Andersen Et Al. - 2000 - The Prenatal Cranial Base Complex and Hand in Turner Syndrome

8/13/2019 Andersen Et Al. - 2000 - The Prenatal Cranial Base Complex and Hand in Turner Syndrome

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Introduction

It is characteristic of Turner syndrome (45 X)that the body length is short (Dalla Palma et al.,1967; Brook et al., 1974). Brook et al. (1974)described the course of growth in untreated girls

with Turner syndrome and found that, unlikenormal girls, there was no pubertal growth spurt.Another characteristic is the occurrence of awebbed neck (Felix et al., 1974; Clark, 1984).

Craniofacial deviations have also been regis-tered in Turner syndrome (Jensen, 1985;Peltomki et al., 1989; Rongen-Westerlaken et al.,1992), and abnormal morphology in teeth, palateand tooth eruption patterns have been described(Ogiuchi et al., 1985; Varrela, 1990; Mayhall

and Alvesalo, 1992; Midtb and Halse, 1992,1994a,b).

Cephalometric studies of patients with Turnersyndrome, aged 1444 years (Jensen, 1985),showed that deviations in size and shape occurredin the cranium in comparison with normal

control groups. The cranial base angle wasextended, the maxilla and mandible wereretrognathic, and the total length of the cranialbase and clivus was short. The study also showeda short maximum length of the maxilla.

Rongen-Westerlaken et al. (1992), in acephalometric investigation of girls with Turnersyndrome aged 3.516.6 years, found that a largecranial base angle, maxillary and mandibularretrognathism, and a reduced posterior, and a

European Journal of Orthodontics 22 (2000) 185194 2000 European Orthodontic Society

The prenatal cranial base complex and

hand in Turner syndrome

E. Andersen, L. Sonnesen, M. S. Kjaer, B. Fischer Hansen* and I. KjrDepartment of Orthodontics, School of Dentistry, University of Copenhagen and*Department of Pathology, Hvidovre University Hospital, Denmark

SUMMARY From early childhood, Turner syndrome patients have a flattened cranial base,maxillary retrognathism, and short hands. There are, however, no studies that show whenthese genotype-determined abnormalities occur prenatally. The purpose of the presentstudy was to measure craniofacial profile and hand radiographs of second trimesterfoetuses with Turner syndrome and compare the results with similar measurements fromnormal foetuses.

The subjects consisted of 12 Turner syndrome foetuses, gestational age (GA) varying

between 15 and 24 weeks, and crownrump length (CRL) between 108 and 220 mm. Themid-sagittal block of each cranium was analysed as part of the requested brain analysis(pituitary gland analysis). This block and the right hand from seven foetuses were radio-graphed, and the skeletal maturity of the cranial base complex, i.e. the cranial base and themaxilla, was evaluated from the profile radiographs. Shape and size measurements in thecranial base were performed, and compared with normal values according to cranial maturityand to CRL.

The cranial base angle in Turner syndrome was greater and the maxillary prognathismwas reduced compared with the normal group. The dimensions in the cranial complex andin the hand showed that the bone lengths and distances in relation to CRL were generallysmaller compared with normal foetuses.

This investigation showed that the abnormal shape of the cranial base complex and the

short hands in Turner syndrome are present prenatally.


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normal anterior cranial base length were alreadypresent in early childhood. More recent cephalo-metric analyses of girls with Turner syndrome,aged 716.7 years, have confirmed that thecranial base angle is larger, and the maxilla and

the mandible more retrognathic in girls withTurner syndrome (Midtb et al., 1996). Theirstudy also showed that the total cranial baselength, as well as the posterior cranial base lengthwere reduced, while the length of the anteriorcranial base did not vary from that of the normalgroup. In the same study, it was suggestedthat this abnormal development probably startsduring foetal life, although this has never beeninvestigated.

