A morphometric anatomical and comparative study of the foramen magnum region in a Greek population

A morphometric anatomical and comparative study of the foramen magnum region in a Greek population
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  ORIGINAL ARTICLE A morphometric anatomical and comparative studyof the foramen magnum region in a Greek population K. Natsis  • M. Piagkou  • G. Skotsimara  • G. Piagkos  • P. Skandalakis Received: 27 November 2012/Accepted: 6 April 2013   Springer-Verlag France 2013 Abstract  Background   The foramen magnum (FM), a complex areain craniocervical surgery, poses a challenge for neurosur-geons. The knowledge of the detailed anatomy of the FM,occipital condyles (OC) and variations of the region iscrucial for the safety of vital structures. This study focuseson the FM and OC morphometry, highlights anatomicalvariability and investigates correlations between theparameters studied.  Materials and methods  One hundred and forty-threeGreek adult dry skulls were examined using a digitalsliding calliper (accuracy, 0.01 mm).  Results  Mean FM width and length were found30.31  ±  2.79 and 35.53  ±  3.06 mm, respectively. Thecommonest FM shape was two semicircles (25.9 %),whereas the most unusual was irregular (0.7 %). The OCminimum width, maximum width and length were5.71  ±  1.61, 13.09  ±  1.99 and 25.60  ±  2.91 mm on theright, and 6.25  ±  1.76, 13.01  ±  1.98 and 25.60  ± 2.70 mm on the left side. The commonest OC shape wasS-like and the most unusual was ring, bilaterally. The meananterior and posterior intercondylar distances were19.30  ±  3.25 and 51.61  ±  5.01 mm, respectively. The OCprotruded into the FM in 86.7 % of the skulls. Variationssuch as a third OC existed in 5.6 % and basilar processes in2.8 %. Posterior condylar foramina were present in 75.5 %.The gender was correlated with FM width and length, OClength, bilaterally, anterior intercondylar distance (AID)and posterior intercondylar distance (PID). The OC pro-trusion and existence of posterior condylar foramina werecorrelated. Bilateral asymmetry for OC shape was statis-tically significant. Conclusion  Our results provide useful information thatwill enable effective and reliable surgical intervention inthe FM region with the maximum safety and widest pos-sible exposure. Keywords  Foramen magnum    Occipital condyle   Morphology    Variation    Craniocervical junction Introduction The occipital condyles (OC), an important part of the cra-niovertebral or craniocervical junction are located antero-laterally on either side of the foramen magnum (FM).During embryonic life, the occipital bone is developed atleast from the fusion of the four primitive somites, whichcorrespond to the three primary roots of the hypoglossalnerve [41]. The caudal portion of the fourth occipital somitefuses with the cranial portion of the first cervical somite toform the proatlas, which participates in the OC formation.Specifically, the ventral-rostral component of the neuralarch of proatlas contributes to OC formation [47].Many studies focused on the OC and FM morphometricanalysis highlighting their clinical, orthopedic, neurosur-gical and forensic importance [37]. Pathological FMdimensions, as in achondroplasia and brain herniationcases, can result in compression of the vital structurespassing through it [30, 35] and can influence the flow of  K. NatsisDepartment of Anatomy, Medical School, Aristotle University of Thessaloniki, Plateia Ippodromiou 17, 54621 Thessaloniki,GreeceM. Piagkou ( & )    G. Skotsimara    G. Piagkos    P. SkandalakisDepartment of Anatomy, Medical School, National andKapodistrian University of Athens, M. Asias 75, 11527 Athens,Greecee-mail:  1 3 Surg Radiol AnatDOI 10.1007/s00276-013-1119-z  blood and cerebrospinal fluid [36]. Furthermore, manylesions of the FM region are difficult to reach surgicallybecause of their close relation to inferior vermis, cerebellartonsils, fourth ventricle, lower cranial nerves (9th–12th),caudal aspect of the medulla oblongata, rostral aspect of thespinal cord and the upper cervical nerves C 1  and C 2 . Inaddition, the neurosurgeon must be aware of the vital vas-cular structures, such as the vertebral arteries and theirmeningeal branches, the posterior inferior cerebellar arter-ies, the posterior and anterior spinal arteries, the extraduraland intradural veins, the dural venous sinuses and the spinalvenous plexus. Especially, in cases of bone resection, cra-niocervical instability is a potent complication [6]. As aresult, the anatomic complexity of the FM region and therisk of damaging vital structures or causing craniocervicalinstability due to OC resection make fundamental theknowledge of the FM and OC morphometry [45].In the present study, the FM and OC were classifiedaccording to their shape; their anatomic