosurgery, University Hospital Heidelberg, Heidelberg, Germany
a r t i c l e i n f o
a b s t r a c t
Article history: Paper received 3 September 2014 Accepted 25 February 2015 Available online 12 March 2015
There is still disagreement regarding the intracranial volumes of patients with metopic synostosis compared with healthy patients. This study aimed to compare the intracranial volume of children with metopic synostosis before and after surgery to an age- and sex-matched control cohort using threedimensional (3D) photogrammetry. Eighteen boys with metopic synostosis were operated on using standardized fronto-orbital advancement. Frontal, posterior and total intracranial volumes were measured exactly 1 day preoperatively and 10 days post-operatively, using 3D photogrammetry. To establish an age- and sexmatched control group, the 3D photogrammetric data of 634 healthy boys between the ages of 3 and 13 months were analyzed. Mean age at surgery was 9 months (SD 1.7). Prior to surgery, boys with metopic synostosis showed significantly reduced frontal and total intracranial volumes compared with the reference group, but similar posterior volumes. After surgery, frontal and total intracranial volumes did not differ statistically from the control group. As children with metopic synostosis showed significantly smaller frontal and total intracranial volumes compared with an age- and sex-matched control group, corrective surgery should aim to achieve volume expansion. Furthermore, 3D photogrammetry provides a valuable alternative to CT scans in the measurement of intracranial volume in children with metopic synostosis, which significantly reduces the amount of radiation exposure to the growing brain. © 2015 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved.
Keywords: 3D photogrammetry Fronto-orbital advancement Intracranial volume Metopic synostosis
1. Introduction Premature fusion of the metopic suture results in trigonocephaly, which occurs with a frequency of one case per 15,000 live births and appears either as an isolated event or as one of multiple fused sutures, usually under syndromic conditions (van der Meulen, 2012).
* Corresponding author. Department of Oral and Maxillofacial Surgery, University Hospital Heidelberg, Im Neuenheimer Feld 400, 69120 Heidelberg, Germany. Tel.: þ49 6221 5638462; fax: þ49 6221 564222. E-mail address: [email protected] (C. Freudlsperger).
The metopic suture is the first suture that closes physiologically between the 3rd and 8th month (Vu et al., 2001). However, the morphology of a prematurely fused metopic suture differs from a physiologically closed suture, not only by an obvious metopic ridge over the midline, but also by a lateral growth restriction of the frontal bones (Weinzweig et al., 2003). This growth restriction combined with an increased compensatory growth of the unaffected skull sutures leads to the pathognomonic head shape of trigonocephaly which is characterized by a frontal midline ridge, a keel shaped forehead, hypotelorism with epicanthus, and temporal narrowing with an associated abnormality of the supraorbital rim and increased interparietal width (Engel et al., 2011; van der Meulen, 2012).
http://dx.doi.org/10.1016/j.jcms.2015.02.017 1010-5182/© 2015 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved.
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Interestingly, a significant rise of metopic synostosis has been observed in recent decades, however the reason for this increase remains unclear (van der Meulen et al., 2009). Several authors have indicated an association between metopic craniosynostosis and an increased risk of speech and language difficulties, or other cognitive or behavioral deficits, although a causal relationship remains uncertain (Kapp-Simon et al., 1993; Speltz et al., 2004; Starr et al., 2012). Surgical treatment of metopic craniosynostosis includes remodeling of the forehead and advancement (Aryan et al., 2005; Di Rocco et al., 2013; Engel et al., 2011; Keshavarzi et al., 2009). At our department we prefer fronto-orbital advancement specially applied to trigonocephaly and the insertion of an inter-orbital bone graft, if necessary, to correct the hypotelorism (Engel et al., 2011). There is still disagreement concerning the intracranial volume of patients suffering from metopic synostosis and trigonocephaly. While some published studies have suggested that patients with metopic synostosis present intracranial volumes larger than, or within the range of, the normal population (Posnick et al., 1995; Sgouros et al., 1999), other authors have found evidence that the intracranial volume in trigonocephalic children, at least in boys, is significantly reduced compared with age-matched control groups (Anderson et al., 2004; Sgouros, 2005). This raises the question about the validity of the normal reference cohort and/or the comparability of the measurement techniques used. To measure the intracranial volume, the aforementioned studies have used pre- and postoperative CT scans, which are routinely performed in various craniofacial centers to track and objectify the clinical course of surgical correction of craniosynostoses (Marcus et al., 2006; McKay et al., 2010). As the high radiation exposure of a CT scan increases the risk of malignancies in later life, the diagnostic benefit of CT examinations should be carefully weighed against the biological effects of ionizing radiation, especially in infants. Recently, three-dimensional (3D) photography has been introduced as a valuable alternative to CT scans for objective analysis of skull growth (McKay et al., 2010; Wilbrand et al., 2012). This technique gives accurate measurements, is non-invasive and independent of the examiner (Schaaf et al., 2010). The nature of the relationship between intracranial volume and intracranial pressure (ICP) in craniosynostosis is complex (Sgouros, 2005). Generally, surgical treatment of craniosynostosis should aim to increase the intracranial volume to avoid a negative impact on brain development. The aim of the present study was to evaluate the intracranial volume in patients with trigonocephalus using 3D-photography. Both, the pre- and postoperative intracranial volume were compared with an age- and sex-matched control cohort to measure the effect of fronto-orbital advancement on intracranial volume. Further aims were to evaluate the result of surgery for metopic synostosis by determining frontal and total intracranial volumes before and after surgery, to compare the pre- and postoperative frontal and total intracranial volumes to a control group of similar age. 2. Materials and methods This retrospective study used a standardized measurement protocol, examined and approved by the local Ethics Committee (Ethics number S-237/2009). The study was carried out according to the Declaration of Helsinki and written informed consent was obtained from the caregivers. The database of the Department of Oral and Maxillofacial Surgery at the University Hospital of Heidelberg was searched to identify children who underwent surgery with open fronto-
orbital advancement in isolated non-syndromic metopic synostosis between July 2010 and November 2013. The severity of trigonocephaly was classified as mild, moderate or severe with respect to the extent of clinical features, including the supraorbital retrusion, the hypotelorism, the triangular forehead, the bitemporal shortening and biparietal widening. In the present study, only children with moderate or severe forms of trigonocephaly have been included. Furthermore, the following data were retrospectively collected: name, date of birth, sex, and age at point of operative correction. In order to create a homogenous study population we only included patients who were: (1) male; (2) aged between 7 and 12 months at the time of surgery; and (3) had available 3D photogrammetric scans taken one day before the operative procedure and exactly 10 days after the operation. All photographic scans were performed using a Canfield VECTRA-360-nine-pod system (Canfield Science, Fairfield, NJ, USA). The 3D data were generated using a standardized recording protocol. Using nine synchronized cameras systems, a non-invasive 360 data acquisition based on the stereophotogrammetric method could be guaranteed. Only one scan with a recording time of 1.5 ms was required. To avoid artifacts due to hair on the head, each infant was fitted with a tight nylon cap before recording. The 3D photogrammetric data were analyzed using Cranioform Analytics 4.0 software (Cranioform, Alpnach, Switzerland). The software created a 3D coordinate system with the y-axis through the midpoint (M) between the tragus markers (Tr) and the subnasale marker (SN). The x-axis was applied as a perpendicular plane through the midpoint. The z-axis was an additional perpendicular plane to the x and y planes, through the vertex of the head. The intracranial volume was subsequently analyzed at 11 parallel levels to the original plane (TreTreSN): Q1 was the volume of the anterior left cranial quadrant, Q2 of the right anterior quadrant, Q3 of the posterior right quadrant and Q4 of the posterior left quadrant. The ‘frontal volume’ was given by the sum of Q1 and Q2, and the ‘posterior volume’ by the sum of Q3 and Q4. All volumes were measured in ml. To establish an age- and sex-matched reference data set, 3D photogrammetric scans of healthy children between the age of 3 and 13 months were used. As according to the inclusion criteria only boys with metopic synostosis were included in the study, the control cohort also only consisted of boys. In order to exclude children with plagiocephaly, we have only included children for the control cohort, who presented with a cranial vault asymmetry index (CVAI) < 3.5% and a cranial index (CI) of <90. The mean frontal, posterior and total volume was calculated and plotted against the respective age in months in order to create the intracranial volume growth curves. Surgical correction of metopic synostosis was carried out using fronto-orbital advancement specially applied to trigonocephaly as described previously (Engel et al., 2011). To visualize the areas of the skull where the intracranial volume was increased or reduced, pre- and postoperative photogrammetric data was analyzed using Geomagic Studio 6.0 (Raindrop Inc., Durham, NC, USA). To clarify if the intracranial volume of children with metopic synostosis differs from the age- and sex-matched reference group, the mean pre-operative intracranial volume measurements (frontal, posterior and total volume) were compared with the reference group. Furthermore, to measure the effect of fronto-orbital advancement on intracranial volume changes, the mean pre-operative intracranial volume measurements (total, frontal and posterior volume) were compared with the postoperative volume measurements and to the reference group. The Student's unpaired t-test was used to compare pre- and postoperative intracranial volumes against each other and against
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the age- and sex-matched control group. All p-values were considered significant when less than 0.05. Statistical analysis was performed with SPSS version 19.0.0 (IBM SPSS Statistics; SPSS Inc., Chicago, IL).
