Shape and Volume of Craniofacial Cavities in IntentionalSkull Deformations

R.H. Khonsari,1,2* M. Friess,3 J. Nysj€o,4 G. Odri,5 F. Malmberg,4 I. Nystr€om,4 E. Messo,6

J.M. Hirsch,6 E.A.M. Cabanis,7 K.H. Kunzelmann,8 J.M. Salagnac,1 P. Corre,1 A. Ohazama,2

P.T. Sharpe,2 P. Charlier,9 and R. Olszewski10

1Service de Chirurgie Maxillofaciale et Stomatologie, CHU Hotel-Dieu, Nantes, France2Department of Craniofacial Development and Stem Cell Research, Dental Institute, King’s College London, UK3D�epartement Hommes, Natures, Soci�et�es & CNRS UMR 7206, Mus�eum National d’Histoire Naturelle, Mus�ee del’Homme, Paris, France4Centre for Image Analysis, Uppsala University, Uppsala, Sweden5Clinique Chirurgicale Orthop�edique et Traumatologique, CHU Hotel-Dieu, Nantes, France6Department of Surgical Sciences, Oral and Maxillo-facial Surgery, Medical Faculty, Uppsala University, Uppsala,Sweden7Service de Neuroradiologie, Centre Hospitalier National Ophtalmologique des XV-XX, Paris, France8Poliklinic f€ur Zahnerhaltung und Parodontologie, Ludwig-Maximilians-Universit€at, M€unich, Germany9Service d’anatomopathologie, Hopital Raymond-Poincar�e, Garches, France10Service de Chirurgie Maxillofaciale et Stomatologie, Hopital Saint-Luc, Universit�e Catholique de Louvain,Bruxelles, Belgique

KEY WORDS orbit; maxillary sinus; bone thickness; haptic-aided semi-automaticsegmentation; intracranial volume; intentional skull deformation

ABSTRACT Intentional cranial deformations (ICD)have been observed worldwide but are especially preva-lent in preColombian cultures. The purpose of this studywas to assess the consequences of ICD on three cranialcavities (intracranial cavity, orbits, and maxillarysinuses) and on cranial vault thickness, in order toscreen for morphological changes due to the externalconstraints exerted by the deformation device. Weacquired CT-scans for 39 deformed and 19 control skulls.We studied the thickness of the skull vault using quali-tative and quantitative methods. We computed the vol-umes of the orbits, of the maxillary sinuses, and of theintracranial cavity using haptic-aided semi-automaticsegmentation. We finally defined 3D distances andangles within orbits and maxillary sinuses based on 27

anatomical landmarks and measured these features onthe 58 skulls. Our results show specific bone thicknesspatterns in some types of ICD, with localized thinning inregions subjected to increased pressure and thickeningin other regions. Our findings confirm that volumes ofthe cranial cavities are not affected by ICDs but that theshapes of the orbits and of the maxillary sinuses aremodified in circumferential deformations. We concludethat ICDs can modify the shape of the cranial cavitiesand the thickness of their walls but conserve their vol-umes. These results provide new insights into the mor-phological effects associated with ICDs and call forsimilar investigations in subjects with deformational pla-giocephalies and craniosynostoses. Am J Phys Anthropol000:000–000, 2013. VC 2013 Wiley Periodicals, Inc.

Intentional cranial deformations (ICD) are describedin all cultures (Dingwall, 1931) including WesternEurope. By applying an external device on the skull ofnewborns during early childhood, the purpose of thispractice was to interfere with normal skull growth andinduce the appearance of a specific skull outline(Gerszten et al., 1995AQ1 ). Two main deformation types aredescribed in South American preColombian cultures: theanteroposterior deformation (AP, Fig.F1 1a), where theskull was squeezed between two rigid frontal and occipi-tal plates held together by bands, and the circumferen-tial deformation (C, Fig. 1b) where the skull was moldedinto a tubular shape by tight cloths (Dingwall, 1931;Ant�on, 1989). In France, a specific kind of skull deforma-tion is known as the Toulouse deformation (T) and isobtained by mechanisms similar to C deformations(Broca, 1871; Dingwall, 1931).

