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Keywords:

  • atlas occipitalization;
  • atlanto-occipital fusion;
  • congenital;
  • Apollonia Pontica;
  • Bulgaria

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Case descriptions
  5. Discussion and conclusions
  6. Acknowledgements
  7. Conflict of Interest
  8. References

Occipitalization of the atlas was observed in two adult female skeletons from the Greek colonial site of Apollonia Pontica (5th to 3rd centuries BC), located on the Bulgarian Black Sea coast. Representing a rare congenital anomaly of the atlanto-occipital junction, this condition has been documented in very few skeletal remains from Classical antiquity. Postmortem damage to one of the specimens prevented an evaluation of its clinical significance. The dimensions of the second specimen, however, suggest that the affected individual may have experienced some neurological symptoms associated with her condition. The burial of the two females in close proximity to one another raises the possibility that they may have been biologically related. Copyright © 2012 John Wiley & Sons, Ltd.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Case descriptions
  5. Discussion and conclusions
  6. Acknowledgements
  7. Conflict of Interest
  8. References

Congenital occipitalization of the atlas, also referred to as atlanto-occipital fusion or atlanto-occipital assimilation, is the partial or complete fusion of the atlas to the base of the occipital bone. Representing a transitional vertebra at the occipito-cervical border, it results from failure of segmentation of the fourth occipital and first cervical sclerotomes such that the caudal part of the fourth occipital sclerotome fuses with the entire first cervical sclerotome and the cranial part of the second one (Black & Scheuer, 1996). Its expression is variable, and any part of the atlas (i.e. anterior arch, lateral masses, and/or posterior arch) may be affected (Gholve et al., 2007). Fusion may be partial or complete (Nayak et al., 2005; Al-Motabagani & Surendra, 2006; Ranade et al., 2007), and unilateral or bilateral (Gholve et al., 2007; Kassim et al., 2010). Its etiology is unknown, but both genetic and environmental factors have been implicated, and its occurrence within families has been documented (Kalla et al., 1989). It may be associated with other vertebral anomalies such as spina bifida and block vertebrae (Merbs & Euler, 1985; Jayanthi et al., 2003; Gholve et al., 2007).

Although occipitalization of the atlas is present at birth, it is typically diagnosed fortuitously through radiography, or inadvertently detected through autopsy or dissection (Kassim et al., 2010). Thus, it often goes undetected in living individuals, making the calculation of its incidence in contemporary populations difficult. Although it is one of the most common anomalies of the atlanto-occipital junction (Lang, 1995), it is relatively rare in the general population, with reported rates ranging from 0.14% to 0.75%. A number of studies have found both sexes to be equally affected (Al-Motabagani & Surendra, 2006), while others report a male predominance (Gholve et al., 2007).

While this anomaly is often asymptomatic, it may be associated with a variety of symptoms if the failure of segmentation results in asymmetry and altered joint dynamics. These include headache and neck pain, restricted head and neck movements, an abnormally short neck, torticollis, and numbness and pain in the limbs (McRae & Barnum, 1953). Compression of the vertebral artery can lead to dizziness, seizures, and fainting due to reduced blood flow to the brain (Jayanthi et al., 2003; Kassim et al., 2010), and neurological symptoms can arise from compression of the spinal cord or brain stem due to a narrowing of the foramen magnum (Jayanthi et al., 2003; Saini et al., 2009; Kassim et al., 2010). Neurological symptoms are uncommon in younger individuals, however, and usually do not appear until the third or fourth decade of life (Gholve et al., 2007). In severe cases, sudden death may occur (Vakili et al., 1985).

Case descriptions

  1. Top of page
  2. Abstract
  3. Introduction
  4. Case descriptions
  5. Discussion and conclusions
  6. Acknowledgements
  7. Conflict of Interest
  8. References

The two individuals described in this report were excavated from the Kalfata–Budjaka necropolis associated with the ancient Greek colonial site of Apollonia Pontica, located on the Black Sea coast of Bulgaria. Founded in 610 BC by colonists from the city of Miletus, the settlement and in particular its cemeteries have been the focus of archaeological research since the 1940s (see Nedev & Panayotova, 2003 for a detailed description of the site). Since 1992, more than 1500 graves dating from the 5th to 3rd centuries BC have been excavated from the necropolis, and many of the skeletons contained within these graves have been the focus of previous studies by the author. Of the more than 500 adult and subadult skeletons recovered from the necropolis and analyzed to date, two out of 218 adults (105 males and 113 females) with a preserved atlas exhibited occipitalization of the atlas, yielding a prevalence of 0.9% (0% for males and 1.8% for females).