3. Results 3.1. Establishment of an age- and sex-matched reference group for intracranial volume using 3D photogrammetry To establish an age- and sex-matched control group we have analyzed the 3D photogrammetric scans from 634 healthy boys between the ages of 3 and 13 months (Fig. 1A). From the 3D photogrammetric data, the mean frontal, posterior and total intracranial volume was calculated and plotted against the age in months to generate intracranial volume growth curves (Fig. 1B). During this time period, the mean total intracranial volume increased from 1173.3 ml to 1593.6 ml, the mean frontal volume increased from 683.8 ml to 927.9 ml, and the mean posterior volume from 489.4 ml to 665.7 ml (Table 1).
3.2. Children with metopic synostosis show reduced frontal and total intracranial volumes compared with the reference group Eighteen male patients were operated on for isolated metopic craniosynostosis between July 2010 and November 2013 in our department and matched our study criteria (Table 2). The diagnosis of isolated metopic synostosis was made by clinical examination and no pre-operative CT scans were performed. Mean age at surgery was 9 months (SD 1.7). All children were operated on by the same craniofacial team consisting of two cranio-maxillofacial surgeons (ME and CF) and one pediatric neurosurgeon (HB) using standardized fronto-orbital advancement specially applied to trigonocephaly as described previously (Fig. 2) (Engel et al., 2011). All children received 3D photogrammetric scans one day before the operative procedure and exactly 10 days after the operation during the first outpatient appointment for removal of the skin clips. Analysis of the areas where intracranial volume was increased or reduced showed a considerable increase of intracranial volume at the lateral forehead and a decrease of volume at the former keel shaped forehead (Fig. 3).
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3.3. Fronto-orbital advancement increases frontal and total intracranial volume The measurement of the mean pre- and post-operative intracranial volume revealed a significant increase of the frontal volume (707.5 ml vs. 833.3 ml) (p ¼ 0.0054) after fronto-orbital advancement (Fig. 4). The effect on the mean posterior volume was less pronounced (654.5 ml vs. 686.0 ml) (p ¼ 0.3376). Consequently the operative procedure increased the mean total volume (1362.0 ml vs. 1519.3 ml) in a significant manner (p < 0.01). 3.4. Children with metopic synostosis show decreased frontal volume but normal posterior volume compared with age- and sexmatched control group To compare the pre- and postoperative volumes for boys with metopic synostosis to the age- and sex-matched control group, the mean frontal, posterior and total volume of healthy boys between the ages of 7 and 12 months were calculated. Pre-operatively, the mean frontal volume of children with metopic synostosis was significantly lower compared with the control group (654.5 ml vs. 911.0 ml) (p < 0.001). Consequently, mean total volume was significantly decreased (1362.0 ml vs. 1541.8 ml) (p ¼ 0.0031). On the other hand, posterior volume did not differ from the control group in a significant manner (654.5 ml vs. 630.8 ml) (p ¼ 0.4322) (Fig. 4). Post-operatively, no significant difference in the frontal, posterior and total volume was present, indicating a considerable increase in the intracranial volume especially in the frontal area due to the fronto-orbital advancement (Fig. 4). 4. Discussion Concerning the intracranial volume in metopic synostosis, there are disagreements in the literature, it has been variously reported to be greater, less, or equal to healthy children (Gault et al., 1990; Posnick et al., 1995; Sgouros et al., 1999). In the present study, 3D photogrammetry was used to analyze the intracranial volume of children with metopic synostosis in comparison to an age- and sex-matched control group. Furthermore, we evaluated the intracranial volume change following fronto-orbital advancement. Using our control group, we demonstrated that frontal volume, and consequently the total intracranial
Fig. 1. Age- and sex-matched control cohort. (A) Distribution of age in the reference group. 634 healthy boys between the ages of 3 and 13 months were included. (B) Growth curves of total, frontal and posterior intracranial volumes between the ages of 3 and 13 months.