Among other characteristic skeletal findings

are abnormalities in the sternum (Mehta et al.,1993) and many reports deal with analysis ofhand bones (Archibald et al., 1959; Barr, 1974;Park, 1977; Poznanski et al., 1977; Clevelandet al., 1985; Meyer and Ranke, 1991; van derWerff ten Bosch and Bot, 1992). Archibald et al.(1959) found short fourth metacarpal bones inTurner syndrome, while Park (1977) reportedthat Turner syndrome patients, in general, haveshorter hand bones than normal girls in thecorresponding age group. Park (1977) also foundthat the distal phalangeal bones are less reduced

in size than the more proximally located meta-carpal bones. When and how these dimensionalchanges in the hand arise in Turner syndromepatients is not known. Apart from skeletalalterations, mineralization changes have alsobeen reported (Weiss and Reynolds, 1972;Armstrong and Morettin, 1973).

There are very few studies of skeletal develop-ment in the prenatal period in Turner syndrome.In a recent investigation, Kjr and FischerHansen (1997) reported that cervical ribs were a

characteristic finding in Turner syndrome foetuses.The purpose of the present study was to analyse

craniofacial profile radiographs of foetuses withTurner syndrome and compare cephalometricvalues with standardized measurements, especiallyof the cranial base angle and maxillary prognath-ism on normal foetuses (van den Eynde et al.,1992). It was also the intention to comparedimensions in the cranial base and maxillary com-plex, including the nasal bone, in Turner syndrome

foetuses with normal values (Kyrkanides et al.,1993; Sandikcioglu et al., 1994; Silau et al.,1994; Eriksen et al., 1995). A further aim wasto investigate hand dimensions in foetuseswith Turner syndrome and compare them with

recently published normal values (Kjaer andKjr, 1998).

Subjects

Twelve Turner syndrome foetuses were exam-ined, with parental consent, in connection withautopsy, including brain autopsy. Gestational age(GA) varied between 15 and 24 weeks, crownrump length (CRL) between 108 and 220 mm,and total number of ossified (TNO) bones visible

in the hand and foot, which is a general skeletalmeasure of maturity, varied between 25 and 30.The skeletal maturity pattern of the hand andfoot was normal for the CRL range of the sample(Kjr, 1974). The diagnosis of Turner syndromewas based on intra-uterine CT, autopsy findings,and chromosomal analysis, performed eitherintra-uterinely on amniotic fluid or extra-uterinely on skin biopsy from the heel. In twocases of intra-uterine death and maceration,the diagnosis was based exclusively on autopsyfindings, including whole-body radiography. The

genetic diagnosis was performed by a pathologistin collaboration with geneticists.

Prior to radiography of the cranium and thehead, a mid-sagittal block was dissected freefrom the cranial base by two vertical parasagittalincisions parallel to the crista galli through themedial part of the orbit (Kjr, 1990). Handradiographs, with the right hand in a stretchedposition, were available for seven of these 12foetuses.

Methods

Radiographic examination

The mid-sagittal block of each cranium andthe hand were radiographed using a Grenz rayradiographic apparatus (Hewlett PackardFaxitron, Model 43855A, McMinniville, Oregon,USA). The tube voltage varied between 30 and60 kV, and the exposure time from 10 to 60

186 E . A N DE R SE N E T A L.


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seconds at 2.83.0 mA. The film used was KodakX-omat MA (Kodak-Industrie, France), routinelyprocessed. The skeletal maturity of the cranialbase section, placed on a thin acrylic sheet onthe film envelope, was evaluated from theseradiographs and cephalometric analysis wascarried out. The hand was placed on a thin acrylicsheet, stretched, and fixed with tape. The sheetwas placed directly on the film envelope.

Cranial base complex

Maturity stages of the cranium. The develop-ment of the mid-sagittal part of the cranium wasassessed on the basis of the shape of the frontal,occipital, sphenoid, and ethmoid bones, and thecranial maturity was classified into mid-sagittalsegment stages (MSS) from MSS I to MSS VII(Kjr, 1990). In the present study, the maturityof the material lay in the range MSS IV to MSSVI, which is normal for foetuses within the CRLrange concerned (Kjr, 1990; Figure 1).