The morphological correlates of ICD, mainly in theface and base, have been the subject of previous studies,though reported findings are not always in agreement.Briefly put, in AP deformed skulls the growth

restrictions imposed by the deforming device lead to lat-eral expansion of the vault, whereas C type deforma-tions result in postero-superior vault expansion. Several

Additional Supporting Information may be found in the onlineversion of this article.

R.H. Khonsari and M. Friess contributed equally to this work.

Grant sponsor: Fondation Les Geules Cass�ees.

*Correspondence to: Roman H. Khonsari, Service de ChirurgieMaxillofaciale et Stomatologie, Centre Hospitalier Universtaire deNantes, 1 place Alexis Ricordeau, 44000 Nantes, France. E-mail:roman.khonsari@kcl.ac.uk

Received 24 April 2012; accepted 19 February 2013

DOI: 10.1002/ajpa.22263Published online 00 Month 2013 in Wiley Online Library

(wileyonlinelibrary.com).

� 2013 WILEY PERIODICALS, INC.

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 00:000–000 (2013)

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studies have reported changes in basicranial flexion,facial height and width, orbital height and facial progna-thism in one or both deformation types, and differencesin classification systems may account for some of the dif-ferences in reported effects (see reviews in Anton, 1989;Friess and Baylac, 2003). Very few studies have investi-gated effects on internal structures. Grupe (1984) founddilated diploic veins in circumferentially deformedskulls, which are also reported in AP deformed skulls(Dean, 1995; O’Loughlin, 1996).

The pathological consequences of ICD are poorlyunderstood, due to the lack of modern medical data onindividuals subjected to this practice. The main health-related question with ICDs is the risk of cognitiveimpairment (Lekovic et al., 2007), and this issue is stillnot solved. We focused our study on the cranial cavitiesand on their walls. We first explored the consequences ofskull deformations on three medically relevant craniofa-cial structures by measuring the volumes of the intra-cranial cavity, of the orbits and of the maxillary sinuses.We used an innovative technique based on haptic-aidedsemi-automatic segmentation (Nystr€om et al., 2011). Wethen analyzed modifications in the thickness of the skullvault and described the 3D structure of the orbits andthe maxillary sinuses.

The conservation of the volumes despite changes in3D shape illustrated the fact that skull growth modulescan adapt to abnormal external constraints. We

described typical modifications in shapes and bone thick-ness that could be related to specific deformation types.

MATERIAL AND METHODS

The study sample consisted of 19 nondeformed (NC)skulls, 24 skulls with antero–posterior (AP, Fig. 1a)deformations, 8 skulls with circumferential (C, Fig. 1b)deformations, and 7 skulls with Toulouse (T) deforma-tions. This classification followed previously proposeddefinitions of circumferential and antero–posterior defor-mations (Ant�on, 1989; Cheverud et al., 1992; Kohnet al., 1993; Friess and Baylac, 2003). The Toulouse-typeis akin to circumferential deformations in that it isachieved by head banding and results in a similar shape(Broca, 1871). For the purposes of this study, it was con-sidered a separate group. All AP and C deformed skullswere from Bolivia, while all T types were from south-western France. Undeformed skulls were sampled fromthe same two regions. All skulls are part of the collec-tions of the Mus�ee de l’Homme in Paris.

Only adult individuals, selected based on the fusion ofthe spheno-occipital synchondrosis, were included. Infor-mation on sex was not generally available, and thereforenot taken into account in our analyses. Each skull wassubjected to paleopathological examination in order torule out craniosynostoses (based on the patency of skullvault sutures), trauma sequelae (Fig. 1c), and

Fig. 1. (a) antero–posterior deformation; (b) circumferential deformation; (c) zygomatic bone fracture (arrow); (d) taphonomicdeformation witnessed by a postnatal spacing of the squamosal suture (arrow).

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taphonomic deformations (Fig. 1d). The skulls werescanned using a standard medical CT-scan according toa previously published protocol adapted to anthropologi-cal material (Badawi-Fayad et al., 2005 and Table S1).