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Table 1 Overview of the age- and sex-matched reference group. Distribution of 634 healthy boys between the ages of 3 and 13 month and the respective mean total, frontal and posterior intracranial volume. Age [months] Number of patients Mean intracranial volume [ml]
Total Frontal Posterior
3 20 1173.3 683.8 489.4
4 55 1254.5 735.9 518.5
5 86 1336.1 796.9 539.3
6 85 1428.1 832.5 595.5
7 98 1470.4 869.2 601.2
8 72 1519.0 891.6 627.4
9 67 1546.6 927.4 619.2
10 64 1594.9 947.0 647.9
11 40 1619.3 948.0 671.3
12 28 1606.9 932.8 674.1
13 19 1593.6 927.9 665.7
Table 2 Overview of the study group. Eighteen boys with trigonocephalus between the ages of 7 and 12 month and the respective pre- and post-operative intracranial volume. Patient
Date of birth
K.W. 25.07.2012 L.G. 16.09.2012 B.B. 03.04.2013 L.K. 06.04.2011 L.M. 31.07.2011 F.G. 02.05.2012 K.S. 31.07.2012 C.L. 19.10.2009 V.H. 09.03.2010 N.R. 26.09.2011 N.S. 05.12.2011 N.L. 24.03.2010 G.R. 04.03.2010 J.H. 05.03.2010 B.B. 04.02.2010 M.D. 01.12.2011 D.S. 05.11.2009 D.G. 30.05.2012 Mean (SD)
Sex
Diagnosis
Age at surgery [months]
Pre-operative volume [cm3]
Post-operative volume [cm3]
Frontal
Posterior
Total
Frontal
Posterior
Total
m m m m m m m m m m m m m m m m m m
Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus
7 7 7 8 8 8 8 9 9 9 9 10 11 11 11 11 12 12 9.3 (1.7)
638.0 705.0 701.1 647.0 751.0 711.6 797.3 668.0 669.0 752.0 718.0 688.0 736.0 721.0 602.0 658.0 767.0 805.0 707.5 (55.1)
556.0 536.0 665.5 667.0 660.0 711.6 627.0 556.0 707.0 738.0 556.0 667.0 564.0 738.0 686.0 649.0 660.0 836.0 654.5 (79.2)
1194.0 1241.0 1366.6 1314.0 1411.0 1423.2 1424.3 1224.0 1376.0 1490.0 1274.0 1355.0 1300.0 1459.0 1288.0 1307.0 1427.0 1641.0 1362.0 (109.1)
800.0 754.0 712.3 805.0 784.0 865.9 864.9 762.0 1000.0 919.0 1145.0 750.0 808.0 785.0 790.0 783.0 815.0 856.0 833.3 (102.9)
713.6 640.0 710.5 655.0 698.0 696.8 637.9 637.9 690.0 751.0 645.0 698.0 645.0 597.0 713.0 670.0 696.8 852.0 686.0 (56.2)
1513.6 1394.0 1422.8 1460.0 1482.0 1562.7 1502.8 1399.9 1690.0 1670.0 1790.0 1448.0 1453.0 1382.0 1503.0 1453.0 1511.8 1708.0 1519.3 (118.9)
Fig. 2. Intraoperative viewing of fronto-orbital advancement in metopic synostosis. (A) pre-operative view with typical clinical signs of trigonocephaly. (B) Replacement and fixation of the supraorbital bar after remodeling. (C) Final results after fronto-orbital advancement.
Fig. 3. Intracranial volume change following fronto-orbital advancement. (A) View from above (B) frontal view. Pre- and post-operative 3D photogrammetric data were merged and areas of volume changes were indicated in colors (red: increase of intracranial volume; blue: decrease of intracranial volume).
volume, of boys with metopic synostosis was significantly lower compared with the controls, while the posterior volume did not differ from the controls in a significant manner. After fronto-orbital advancement, the frontal and total volumes increased, so that no statistical difference to the control group was present. Netherway et al. (2005) have shown, that boys with metopic synostosis had a tendency toward smaller intracranial volumes than did healthy patients, more precisely patients younger than 7 months of age (17 boys) had normal intracranial volumes whereas patients older than 7 months (8 boys) had smaller volumes. Most recently, Maltese et al. (2014) have demonstrated, that children with metopic synostosis, at least up to the ninth months, show normal intracranial volumes as a consequence of the bi-parietal widening. However, the proportion of the intracranial volume anterior to the coronal sutures is about 30% lower than normal. Interestingly, remodeling of the forehead led to a redistribution of
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Fig. 4. Intracranial volume change following fronto-orbital advancement compared with age- and sex-matched control cohort. Mean intracranial volume (frontal, posterior and total) of 18 boys with metopic synostosis was measured preand post-operatively and compared with an age- and sex-matched control group consisting of 634 healthy boys. Pre-operatively, the frontal and total but not posterior intracranial volume in metopic synostosis was significantly lower compared with the controls. Post-operatively, frontal, posterior and total intracranial volume did not differ statistically. n.s.: not significant, p > 0.05; **p < 0.01; ***p < 0.001.
the intracranial volume, as reflected by a significant improvement in the frontal-to-total intracranial volume ratio toward that of the normal population (Maltese et al., 2014). Conversely, Paniagua et al. (2013) have demonstrated in three children with metopic synostosis using pre- and postoperative CT scans, that brain volumes were larger than age-matched controls pre- and postoperatively. This is in line with Posnick et al. (1995) who showed that the preoperative intracranial volume of 10 patients with metopic synostosis (seven male and three female patients) was generally above the age- and sex-matched norms of Lichtenberg (1960). As a major drawback of the aforementioned studies, the authors used pre- and postoperative CT scans to evaluate the changes in the intracranial volume. Traditionally, CT scans have been broadly used in craniofacial surgery to confirm the clinical diagnosis of a craniosynostosis, to obtain pre-operative information about the underlying brain and to objectively evaluate the surgical results (Marcus et al., 2006). However, pediatric tissue is more susceptible to ionizing radiation with an increased lifetime risk of inducing malignancies (Brenner et al., 2001). Hence, we and several authors have already questioned the routine use of CT scans in patients suffering from craniosynostis, especially in cases of non-syndromic, single suture synostosis, as a certain diagnosis is usually possible by clinical examination only (Engel et al., 2012, Fearon et al., 2007; Schweitzer et al., 2012). 3D stereophotogrammetry is a valuable tool for evaluating the postoperative outcome in craniofacial surgery. It is quick and easy perform, and avoids any exposure to radiation or sedation as recently described by others (McKay et al., 2010; Schaaf et al., 2010; Wilbrand et al., 2011). Besides the accurate quantification of standard anthropometric parameters, the applicability of 3D photogrammetry for measuring cranial vault volume has been recently demonstrated, especially in comparison to CT scans as the gold standard (McKay et al., 2010). Measurements by McKay et al. showed a strong correlation between volume as measured by CT and 3D photogrammetry in more than 70 patients (correlation coefficient 0.91; p < 0.001). Wilbrand et al. (2012) have already used 3D photogrammetry to measure the change of intracranial volume after surgery in children with trigonocephaly. Twelve children (male:female ratio 8:4)