metric values wereevaluated, the morphological abnormalities in the regionwere reported, and possible correlations between theparameters studied, were investigated, as an orientationpoint in cases requiring craniocervical surgery. Materials and methods One hundred and forty-three adult non-pathological dryskulls of unknown age were examined in order to evaluatethe FM region. All skulls were Greek and the gender wasknown (77 males and 66 females). The sample includedskulls from the collection of the Departments of Anatomy of AristotleUniversity(Thessaloniki)andNational-KapodistrianUniversity (Athens). The parameters examined were:1. The FM width ( w ) (transverse diameter, was definedas the distance between the lateral margins of the FMat the point of greatest lateral curvature)2. The FM length ( h ) (rostral  -  caudal diameter, wasdefined as the direct distance from basion toopisthion)3. The FM shape4. The OC maximum width (OCW max , was defined asthe distance from the articular edges along a lineperpendicular to the long axis)5. The OC minimum width (OCW min )6. The OC length (OCL, was defined as the distancealong the long axis from the edges of the articularsurface)7. The anterior intercondylar distance (AID) betweenthe anterior OC tips, bilaterally8. The posterior intercondylar distance (PID) betweenthe posterior OC tips, bilaterally9. The OC shape bilaterally10. The OC protrusion into the FM11. The presence of posterior condylar foraminabilaterally12. The existence of anomalies of the hypochordal bowof proatlas, such as basilar processes (small bonyeminences at the anterior edge of the FM, extendingfrom the OC direction), or a third OC (median OC,projecting downward in the midline from the anterioraspect of the basiocciput along the FM anteriormargin and its articular facet) [42].13. The existence of septated hypoglossal canals (com-plete osseous bridges in the internal, external surfaceor along the entire canal).All distances were measured using a digital slidingcaliper (Mitutoyo ABSOLUTE 500-196-20), accurate to0.01 mm (Fig. 1). Descriptive statistics (mean, median,minimum, maximum, standard deviation) were evaluatedfor all the parameters collected from the skull measure-ments. The Mann–Whitney  U   test was used to investigate apossible correlation between the descriptive variables(gender, OC protrusion and existence of posterior condylarforamina) and metric variables ( w ,  h , OCW max , OCW min ,OCL, AID and PID). The Chi-square test was used toinvestigate a possible correlation between the descriptivevariables (gender, OC protrusion, existence of posteriorcondylar foramina, FM and OC shape). For all the analy-ses,  p \ 0.05 was accepted as statistically significant andstatistical analysis was performed using IBM SPSS Sta-tistics for Windows Version 20.0.The FM shape was classified into seven types as fol-lows: two semicircles, pear, egg, rhomboid, oval, roundand irregular (Fig. 2). The OC shape was classified intoeight types as follows: oval, kidney-like, S-like, eight-like, Fig. 1  Measured parameters studied ( 1 h ,  2 w ,  3  OCW min ,  4 OCW max ,  5  OCL,  6   AID,  7   PID).  OC   occipital condyle,  FM   foramenmagnumSurg Radiol Anat  1 3  triangle, ring-like, two-portioned and deformed OC(Fig. 3). Results The results obtained from the metric parameters are pre-sented in Table 1. The average  w  and  h  were found to be30.31  ±  2.79 and 35.53  ±  3.06 mm, respectively. Themost common FM shape was two semicircles (25.9 %),whereas the most unusual was the irregular (0.7 %). Othershapes were seen in the following frequencies: pear,22.4 %; egg, 21 %; oval, 14.7 %; rhomboid, 14 % andround, 1.4 %.The mean OCW max , OCW min  and OCL were found13.09  ±  1.99, 5.71  ±  1.61 and 25.60  ±  2.91 mm on theright, and 13.01  ±  1.98, 6.25  ±  1.76 and 25.60  ±  2.70mm on the left side, respectively. The mean AID and PIDwere 19.30  ±  3.25 and 51.61  ±  5.01 mm, respectively.We also classified the OC according to their length. TheOC of 26  ±  3 mm (i.e., mean length  ±  standard devia-tion) (23–29 mm) was classified as moderate, OC \ 23mm as short and OC [ 29 mm as long. Twenty OC (7 %)were short, 217 moderate (75.9 %) and 49 long (17.1 %).The OC protruded into the FM in 86.7 %. The OC shapewas classified in eight types (Fig. 3). On the right side,33.1 % of the OC were S-like, 16.5 % two-portioned,15.8 % triangle, 12.2 % eight-like, 8.6 % oval, 6.5 %kidney-like, 4.3 % deformed and 2.9 % ring-like. Theleft OC did not always have the same shape as the rightones, which suggests the existence of bilateral asym-metry (  p \ 0.001) (Fig. 4a). On the left side, the S-liketype was observed in 28.3 %, the triangle and two-por-tioned in 16.7 %, the eight-like in 13 %, the deformed in7.2 %, the oval in 6.5 %, the kidney and the ring-like in5.8 %.Meanwhile, in eight skulls (5.6 %), a third (median) OCwas observed (Fig. 4a). In four skulls (2.8 %), we observedbasilar processes, as a manifestation of a partial proatlas(Fig. 4b). Posterior condylar foramina were present in75.5 % (11.9 % on the right, 16.1 % on the left and 47.6 %bilaterally) (Fig. 4c). We also observed a septum in 25.5 %of the hypoglossal canals (Fig. 4d).A possible correlation between gender and metricparameters was investigated (Table 2). A statistically sig-nificant correlation has been achieved between gender and w ,  h , OCL right and left, PID (  p \ 0.001) and AID(  p \ 0.05). Contrariwise, there was not a statistically sig-nificant correlation between gender and OCW max  andOCW min , bilaterally. The FM types of shape appeared in Fig. 2  Types of the FM shape.  a  Two semicircles,  b  pear,  c  oval,  d  egg,  e  round,  f   rhomboid,  g  irregularSurg Radiol Anat  1 3  different frequencies between men and women. The eggshape was more common in men (23.4 %), while twosemicircles in women (33.3 %). The incidence of the othertypes in both genders is presented in Table 3. Meanwhile, acorrelation between gender and FM shape was notachieved. The OC protrusion did not indicate differentfrequency among males and females neither did the exis-tence of posterior condylar foramina.The frequency of the OC shape bilaterally for bothgenders is separately presented in Table 4. In order of frequency, the appearance of different types in men isdifferent compared to that of women bilaterally. Unfortu-nately, a statistically significant correlation between genderand OC shape could not be achieved bilaterally. In addi-tion, a possible correlation between the OC protrusion and w ,  h , OCW max , OCW min , OCL, bilaterally, AID and PIDwas investigated but no correlation could be achieved. Nocorrelation was found between the OC protrusion and theFM or the OC shape. Similarly, a possible correlation wasinvestigated between the existence of posterior condylar Fig. 3  Types of the OC shape.  a  eight- like,  b  oval,  c  two-portioned condyle,  d  triangle,  e  ring-like,  f   kidney-like,  g  S-like,  h  deformed Table 1  The results of the metric parameters of the FM and OC (in mm)Parameters Minimum (mm) Maximum (mm) Median (mm) Mean  ±  SD (mm)  p  valueFM width ( w ) 15.42 35.48 30.57 30.31  ±  2.79 0.10FM length ( h ) 20.27 42.70 35.85 35.53  ±  3.06 0.54OCW max  (R) 10.01 21.88 12.57 13.09  ±  1.99 0.08OCW min  (R) 2.90 12.11 5.36 5.71  ±  1.61 0.09OCL (R) 17.92 34.20 25.57 25.60  ±  2.91 0.67OCW max  (L) 7.92 24.38 12.68 13.01  ±  1.98 0.34OCW min  (L) 1.16 12.12 6.07 6.25  ±  1.76 0.24OCL (L) 17.76 35.51 25.59 25.60  ±  2.70 0.46AID 10.10 26.39 19.42 19.30  ±  3.25 0.63PID 21.80 68.86 51.33 51.61  ±  5.01 0.07  R  right,  L   leftSurg Radiol Anat  1 3  foramina and  w ,  h , OCW max , OCW min , OCL, bilaterally,AID, PID, FM and OC shape, but it was not found. Yet,there was a correlation between the existence of posteriorcondylar foramina and the OC protrusion (  p \ 0.05). Discussion The FM and OC dimensions in the Greek population seemto be in agreement with the dimensions of variouspopulations (Table 5). It should be taken under consider-ation, though, that several authors have used differenttechniques for the metric measurements. For example, incontrast with our technique, Govsa et al. [19] and Ozeret al. [31] have used the 3-D doctor computer program andAvci et al. [2] has used both the digital caliper and theradiologic method (3D CT).Traditionally, the lesions of the craniocervical junctionhave posed a surgical challenge and in the past have beenassociated with high mortality, morbidity and incomplete Fig. 4 a  Existence of a median occipital condyle (MOC) and asymmetry between the occipital condyles bilaterally,  b  existence of basilarprocesses (BP),  c  existence of posterior condylar foramina (*),  d  septate hypoglossal canal (*) Table 2  The mean values  ±  SD of the metric parameters among male and female subjects Gender  h  (mm)  w  (mm) OCW max  (mm) OCW min  (mm) OCL (mm) AID (mm) PID (mm)M 36.20  ±  3.39 30.92  ±  3.15 13.13  ±  2.01 (R)13.24  ±  2.20 (L)5.83  ±  1.69 (R)6.29  ±  1.85 (L)26.30  ±  2.92(R)26.48  ±  2.80 (L)19.82  ±  3.19 52.80  ±  4.93F 34.79  ±  2.39 29.61  ±  2.08 13.04  ±  1.99 (R)12.74  ±  1.63 (L)5.57  ±  1.51 (R)6.19  ±  1.65 (L)24.70  ±  2.66 (R)24.57  ±  2.13 (L)18.77  ±  3.26 50.13  ±  4.71  p  value  \ 0.001  \ 0.001  [ 0.05 (R, L)  [ 0.05 (R, L)  \ 0.001 (R, L)  \ 0.05  \ 0.001  R  right,  L   left Table 3  The results of the correlation between gender and FM shapeGender FM shapeOval (%) Two semicircles (%) Pear (%) Egg (%) Round (%) Rhomboid (%) Irregular (%)M 13 19.5 22.1 23.4 2.6 18.2 1.3F 16.7 33.3 22.7 18.2 0 9.1 0Surg Radiol Anat  1 3
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