To study the shape of the orbit, we defined 12 3Dlandmarks: posterior choanae (1), anterior nasal spine(2), lacrimal canal (3), fronto-zygomatic suture (4),fronto-nasal suture (5), superior orbital fissure (antero–superior end) (6), superior orbital fissure (postero–inferior end) (7), anterior clinoid process (8), medialinferior orbital fissure (9), foramen caecum (10), planumsphenoidale (11), and small wing of the sphenoid (12).All landmarks except the anterior nasal spine (2) werebilateral.F2 Details on the 3D anatomical position of thelandmarks are given in Figure 2 and TableT1 1. The land-marking and the measurements were performed usingMaxilim (Medicim, Leuwen, Belgium) according toOlszewski et al. (2008) and Olszewski et al. (2010). Thesame procedure was applied to the maxillary sinuses, forwhich 2 specific landmarks were defined: the incisivecanal (13) and the infra-orbital groove (14) (Fig. 2 andTable 1). The following 4 landmarks defined for theorbital analysis were also used for the sinuses: posteriorchoanae (1), anterior nasal spine (2), lacrimal canal (3),and medial inferior orbital fissure (9).

After having defined the landmarks anatomically, wetested the reliability of their placement by using the 3Dcoordinates of the landmarks from a subset of 10 normalskulls in order to calculate the Euclidian distancebetween two successive measurements made on eachskull by the same observer (Richtsmeier et al., 1995;Olszewski et al., 2008; Plooij et al., 2009; Olszewskiet al., 2010). We checked if this distance was smallerthan an anatomically relevant threshold of 1.5 mm usinga one-tailed Student t-test.

The 23 orbital landmarks (11 bilateral and one unilat-eral) were used to define 6 planes (Table T22). On the basisof these 6 planes and the previously defined landmarks,5 angles and 8 distances were measured (Table T33). The 9sinus landmarks (4 bilateral and one unilateral) wereused to define 3 planes (Table 2) and 3 distances (Table3). To test for the intra-observer reliability of the orbitaldistances and angles, we first computed the intraclasscorrelation coefficient using two-way random singlemeasures for absolute agreement (ICC 2.1 model, Shroutand Fleiss, 1979 AQ2) based on two successive landmarkingsby the same observer. We then computed the intraclasscorrelation coefficient for the inter- and intra-observerreliabilities of the sinus distances based on two land-markings by two blinded independent observers (RHKand RO).

To analyze the angle and distance values statistically,due to the small number of skulls in the C and T groups,we used the Kruskal–Wallis (KWT) one-way analysis ofvariance by ranks as a nonparametric alternative to theone-way analysis of variance (ANOVA) and the Dunnettpost hoc test (DT) in order to spot the group with dis-criminant values as compared to the nondeformed group.The difference was considered significant when P< 0.05.The difference was defined as a tendency when0.05<P< 0.1.

The total thickness of the skull vault was measuredand plotted using the Wall Thickness Analysis moduleof VGStudio Max (Volume Graphics, Heidelberg,Germany). Briefly, the skulls were cropped along a hori-zontal plane passing anteriorly above the frontal sinusand posteriorly above the external occipital protuber-ance. For each skull, the average total thickness, itsstandard deviation and the skull vault volume werecomputed within this spherical skull cap. The volume

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Fig. 2. Skeletal landmarks used for orbit and sinus cephalometry. Posterior choanae (1), anterior nasal spine (2), lacrimal canal(3), fronto-zygomatic suture (4), fronto-nasal suture (5), superior orbital fissure (antero-superior end) (6), superior orbital fissure(postero-inferior end) (7), anterior clinoid process (8), medial inferior orbital fissure (9), foramen caecum (10), planum sphenoidale(11), small wing of the sphenoid (12), incisive canal (13), infra-orbital groove (14). See Table 1 for anatomical details.

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corresponding to the vault bones was computed by con-sidering the space between the external limit of theouter table and the internal limit of the inner tablealong the cropped spherical cap. A red-green-blue(respectively 0–15-30 mm) continuous color map forthickness values was plotted over the 3D rendering ofthe spherical cap.

Discrete measurements of thickness using the CT-scandata were also performed. For each skull we definedthree planes (mid-sagittal, sub-coronal through meto-pion, and sub-coronal through vertex). The mid-sagittalplane was defined as going through nasion, bregma, andbasion; the coronal planes were defined as perpendicular

to the mid-sagittal plane and rotated to fit throughmetopion/vertex. Thickness measurements wereobtained following the half-maximum-height (HMH) pro-tocol (Spoor et al., 2011 AQ3). This standard technique relieson the computation of the limit between two tissues (orone tissue and air) as the median threshold value on theHounsfield scale. Measurements were taken by a singleobserver (MF) at metopion, center of the frontal and pa-rietal, and the highest point above the lambda-inionchord. Computations were performed in ImageJ (Ras-band, 1997–2012).