Cephalometric analysis. Magnification of theradiographs was performed in a stereomacro-scope (Wild Heerbrugg macroscope M 420) andthe cephalometric measurements between refer-ence points were made with a digital slidingcalliper (Sylvac SA, 1023 Crissier, Switzerland).The following cephalometric reference points,illustrated in Figure 2, were used:

Basion (ba): the most caudal point on the lowerborder of the basilar part of the occipital bone.

Sella (s): centre of the sella turcica. From MSSIV to MSS VII the sella is found according tomethods described by van den Eynde et al.(1992).

Nasion (n): the point of intersection between aline tangential to the nasal bone and a linetangential to the lower 5 mm of the frontal aspectof the frontal bone (van den Eynde et al., 1992).

CRANIAL BASE AND HAND IN TURNER SYNDROME 187

Figure 1 MSS radiograph showing the mid-sagittal part of the cranial base and the maxillary complex of Turner syndromefoetuses (1). (a) MSS IV, GA = 17 weeks, CRL = 120 mm, TNO = 29/3, cranial base angle nsba = 141, maxillaryprognathism smsp = 85. (b) MSS V, GA = 18 weeks, CRL = 138 mm, TNO = 29/3, cranial base angle nsba = 146,maxillary prognathism smsp = 84. (c) MSS V, GA = 18 weeks, CRL = 145 mm, TNO = 29/3, cranial base angle nsba =147.5, maxillary prognathism smsp = 84. (d) MSS VI, GA = 22 weeks, CRL = 220 mm, TNO = 31, cranial base angle nsba= 143.5, maxillary prognathism smsp = 81.5.

Figure 2 Drawing of a cranial base block, including themaxilla, from a human foetus with skeletal maturity MSS V.The drawing corresponds to the radiograph in Figure 1c.Fixed points: ba, basion; s, sella; n, nasion; sp, anterior nasalspine. Distances: oo, length of the basilar part of theoccipital bone; on, length of the nasal bone; om, length ofthe maxilla; op, length of the palatine bone; mp, lengthof the hard palate. N indicates the earlier location ofthe notochord. FL, field line, indicates an approximateboundary line between the notochordal development field(dotted) and the antenotochordal development field(shaded).


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Spinal point (sp): the apex of the anterior nasalspine.

Shape measurements.

nsba: the cranial base angle.

snsp: maxillary prognathism.

Size measurements. The region of the posteriorcranial fossa:

sba: length of the posterior cranial base.

oo: length of the basilar part of the occipital bone.

The region of the anterior cranial fossa,including the maxillary complex:

ns: length of the anterior cranial base.

nsp: anterior facial height.

om: length of the maxillary component of thehard palate.

op: length of the palatinal component of the hardpalate.

mp: total length of the hard palate.

on: length of the nasal bone.

For comparisons with normal standards, MSSand CRL values were used as reference meas-urements. For purposes of visualizing the com-parison with normal values, the individual size ofeach measurement was entered on a diagram

with the CRL means for normal values.The statistical analysis of the distributions of

the cephalometric measurements was performedwith the SAS Statistical Programme Package(SAS Institute Inc., 1988; Table 1).

Method error. The method error of the cephalo-metric measurements was assessed by remeas-urement of the previously recorded radiographs.The reference points were removed from thefilms and were marked again. The variables werecalculated and the differences between the two

sets of recordings were evaluated. The analysisshowed no sytematic errors between the two setsof recordings. The method errors, s(i), of theshape measurements were 1.07 and 1.22 degrees.The method errors, s(i), of the size measure-ments ranged from 0.11 to 0.44 mm. The methoderror of the cephalometric variables wascalculated by Dahlbergs formula (Dahlberg,1940).


Table 1 Statistical description of shape and size measurements in the cranial base complex according to (A)

cranial base maturity (stages MSS IV, V and VI) and (B) to crownrump length (CRL).

