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Ultrasonography for the diagnosis of craniosynostosis
European Journal of Radiology 90 (2017) 250–255
Contents lists available at ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Ultrasonography for the diagnosis of craniosynostosis Maïa Proisy a,b,∗ , Laurent Riffaud c , Kamal Chouklati a , Catherine Tréguier a , Bertrand Bruneau a a b c
CHU Rennes, Department of Radiology, Hôpital Sud, F-35203 Rennes, France INSERM U1228 VisAGeS Unit, CNRS UMR 6074, Université de Rennes 1, F-35042 Rennes, France CHU Rennes, Department of Neurosurgery, CHU de Rennes, F-35033 Rennes, France
a r t i c l e
i n f o
Article history: Received 17 December 2016 Received in revised form 9 March 2017 Accepted 15 March 2017 Keywords: Craniosynostosis Ultrasound Nonsynostotic plagiocephaly Infant Skull Positional plagiocephaly
a b s t r a c t Objectives: The aim of this study was to report our experience with ultrasonography in our routine practice for the diagnosis of cranial deformity in infants. Methods: We conducted a single-institution retrospective study of infants referred to our department because of skull deformity. We only included in this study infants having undergone both US and 3D-CT to ensure accurate comparisons. Each cranial suture was described as normal or closed (partial or complete closure). Sonography examination results were correlated with 3D-CT findings as a gold-standard. Results: Forty infants were included with a mean age of 5.2 ± 4.9 months. Thirty had a craniosynostosis and 10 children had a postural deformity with normal sutures. Correlation between US and 3D-CT for the diagnosis of normal or closed suture had a specificity and a sensitivity of 100%. US examination for the diagnosis of complete or incomplete synostosis had a sensitivity of 100%. Conclusions: Cranial US is an effective technique to make a positive or negative diagnosis of prematurely closed suture. US examination of sutures is a fast and non-radiating technique, which may serve as a first-choice imaging modality in infants with skull deformity. © 2017 Elsevier B.V. All rights reserved.
1. Introduction Cranial deformity is common in children. The 2 main causes remain positional plagiocephaly and craniosynostosis. Positional plagiocephaly is becoming more and more frequent since recommendations to place infants on their backs for sleeping in order to prevent sudden infant death syndrome. On the contrary, craniosynostosis caused by the premature closure of one or more sutures of the cranial bones is a much more uncommon condition occurring in only 3–6 infants per 10,000 live births [1]. Consequences of these 2 deformities may be very different as craniosynostosis may lead to severe chronic intracranial hypertension and thus need surgical correction. Differential diagnosis between these 2 malformations sometimes remains challenging. Although physical examination is sufficient to differentiate craniosynostosis and deformational plagiocephaly in most cases, cranial imaging is still regularly needed
to confirm the diagnosis especially for non-specialized practitioners [1]. Conventional cranial X-ray has traditionally been the first imaging modality but its interpretation is particularly demanding and it is a source of radiation. Three-dimensional computed tomography (3D-CT) has high diagnosis accuracy, and is considered as the gold standard [2] but acquisition may need sedation and it is also a source of radiation. Very recently, ultrasonography (US) has been proposed to assist practitioners in the diagnosis of craniosynostosis with excellent efficiency [3,4]. However, although US has multiple advantages such as low cost and non-ionising technique few studies have as yet been conducted [5–10]. To date US is not yet considered as a screening tool for craniosynostosis. The aim of this study was to report our experience with US in our routine practice for the diagnosis of cranial deformity in infants and to demonstrate its high accuracy in the diagnosis of craniosynostosis.
2. Materials and methods Abbreviations: 3D-CT, three dimensional computed tomography; US, Ultrasound. ∗ Corresponding author at: CHU Rennes, Department of Radiology, Paediatric Imaging, Hôpital Sud, 16 Boulevard de Bulgarie, BP 90347, 35203 Rennes Cedex 2, France. E-mail address: [email protected] (M. Proisy). http://dx.doi.org/10.1016/j.ejrad.2017.03.006 0720-048X/© 2017 Elsevier B.V. All rights reserved.