The volume of the orbits was obtained using a haptic-aided semiautomatic segmentation method (Nystr€om

TABLE 1. Skeletal landmarks used for orbit and sinus measurements

Number Name Definition Type

1 Posterior choanae Lower lateral corner of the posterior choanae At the junctionbetween the palatine bone and the pterygoid process

Orbit and sinus-bilateral

2 Anterior nasal spine Pointed process at the tip of the maxilla Overlying themaxillary notch on the midline

Orbit and sinus-unilateral

3 Lacrimal canal Antero-lateral border of the orbital opening of thenaso-lacrimal duct At the junction between thelacrimal bone and the maxillary bone

Orbit and sinus-bilateral

4 Fronto-zygomatic suture Orbital border of the fronto-zygomatic suture At theintersection with the naso-maxillary suture

Orbit-bilateral

5 Fronto-nasal suture Orbital border of the fronto-nasal suture Correspondsto the highest concavity of the lateral orbital rim

Orbit-bilateral

6 Superior orbital fissure(antero–superior end)

Upper lateral tip of the superior orbital fissure At thejunction between the lesser and the greater wingsof the sphenoid bone

Orbit-bilateral

7 Superior orbital fissure(postero–inferior end)

Lower medial tip of the superior orbital fissure At thejunction between the maxillary and the zygomatic bones

Orbit-bilateral

8 Anterior clinoid process Infero-lateral aspect of the anterior clinoid process On thelesser wing of the sphenoid, lateral to the optic canal

Orbit-bilateral

9 Medial inferior orbitalfissure

Most anterior concavity of the inferior orbital fissure Onthe orbital surface of the zygomatic bone

Orbit-bilateral

10 Foramen caecum Lower end of the frontal crest of the frontal bone At thejunction with the ethmoid bone on the skull base

Orbit-bilateral

11 Planum sphenoidale Upper surface of the lesser wing of the sphenoid bone Onthe highest concavity of upper border of the optic canal

Orbit-bilateral

12 Small wing of thesphenoid

Lateral border of the small wing of the sphenoid bone Atthe junction with the orbital plate of the frontal bone

Orbit-bilateral

13 Incisive canal Anterio–medial border of the incisive canal On thesurface of the maxillary sinus

Sinus-bilateral

14 Infra-orbital groove Lateral aspect of the infra-orbital groove On the posteriorborder of the orbital surface of the maxilla

Sinus-bilateral

The numbers correspond to the legend of Figure 2.

TABLE 2. Orbital and sinus planes defined using 23 skeletal landmarks for the orbits and 9 skeletal landmarks for the sinuses(see Fig. 2 and Table 1 for the anatomical definition of the landmarks)

Name Definition Type

Horizontal maxillaryplane

Anterior nasal spine, right posterior choane, left posterior choane Plane defined by 3 points

Orbital floor Lacrimal canal, superior orbital fissure (postero–inferior end),medial inferior orbital fissure

Plane defined by 3 points

Lateral orbital wall Superior orbital fissure (antero–superior end), superior orbitalfissure (postero–inferior end), medial inferior orbital fissure

Plane defined by 3 points

Orbital roof Foramen caecum, planum sphenoidale, small wing of the sphenoid Plane defined by 3 pointsMedial orbital wall Superior orbital fissure (antero–superior end), anterior clinoid

process, fronto–maxillary suturePlane defined by 3 points

Anterior orbital wall(virtual boundary)

Fronto–maxillary suture, fronto–zygomatic suture, perpendicularto the horizontal maxillary plane

Plane defined by 2 points andperpendicular to another plane

Anterior sinus wall Right lacrimal canal, left lacrimal canal, perpendicular to thehorizontal maxillary plane

Plane defined by 2 points andperpendicular to another plane

Medial sinus wall Posterior choane perpendicular to the horizontal maxillaryplane perpendicular to the anterior sinus wall