A Variable Mean (SD) normal maturity stages

Mean values SD MSS IVVIMSS IV MSS V MSS VI MMS IVVI for Turner syndrome

for Turner syndrome

nsba (degrees) 132.6 (9.6) 127.7 (7.0) 124.9 (5.7) 142.9 6.6snsp (degrees) 85.0 (6.9) 90.6 (4.7) 93.6 (4.3) 81.2 4.4ns (mm) 17.2 (3.8) 22.6 (2.5) 25.5 (2.7) 18.3 4.8sba (mm) 11.7 (2.5) 14.9 (1.2) 17.1 (1.5) 11.9 2.6nsp (mm) 8.5 (2.1) 11.5 (1.5) 13.2 (1.2) 9.2 2.3

B Variable Normal sizes (according to CRL)

Reference Mean for SD for70 100 125 170 200 225 Turner Turner

syndrome syndrome

oo (mm) 3 () 5 () 7 () 9.1 () 11 () 12.9 () Kyrkanides et al., 1993 6.8 (108220) 1.8on (mm) 1.5 () 2.5 () 4.2 () 6 () 7 () 8 () Sandikcioglu et al. , 1994 3.4 (108220) 1.1om (mm) 5 () 2 () 9 () 13 () 15 () 18 () Silau et al., 1994 9.9 (108225) 2.4op (mm) 1.5 () 2 () 3 () 4 () 5 () 6 () Silau et al., 1994 3.5 (108220) 1.3mp (mm) 6 () 9 () 12 () 15 () 19 () 21 () Silau et al., 1994 12.0 (108220) 3.1


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Hand

A hand radiograph of a Turner syndrome foetusis illustrated in Figure 3. The following hand

dimensions, illustrated in Figure 4, were recordedon the third finger according to Kjaer and Kjr(1998).

Digital-metaphalangeal length (DM): Thedistance from the most distal part of the distalphalangeal bone to the most proximal part of themetacarpal bone. This measurement expressedthe hand length.

Proximal phalangeal bone length (PP): Thedistance from the most distal part to the most

proximal part of the proximal phalangeal bone.Metacarpal bone length (MC): The distance fromthe most distal part to the most proximal part ofthe metacarpal bone.

The hand measurements (DM, PP, and MC)for Turner foetuses were plotted on diagrams withregression lines for comparable measurementsfrom 251 normal hands related to CRL values(Kjaer and Kjr, 1998). The groups werecompared by analysis of covariance (ANCOVA,BMDP Software, 1988) and P values were

reported.

Results

Cranial base complex

Shape. The mean for the cranial base angle(nsba) corresponding to CRL in the presentstudy was generally larger than standard valuesfor normal foetuses (van den Eynde et al., 1992;

Figure 5). Ten of the 12 foetuses had a largernsba angle corresponding to CRL comparedwith the normal group. On the other hand, themean for the maxillary prognathism (snsp)corresponding to CRL was generally smaller

than standard values for normal foetuses (vanden Eynde et al., 1992; Figure 5). Eleven of the12 foetuses had a smaller snsp angle corres-ponding to CRL compared with the normalgroup. The same tendency was observed whencomparison was made with MSS maturity values.

Size. The means for the size measurements inthe regions of the posterior and anterior cranialfossa, including the maxillary complex corres-ponding to CRL, were generally smaller thanstandard values for normal cranial base dimen-

sions and anterior facial height when comparisonwas made according to CRL (Eriksen et al., 1995;Figure 6). The same applied to the lengths of thebasilar part of the occipital bone (Kyrkanideset al., 1993; Figure 7) and of the nasal bone(Sandikcioglu et al., 1994; Figure 7), and ofosseous palatal lengths (Silau et al., 1994;Figure 8). Ten of the 12 foetuses had a smallerlength of the anterior cranial base (ns) and asmaller length of the basilar part of the occipital


Figure 3 Hand radiograph of a Turner syndrome foetus,GA 17 weeks, CRL 120 mm (1). The hand appears short.