2.1. Study group We conducted a single-institution retrospective study between 2004 and 2014 in our paediatric radiology department. During
M. Proisy et al. / European Journal of Radiology 90 (2017) 250–255
251
Fig. 1. Diagnostic approach of craniosynostosis in Rennes University Hospital for children under 8 months old.
this period, infants that were referred to our department by a general practitioner or a paediatrician for skull deformity and suspicion of craniosynostosis underwent both a cranial US and a plain radiography or 3D-CT according to the practitioner’s prescription. Ultrasonography was performed in all cases by one of the paediatric radiologist from our department (CT, BB, KC with respectively 30, 15 and 10 years of experience). Given the US experience acquired during the first 7 years, we changed our practice after 2011 in agreement with the paediatric neurosurgeon (LR). After this date, US was performed as a first-line radiological examination in cases of suspicion of craniosynostosis and considered as an alternative to classic plain radiography or 3D-CT for the diagnosis of craniosysnostosis (Fig. 1). For this retrospective study, we only included infants having undergone both US and 3D-CT in order to compare the sutures in the most reliable manner. We considered that comparison of all the sutures was not possible with plain radiography. Each child was examined first by US and then by 3D-CT. The study was approved by the local ethics committee and did not require informed consent from the relatives. 2.2. Ultrasonography procedure All US examinations were performed on a Philips HDI 5000 Sonoct from 2004 to 2008, then a Philips IU 22 machine from 2008 onwards (Philips Medical System, The Netherlands) using a high frequency linear transducer (12,5 and/or 17,5 MHz transducer). The probe was positioned perpendicular to the expected linear course of the suture. Coronal, sagittal, lambdoïd and metopic sutures were systematically analysed. During US examination, the cranial sutures were followed along their whole length. A cranial suture was considered as normal (patent suture) if a hypoechoic gap was identified between two hyperechoic bony plates, with end-to-end appearance or bevelled or overlapped
appearance [3]. A suture was considered closed (synostosed suture) if there was a loss of hypoechoic fibrous gap between bony plates [4]. Paediatric radiologists paid particular attention to partial or complete closure of sutures. Image and video recordings were systematically performed during examination and reviewed for comparison with 3D-CT findings. 2.3. CT acquisition All CT examinations were performed using the same 16-slice multidetector CT (Philips Brilliance, Cleveland, Ohio, USA) with a stereotyped protocol. The imaging parameters used were as follows: tube voltage 120 kV, tube current 100 mAs, collimation 16 × 0.75, pitch 0.688, rotation time 0.5 s, slice thickness 0.8 mm, increment 0.4 mm. 3D-CT volume rendering reconstruction were systematically performed. 2.4. Data analysis Sonography examination was correlated with 3D-CT findings as a gold-standard. The sensitivity, specificity, positive and negative predictive values of ultrasound for the diagnosis of craniosynostosis was calculated. 3. Results 3.1. Study group description A total of 40 infants were finally included. There were 7 girls and 33 boys. Thirty children had a craniosynostosis including 20 scaphocephaly, 4 trigonocephaly, 3 plagiocephaly, 2 brachycephaly, and 1 atypical craniosynostosis. The case of atypical craniosynostosis was one case with both sagittal and left coronal suture synostosis. Ten children had a postural deformity with
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normal sutures including 8 positional plagiocephaly and 2 nonsynostotic scaphocephaly. The mean age of the 40 children was 5.2 ± 4.9 months. There was no significant difference between ages in the craniosynostosis group (mean age = 4.9 ± 5.0 months) and in the postural deformity group (mean age = 6.0 ± 4.8 months) (p = 0.50). 3.2. US accuracy for the diagnosis of craniosynostosis Correlation between US and 3D-CT for the diagnosis of normal or closed suture was excellent. Cranial US for the diagnosis of a closed suture had a specificity of 100%, a sensitivity of 100%, positive and negative predictive values of 100% and 100%. 3.3. US accuracy for the diagnosis of complete/incomplete synostosis The correlation between US and 3D-CT for the diagnosis of complete or incomplete synostosis was excellent. There was a sensitivity of 100%. 3.4. Case illustrations Figs. 2–5 . 4. Discussion During recent years, the incidence of positional plagiocephaly in young children has increased by up to 20% [11] due to recommendations to position infants on their back [12]. Thus, it is now a frequent finding [13,14]. In such cases, it is important to exclude craniosynostosis. Although diagnosis of positional plagiocephaly could be assessed by physical examination with some typical features such as trapezoidal head shape, mastoid bulge, tilt of the cranial base and pushed-forwards ear position [15], clinical differentiation with isolated unilateral lambdoid or coronal synostosis could be difficult, especially for general practitioners. A CT scan is then considered as the gold standard to distinguish these cranial deformities but it requires sedation in young children and exposure to ionizing radiations in this more