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showed a mean increase in the frontal volume from 528.3 ml to 601.4 ml. However, 3D photographs were obtained pre-operatively between 1 day and 2 weeks (mean: 5.9 days) and post-operatively between 10 days and 8 weeks (mean 39.4 days), so a statistical covariance analysis had to be performed to exclude the changes which result from physiological growth. A major problem when comparing the intracranial volume of patients with craniosynostosis to healthy patients is the validity of the normal reference group. The traditionally used norms of Lichtenberg (1960) are based on CT-determined data sets which were pooled for boys and girls younger than 12 months of age and several authors have already questioned their validity as a reference group (Gault et al., 1990; Netherway et al., 2005; Posnick et al., 1995). Other reference data sets for volume measurement in the first years of life are limited by small sample sizes (Abbott et al., 2000; Kamdar et al., 2009). In the study of Kamdar and colleagues, the CT-determined intracranial volume of 123 healthy children up to 6 years of age was used to perform a reference volume growth curve, however, only 25 boys in their first year of life were included in this study (Kamdar et al., 2009). On the other hand, it should be imperative that the normative data set has been obtained using the same methodology and technology as for analysis of the synostosis group. As, up to now, there was no longitudinal continuous data available for the changes of intracranial volume in the first year of life, the present study is the first, which uses 3D photogrammetry to establish a normative control group, which describes the physiological increase of the intracranial volume, using the data of 634 male infants between the age of 3 and 13 months. Meyer-Marcotty et al. (2014) have described the physiological growth of the infant's cranium using the 3D data from 52 infants (27 females and 25 males) where 3D photography was performed at only two time points 6 and 12 months. However, the values for the total intracranial volume in male infants (n ¼ 25) at 6 months (1257.30 ml) and 12 months (1502.47 ml) are comparable to the values of the present study (1281.40 and 1428.10, respectively). It is well documented, that a subset of non-syndromic suture fusion patients show an elevated intracranial pressure (ICP) with a potential negative impact on brain development (Florisson et al., 2010). However, the exact relationship between ICP, intracranial volume and impaired brain development remains unclear. Fok et al. (1992) have revealed no correlation between constricted intracranial volume and elevated ICP. In addition, Sgouros (2005) measured elevated ICP in decreased, normal and increased cranial vault volume. On the other hand, cumulative neuropsychological abnormalities have been described in children with metopic synostosis, which might be due to the reduced frontal volume (Shimoji and Tomiyama, 2004; Starr et al., 2012). In addition, Di Rocco (2011) has previously shown, that there is a significant reduction in cerebral perfusion in the frontal lobes in metopic synostosis, which might have an impact on neurocognitive deficits. Although the connection between intracranial volume and aberrations in ICP and/or the development of neurocognitive deficits remains complex, we believe surgery for metopic synostosis should aim to correct the shape of the forehead and to simultaneously increase the intracranial volume. Moreover, measurement of the intracranial volume is an important parameter to objectively evaluate the postoperative result and even to compare different operation techniques adequately. 5. Conclusion This is the first study using 3D photogrammetry to measure the intracranial volume change in children with metopic synostosis following fronto-orbital advancement. The ability to measure the
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intracranial volume using 3D photogrammetry especially in combination with an age- and sex-matched control cohort adds important information to pre-operative evaluation and objectifies post-operative results in craniofacial surgery. Using 3D photogrammetry might replace the need for routine pre- and postoperative CT scanning and reduce the radiation exposure of infants. Competing interests None declared. Ethical approval Received. Acknowledgments Funding: The study was supported by the Austrian Cleft Palate Craniofacial Association. References Abbott AH, Netherway DJ, Niemann DB, Clark B, Yamamoto M, Cole J, et al: CTdetermined intracranial volume for a normal population. J Craniofac Surg 11: 211e223, 2000 Anderson PJ, Netherway DJ, Abbott A, David DJ: Intracranial volume measurement of metopic craniosynostosis. J Craniofac Surg 15: 1014e1016, 2004 [discussion 1017-1018] Aryan HE, Jandial R, Ozgur BM, Hughes SA, Meltzer HS, Park MS, et al: Surgical correction of metopic synostosis. Childs Nerv Syst 21: 392e398, 2005 Brenner D, Elliston C, Hall E, Berdon W: Estimated risks of radiation-induced fatal cancer from pediatric CT. AJR Am J Roentgenol 176: 289e296, 2001 Di Rocco C, Frassanito P, Tamburrini G: The shell technique: bilateral fronto-orbital reshaping in trigonocephaly. Childs Nerv Syst 12: 2189e2194, 2013 Di Rocco F: Frontal lobe perfusion in metopic synostosis: the role of surgery. In: ISCFS XIV Biennal International Congress, 2011 [Livingstone, Zambia] Engel M, Castrillon-Oberndorfer G, Hoffmann J, Freudlsperger C: Value of preoperative imaging in the diagnostics of isolated metopic suture synostosis: a riskbenefit analysis. J Plast Reconstr Aesthet Surg 65: 1246e1251, 2012 Engel M, Thiele OC, Mühling J, Hoffmann J, Freier K, Castrillon-Oberndorfer G, et al: Trigonocephaly: results after surgical correction of nonsyndromatic isolated metopic suture synostosis in 54 cases. J Craniomaxillofac Surg 40: 347e353, 2011 Fearon JA, Singh DJ, Beals SP, Yu JC: The diagnosis and treatment of single-sutural synostoses: are computed tomographic scans necessary? Plast Reconstr Surg 120: 1327e1331, 2007 Florisson JM, van Veelen ML, Bannink N, van Adrichem LN, van der Meulen JJ, Bartels MC, et al: Papilledema in isolated single-suture craniosynostosis: prevalence and predictive factors. J Craniofac Surg 21: 20e24, 2010 Fok H, Jones BM, Gault DG, Andar U, Hayward R: Relationship between intracranial pressure and intracranial volume in craniosynostosis. Br J Plast Surg 45: 394e397, 1992 Gault DT, Renier D, Marchac D, Ackland FM, Jones BM: Intracranial volume in children with craniosynostosis. J Craniofac Surg 1: 1e3, 1990 Kamdar MR, Gomez RA, Ascherman JA: Intracranial volumes in a large series of healthy children. Plast Reconstr Surg 124: 2072e2075, 2009 Kapp-Simon KA, Figueroa A, Jocher CA, Schafer M: Longitudinal assessment of mental development in infants with nonsyndromic craniosynostosis with and