Figure 4 Drawing illustrating the hand length as the DMdistance on the third finger from the distal tip of the distalphalangeal bone to the proximal tip of the metacarpal bone.In addition, the length of the proximal bone (PP) and of

the metacarpal bone (MC) on the third finger are shown.Reprinted from Early Human Development, Vol. 50, Kjaerand Kjr, Human fetal hand size and hand maturity in thefirst half of the prenatal period, pp. 193207, 1998, withpermission from Elsevier Science.


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bone (oo) compared with the normal group, and11 out of 12 foetuses had a smaller length of theposterior cranial base (sba) and a smalleranterior facial height (nsp). The same tendencywas observed when comparison was made with

MSS maturity values. Furthermore, a smallerlength of the maxillary component of the hardpalate (om), and a smaller length of the palatalcomponent of the hard palate (op) were seen in11 out of 12 foetuses when compared with thenormal group based on CRL standards. Lastly,all 12 foetuses had a smaller length of the nasalbone (on) and a smaller length of the hard palate(mp) corresponding to CRL compared with thenormal group.


Figure 5 Cranial base complex in 12 cases of prenatalTurner syndrome. (a) Cranial base angle (nsba);(b) Maxillary prognathism (snsp), indicating that 10 outof 12 Turner syndrome foetuses (dots) had a larger nsba

angle, and 11 of the 12 foetuses had a smaller nssp anglecompared with normal standards (straight lines; van denEynde et al., 1992). The shape of the prenatal cranial base,including the maxilla, was abnormal in Turner syndromefoetuses compared with body size (CRL in mm).

Figure 6 Cranial base dimensions in 12 cases of prenatalTurner syndrome. (a) Length of the anterior cranial base(ns) was generally shorter in Turner syndrome (dots) than

in normal foetuses (straight line). (b) Distance of theposterior cranial base from the sella turcica to the foramenmagnum (sba) was generally shorter in Turner syndrome(dots) than in normal foetuses (straight line). (c) Anteriorfacial height (nsp) was generally shorter in Turnersyndrome (dots) than in normal foetuses (straight line). Fornormal values, see Eriksen et al. (1995). The three dimen-sions illustrated were smaller in Turner syndrome foetusesthan in genetically normal foetuses in relation to body size(CRL in mm).


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1985; Rongen-Westerlaken et al., 1992; Midtbet al., 1996), are also present prenatally. Theabnormality was registered at a very early stage,from the commencement of ossification. Postnatalstudies of Turner syndrome show, moreover,

reduced mandibular prognathism compared withnormal groups. In this study, mandibular prog-nathism was not included, because the cranialbase blocks, which are essential for recognitionof the mid-sagittal structures, do not include thecondylar processes, which are necessary forcorrect measurement of the mandibular position.

The pathogenesis related to the shape of thecranial base in the Turner group is not known.General oedema in varying degrees is seen inTurner foetuses and, in particular, extensive neck

hygroma. It is probable that the foetuses in thisgroup, where extensive nuchal hygroma hadbeen registered intra-uterinely or where thefoetus had died intra-uterinely, show greaterphenotypic anomalies than children born withTurner syndrome. One may therefore supposethat the anomalies registered here are greaterthan in Turner foetuses with a more moderatephenotypic appearance. Moreover, heart, majorblood vessels, and kidney defects are often seenin Turner syndrome (Keeling, 1994). It is possibleto imagine that the regional changes in the

cervical region (Kjr and Fischer Hansen, 1997),could be associated with the increased cranialbase angle. Further investigations are needed todetermine whether there is a relationship betweenthe extent of the hygroma in the cervical regionand the changes in the cranial base. It is alsoconceivable that changes in brain developmentin Turner foetuses might result in changes in theshape of the cranial base.