radiosensitive population [16,17]. For this last reason, several studies have investigated the impact of dose reduction on image quality for specific 3D-CT protocols [18,19] but alternative procedures without any ionizing radiations should be considered. Sonographic appearance and measurement of normal major cranial sutures in neonates and infants were first described in 1997 [3] and high-resolution sonography of the abnormal cranial suture was described one year later by the same author [4]. Only a few studies have shown the effectiveness of US in craniosynostosis. So far, US is not yet used as a routine screening tool. Its use in diagnosing craniosynotosis would become far more common if more specifically adapted examinations were requested and carried out. Sze et al. [5] demonstrated that sonography of the lambdoid sutures had excellent results as a screening test of lambdoid sutural patency among 41 children. In another study concerning 100 paediatric patients who were admitted with an abnormal head shape suggesting deformational plagiocephaly, Regelsberger et al. [9] described that patency of the lambdoid sutures was confirmed by US in 99 cases. In one patient, partial synostosis was diagnosed. Further reports demonstrated that US was an effective method for the other sutures [6,7,10]. In our study, cranial US for the diagnosis of a closed suture had a specificity of 100% and a sensitivity of 100%. These results are similar to those of another recent study [8], but we also evaluated complete or incomplete closure of the sutures with a sensitivity of 100%. For these reasons, we think that US is an effective and reliable technique which may serve as a first imaging tool when
Fig. 2. Posterior positional plagiocephaly in a 4-month-old boy. Vertex view of 3DCT (A) shows the head shape and demonstrates the parallelogram appearance of the skull. The US image of the left coronal suture performed at the level of the blue line positioned on the 3D-CT shows the hypoechoic gap between hyperechoic calvarial bones (B). Lambdoid sutures were also patent on US examination and 3D-CT (not shown on this Figure).
a clinical diagnosis of craniosynostosis is suspected. Moreover, US has many advantages: it is a fast, non-ionising technique that does not require any sedation. However, there are some limitations with US examination. Ultrasound imaging is often described as an “operator-dependent” technique. Although education of radiologists is recommended, imaging of the cranial sutures is relatively easy to learn. Furthermore, this method did not show any interobserver variability between two independent investigators in Regelsberger et al’s study [9]. Another limitation of US is the inability to assess sutural patency after a certain age. In our experience, the earlier the US is performed the more reliable the examination is. Reliability of US decreased with age because of hair growth, skull growth and thinner sutures, especially coronal sutures. According to our experience, US is limited by age with the upper limit at 8 months old. Regelsberger et al. considered the age limit of 13 months [9] for the technique and Sze et al. [5] were able to distinguish patent from fused sutures in one patient scanned at 18 months. As most children with cranial deformity are usually seen before the age of 10 months, we recommend carrying out US examination as soon as possible when diagnosis is suspected, ideally before the age of 8 months. Special attention must be paid to the metopic suture.
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Fig. 3. Unilateral coronal synostosis in a 2-month-old boy. Antero-superior 3D-CT view (A) shows the elevated left orbital roof and the complete fusion of the left coronal suture. The US image performed at the level of the blue line positioned on the 3D-CT shows the synostosed left coronal suture with a continuous hyperechoic calvarian bone and no hypoechoic gap (B).
Indeed, physiological closure of this suture occurs much earlier than the others. As fusion normally arises between the age of 3 and 9 months [20], complete fusion of the metopic suture does not necessary mean trigonocephaly. Typical triangular frontal deformation and hypotelorism should also be associated with complete fusion of this suture to diagnose trigonocephaly with certainty. 3D-CT is an important imaging technique in diagnosis of craniosynostosis. However, 3D-CT should not be used as a first tool imaging procedure as is still the case in many centres. We consider that it should concern only children with uncertain clinical situations and those with positive findings at US as a preoperative planning. Regarding preoperative surgical planning in our institution, 3D-CT examination was only performed in cases of metopic, coronal or complex craniosynostosis. US demonstrated diagnosis of craniosynostosis in an initial step and then allowed us to wait for the right moment to perform 3D-CT (one month before surgery). Furthermore, we considered that a child with a charac-
Fig. 4. Scaphocephaly in a 1-month-old boy. Superior view of the 3D-CT (A) shows the particular head shape with elongated cranium and the sub-total sagittal synostosis, with the corresponding US images (B) showing a continuous hyperechoic bone at the anterior part of the suture, with bridging at the half-posterior part and a very small part of the posterior patent suture with persistence of an hypoechoic gap.
