International Journal of Osteoarchaeology

Int. J. Osteoarchaeol. (2011) Published online in Wiley Online Library (wileyonlinelibrary.com) DOI: 10.1002/oa.1236

SHORT REPORT

Anthropological Analysis of the Phenomenon of Atlas Occipitalisation ra Exemplied by a Skull from Twardogo (17th c.)Southern Poland
M. SENATOR a* AND S. GRONKIEWICZ b
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ABSTRACT

Occipitalisation of the atlas is one of the most frequent osseous anomalies of the atlas. It is characterised by the adhesion of the rst cervical vertebra with the basilar part of the occipital bone. The most probable cause of the occipitalisation is a congenital disorder. The atlanto-occipital fusion may lead to narrowing of the space for medulla oblongata, spinal cord and vertebral artery. This in turn may lead to many physiological symptoms. ra, Southern Poland, showed partial atlanto-occipital fusion and presented an The skull from Twardogo asymmetry in structure and shape of apertures for the vessels and nerves around the foramen magnum. Copyright 2011 John Wiley & Sons, Ltd. Key words: atlanto-occipital fusion; congenital anomaly; neurological symptoms; palaeopathology

Introduction
Occipitalisation of the atlas (atlanto-occipital fusion, atlas assimilation), that is the adhesion of the atlas with the basis of occipital bone of the skull, is a rare anomaly, but has been reported in medical (clinical, particularly neurological) and anthropological literature. It was rst described in the second half of the 16th century by Matteo Realdo Colombo, an anatomist and surgeon from Cremona, and 200 years later by the Italian anatomist Giambattista Morgagni. A case of atlas assimilation to the basis of the occipital bone is also known in an Egyptian mummy from before four thousand years ago (Wrzosek, 1935). In 1991, Arthur ller (a pioneer of neuroradiology) presented that Schu anomaly by means of roentgenography (Al-Motabagani & Surendra, 2006). At present, for diagnosing occipilisation, computed tomography and magnetic resonance are used.
* Correspondence to: Department of Anthropology, University of nicza 35, 50-138 Wroclaw, Poland. Wroclaw, ul. Kuz e-mail: m.senator@antropo.uni.wroc.pl

The cervical vertebral column makes a stable support for the head, enabling its considerable mobility. In it the cervical section of the spinal cord is located, from which the nerves of the cervical and brachial plexus branch off. It is also the point of support for vertebral arteries on their way into the skull cavity. The atlanto-occipital fusion is the most frequent osseous anomaly of the upper section of the cervical vertebral column (McKechnie, 1994; Jayanthi et al., 2003; Ranade et al., 2007). It is characterised by complete or partial fusion. The partial fusion is more common (Wysocki et al., 2003; Al-Motabagani & Surendra, 2006). The assimilation of atlas to the basilar part of the occipital bone occurs in about 0.140.75% of cases. Many cases of atlas assimilation (0.51%) were observed in Indian and Havaiian populations (Kalla et al., 1989; Nayak et al., 2005; Al-Motabagani & Surendra, 2006). The occipitalisation of the atlas may be accompanied by a series of abnormalities, e.g. basilar impression of foramen magnum rims into the skull, with consequent reduction of capacity of the posterior cranial fossa; platybasis (Wysocki et al., 2003); spina
Received 3 May 2010 Revised 28 November 2010 Accepted 2 December 2010

Copyright # 2011 John Wiley & Sons, Ltd.

Department of Anthropology, University of Wrocl aw, 50-138 Wrocl aw, Poland Institute of Anthropology, Polish Academy of Sciences, 50-138 Wrocl aw, Poland