In earlier studies of pathological developmentof the cranial base, the sella turcica region has

been described as a boundary region between anotochordal developmental field behind the sellaturcica and a prenotochordal developmentalfield in front of the sella turcica, illustrated inFigure 2 (Kjr, 1998). The cause of this fieldboundary has been ascribed to the difference inthe functions of the notochord in the two regions.When changes in shape are observed in a pre-natal cephalometric analysis such as in thepresent study of Turner foetuses, it is reasonable


Figure 9 (a) Hand length (DM) of seven foetuses withTurner syndrome in relation to regression line for normal

hand length in relation to body size (CRL). The Turnersyndrome foetuses have small hands compared with normalsizes in relation to body size. (b) Proximal phalangeal bonelength (PP) of seven foetuses with Turner syndrome inrelation to regression line for PP bone length in normalfoetuses in relation to body size (CRL). The Turner syndromefoetuses have a reduced PP length compared with normalfoetuses in relation to body size. (c) Metacarpal bone length(MC) of seven foetuses with Turner syndrome in relation toregression line for MC bone length in normal foetuses inrelation to body size (CRL). The Turner syndrome foetusesare seen to have reduced MC length compared with normalfoetuses in relation to body size.


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to clarify whether there is defective developmentof the notochordal field, or of the prenotochordalfield, or perhaps of both. Studies of the sizes ofthe individual cranial components have there-fore concentrated on an analysis of the shape

relationships behind and in front of the sellaturcica. In the present study, this analysis sug-gests that the abnormalities in shape and size arelocated both in the prenotochordal and in thenotochordal fields. In other words, according tothe results of this study, the areas in front of andbehind the sella turcica are affected in Turnersyndrome. It is shown that the nasal bone isshorter than in normal foetuses. It seems possiblethat a deviation in the length of the nasal bone alsooccurs postnatally in Turner syndrome, since an

upturned nose is a well-known phenotypic char-acteristic of this syndrome (Keeling, 1994). It isalso well-known that girls with Turner syndromeare shorter than girls with a normal genotype.

The present study has shown, on limited foetalmaterial, that the hand length and the lengthof the bones in the third finger are smallercompared with CRL in Turner syndrome than innormal individuals. This was not previouslyknown. It is important to increase the samplesize for analysis in further research studies onTurner syndrome prenatally.

An overriding problem when one refers to themeasurement of prenatal dimensions on foetuseswith Turner syndrome, which are probably alsosmaller in size (CRL) than normal foetuses of thesame gestational age, is that normal in relationto a CRL scale in reality is less than normal inrelation to the actual age, which is not known.Therefore, when, for example, the maxillarycomplex is measured and found to be less thanthe normal values, it is likely that the maxillarycomplex is even less in relation to the real age.

Prenatal studies of Turner syndrome foetuseshave, with the aid of radiographic investigationsof the cervical column, shown the presence ofunilateral or bilateral cervical ribs (Kjr andFischer Hansen, 1997). It is not known whetherthis circumstance is related to the findings ofshort hands in Turner syndrome. In general,there are no studies which compare the findingsin the body axis with the limb findings. It isof interest to do this in the future, since the

development of the limbs originates from theparaxial mesoderm.

In cases where chromosomal analysis cannotbe performed or where the analysis is unsuc-cessful, prenatal cephalometric measurements

can supplement the description of a phenotypesuspected of Turner syndrome. Furthermore,studies such as the present one can contribute toa better understanding of postnatal genotype-determined disorders. Therefore, it is importantfor orthodontic research to collaborate not onlywith geneticists, but also with pathologists con-cerning material from different chromosomaldisorders.

Address for correspondence

Inger KjrDepartment of OrthodonticsSchool of DentistryFaculty of Health SciencesUniversity of CopenhagenNrre All 20DK-2200 Copenhagen NDenmark

Acknowledgements

This study was supported by grants from theDanish Medical Research Council, the Vera andCarl Johan Michaelsen Foundation, and from theIMK Almene Fond.

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Andersen Et Al. - 2000 - The Prenatal Cranial Base Complex and Hand in Turner Syndrome