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teristic nonsyndromic scaphocephaly and a positive US for sagittal synostosis should be operated on without additional imaging studies. In the literature some authors suggest that operative correction of isolated sagittal synostosis can proceed without any radiological investigations, unless clinical examination exhibits atypical features [20]. Considering potential side effects from ionizing radiation, risks of sedation, and costs, Fearon et al. [21] also suggested that surgeons should reserve computed tomographic scans for infants in whom physical examination was not clear. Finally and regarding literature [22] and our 2 cases of nonsynostotic scaphocephaly (illustration: case 5), we advise that craniosynostosis should always be confirmed by radiological imaging except for typical positional plagiocephaly, with US as a first step diagnosis. 5. Conclusion US examination of sutures is a fast, effective and non-irradiating technique that may serve as a first choice imaging modality in infants (particularly under 8 months old) with skull deformity when craniosynostosis is suspected. In our study, we demonstrated that US was an effective technique for positive diagnosis of a prematurely closed suture. Diagnosis of craniosynostosis can be ruled out if US examination of the entire coronal, sagittal and lambdoid sutures demonstrates normal patent sutures. 3D-CT should only be recommended either in atypical cases or in a pre-operative setting when the diagnosis of craniosynostosis has been acquired on US examination. Thus 3D-CT could be organised at the appropriate time before surgery according to the surgeon’s recommendations in order to optimize surgical planning. References
Fig. 5. Nonsynostotic scaphocephaly in a 10 month-old boy. Vertex view of the 3D-CT shows the head deformity with an elongated cranium suggestive of scaphocephaly but patent coronal, sagittal and lambdoid sutures. Corresponding US images at the level of blue lines show patent sutures with persistence of a hypoechoic gap between calvarial bones (B).
[1] S. Nagaraja, P. Anslow, B. Winter, Craniosynostosis, Clin. Radiol. 68 (2013) 284–292. [2] M.W. Vannier, C.F. Hildebolt, J.L. Marsh, T.K. Pilgram, W.H. McAlister, G.D. Shackelford, C.J. Offutt, R.H. Knapp, Craniosynostosis: diagnostic value of three-dimensional CT reconstruction, Radiology 173 (1989) 669–673. [3] D. Soboleski, D. McCloskey, B. Mussari, E. Sauerbrei, M. Clarke, A. Fletcher, Sonography of normal cranial sutures, Am. J. Roentgenol. 168 (1997) 819–821. [4] D. Soboleski, B. Mussari, D. McCloskey, E. Sauerbrei, F. Espinosa, A. Fletcher, High-resolution sonography of the abnormal cranial suture, Pediatr. Radiol. 28 (1998) 79–82. [5] R.W. Sze, M.T. Parisi, M. Sidhu, A.M. Paladin, A.-V. Ngo, K.D. Seidel, E. Weinberger, R.G. Ellenbogen, J.S. Gruss, M.L. Cunningham, Ultrasound screening of the lambdoid suture in the child with posterior plagiocephaly, Pediatr. Radiol. 33 (2003) 630–636. [6] M. Krimmel, B. Will, M. Wolff, S. Kluba, K. Haas-Lude, J. Schaefer, M.U. Schuhmann, S. Reinert, Value of high-resolution ultrasound in the differential diagnosis of scaphocephaly and occipital plagiocephaly, Int. J. Oral Maxillofac. Surg. 41 (2012) 797–800. [7] N. Simanovsky, N. Hiller, B. Koplewitz, K. Rozovsky, Effectiveness of ultrasonographic evaluation of the cranial sutures in children with suspected craniosynostosis, Eur. Radiol. 19 (2009) 687–692. [8] H. Alizadeh, N. Najmi, M. Mehdizade, N. Najmi, Diagnostic accuracy of ultrasonic examination in suspected craniosynostosis among infants, Indian Pediatr. 50 (2013) 148–150. [9] J. Regelsberger, G. Delling, M. Tsokos, K. Helmke, G. Kammler, H. Kränzlein, M. Westphal, High-frequency ultrasound confirmation of positional plagiocephaly, J. Neurosurg. 