Plane defined by 1 point andperpendicular to 2 other planes

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et al., 2011). In brief, we first extracted the boundariesof the orbital bones by using hysteresis thresholding fol-lowed by morphological boundary extraction. The thresh-olds we used in this step were based on the Hounsfieldnumbers for bone tissue (values: 70–90). Using a haptic3D input device (Table S2), we then placed four land-marks on the orbital rim. These landmarks were subse-quently used to calculate a planar barrier that definedthe anterior limit of the orbital cavity. The resulting bar-rier was rasterized and included into the boundary map.We proceeded by computing a distance potential forcefrom the modified boundary map and initialized a de-formable simplex mesh as a coarse sphere inside theorbit. This simplex mesh was then automaticallydeformed by the distance potential force to fit the orbit.During the deformation process, we could refine the sim-plex mesh one or several times and also apply hapticforces on selected mesh faces to guide or correct the seg-mentation. As a final step, we rasterized the simplexmesh and calculated the orbital volume. The procedureis summed up in FigureF3 3. The same segmentationmethod, but without the landmark positioning step, wasused to compute the maxillary sinus and intracranialvolumes, as no artificial limit such as the one requiredfor the orbital opening had to be defined for these twocavities. The inter- and intra-individual reproducibilitiesof the orbit volume measurements provided by the seg-mentation have been previously assessed and comparedto manual segmentation (Nystr€om et al., 2011).

RESULTS

The qualitative analysis of the vault thickness showedconstant frontal bone thinning in AP skulls when com-pared with ND controls (Fig.F4 4). Furthermore, we founda characteristic notch at the level of the bregma in Cdeformations (Fig.F5 5) that was not observed in any othergroup and associated with a lateral parietal and tempo-ral bone thinning. The T skulls did not present bonethickness modifications (Fig. 5). The comparison of

average thicknesses and vault volumes between groupsdid not show any significant differences. Nevertheless,there was a tendency for C skulls to have more dis-persed thickness values (KWT: 0.1003, DT: 0.0081, seeTable S3 for further details).

Interestingly, for AP deformations, discrete thicknessmeasurements showed a significant thinning at meto-pion in midline sagittal sections, affecting the outer(KWT: 0.0051, DT: 0.0092) and inner (KWT: 0.0417, DT:0.0234) tables, as well as the total thickness (KWT:0.0121, DT: 0.0329). The outer table (KWT: 0.0068, DT:0.0305) and the total thickness (KWT: 0.0197, DT:0.0124) were reduced in midline sagittal sections at theocciput for AP deformations. The total thickness of thefrontal bone was also reduced in coronal sections for Cdeformations (KWT: 0.0007, DT: 0.0011) and had a tend-ency toward reduction for AP deformations (KWT:0.0007, DT: 0.0635). The parietal bone thickness waspreserved in all deformed skulls. In T deformations, weobserved an increase in the thickness of the diploe atthe metopion (KWT:0.0055, DT: 0.0133). See Table S4 forfurther details.

Volumes of the orbits and the maxillary sinuses werenot affected in AP, C, or T deformations. The volume ofthe cranial cavity was overall normal but there was atendency toward increased volume in C skulls (KWT:0.0813, DT: 0.0296). Further details are provided in Ta-ble S5.

We confirmed the inter- and intra-individual reprodu-cibilities of the measured distances for the sinuses andthe intra-individual reproducibility of the measured dis-tances and angles for the orbits (Tables S6, S7, and S8).We also confirmed the inter-individual reproducibility oflandmark placement in 3D (Table S9). On the basis ofthese landmarks, we found that the shape of the orbitswas significantly modified in C deformations (full detailsin Table S10). Briefly, we described a bilateral increasein the vertical orbital angle (KWT: 0.0085, DT: 0.0003for the left angle and KWT: 0.0302, DT: 0.0017 for theright angle). We also found bilateral decreases in the

TABLE 3. Angles and distances used in orbital and sinus measurements

Name Definition Type

Medio-lateral orbital angle Median orbital wall lateral orbital wall Angle between 2 planesMedian orbital angle Left medial orbital wall right medial orbital wall Angle between 2 planesVertical orbital angle Orbital roof orbital floor Angle between 2 planesRelative lateral orbital angle Lateral orbital wall orbital floor Angle between 2 planesRelative medial orbital angle Medial orbital wall orbital floor Angle between 2 planesAnterior orbital width Fronto–zygomatic suture fronto–nasal suture Distance between 2 pointsLateral orbital depth Fronto–zygomatic suture superior orbital

fissure (postero–inferior end)Distance between 2 points

Median orbital depth Fronto–maxillary suture superior orbitalfissure (postero–inferior end)