without cranial release and reconstruction. Plast Reconstr Surg 92: 831e839, 1993 [discussion 840-831] Keshavarzi S, Hayden MG, Ben-Haim S, Meltzer HS, Cohen SR, Levy ML: Variations of endoscopic and open repair of metopic craniosynostosis. J Craniofac Surg 20: 1439e1444, 2009 Lichtenberg R: These pour le Doctorant en Medecine. Radiographie du Crane de 226 Enfants Normaux de la Naissance a 8 Ans: Impressions Digitiformes, Capacite, Angle et Indices. Paris: University of Paris, 1960 €f JH, Tovetja €rn R, et al: Maltese G, Tarnow P, Wikberg E, Bernhardt P, Lagerlo Intracranial volume before and after surgical treatment for isolated metopic synostosis. J Craniofac Surg 25: 262e266, 2014 Marcus JR, Stokes TH, Mukundan S, Forrest CR: Quantitative and qualitative assessment of morphology in sagittal synostosis: mid-sagittal vector analysis. J Craniofac Surg 17: 680e686, 2006 McKay DR, Davidge KM, Williams SK, Ellis LA, Chong DK, Teixeira RP, et al: Measuring cranial vault volume with three-dimensional photography: a method of measurement comparable to the gold standard. J Craniofac Surg 21: 1419e1422, 2010 € hm H, Linz C, Kochel J, Stellzig-Eisenhauer A, Schweizer T: Meyer-Marcotty P, Bo Three-dimensional analysis of cranial growth from 6 to 12 months of age. Eur J Orthod 5: 489e496, 2014 Netherway DJ, Abbott AH, Anderson PJ, David DJ: Intracranial volume in patients with nonsyndromal craniosynostosis. J Neurosurg 103: 137e141, 2005 Paniagua B, Emodi O, Hill J, Fishbaugh J, Pimenta LA, Aylward SR, et al: 3D of brain shape and volume after cranial vault remodeling surgery for craniosynostosis correction in infants. Proc Soc Photo Opt Instrum Eng 8672: 86720V, 2013 Posnick JC, Armstrong D, Bite U: Metopic and sagittal synostosis: intracranial volume measurements prior to and after cranio-orbital reshaping in childhood. Plast Reconstr Surg 96: 299e309, 1995 [discussion 310-295] Schaaf H, Pons-Kuehnemann J, Malik CY, Streckbein P, Preuss M, Howaldt HP, et al: Accuracy of three-dimensional photogrammetric images in non-synostotic cranial deformities. Neuropediatrics 41: 24e29, 2010 € hm H, Meyer-Marcotty P, Collmann H, Ernestus RI, Krauß J: Schweitzer T, Bo Avoiding CT scans in children with single-suture craniosynostosis. Childs Nerv Syst 28: 1077e1082, 2012 Sgouros S: Skull vault growth in craniosynostosis. Childs Nerv Syst 21: 861e870, 2005 Sgouros S, Hockley AD, Goldin JH, Wake MJ, Natarajan K: Intracranial volume change in craniosynostosis. J Neurosurg 91: 617e625, 1999 Shimoji T, Tomiyama N: Mild trigonocephaly and intracranial pressure: report of 56 patients. Childs Nerv Syst 20: 749e756, 2004 Speltz ML, Kapp-Simon KA, Cunningham M, Marsh J, Dawson G: Single-suture craniosynostosis: a review of neurobehavioral research and theory. J Pediatr Psychol 29: 651e668, 2004 Starr JR, Collett BR, Gaither R, Kapp-Simon KA, Cradock MM, Cunningham ML, et al: Multicenter study of neurodevelopment in 3-year-old children with and without single-suture craniosynostosis. Arch Pediatr Adolesc Med 166: 536e542, 2012 van der Meulen J: Metopic synostosis. Childs Nerv Syst 28: 1359e1367, 2012 van der Meulen J, van der Hulst R, van Adrichem L, Arnaud E, Chin-Shong D, Duncan C, et al: The increase of metopic synostosis: a pan-European observation. J Craniofac Surg 20: 283e286, 2009 Vu HL, Panchal J, Parker EE, Levine NS, Francel P: The timing of physiologic closure of the metopic suture: a review of 159 patients using reconstructed 3D CT scans of the craniofacial region. J Craniofac Surg 12: 527e532, 2001 Weinzweig J, Kirschner RE, Farley A, Reiss P, Hunter J, Whitaker LA, et al: Metopic synostosis: defining the temporal sequence of normal suture fusion and differentiating it from synostosis on the basis of computed tomography images. Plast Reconstr Surg 112: 1211e1218, 2003 Wilbrand JF, Szczukowski A, Blecher JC, Pons-Kuehnemann J, Christophis P, Howaldt HP, et al: Objectification of cranial vault correction for craniosynostosis by three-dimensional photography. J Craniomaxillofac Surg 40: 726e730, 2012 Wilbrand JF, Wilbrand M, Pons-Kuehnemann J, Blecher JC, Christophis P, Howaldt HP, et al: Value and reliability of anthropometric measurements of cranial deformity in early childhood. J Craniomaxillofac Surg 39: 24e29, 2011
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Metopic synostosis: Measuring intracranial volume change following fronto-orbital advancement using three-dimensional photogrammetry €chli b, Elek Somlo a, Christian Freudlsperger a, *, Sahra Steinmacher a, Heidi Ba a a Jürgen Hoffmann , Michael Engel a b
Department of Oral and Maxillofacial Surgery, University Hospital Heidelberg, Heidelberg, Germany Department of Neurosurgery, University Hospital Heidelberg, Heidelberg, Germany
a r t i c l e i n f o
a b s t r a c t
Article history: Paper received 3 September 2014 Accepted 25 February 2015 Available online 12 March 2015
There is still disagreement regarding the intracranial volumes of patients with metopic synostosis compared with healthy patients. This study aimed to compare the intracranial volume of children with metopic synostosis before and after surgery to an age- and sex-matched control cohort using threedimensional (3D) photogrammetry. Eighteen boys with metopic synostosis were operated on using standardized fronto-orbital advancement. Frontal, posterior and total intracranial volumes were measured exactly 1 day preoperatively and 10 days post-operatively, using 3D photogrammetry. To establish an age- and sexmatched control group, the 3D photogrammetric data of 634 healthy boys between the ages of 3 and 13 months were analyzed. Mean age at surgery was 9 months (SD 1.7). Prior to surgery, boys with metopic synostosis showed significantly reduced frontal and total intracranial volumes compared with the reference group, but similar posterior volumes. After surgery, frontal and total intracranial volumes did not differ statistically from the control group. As children with metopic synostosis showed significantly smaller frontal and total intracranial volumes compared with an age- and sex-matched control group, corrective surgery should aim to achieve volume expansion. Furthermore, 3D photogrammetry provides a valuable alternative to CT scans in the measurement of intracranial volume in children with metopic synostosis, which significantly reduces the amount of radiation exposure to the growing brain. © 2015 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved.
Keywords: 3D photogrammetry Fronto-orbital advancement Intracranial volume Metopic synostosis
1. Introduction Premature fusion of the metopic suture results in trigonocephaly, which occurs with a frequency of one case per 15,000 live births and appears either as an isolated event or as one of multiple fused sutures, usually under syndromic conditions (van der Meulen, 2012).
* Corresponding author. Department of Oral and Maxillofacial Surgery, University Hospital Heidelberg, Im Neuenheimer Feld 400, 69120 Heidelberg, Germany. Tel.: þ49 6221 5638462; fax: þ49 6221 564222. E-mail address: [email protected] (C. Freudlsperger).
The metopic suture is the first suture that closes physiologically between the 3rd and 8th month (Vu et al., 2001). However, the morphology of a prematurely fused metopic suture differs from a physiologically closed suture, not only by an obvious metopic ridge over the midline, but also by a lateral growth restriction of the frontal bones (Weinzweig et al., 2003). This growth restriction combined with an increased compensatory growth of the unaffected skull sutures leads to the pathognomonic head shape of trigonocephaly which is characterized by a frontal midline ridge, a keel shaped forehead, hypotelorism with epicanthus, and temporal narrowing with an associated abnormality of the supraorbital rim and increased interparietal width (Engel et al., 2011; van der Meulen, 2012).
http://dx.doi.org/10.1016/j.jcms.2015.02.017 1010-5182/© 2015 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved.