105 (2006) 413–417. [10] J. Regelsberger, G. Delling, K. Helmke, M. Tsokos, G. Kammler, H. Kränzlein, M. Westphal, Ultrasound in the diagnosis of craniosynostosis, J. Craniofac. Surg. 17 (2006) (623–625-628). [11] C.M. McKinney, M.L. Cunningham, V.L. Holt, B. Leroux, J.R. Starr, Characteristics of 2733 cases diagnosed with deformational plagiocephaly and changes in risk factors over time, Cleft Palate-Craniofac. J. 45 (2008) 208–216. [12] American Academy of Pediatrics AAP Task Force on Infant Positioning and SIDS: Positioning and SIDS, Pediatrics 89 (1992) 1120–1126. [13] B.L. Hutchison, L.A.D. Hutchison, J.M.D. Thompson, E.A. Mitchell, Plagiocephaly and brachycephaly in the first two years of life: a prospective cohort study, Pediatrics 114 (2004) 970–980. [14] W.K. Peitsch, C.H. Keefer, R.A. LaBrie, J.B. Mulliken, Incidence of cranial asymmetry in healthy newborns, Pediatrics 110 (2002) e72. [15] L. Pogliani, C. Mameli, V. Fabiano, G.V. Zuccotti, Positional plagiocephaly: what the pediatrician needs to know. A review, Childs Nerv. Syst. 27 (2011) 1867–1876.
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[19] J.L. Vazquez, M.A. Pombar, J.M. Pumar, V.M. del Campo, Optimised low-dose multidetector CT protocol for children with cranial deformity, Eur. Radiol. 23 (2013) 2279–2287. [20] D. Agrawal, P. Steinbok, D.D. Cochrane, Diagnosis of isolated sagittal synostosis: are radiographic studies necessary? Childs Nerv. Syst. 22 (2006) 375–378. [21] J.A. Fearon, D.J. Singh, S.P. Beals, J.C. Yu, The diagnosis and treatment of single-sutural synostoses: are computed tomographic scans necessary? Plast. Reconstr. Surg. 120 (2007) 1327–1331. [22] J.E. Baumgartner, K. Seymour-Dempsey, J.F. Teichgraeber, J.J. Xia, A.L. Waller, J. Gateno, Nonsynostotic scaphocephaly: the so-called sticky sagittal suture, J. Neurosurg. Pediatr. 101 (2004) 16–20.
Contents lists available at ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Ultrasonography for the diagnosis of craniosynostosis Maïa Proisy a,b,∗ , Laurent Riffaud c , Kamal Chouklati a , Catherine Tréguier a , Bertrand Bruneau a a b c
CHU Rennes, Department of Radiology, Hôpital Sud, F-35203 Rennes, France INSERM U1228 VisAGeS Unit, CNRS UMR 6074, Université de Rennes 1, F-35042 Rennes, France CHU Rennes, Department of Neurosurgery, CHU de Rennes, F-35033 Rennes, France
a r t i c l e
i n f o
Article history: Received 17 December 2016 Received in revised form 9 March 2017 Accepted 15 March 2017 Keywords: Craniosynostosis Ultrasound Nonsynostotic plagiocephaly Infant Skull Positional plagiocephaly
a b s t r a c t Objectives: The aim of this study was to report our experience with ultrasonography in our routine practice for the diagnosis of cranial deformity in infants. Methods: We conducted a single-institution retrospective study of infants referred to our department because of skull deformity. We only included in this study infants having undergone both US and 3D-CT to ensure accurate comparisons. Each cranial suture was described as normal or closed (partial or complete closure). Sonography examination results were correlated with 3D-CT findings as a gold-standard. Results: Forty infants were included with a mean age of 5.2 ± 4.9 months. Thirty had a craniosynostosis and 10 children had a postural deformity with normal sutures. Correlation between US and 3D-CT for the diagnosis of normal or closed suture had a specificity and a sensitivity of 100%. US examination for the diagnosis of complete or incomplete synostosis had a sensitivity of 100%. Conclusions: Cranial US is an effective technique to make a positive or negative diagnosis of prematurely closed suture. US examination of sutures is a fast and non-radiating technique, which may serve as a first-choice imaging modality in infants with skull deformity. © 2017 Elsevier B.V. All rights reserved.