Distance between 2 points

Deep orbital height Superior orbital fissure (postero–inferiorend) orbital roof

Distance between a point and a plane

Sphenoidal orbital height Medial inferior orbital fissure orbital roof Distance between a point and a planeAnterior orbital height Lacrimal canal orbital roof Distance between a point and a planePosterior orbital width Superior orbital fissure (antero–superior

end) lateral orbital wallDistance between a point and a plane

Central orbital depth Superior orbital fissure (postero–inferiorend) anterior orbital wall

Distance between a point and a plane

Medial sinus depth Posterior choane anterior sinus plane Distance between a point and a planePosterior sinus width Medial inferior orbital fissure medial

sinus wallDistance between a point and a plane

Anterior sinus height Lacrimal canal horizontal maxillary plane Distance between a point and a plane

See Table 1, Table 2, and Figure 2 for the anatomical definition of the landmarks and the planes.

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anterior orbitals width (KWT: 0.0014, DT: 0.0001 for theleft width and KWT: 0.0023, DT: 0.0001 for the rightwidth), in the lateral orbital depth (KWT: 0.0009, DT:0.0023 for the left depth and KWT: 0.0032, DT: 0.0012for the right depth), in the median orbital depth (KWT:0.0236, DT: 0.0489 for the left depth and KWT: 0.0027,DT: 0.0056 for the right depth) and deep orbital heights

(KWT: 0.0191, DT: 0.0182 for the left height and KWT:0.0143, DT: 0.0729 for the right height).

The overall shape of the orbit in C deformations wasreduced mediolaterally. Orbital height was increasedanteriorly but decreased posteriorly.

This deformation pattern was also partly found in APdeformations, where a decrease in the lateral orbital

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Fig. 3. Semiautomatic orbit segmentation. (a) Haptic-aided landmarking used to define the anterior limit of the orbital cavity.(b) Initialization of a deformable mesh inside the orbit. (c) The mesh is fitted to the orbit by a distance potential force computedfrom the CT-scan. During the deformation process, the user can refine the mesh as well as reshape it by applying haptic interactiveforces on selected mesh faces (yellow patches). (d) Segmented orbit. (e) Rasterized segmentation result (purple) overlaid on themultiplanar reformatting visualization. (f) Snapshot of the segmentation interface developed by the Center for Image Analysis,Uppsala University, Sweden.

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depth was reported (KWT: 0.0009, DT: 0.0073 for the leftdepth and KWT: 0.0032, DT: 0.0218 for the right width)and in T deformations, where a decrease in the deep or-bital height was observed (KWT: 0.0191, DT: 0.0084 forthe left height and KWT: 0.0143, DT: 0.0129 for theright height).

For all deformation patterns, orbits had a tendency forbeing shallow, reduced mediolaterally with an anteriorincrease in height and a posterior decrease. Furtherdetails are provided in Table S10.

The posterior width of the maxillary sinuses wasdecreased in C deformations (KWT: 0.0126, DT: 0.0057for the left width and KWT: 0.0068, DT: 0.0378 for theright width). More details are provided in Table S11.

DISCUSSION

Orbital volume and shape in intentionaldeformations

The conservation of the orbital volume in ICD is not asurprise as the globe of the eye is the major determinantof this parameter (Enlow, 1968). Interestingly, in Cdeformations, the shape of the orbit is significantlymodified: the orbit is shallow and narrow as compared tonondeformed skulls. C deformations mainly affect thevertical dimension of the cranial part of the orbit, that isthe measures involving the sphenoid and the frontalbones, which is consistent with the fact that the

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Fig. 4. (a) Thickness maps in dorsal view for 11 nondeformed skulls compared with (b) 11 skulls with antero–posterior defor-mation. The antero-posterior deformed skulls show a constant thinning of the frontal region. The red-blue color scale refers to bonethickness: red stands for 0 mm and blue for 30 mm.

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Fig. 5. (a) Lateral thickness maps for 3 skulls of the nondeformed, (b) antero-posterior, (c) circumferential, and (d) Toulousegroups. The bregmatic bulging and the temporal thinning are apparent in the T group. The red-blue color scale refers to bonethickness: red stands for 0 mm and blue for 30 mm.