The first individual (#5536-13) was determined to be female based on morphological features of the cranium and pelvic bones (Buikstra & Ubelaker, 1994). The age-at-death was estimated to be 21 to 35 years based on auricular surface morphology (Lovejoy et al., 1985), complete union of all epiphyses, and minimal tooth wear. The atlas had been damaged postmortem, and the remaining left fragment exhibited complete fusion of the superior articular facet with the left occipital condyle, and the anterior arch to the anterior rim of the foramen magnum (Figure 1). Two small foramina are visible along the line of fusion, one located directly superior to the anterior arch and the second one situated between the anterior arch and the occipital condyle. The right articular facet, transverse process and foramen, and posterior arch had broken off postmortem. The left transverse foramen was visible but incomplete due to postmortem damage, the left hypoglossal canal was intact and normal in appearance (Figure 2), an additional small foramen was present inferior to the canal, and the left inferior articular facet was almost completely flat. The skeleton exhibited no other evidence of pathology with the exception of cribra orbitalia in both orbits, carious lesions in three maxillary molars, and calculus deposits on most of the teeth.

image

Figure 1. Anterior view of the left atlas fragment of individual #5536-13. The left superior articular facet is fused with the left occipital condyle, and the anterior arch is fused with the anterior rim of the foramen magnum. This figure is available in colour online at wileyonlinelibrary.com/journal/oa.

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image

Figure 2. View of the left inferior articular facet of the atlas of individual #5536-13. The hypoglossal canal is normal, and an additional small foramen is located inferior to the canal. This figure is available in colour online at wileyonlinelibrary.com/journal/oa.

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The second individual (#5536-17) was determined to be female based on morphological features of the cranium and pelvic bones (Buikstra & Ubelaker, 1994). The age-at-death was estimated to be 36–50 years based on pubic symphysis morphology (Brooks & Suchey, 1990), ectocranial suture closure (Meindl & Lovejoy, 1985), and the presence of moderate tooth wear. The base of the occipital bone had broken way from the rest of the occipital bone postmortem, the superior articular facets of the atlas were completely assimilated into the occipital condyles, and the atlas exhibited a very slight inclination to the left side (Figure 3). One small foramen was visible superior to the right superior articular facet, and the left and right inferior articular facets were smooth and flat. The transverse processes were morphologically normal and separate from the occipital bone. The right transverse foramen was intact, and the left foramen was visible but incomplete due to postmortem damage. Some damage had also occurred to the posterior arch, but both the anterior and posterior arches were intact and were separate from the margins of the foramen magnum (Figures 3 and 4). The left and right hypoglossal canals were normal in appearance. This individual also had Schmorl's nodes in the superior body of an unidentified lower thoracic and upper lumbar vertebrae, and a possible healed fracture to the distal end of the right 5th metacarpal.

image

Figure 3. Anterior view of the occipitalized atlas in individual #5536-17. The superior articular facets are fused with the occipital condyles, and there is a very slight inclination of the atlas to the left side. The anterior arch is separate from the anterior margin of the foramen magnum. This figure is available in colour online at wileyonlinelibrary.com/journal/oa.

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image

Figure 4. Posterior view of the occipitalized atlas in individual #5536-17. The posterior arch is separate from the posterior margin of the foramen magnum. This figure is available in colour online at wileyonlinelibrary.com/journal/oa.

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Discussion and conclusions

  1. Top of page
  2. Abstract
  3. Introduction
  4. Case descriptions
  5. Discussion and conclusions
  6. Acknowledgements
  7. Conflict of Interest
  8. References

Isolated cases of atlas occipitalization have been documented in archaeological remains from ca. 600–500 BC and Greco-Roman Egypt (Barclay-Smith, 1911; Hussien et al., 2009), Late Roman Corinth (Gejvall & Henschen, 1968), 1st century BC to 3rd century AD Armenia (Khudaverdyan, 2011), Anasazi sites (AD 750 to proto-historic) in the American Southwest (Palkovich, 1980; Reed, 1981; Merbs & Euler, 1985; Akins, 1986; Barnes, 1994), an 11th to 12th century sample from Devín, Slovakia (Masnicová & Beňuš, 2003), the 17th century site of Twardogóra in southern Poland (Senator & Gronkiewicz, ), a 16th to 19th century monastery in Split, Croatia (Bašić et al., ), and Spain, Morocco, Illinois, and the Canary Islands (Aufderheide & Rodríguez-Martin, 1998). In a number of these cases, the occipitalized atlas was associated with other vertebral anomalies, including block vertebrae and supernumerary cervical vertebrae (Barclay-Smith, 1911; Merbs & Euler, 1985).

As noted earlier, occipitalization of the atlas may be associated with restricted head and neck movements and torticollis. In their description of an early 19th century skeleton from London, Black & Scheuer (1996) note, for instance, that lateral displacement and slight rotation of the atlas to the right side meant that the individual whom they described likely carried her head slightly tilted to the right. Similarly, slight tilting of the atlas to the left and marked cranial asymmetry in an archaeological specimen from Poland suggest that the neck of the affected individual was habitually turned to one side (Senator & Gronkiewicz, ). In the case of individual #5536-17 described in this report, the atlas was slightly inclined to the left side. The angle of the inclination, however, was very small and as such, she likely had no visible torticollis.