1. Introduction Cranial deformity is common in children. The 2 main causes remain positional plagiocephaly and craniosynostosis. Positional plagiocephaly is becoming more and more frequent since recommendations to place infants on their backs for sleeping in order to prevent sudden infant death syndrome. On the contrary, craniosynostosis caused by the premature closure of one or more sutures of the cranial bones is a much more uncommon condition occurring in only 3–6 infants per 10,000 live births [1]. Consequences of these 2 deformities may be very different as craniosynostosis may lead to severe chronic intracranial hypertension and thus need surgical correction. Differential diagnosis between these 2 malformations sometimes remains challenging. Although physical examination is sufficient to differentiate craniosynostosis and deformational plagiocephaly in most cases, cranial imaging is still regularly needed
to confirm the diagnosis especially for non-specialized practitioners [1]. Conventional cranial X-ray has traditionally been the first imaging modality but its interpretation is particularly demanding and it is a source of radiation. Three-dimensional computed tomography (3D-CT) has high diagnosis accuracy, and is considered as the gold standard [2] but acquisition may need sedation and it is also a source of radiation. Very recently, ultrasonography (US) has been proposed to assist practitioners in the diagnosis of craniosynostosis with excellent efficiency [3,4]. However, although US has multiple advantages such as low cost and non-ionising technique few studies have as yet been conducted [5–10]. To date US is not yet considered as a screening tool for craniosynostosis. The aim of this study was to report our experience with US in our routine practice for the diagnosis of cranial deformity in infants and to demonstrate its high accuracy in the diagnosis of craniosynostosis.
2. Materials and methods Abbreviations: 3D-CT, three dimensional computed tomography; US, Ultrasound. ∗ Corresponding author at: CHU Rennes, Department of Radiology, Paediatric Imaging, Hôpital Sud, 16 Boulevard de Bulgarie, BP 90347, 35203 Rennes Cedex 2, France. E-mail address: [email protected] (M. Proisy). http://dx.doi.org/10.1016/j.ejrad.2017.03.006 0720-048X/© 2017 Elsevier B.V. All rights reserved.
2.1. Study group We conducted a single-institution retrospective study between 2004 and 2014 in our paediatric radiology department. During
M. Proisy et al. / European Journal of Radiology 90 (2017) 250–255
251
Fig. 1. Diagnostic approach of craniosynostosis in Rennes University Hospital for children under 8 months old.
this period, infants that were referred to our department by a general practitioner or a paediatrician for skull deformity and suspicion of craniosynostosis underwent both a cranial US and a plain radiography or 3D-CT according to the practitioner’s prescription. Ultrasonography was performed in all cases by one of the paediatric radiologist from our department (CT, BB, KC with respectively 30, 15 and 10 years of experience). Given the US experience acquired during the first 7 years, we changed our practice after 2011 in agreement with the paediatric neurosurgeon (LR). After this date, US was performed as a first-line radiological examination in cases of suspicion of craniosynostosis and considered as an alternative to classic plain radiography or 3D-CT for the diagnosis of craniosysnostosis (Fig. 1). For this retrospective study, we only included infants having undergone both US and 3D-CT in order to compare the sutures in the most reliable manner. We considered that comparison of all the sutures was not possible with plain radiography. Each child was examined first by US and then by 3D-CT. The study was approved by the local ethics committee and did not require informed consent from the relatives. 2.2. Ultrasonography procedure All US examinations were performed on a Philips HDI 5000 Sonoct from 2004 to 2008, then a Philips IU 22 machine from 2008 onwards (Philips Medical System, The Netherlands) using a high frequency linear transducer (12,5 and/or 17,5 MHz transducer). The probe was positioned perpendicular to the expected linear course of the suture. Coronal, sagittal, lambdoïd and metopic sutures were systematically analysed. During US examination, the cranial sutures were followed along their whole length. A cranial suture was considered as normal (patent suture) if a hypoechoic gap was identified between two hyperechoic bony plates, with end-to-end appearance or bevelled or overlapped