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Interestingly, a significant rise of metopic synostosis has been observed in recent decades, however the reason for this increase remains unclear (van der Meulen et al., 2009). Several authors have indicated an association between metopic craniosynostosis and an increased risk of speech and language difficulties, or other cognitive or behavioral deficits, although a causal relationship remains uncertain (Kapp-Simon et al., 1993; Speltz et al., 2004; Starr et al., 2012). Surgical treatment of metopic craniosynostosis includes remodeling of the forehead and advancement (Aryan et al., 2005; Di Rocco et al., 2013; Engel et al., 2011; Keshavarzi et al., 2009). At our department we prefer fronto-orbital advancement specially applied to trigonocephaly and the insertion of an inter-orbital bone graft, if necessary, to correct the hypotelorism (Engel et al., 2011). There is still disagreement concerning the intracranial volume of patients suffering from metopic synostosis and trigonocephaly. While some published studies have suggested that patients with metopic synostosis present intracranial volumes larger than, or within the range of, the normal population (Posnick et al., 1995; Sgouros et al., 1999), other authors have found evidence that the intracranial volume in trigonocephalic children, at least in boys, is significantly reduced compared with age-matched control groups (Anderson et al., 2004; Sgouros, 2005). This raises the question about the validity of the normal reference cohort and/or the comparability of the measurement techniques used. To measure the intracranial volume, the aforementioned studies have used pre- and postoperative CT scans, which are routinely performed in various craniofacial centers to track and objectify the clinical course of surgical correction of craniosynostoses (Marcus et al., 2006; McKay et al., 2010). As the high radiation exposure of a CT scan increases the risk of malignancies in later life, the diagnostic benefit of CT examinations should be carefully weighed against the biological effects of ionizing radiation, especially in infants. Recently, three-dimensional (3D) photography has been introduced as a valuable alternative to CT scans for objective analysis of skull growth (McKay et al., 2010; Wilbrand et al., 2012). This technique gives accurate measurements, is non-invasive and independent of the examiner (Schaaf et al., 2010). The nature of the relationship between intracranial volume and intracranial pressure (ICP) in craniosynostosis is complex (Sgouros, 2005). Generally, surgical treatment of craniosynostosis should aim to increase the intracranial volume to avoid a negative impact on brain development. The aim of the present study was to evaluate the intracranial volume in patients with trigonocephalus using 3D-photography. Both, the pre- and postoperative intracranial volume were compared with an age- and sex-matched control cohort to measure the effect of fronto-orbital advancement on intracranial volume. Further aims were to evaluate the result of surgery for metopic synostosis by determining frontal and total intracranial volumes before and after surgery, to compare the pre- and postoperative frontal and total intracranial volumes to a control group of similar age. 2. Materials and methods This retrospective study used a standardized measurement protocol, examined and approved by the local Ethics Committee (Ethics number S-237/2009). The study was carried out according to the Declaration of Helsinki and written informed consent was obtained from the caregivers. The database of the Department of Oral and Maxillofacial Surgery at the University Hospital of Heidelberg was searched to identify children who underwent surgery with open fronto-
orbital advancement in isolated non-syndromic metopic synostosis between July 2010 and November 2013. The severity of trigonocephaly was classified as mild, moderate or severe with respect to the extent of clinical features, including the supraorbital retrusion, the hypotelorism, the triangular forehead, the bitemporal shortening and biparietal widening. In the present study, only children with moderate or severe forms of trigonocephaly have been included. Furthermore, the following data were retrospectively collected: name, date of birth, sex, and age at point of operative correction. In order to create a homogenous study population we only included patients who were: (1) male; (2) aged between 7 and 12 months at the time of surgery; and (3) had available 3D photogrammetric scans taken one day before the operative procedure and exactly 10 days after the operation. All photographic scans were performed using a Canfield VECTRA-360-nine-pod system (Canfield Science, Fairfield, NJ, USA). The 3D data were generated using a standardized recording protocol. Using nine synchronized cameras systems, a non-invasive 360 data acquisition based on the stereophotogrammetric method could be guaranteed. Only one scan with a recording time of 1.5 ms was required. To avoid artifacts due to hair on the head, each infant was fitted with a tight nylon cap before recording. The 3D photogrammetric data were analyzed using Cranioform Analytics 4.0 software (Cranioform, Alpnach, Switzerland). The software created a 3D coordinate system with the y-axis through the midpoint (M) between the tragus markers (Tr) and the subnasale marker (SN). The x-axis was applied as a perpendicular plane through the midpoint. The z-axis was an additional perpendicular plane to the x and y planes, through the vertex of the head. The intracranial volume was subsequently analyzed at 11 parallel levels to the original plane (TreTreSN): Q1 was the volume of the anterior left cranial quadrant, Q2 of the right anterior quadrant, Q3 of the posterior right quadrant and Q4 of the posterior left quadrant. The ‘frontal volume’ was given by the sum of Q1 and Q2, and the ‘posterior volume’ by the sum of Q3 and Q4. All volumes were measured in ml. To establish an age- and sex-matched reference data set, 3D photogrammetric scans of healthy children between the age of 3 and 13 months were used. As according to the inclusion criteria only boys with metopic synostosis were included in the study, the control cohort also only consisted of boys. In order to exclude children with plagiocephaly, we have only included children for the control cohort, who presented with a cranial vault asymmetry index (CVAI) < 3.5% and a cranial index (CI) of <90. The mean frontal, posterior and total volume was calculated and plotted against the respective age in months in order to create the intracranial volume growth curves. Surgical correction of metopic synostosis was carried out using fronto-orbital advancement specially applied to trigonocephaly as described previously (Engel et al., 2011). To visualize the areas of the skull where the intracranial volume was increased or reduced, pre- and postoperative photogrammetric data was analyzed using Geomagic Studio 6.0 (Raindrop Inc., Durham, NC, USA). To clarify if the intracranial volume of children with metopic synostosis differs from the age- and sex-matched reference group, the mean pre-operative intracranial volume measurements (frontal, posterior and total volume) were compared with the reference group. Furthermore, to measure the effect of fronto-orbital advancement on intracranial volume changes, the mean pre-operative intracranial volume measurements (total, frontal and posterior volume) were compared with the postoperative volume measurements and to the reference group. The Student's unpaired t-test was used to compare pre- and postoperative intracranial volumes against each other and against
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the age- and sex-matched control group. All p-values were considered significant when less than 0.05. Statistical analysis was performed with SPSS version 19.0.0 (IBM SPSS Statistics; SPSS Inc., Chicago, IL).
3. Results 3.1. Establishment of an age- and sex-matched reference group for intracranial volume using 3D photogrammetry To establish an age- and sex-matched control group we have analyzed the 3D photogrammetric scans from 634 healthy boys between the ages of 3 and 13 months (Fig. 1A). From the 3D photogrammetric data, the mean frontal, posterior and total intracranial volume was calculated and plotted against the age in months to generate intracranial volume growth curves (Fig. 1B). During this time period, the mean total intracranial volume increased from 1173.3 ml to 1593.6 ml, the mean frontal volume increased from 683.8 ml to 927.9 ml, and the mean posterior volume from 489.4 ml to 665.7 ml (Table 1).
3.2. Children with metopic synostosis show reduced frontal and total intracranial volumes compared with the reference group Eighteen male patients were operated on for isolated metopic craniosynostosis between July 2010 and November 2013 in our department and matched our study criteria (Table 2). The diagnosis of isolated metopic synostosis was made by clinical examination and no pre-operative CT scans were performed. Mean age at surgery was 9 months (SD 1.7). All children were operated on by the same craniofacial team consisting of two cranio-maxillofacial surgeons (ME and CF) and one pediatric neurosurgeon (HB) using standardized fronto-orbital advancement specially applied to trigonocephaly as described previously (Fig. 2) (Engel et al., 2011). All children received 3D photogrammetric scans one day before the operative procedure and exactly 10 days after the operation during the first outpatient appointment for removal of the skin clips. Analysis of the areas where intracranial volume was increased or reduced showed a considerable increase of intracranial volume at the lateral forehead and a decrease of volume at the former keel shaped forehead (Fig. 3).