M. Senator and S. Gronkiewicz

bidia (mainly of the posterior arch of the atlas) (Jayanthi et al., 2003), dislocation of the atlantooccipital joints (60% of cases), unnaturally developed and/or translocated dens of the second cervical vertebra; adhesions of cervical vertebrae, mainly C2/C3 (Wysocki et al., 2003; Tun et al., 2004; AlMotabagani & Surendra, 2006); hypoplasia of the basis of occipital bone (Jayanthi et al., 2003); achondroplasia, diastrophic dysplasia (caused by disturbances in circulation and lower skull nerves) (Jayanthi et al., 2003; Tun et al., 2004; Nayak et al., 2005), myelopathy, Klippel-Feil syndrome, Arnold-Chiaris malformation, rickets, hyperparathyroidism (Kalla et al., 1989; Black & Scheuer, 1996; Erdil et al., 2003; Wysocki et al., 2003; Scuderi et al., 2005; Zdarkiewicz & Kaczmarczyk, 2007). In general, the occipitalisation is associated with the occurrence of abnormalities in neurovascular and skeleto-muscular structures in cranio-vertebral junction. The aim of the paper is the description of the phenomenon of atlas occipitalisation, its possible reasons (etiology) and consequences for functioning of the human being and assertion of other changes, ra. using as example the skull from Twardogo

Figure 1. Skull with occipitalisation of atlasfrontal view ra). This gure is available in colour at (skull from Twardogo wileyonlinelibrary.com.

artery was more deep on the left side than on the right side. The vertebra appeared to be tilted slightly to its left. Also there was a considerable degree of skull asymmetry, which was visible in the course of nuchal lines of the occipital bone.

Discussion Case report

The analysed skull came from the archeological site ra (South-Western Poland) and is dated in Twardogo to about the 17th century. It belonged to a female specimen of age group maturus (5055 years old). On the skull a fusion of the rst cervical vertebra (atlas) to the basis of the occipital bone was found. The anterior and posterior arches of the atlas were fused with the anterior and posterior rims of the large occipital foramen (foramen magnum). The parts of the arches close to the anterior and posterior tubercles were attached to the occipital bone (black circles in Figure 1 and Figure 2). The superior articular facets of the atlas were totally fused to the occipital bone in the region of the occipital condyles. The transverse processes were partially destroyed, but in spite of that, the fusion of their tubercle with occipital bone was clearly visible (Figure 1black arrows). It was also noted that the right side of the vertebra was distinctly more massive. The left side (mainly massa laterale) was more gracile, and there was a narrowing of the posterior arch near its left end (Figure 2black arrow). The left mastoid process was smaller than the right one (Figure 2white lines). The foramina for the nerves and vessels were also larger on the left side. The groove of the vertebral
Copyright # 2011 John Wiley & Sons, Ltd.

The causes of occipitalisation may be acquired or congenital (Erdil et al., 2003; Ranade et al., 2007). The acquired ones may be due to tuberculosis and other infections. They may also result from mechanical injuries of the cervical region of vertebral column. The injuries may concern ligaments and/or bones (Erdil et al., 2003). Black & Scheuer (1996) analysed a female skeleton with occipitalisation of atlas, who died from progressing tuberculosis. The congenital causes are connected with the appearance of disorders (teratogenic factors, genetic anomalies) during the third week

Figure 2. Skull with assimilated top vertebra to the occipital ra). This gure is boneposterior aspect (skull from Twardogo available in colour at wileyonlinelibrary.com.

Int. J. Osteoarchaeol. (2011)