appearance [3]. A suture was considered closed (synostosed suture) if there was a loss of hypoechoic fibrous gap between bony plates [4]. Paediatric radiologists paid particular attention to partial or complete closure of sutures. Image and video recordings were systematically performed during examination and reviewed for comparison with 3D-CT findings. 2.3. CT acquisition All CT examinations were performed using the same 16-slice multidetector CT (Philips Brilliance, Cleveland, Ohio, USA) with a stereotyped protocol. The imaging parameters used were as follows: tube voltage 120 kV, tube current 100 mAs, collimation 16 × 0.75, pitch 0.688, rotation time 0.5 s, slice thickness 0.8 mm, increment 0.4 mm. 3D-CT volume rendering reconstruction were systematically performed. 2.4. Data analysis Sonography examination was correlated with 3D-CT findings as a gold-standard. The sensitivity, specificity, positive and negative predictive values of ultrasound for the diagnosis of craniosynostosis was calculated. 3. Results 3.1. Study group description A total of 40 infants were finally included. There were 7 girls and 33 boys. Thirty children had a craniosynostosis including 20 scaphocephaly, 4 trigonocephaly, 3 plagiocephaly, 2 brachycephaly, and 1 atypical craniosynostosis. The case of atypical craniosynostosis was one case with both sagittal and left coronal suture synostosis. Ten children had a postural deformity with
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normal sutures including 8 positional plagiocephaly and 2 nonsynostotic scaphocephaly. The mean age of the 40 children was 5.2 ± 4.9 months. There was no significant difference between ages in the craniosynostosis group (mean age = 4.9 ± 5.0 months) and in the postural deformity group (mean age = 6.0 ± 4.8 months) (p = 0.50). 3.2. US accuracy for the diagnosis of craniosynostosis Correlation between US and 3D-CT for the diagnosis of normal or closed suture was excellent. Cranial US for the diagnosis of a closed suture had a specificity of 100%, a sensitivity of 100%, positive and negative predictive values of 100% and 100%. 3.3. US accuracy for the diagnosis of complete/incomplete synostosis The correlation between US and 3D-CT for the diagnosis of complete or incomplete synostosis was excellent. There was a sensitivity of 100%. 3.4. Case illustrations Figs. 2–5 . 4. Discussion During recent years, the incidence of positional plagiocephaly in young children has increased by up to 20% [11] due to recommendations to position infants on their back [12]. Thus, it is now a frequent finding [13,14]. In such cases, it is important to exclude craniosynostosis. Although diagnosis of positional plagiocephaly could be assessed by physical examination with some typical features such as trapezoidal head shape, mastoid bulge, tilt of the cranial base and pushed-forwards ear position [15], clinical differentiation with isolated unilateral lambdoid or coronal synostosis could be difficult, especially for general practitioners. A CT scan is then considered as the gold standard to distinguish these cranial deformities but it requires sedation in young children and exposure to ionizing radiations in this more radiosensitive population [16,17]. For this last reason, several studies have investigated the impact of dose reduction on image quality for specific 3D-CT protocols [18,19] but alternative procedures without any ionizing radiations should be considered. Sonographic appearance and measurement of normal major cranial sutures in neonates and infants were first described in 1997 [3] and high-resolution sonography of the abnormal cranial suture was described one year later by the same author [4]. Only a few studies have shown the effectiveness of US in craniosynostosis. So far, US is not yet used as a routine screening tool. Its use in diagnosing craniosynotosis would become far more common if more specifically adapted examinations were requested and carried out. Sze et al. [5] demonstrated that sonography of the lambdoid sutures had excellent results as a screening test of lambdoid sutural patency among 41 children. In another study concerning 100 paediatric patients who were admitted with an abnormal head shape suggesting deformational plagiocephaly, Regelsberger et al. [9] described that patency of the lambdoid sutures was confirmed by US in 99 cases. In one patient, partial synostosis was diagnosed. Further reports demonstrated that US was an effective method for the other sutures [6,7,10]. In our study, cranial US for the diagnosis of a closed suture had a specificity of 100% and a sensitivity of 100%. These results are similar to those of another recent study [8], but we also evaluated complete or incomplete closure of the sutures with a sensitivity of 100%. For these reasons, we think that US is an effective and reliable technique which may serve as a first imaging tool when
Fig. 2. Posterior positional plagiocephaly in a 4-month-old boy. Vertex view of 3DCT (A) shows the head shape and demonstrates the parallelogram appearance of the skull. The US image of the left coronal suture performed at the level of the blue line positioned on the 3D-CT shows the hypoechoic gap between hyperechoic calvarial bones (B). Lambdoid sutures were also patent on US examination and 3D-CT (not shown on this Figure).