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3.3. Fronto-orbital advancement increases frontal and total intracranial volume The measurement of the mean pre- and post-operative intracranial volume revealed a significant increase of the frontal volume (707.5 ml vs. 833.3 ml) (p ¼ 0.0054) after fronto-orbital advancement (Fig. 4). The effect on the mean posterior volume was less pronounced (654.5 ml vs. 686.0 ml) (p ¼ 0.3376). Consequently the operative procedure increased the mean total volume (1362.0 ml vs. 1519.3 ml) in a significant manner (p < 0.01). 3.4. Children with metopic synostosis show decreased frontal volume but normal posterior volume compared with age- and sexmatched control group To compare the pre- and postoperative volumes for boys with metopic synostosis to the age- and sex-matched control group, the mean frontal, posterior and total volume of healthy boys between the ages of 7 and 12 months were calculated. Pre-operatively, the mean frontal volume of children with metopic synostosis was significantly lower compared with the control group (654.5 ml vs. 911.0 ml) (p < 0.001). Consequently, mean total volume was significantly decreased (1362.0 ml vs. 1541.8 ml) (p ¼ 0.0031). On the other hand, posterior volume did not differ from the control group in a significant manner (654.5 ml vs. 630.8 ml) (p ¼ 0.4322) (Fig. 4). Post-operatively, no significant difference in the frontal, posterior and total volume was present, indicating a considerable increase in the intracranial volume especially in the frontal area due to the fronto-orbital advancement (Fig. 4). 4. Discussion Concerning the intracranial volume in metopic synostosis, there are disagreements in the literature, it has been variously reported to be greater, less, or equal to healthy children (Gault et al., 1990; Posnick et al., 1995; Sgouros et al., 1999). In the present study, 3D photogrammetry was used to analyze the intracranial volume of children with metopic synostosis in comparison to an age- and sex-matched control group. Furthermore, we evaluated the intracranial volume change following fronto-orbital advancement. Using our control group, we demonstrated that frontal volume, and consequently the total intracranial
Fig. 1. Age- and sex-matched control cohort. (A) Distribution of age in the reference group. 634 healthy boys between the ages of 3 and 13 months were included. (B) Growth curves of total, frontal and posterior intracranial volumes between the ages of 3 and 13 months.
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Table 1 Overview of the age- and sex-matched reference group. Distribution of 634 healthy boys between the ages of 3 and 13 month and the respective mean total, frontal and posterior intracranial volume. Age [months] Number of patients Mean intracranial volume [ml]
Total Frontal Posterior
3 20 1173.3 683.8 489.4
4 55 1254.5 735.9 518.5
5 86 1336.1 796.9 539.3
6 85 1428.1 832.5 595.5
7 98 1470.4 869.2 601.2
8 72 1519.0 891.6 627.4
9 67 1546.6 927.4 619.2
10 64 1594.9 947.0 647.9
11 40 1619.3 948.0 671.3
12 28 1606.9 932.8 674.1
13 19 1593.6 927.9 665.7
Table 2 Overview of the study group. Eighteen boys with trigonocephalus between the ages of 7 and 12 month and the respective pre- and post-operative intracranial volume. Patient
Date of birth
K.W. 25.07.2012 L.G. 16.09.2012 B.B. 03.04.2013 L.K. 06.04.2011 L.M. 31.07.2011 F.G. 02.05.2012 K.S. 31.07.2012 C.L. 19.10.2009 V.H. 09.03.2010 N.R. 26.09.2011 N.S. 05.12.2011 N.L. 24.03.2010 G.R. 04.03.2010 J.H. 05.03.2010 B.B. 04.02.2010 M.D. 01.12.2011 D.S. 05.11.2009 D.G. 30.05.2012 Mean (SD)
Sex
Diagnosis
Age at surgery [months]
Pre-operative volume [cm3]
Post-operative volume [cm3]
Frontal
Posterior
Total
Frontal
Posterior
Total
m m m m m m m m m m m m m m m m m m
Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus Trigonocephalus
7 7 7 8 8 8 8 9 9 9 9 10 11 11 11 11 12 12 9.3 (1.7)
638.0 705.0 701.1 647.0 751.0 711.6 797.3 668.0 669.0 752.0 718.0 688.0 736.0 721.0 602.0 658.0 767.0 805.0 707.5 (55.1)
556.0 536.0 665.5 667.0 660.0 711.6 627.0 556.0 707.0 738.0 556.0 667.0 564.0 738.0 686.0 649.0 660.0 836.0 654.5 (79.2)
1194.0 1241.0 1366.6 1314.0 1411.0 1423.2 1424.3 1224.0 1376.0 1490.0 1274.0 1355.0 1300.0 1459.0 1288.0 1307.0 1427.0 1641.0 1362.0 (109.1)
800.0 754.0 712.3 805.0 784.0 865.9 864.9 762.0 1000.0 919.0 1145.0 750.0 808.0 785.0 790.0 783.0 815.0 856.0 833.3 (102.9)
713.6 640.0 710.5 655.0 698.0 696.8 637.9 637.9 690.0 751.0 645.0 698.0 645.0 597.0 713.0 670.0 696.8 852.0 686.0 (56.2)
1513.6 1394.0 1422.8 1460.0 1482.0 1562.7 1502.8 1399.9 1690.0 1670.0 1790.0 1448.0 1453.0 1382.0 1503.0 1453.0 1511.8 1708.0 1519.3 (118.9)
Fig. 2. Intraoperative viewing of fronto-orbital advancement in metopic synostosis. (A) pre-operative view with typical clinical signs of trigonocephaly. (B) Replacement and fixation of the supraorbital bar after remodeling. (C) Final results after fronto-orbital advancement.
Fig. 3. Intracranial volume change following fronto-orbital advancement. (A) View from above (B) frontal view. Pre- and post-operative 3D photogrammetric data were merged and areas of volume changes were indicated in colors (red: increase of intracranial volume; blue: decrease of intracranial volume).
volume, of boys with metopic synostosis was significantly lower compared with the controls, while the posterior volume did not differ from the controls in a significant manner. After fronto-orbital advancement, the frontal and total volumes increased, so that no statistical difference to the control group was present. Netherway et al. (2005) have shown, that boys with metopic synostosis had a tendency toward smaller intracranial volumes than did healthy patients, more precisely patients younger than 7 months of age (17 boys) had normal intracranial volumes whereas patients older than 7 months (8 boys) had smaller volumes. Most recently, Maltese et al. (2014) have demonstrated, that children with metopic synostosis, at least up to the ninth months, show normal intracranial volumes as a consequence of the bi-parietal widening. However, the proportion of the intracranial volume anterior to the coronal sutures is about 30% lower than normal. Interestingly, remodeling of the forehead led to a redistribution of
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Fig. 4. Intracranial volume change following fronto-orbital advancement compared with age- and sex-matched control cohort. Mean intracranial volume (frontal, posterior and total) of 18 boys with metopic synostosis was measured preand post-operatively and compared with an age- and sex-matched control group consisting of 634 healthy boys. Pre-operatively, the frontal and total but not posterior intracranial volume in metopic synostosis was significantly lower compared with the controls. Post-operatively, frontal, posterior and total intracranial volume did not differ statistically. n.s.: not significant, p > 0.05; **p < 0.01; ***p < 0.001.