Complete assimilation of the atlas into the occipital bone can also result in compression of the vertebral artery, leading to dizziness, seizures, and fainting due to reduced blood flow to the brain. In the case of individual #5536-13, postmortem loss of the posterior arch of the atlas made it impossible to evaluate the effect of this anomaly on the vertebral artery. In contrast, the separation of the posterior arch from the posterior margin of the foramen magnum in individual #5536-17 means that the vertebral arteries would not have been impaired.

A significant reduction in the size of the foramen magnum due to overlapping of the margins by the fused atlas can lead to neurological symptoms as a result of compression of the spinal cord or brain stem (Al-Motabagani & Surendra, 2006). Standard sagittal and transverse diameters of the foramen magnum are reported in the clinical literature to range from 28 to 38 mm and 25 to 40 mm, respectively (Lang, 1995), and measurements that fall within these ranges have been interpreted as indicating an absence of neurological symptoms (Skrzat et al., 2010; Jadhav et al., 2012). The sagittal diameter, in particular, is considered to be ‘an important landmark in symptomatic patients’ (Tun et al., 2004: 44), and measurements less than 30 mm are considered to be abnormal (Hayes et al., 1999). A sagittal diameter of 25 mm recorded in an archaeological specimen from Poland, for example, has been interpreted as indicative of possible symptoms (Senator & Gronkiewicz, ). Postmortem damage to the cranium of individual #5536-13 made it impossible to measure the dimensions of the foramen magnum. In individual #5536-17, the sagittal diameter measured 27 mm, a value that falls below the range recorded for other archaeological and modern samples (30 to 43 mm; Gruber et al., 2009). If we consider a sagittal diameter of 30 mm to be the lowest end of the range considered asymptomatic, the measurement obtained for this particular individual would be considered abnormal and thus possibly associated with symptoms. Population variability in the dimensions of the foramen magnum has been documented, although reported values tend to cluster closely together (Gruber et al., 2009). Measurement of the sagittal diameter in a sample of five other adult females excavated from the Kalfata–Budjaka necropolis at Apollonia out of a total of only 36 crania for which craniometric data could be obtained yielded a mean value of 34 mm ±1.3. While this sample size is admittedly very small and may not be representative of the population that once lived at the site, it points to the likelihood that individual #5536-17 did, in fact, have an abnormally small foramen magnum. If so, she may have experienced some neurological symptoms associated with her condition.

It is also important to consider whether the foramen magnum in individuals with atlas occipitalization is reduced in size due to the protrusion of the odontoid process of the axis into the foramen. Spinal cord encroachment resulting from protrusion of the odontoid into the foramen magnum has been defined as being present if the distance from the posterior margin of the foramen magnum or the posterior arch of the atlas to the posterior aspect of the odontoid measures 19 mm or less (McRae & Barnum, 1953) to 13 mm or less (Gholve et al., 2007). As Merbs & Euler (1985) note, however, this dimension also varies by population, and smaller dimensions may be considered normal for some populations. The odontoid process of individual #5536-17 did not appear to be unusually large, and its position when in articulation with the atlas was not abnormally high. As such, it likely did not further reduce the size of the foramen magnum in this individual.

As noted earlier in this report, genetic and environmental factors have been implicated in the development of atlas occipitalization, and its occurrence within families has been documented (Kalla et al., 1989). For this reason, the location within the necropolis of these particular individuals may be informative of biological relationships. Within the Kalfata–Budjaka necropolis, clusters of graves surrounded by stone walls and displaying similar types of artifacts have been interpreted as family plots (Nedev & Panayotova, 2003). Such plots are commonly found in Greek necropoleis (Humphreys, 1980: 101, 106, 108) and appear at Apollonia during the 4th century BC. The skeletons of these women were interred in typical pit graves located in adjacent grid-squares, raising the possibility that they may have been biologically related. While this cannot be determined from the available evidence, DNA analysis and shared non-metric traits have the potential to reveal genetic relationships between individuals with the same congenital condition. Unfortunately, cranial non-metric data could not be gathered for individual #5536-13 due to poor preservation of the cranium, but future DNA analysis, if successful, could be very informative.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Case descriptions
  5. Discussion and conclusions
  6. Acknowledgements
  7. Conflict of Interest
  8. References

The author would like to thank Dimitar Nedev, Director of the Archaeological Museum in Sozopol, and Kristina Panayotova (Institute of Archaeology in Sofia) for granting permission to examine these remains and for providing the burial data.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Case descriptions
  5. Discussion and conclusions
  6. Acknowledgements
  7. Conflict of Interest
  8. References
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