Atlas Assimilation to the Basis of the Occipital Bone

of fetal life in which the occipital and cervical sclerotomes are developing. The fusion takes place as a result of failure of segmentation in the last occipital sclerotome and the rst cervical sclerotome (Erdil et al., 2003; Scuderi et al., 2005). Sclerotomes are the parts of the somites. During their development every sclerotome divides into a cranial part and a caudal part. The cranial part has loosely arranged cells and is smaller; however, the caudal part is larger and the cells are concentrated as a result of their vivid reproduction. The caudal part of one sclerotome is connected with the cranial parts of the next sclerotome, forming a recombined, inter-segmental structure, e.g. vertebral body (Figure 3) (Bochenek & Reicher, 1990; Black & Scheuer, 1996; Al-Motabagani & Surendra, 2006). In the cervico-occipital region four occipital sclerotomes and eight cervical ones are distinguished. The development of the fourth occipital and the rst and second cervical sclerotomes is important in our case. The caudal part of the fourth occipital sclerotome fuses with the cranial part of the rst cervical sclerotome and together they form the proatlas. The proatlas is differentiated into occipital condyles and contributes to the formation of the paracentral part of the basiocciput. It also forms the apex of the odontoid process (dens) of the second cervical vertebra (Black & Scheuer, 1996; Jayanthi et al., 2003; Al-Motabagani & Surendra, 2006; Ranade et al., 2007). The caudal part of the rst cervical sclerotome together with the cranial part of the second cervical sclerotome forms the whole rst vertebra and the odontoid process (dens) of the axis (Figure 4A) (Black & Scheuer, 1996; Ranade et al., 2007). At that stage the separation of the odontoid process from the anterior arch of the atlas occurs (Black & Scheuer, 1996). Occipitalisation of the atlas takes place if the rst cervical sclerotome does not divide into the cranial and caudal components. The atlas gets assimilated to the occipital region, because the caudal part of the fourth occipital sclerotome unites with the whole rst cervical and cranial part of the second cervical sclerotome (Figure 4B) (Black & Scheuer, 1996; Al-Motabagani & Surendra, 2006). In the case of the skull analysed here, the probable cause of assimilation is a congenital defect. Degenerative, post-tuberculosis or traumatic changes were not observed. Besides, the female had reached an advanced age and she died probably of natural causes. The atlanto-occipital fusion to the basis of occipital bone can cause numerous neurological diseases, as the dimensions of foramen magnum undergo reduction (Figure 5). The symptoms concomitant with occipitalisation are connected with compression on the medulla oblongata, spinal cord, vertebral artery, accessory nerves, anterior and posterior spinal arteries and the venal plexus (Kalla et al., 1989; Bochenek & Reicher, 1990; Wysocki et al., 2003; Tun et al., 2004; Nayak et al., 2005; Scuderi et al., 2005; Al-Motabagani & Surendra, 2006; Gholve et al., 2007). The main reason for this is the high position of the dens in relation to the medulla oblongata (McKechnie, 1994; Black & Scheuer, 1996; Jayanthi et al., 2003; Tun et al., 2004; Nayak et al., 2005; Al-Motabagani & Surendra 2006; Ranade et al., 2007). In humans with normally developed atlanto-occipital region, the capital dimension of foramen magnum (measured between the point basion, situated on the middle plane at the anterior rim of the foramen magnum and the point opisthion situated on the middle plane at the posterior rim of foramen magnum) is over 30 mm, whereas in specimens with occipitalisation it is shorter than 25 mm (Tun et al., 2004). The main symptoms associated with assimilation of the atlas with the occipital bone are: headache and neck pain, numbness in limbs, weakness, abnormal head posture, torticollis caused by pressure upon skull nerves, posteriorly located dull aching headache which grows with coughing and neck movements, restricted head and neck movements, disturbances in balance,
Int. J. Osteoarchaeol. (2011)

Figure 3. Scheme of recombinations in vertebral sclerotomes ra). (skull from Twardogo

Copyright # 2011 John Wiley & Sons, Ltd.

M. Senator and S. Gronkiewicz

Figure 4. (A) Differentiation of IV occipital sclerotome and the rst and second cervical sclerotome into the base of occipital bone and ra). the apical vertebra. (B) Failure in segmentation of the rst cervical sclerotomeatlas occypitalisation (skull from Twardogo

ataxia, nystagmus, visual, auditory, sensory disturbances, etc. (Kalla et al., 1989; McKechnie 1994; Black & Scheuer, 1996; Erdil et al., 2003; Jayanthi et al., 2003; Wysocki et al., 2003; Tun et al., 2004; Nayak et al., 2005; Al-Motabagani & Surendra, 2006; Ranade et al., 2007). Moreover, the pressure on the vertebral artery may cause the vertebral-basilar ischemia, which may lead to its injury (Wysocki et al., 2003; Tun et al., 2004; Al-Motabagani & Surendra, 2006). In the case of the ra, the assimilation of the atlas to skull from Twardogo the occipital bone rather signicantly limited the dimension of foramen magnum (Figure 5). This may indicate that the described case would have had several disorders described above.