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deformational forces are applied on the skull and not onthe face. Furthermore, the modification of the orbitalshape in C deformations is consistent with the overallnarrowing and vertical extension of the face previouslyreported (Ant�on, 1989; Kohn et al., 1993).

Despite the absence of an effect on volumes, the signif-icant shape modifications we found in C deformationscan potentially induce variable degrees of exophthalmia,as the orbital volume is preserved while the orbitbecomes shallow and narrow. The same conclusion canbe drawn to a lesser extent for AP and T deformations,which exhibit lesser degrees of orbital deformation.

Interestingly, recent findings on Fgfr-associated cra-niofacial syndromes indicate that the results obtainedfrom the study of ICDs can only partially contribute tothe understanding of disorders such as Crouzon syn-drome. In fact, in a mouse mode of Crouzon syndrome,Mart�ınez-Abad�ıas et al. (2012) have shown that at birth,the eye globe volumes were significantly enlarged whencompared to those of unaffected littermates, indicatingthat exorbitism in this syndrome may result from disor-ders of both the orbit and the globe of the eye.

Influence of external forces onthe maxillary sinuses

The conservation of the volume of the maxillary sinusin C skulls is more surprising, knowing that we found asignificant decrease of the posterior width of this cavitydue to the deformation. In fact, it is generally believedthat maxillary sinuses are formed passively as a conse-quence of the growth of the surrounding structures(Enlow and Bang, 1965). Sinuses do not possess an innerstructure equivalent to the globe of the eye in the orbitthat would drive their growth and prevent their collapse(Rae and Koppe, 2008; Witmer and Ridgely, 2008AQ4 ), andthere is currently no intrinsic mechanism known toensure their pneumatization. Because of the sinus defor-mation we report, we would thus have expected adecrease in the volume of the maxillary sinuses.

In the case of C deformations, as the growth of themaxillary sinuses mainly occurs around the third year oflife (Enlow, 1968), the orbital deformation most probablyinfluenced sinus growth: the orbital floor being the sinusroof, the posterior mediolateral narrowing of the orbitcould account for the posterior narrowing of the maxil-lary sinus.

We show here that the volume of the maxillary sinusis maintained in situations of abnormal mechanicalstress, suggesting the presence of specific and unknownregulatory mechanisms for this parameter.

Effect of intentional deformationson intracranial structures

The intracranial volume is not decreased in ICDs andeven has a tendency for increasing in C deformations(KWT: 0.0813, DT: 0.0296). On the basis of this parame-ter, it thus seems unlikely that ICDs could directlyinduce an increase in intracranial pressure. Accordingly,cultural data are not in favor of a decrease in intellec-tual abilities due to ICDs (Dingwall, 1931). Neverthe-less, the conservation of the intracranial volume is notsufficient to affirm the absence of increase in intracra-nial pressure: it is known for instance that venous con-gestions due to compressions in the cranio-occipital jointcan lead to hydrocephalus by indirect mechanisms (DiRocco et al., 2011). Our data do not enable us to

comment on the cognitive status, but do not support theimpairment hypothesis either. More generally, the issueof cognitive impairment in ICDs is of particular interestwhen related to the same problem in patients with cra-niosynostosis. The conservation of the intracranial vol-ume in cases of ICD with extreme deformation (Figs.1a–1b) is in line with the fact that in craniosynostoses,hydrocephalus cannot be solely related to the deforma-tion of the skull. Interestingly, we have recently shownthat FGFR2-associated craniosynostoses are associatedwith temporal lobe overgrowth and malformations(Khonsari et al., 2012). This result indicates that intra-cranial volume measurements in such syndromes can beinfluenced by intrinsic intracranial factors independentfrom the sole skull deformations, and thus complicatingthe links between ICDs and craniosynostoses.