a clinical diagnosis of craniosynostosis is suspected. Moreover, US has many advantages: it is a fast, non-ionising technique that does not require any sedation. However, there are some limitations with US examination. Ultrasound imaging is often described as an “operator-dependent” technique. Although education of radiologists is recommended, imaging of the cranial sutures is relatively easy to learn. Furthermore, this method did not show any interobserver variability between two independent investigators in Regelsberger et al’s study [9]. Another limitation of US is the inability to assess sutural patency after a certain age. In our experience, the earlier the US is performed the more reliable the examination is. Reliability of US decreased with age because of hair growth, skull growth and thinner sutures, especially coronal sutures. According to our experience, US is limited by age with the upper limit at 8 months old. Regelsberger et al. considered the age limit of 13 months [9] for the technique and Sze et al. [5] were able to distinguish patent from fused sutures in one patient scanned at 18 months. As most children with cranial deformity are usually seen before the age of 10 months, we recommend carrying out US examination as soon as possible when diagnosis is suspected, ideally before the age of 8 months. Special attention must be paid to the metopic suture.
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Fig. 3. Unilateral coronal synostosis in a 2-month-old boy. Antero-superior 3D-CT view (A) shows the elevated left orbital roof and the complete fusion of the left coronal suture. The US image performed at the level of the blue line positioned on the 3D-CT shows the synostosed left coronal suture with a continuous hyperechoic calvarian bone and no hypoechoic gap (B).
Indeed, physiological closure of this suture occurs much earlier than the others. As fusion normally arises between the age of 3 and 9 months [20], complete fusion of the metopic suture does not necessary mean trigonocephaly. Typical triangular frontal deformation and hypotelorism should also be associated with complete fusion of this suture to diagnose trigonocephaly with certainty. 3D-CT is an important imaging technique in diagnosis of craniosynostosis. However, 3D-CT should not be used as a first tool imaging procedure as is still the case in many centres. We consider that it should concern only children with uncertain clinical situations and those with positive findings at US as a preoperative planning. Regarding preoperative surgical planning in our institution, 3D-CT examination was only performed in cases of metopic, coronal or complex craniosynostosis. US demonstrated diagnosis of craniosynostosis in an initial step and then allowed us to wait for the right moment to perform 3D-CT (one month before surgery). Furthermore, we considered that a child with a charac-
Fig. 4. Scaphocephaly in a 1-month-old boy. Superior view of the 3D-CT (A) shows the particular head shape with elongated cranium and the sub-total sagittal synostosis, with the corresponding US images (B) showing a continuous hyperechoic bone at the anterior part of the suture, with bridging at the half-posterior part and a very small part of the posterior patent suture with persistence of an hypoechoic gap.
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teristic nonsyndromic scaphocephaly and a positive US for sagittal synostosis should be operated on without additional imaging studies. In the literature some authors suggest that operative correction of isolated sagittal synostosis can proceed without any radiological investigations, unless clinical examination exhibits atypical features [20]. Considering potential side effects from ionizing radiation, risks of sedation, and costs, Fearon et al. [21] also suggested that surgeons should reserve computed tomographic scans for infants in whom physical examination was not clear. Finally and regarding literature [22] and our 2 cases of nonsynostotic scaphocephaly (illustration: case 5), we advise that craniosynostosis should always be confirmed by radiological imaging except for typical positional plagiocephaly, with US as a first step diagnosis. 5. Conclusion US examination of sutures is a fast, effective and non-irradiating technique that may serve as a first choice imaging modality in infants (particularly under 8 months old) with skull deformity when craniosynostosis is suspected. In our study, we demonstrated that US was an effective technique for positive diagnosis of a prematurely closed suture. Diagnosis of craniosynostosis can be ruled out if US examination of the entire coronal, sagittal and lambdoid sutures demonstrates normal patent sutures. 3D-CT should only be recommended either in atypical cases or in a pre-operative setting when the diagnosis of craniosynostosis has been acquired on US examination. Thus 3D-CT could be organised at the appropriate time before surgery according to the surgeon’s recommendations in order to optimize surgical planning. References
Fig. 5. Nonsynostotic scaphocephaly in a 10 month-old boy. Vertex view of the 3D-CT shows the head deformity with an elongated cranium suggestive of scaphocephaly but patent coronal, sagittal and lambdoid sutures. Corresponding US images at the level of blue lines show patent sutures with persistence of a hypoechoic gap between calvarial bones (B).
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