Figure 5. Size of foramen magnum after atlanto-occipital fusion ra). This gure is available in colour at (skull from Twardogo wileyonlinelibrary.com.

Black & Scheuer (1996) and Al-Motabagani & Surendra (2006), who examined occipitalisation on skeletal material, noticed a considerable asymmetry of skull bones, with the possibility of a torticollis. In the case that we are presenting, the left part of the atlas was narrower and it seemed as if the person had more movement of the neck to the left side. Furthermore, the left mastoid process was smaller than the right, probably as a result of the fact that the muscles sternocleidomastoid, splenius and the longissimus capitis (those muscles have their insertion on mastoid processes) worked more intensely and more frequently on the right side than the left. In the cases such as the one that we present, an asymmetry of arteries, and one-sided blocking of the vertebral artery can occur (Bergman, 1967; Sartor et al., 1974). This may be a consequence of an error during formation of recombined inter-segmental structures (Al-Motabagani & Surendra, 2006). Symptoms caused by occipitalisation appear usually in the third or fourth decade of life. Younger cases are commonly asymptomatic. This is connected with the fact that the central nervous system becomes less tolerant to repeated blows from the dens of the second cervical vertebra. Also with age, the degree of ligamentous laxity increases and they become less stable (e.g. the transversal ligament of the atlas) (McKechnie, 1994; Erdil et al., 2003; Jayanthi et al., 2003; Tun et al., 2004; Nayak et al., 2005; Ranade et al., 2007). The rst symptoms may appear suddenly even with a small injury and can lead to death later on, although they usually appear gradually (McKechnie, 1994; Jayanthi et al., 2003; Tun et al., 2004; AlMotabagani & Surendra, 2006; Ranade et al., 2007). In order to state whether there are differences between the individuals with atlas assimilation and
Int. J. Osteoarchaeol. (2011)

Copyright # 2011 John Wiley & Sons, Ltd.

Atlas Assimilation to the Basis of the Occipital Bone

ra with skulls of female from Sypniewo Table 1. Comparison of skull from Twardogo Skull measurements Examined skull [mm] 167 89 15 143 120? 25 20 X of the population from Sypniewo (females) n 66 [mm] 172 96 20 33 138 129 No. of measurements according to Martin M1 M5 M6 M7 M8 M17 M10 M11

Skull length (g-op) Basis skull length (n-ba) Occipital bone length (ba-sphba) Foramen magnum length (ba-o) Skull breadth (eu-eu) Skull height (ba-b) Vertebra measurements Sagittal dimension foramen vertebrale of atlas Transversal dimension foramen vertebrale of atlas Xmean of measurements.

Conclusions
Congenital or acquired craniovertebral junction abnormality can cause pressure and lead to disturbances of neural structures, the vascular system and the canal of the cerebrospinal uid. The atlanto-occipital fusion reduces the dimensions of foramen magnum, leading to neurological complications caused by narrowing of the space available for the spinal cord or brainstem. Knowledge about atlanto-occipital fusion can be signicant for radiology, anaesthesiology, orthopaedics and neurological surgery, because disturbances in the atlanto-occipital region can be the cause of a number of symptoms and also sudden death. In the case reported here, the female would have suffered from symptoms described above, which, in a certain degree, could have inuenced her normal functioning. She would have had either a torticollis or habitually kept her neck turned to one side.
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Int. J. Osteoarchaeol. (2011)

those with a normally developed atlanto-occipital region, additional measurements of the skeleton are performed. In the case we are presenting only the skull was preserved, hence some measurements of the skull were made, using Martin & Knussmanns (1988) technique. For comparison a series of medieval females skulls from Poland (Sypniewo) were used. Eight anthropological measurements were carried out on the skull (Table 1). There were noticeable differences in measurements between the skull with occipitalisation and the mean of the series of female skulls from Sypniewo. The dimensions were lower in the specimen with atlanto-occipital fusion. Kalla et al. (1989) noticed that persons with fused atlas to occiput had lower values in body height, body weight, length of limbs or body mass index. Probably the female whose skull we are presenting also had similar features.

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