Bone thickness and deformation device

The qualitative analysis of the skull vault thickness indeformed skulls (Figs. 4 and 5) is of potential use in thereconstruction of the deformation device, if we hypothe-size that the regions with increased thinning are theregions where the device was exerting the highest pres-sure. In fact, in hydrocephalus, where durable and ex-cessive hydrostatic pressure is exerted on the inner sideof the skull vault, a deformation pattern known as gyralimpressions can appear, with numerous areas of bonethinning (Tuite et al., 1996; Sgouros, 2005). More inter-estingly, it has been shown in rats that self-activatinghydrogel expanders, used in reconstructive surgery toaugment soft-tissue space, induce localized thinning ofthe skull vault in the regions where the device exertsthe highest pressure (Stuehmer et al., 2009; von Seeet al., 2010), while the bone surrounding the expander isnot affected and keeps its normal thickness. These datasupport the use of thickness maps to reconstruct areaswhere deformation devices were exerting the highestpressures on the skull vault of children subjected toICDs. On the basis of our data, we can thus hypothesizethat in AP and C deformations, the devices were prefer-entially exerting frontal constraints (see Table S4 fordetails), which is in line with the cultural data on thedeformation devices used in preColumbian cultures(Dingwall, 1931). A specific coronal pattern is observedposterior to the bregma in C types, which is consistentwith the location of bandages from ethnographic descrip-tions (Flower, 1881). This postbregmatic sulcus has beendescribed by D’Orbigny (1839) as characteristic of cir-cumferentially deformed crania, whereas Dembo andImbelloni (1938) also note it in some AP skulls, whileemphasizing the great uncertainty in the position of thedeforming devices. Our limited sample size does notallow us to exclude its presence in AP deformed skulls,but we feel it is more plausible to reflect the impact ofsoft tissue bands along the coronal suture.

The thinning of the frontal bone in AP deformationswe observed graphically is supported by our quantitativedata, and affects the three layers of the vault. In skullswith moderate deformation and when the diagnosis ofICD is not straightforward, a local thinning of the boneoccurring in areas expected to have been subjected toabnormal pressures (such as the frontal bones in AP andC deformations) could be of help in screening for defor-mations. Interestingly, the preservation of the global vol-ume of the vault suggests that bone thicknessmodifications occur by a redistribution of a constant pool

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of vault bone rather by bone loss. This fact may accountfor the local increase of thickness we observed in Tskulls in the region of the metopion.

Intentional skull deformations, positionalplagiocephaly, and craniosynostoses

Currently, the most common cause of accidental or non-intentional skull deformation is positional posterior pla-giocephaly (Dec and Warren, 2011). The treatment ofpositional plagiocephaly is controversial: apart from therare cases requiring surgery, craniofacial surgeons recom-mend either passive positional treatments or active hel-met-based therapies (Marchac et al., 2011). Helmets havemany common points with the devices used to induceICDs, as they exert a continuous external pressure atdefined points of the skull vault. Our results on theeffects of ICDs on the orbits and the sinuses suggest thathelmet therapy most probably induces changes in cranio-facial morphology that require further investigations.

The situation is different in craniosynostoses as thedeformation is not due to focal zones of external pres-sure. It is known that craniosynostoses are not associ-ated with major changes in intracranial and orbitalvolumes (Gault et al., 1990; Bentley et al., 2002; Hillet al., 2011). Nevertheless, using a mouse model Crouzonsyndrome, Mart�ınez-Abad�ıas et al. (2012) have recentlyshown that this disorder includes soft tissue abnormal-ities such as increased volume of the globe of the eyeand modified shape of the brain. These results indicatethat the malformations observed in mutant individualsare the combined result of deformations due to abnormalmechanical constraints and malformations due to FGFRover-expression. On the basis of the results obtainedfrom the study of ICDs—a purely mechanical system—precise cephalometric studies of the orbits and maxillarysinuses in craniosynostoses could be of help in revealingthe differences between the effects of mechanical con-straints and intrinsic growth abnormalities.

CONCLUSION

ICDs subject the skull to abnormal external mechanicalconstraints and induce specific deformations in structuresthat are distant from the deformation devices. In fact, byfocusing on the structure of craniofacial cavities in ICDs,we show here for the first time that the shapes of the orbitsand the maxillary sinuses are modified by the deforma-tions, and that the thickness of the vault is affected by thedeformation. For this, we provide new tools for the mea-surement of the volumes of open cavities.

This study calls for similar investigations in craniosy-nostoses and deformational plagiocephalies, where thedistribution of internal and external constraints is differ-ent than in ICDs and where the shape of craniofacialcavities in affected individuals is currently not preciselydescribed.

ACKNOWLEDGMENTS

Special thanks to Philippe Mennecier for having pro-vided us with access to the anthropological collections ofthe Mus�ee de l’Homme in Paris.

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