the intracranial volume, as reflected by a significant improvement in the frontal-to-total intracranial volume ratio toward that of the normal population (Maltese et al., 2014). Conversely, Paniagua et al. (2013) have demonstrated in three children with metopic synostosis using pre- and postoperative CT scans, that brain volumes were larger than age-matched controls pre- and postoperatively. This is in line with Posnick et al. (1995) who showed that the preoperative intracranial volume of 10 patients with metopic synostosis (seven male and three female patients) was generally above the age- and sex-matched norms of Lichtenberg (1960). As a major drawback of the aforementioned studies, the authors used pre- and postoperative CT scans to evaluate the changes in the intracranial volume. Traditionally, CT scans have been broadly used in craniofacial surgery to confirm the clinical diagnosis of a craniosynostosis, to obtain pre-operative information about the underlying brain and to objectively evaluate the surgical results (Marcus et al., 2006). However, pediatric tissue is more susceptible to ionizing radiation with an increased lifetime risk of inducing malignancies (Brenner et al., 2001). Hence, we and several authors have already questioned the routine use of CT scans in patients suffering from craniosynostis, especially in cases of non-syndromic, single suture synostosis, as a certain diagnosis is usually possible by clinical examination only (Engel et al., 2012, Fearon et al., 2007; Schweitzer et al., 2012). 3D stereophotogrammetry is a valuable tool for evaluating the postoperative outcome in craniofacial surgery. It is quick and easy perform, and avoids any exposure to radiation or sedation as recently described by others (McKay et al., 2010; Schaaf et al., 2010; Wilbrand et al., 2011). Besides the accurate quantification of standard anthropometric parameters, the applicability of 3D photogrammetry for measuring cranial vault volume has been recently demonstrated, especially in comparison to CT scans as the gold standard (McKay et al., 2010). Measurements by McKay et al. showed a strong correlation between volume as measured by CT and 3D photogrammetry in more than 70 patients (correlation coefficient 0.91; p < 0.001). Wilbrand et al. (2012) have already used 3D photogrammetry to measure the change of intracranial volume after surgery in children with trigonocephaly. Twelve children (male:female ratio 8:4)
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showed a mean increase in the frontal volume from 528.3 ml to 601.4 ml. However, 3D photographs were obtained pre-operatively between 1 day and 2 weeks (mean: 5.9 days) and post-operatively between 10 days and 8 weeks (mean 39.4 days), so a statistical covariance analysis had to be performed to exclude the changes which result from physiological growth. A major problem when comparing the intracranial volume of patients with craniosynostosis to healthy patients is the validity of the normal reference group. The traditionally used norms of Lichtenberg (1960) are based on CT-determined data sets which were pooled for boys and girls younger than 12 months of age and several authors have already questioned their validity as a reference group (Gault et al., 1990; Netherway et al., 2005; Posnick et al., 1995). Other reference data sets for volume measurement in the first years of life are limited by small sample sizes (Abbott et al., 2000; Kamdar et al., 2009). In the study of Kamdar and colleagues, the CT-determined intracranial volume of 123 healthy children up to 6 years of age was used to perform a reference volume growth curve, however, only 25 boys in their first year of life were included in this study (Kamdar et al., 2009). On the other hand, it should be imperative that the normative data set has been obtained using the same methodology and technology as for analysis of the synostosis group. As, up to now, there was no longitudinal continuous data available for the changes of intracranial volume in the first year of life, the present study is the first, which uses 3D photogrammetry to establish a normative control group, which describes the physiological increase of the intracranial volume, using the data of 634 male infants between the age of 3 and 13 months. Meyer-Marcotty et al. (2014) have described the physiological growth of the infant's cranium using the 3D data from 52 infants (27 females and 25 males) where 3D photography was performed at only two time points 6 and 12 months. However, the values for the total intracranial volume in male infants (n ¼ 25) at 6 months (1257.30 ml) and 12 months (1502.47 ml) are comparable to the values of the present study (1281.40 and 1428.10, respectively). It is well documented, that a subset of non-syndromic suture fusion patients show an elevated intracranial pressure (ICP) with a potential negative impact on brain development (Florisson et al., 2010). However, the exact relationship between ICP, intracranial volume and impaired brain development remains unclear. Fok et al. (1992) have revealed no correlation between constricted intracranial volume and elevated ICP. In addition, Sgouros (2005) measured elevated ICP in decreased, normal and increased cranial vault volume. On the other hand, cumulative neuropsychological abnormalities have been described in children with metopic synostosis, which might be due to the reduced frontal volume (Shimoji and Tomiyama, 2004; Starr et al., 2012). In addition, Di Rocco (2011) has previously shown, that there is a significant reduction in cerebral perfusion in the frontal lobes in metopic synostosis, which might have an impact on neurocognitive deficits. Although the connection between intracranial volume and aberrations in ICP and/or the development of neurocognitive deficits remains complex, we believe surgery for metopic synostosis should aim to correct the shape of the forehead and to simultaneously increase the intracranial volume. Moreover, measurement of the intracranial volume is an important parameter to objectively evaluate the postoperative result and even to compare different operation techniques adequately. 5. Conclusion This is the first study using 3D photogrammetry to measure the intracranial volume change in children with metopic synostosis following fronto-orbital advancement. The ability to measure the
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intracranial volume using 3D photogrammetry especially in combination with an age- and sex-matched control cohort adds important information to pre-operative evaluation and objectifies post-operative results in craniofacial surgery. Using 3D photogrammetry might replace the need for routine pre- and postoperative CT scanning and reduce the radiation exposure of infants. Competing interests None declared. Ethical approval Received. Acknowledgments Funding: The study was supported by the Austrian Cleft Palate Craniofacial Association. References Abbott AH, Netherway DJ, Niemann DB, Clark B, Yamamoto M, Cole J, et al: CTdetermined intracranial volume for a normal population. J Craniofac Surg 11: 211e223, 2000 Anderson PJ, Netherway DJ, Abbott A, David DJ: Intracranial volume measurement of metopic craniosynostosis. J Craniofac Surg 15: 1014e1016, 2004 [discussion 1017-1018] Aryan HE, Jandial R, Ozgur BM, Hughes SA, Meltzer HS, Park MS, et al: Surgical correction of metopic synostosis. Childs Nerv Syst 21: 392e398, 2005 Brenner D, Elliston C, Hall E, Berdon W: Estimated risks of radiation-induced fatal cancer from pediatric CT. AJR Am J Roentgenol 176: 289e296, 2001 Di Rocco C, Frassanito P, Tamburrini G: The shell technique: bilateral fronto-orbital reshaping in trigonocephaly. Childs Nerv Syst 12: 2189e2194, 2013 Di Rocco F: Frontal lobe perfusion in metopic synostosis: the role of surgery. In: ISCFS XIV Biennal International Congress, 2011 [Livingstone, Zambia] Engel M, Castrillon-Oberndorfer G, Hoffmann J, Freudlsperger C: Value of preoperative imaging in the diagnostics of isolated metopic suture synostosis: a riskbenefit analysis. J Plast Reconstr Aesthet Surg 65: 1246e1251, 2012 Engel M, Thiele OC, Mühling J, Hoffmann J, Freier K, Castrillon-Oberndorfer G, et al: Trigonocephaly: results after surgical correction of nonsyndromatic isolated metopic suture synostosis in 54 cases. J Craniomaxillofac Surg 40: 347e353, 2011 Fearon JA, Singh DJ, Beals SP, Yu JC: The diagnosis and treatment of single-sutural synostoses: are computed tomographic scans necessary? Plast Reconstr Surg 120: 1327e1331, 2007 Florisson JM, van Veelen ML, Bannink N, van Adrichem LN, van der Meulen JJ, Bartels MC, et al: Papilledema in isolated single-suture craniosynostosis: prevalence and predictive factors. J Craniofac Surg 21: 20e24, 2010 Fok H, Jones BM, Gault DG, Andar U, Hayward R: Relationship between intracranial pressure and intracranial volume in craniosynostosis. Br J Plast Surg 45: 394e397, 1992 Gault DT, Renier D, Marchac D, Ackland FM, Jones BM: Intracranial volume in children with craniosynostosis. J Craniofac Surg 1: 1e3, 1990 Kamdar MR, Gomez RA, Ascherman JA: Intracranial volumes in a large series of healthy children. Plast Reconstr Surg 124: 2072e2075, 2009 Kapp-Simon KA, Figueroa A, Jocher CA, Schafer M: Longitudinal assessment of mental development in infants with nonsyndromic craniosynostosis with and
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