A case of enchondroma from Carolingian necropolis of St. Pere De Terrassa (Spain): An insight into the archaeological record

A case of enchondroma from Carolingian necropolis of St. Pere De Terrassa (Spain): An insight into the archaeological record

International Journal of Paleopathology xxx (xxxx) xxx–xxx Contents lists available at ScienceDirect International Journal of Paleopathology journal...

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International Journal of Paleopathology xxx (xxxx) xxx–xxx

Contents lists available at ScienceDirect

International Journal of Paleopathology journal homepage: www.elsevier.com/locate/ijpp

A case of enchondroma from Carolingian necropolis of St. Pere De Terrassa (Spain): An insight into the archaeological record Hannah K.M. McGlynna, Miriam Montanes-Gonzalvoa, Assumpció Malgosaa, Giampaolo Pigab, ⁎ Albert Isidroa,c, a b c

Unitat d’Antropologia Biològica, Department BABVE, Facultat de Biociències, Universitat Autònoma de Barcelona, Barcelona, Spain POLCOMING, Department of Political Science, Communication, Engineering and Information Technologies, University of Sassari, Sassari, Italy Hospital Universitari Sagrat Cor de Barcelona, Barcelona, Spain

A R T I C L E I N F O

A B S T R A C T

Keywords: Benign tumour Medieval Paleopathology X-Ray CT scan

Enchondromas occur with an estimated modern incidence rate of 27.7% of benign bone tumors (Hauben and Hogendoorn, 2010), but few are represented in the paleopathological record. The medieval site of St. Pere in Spain has produced a convincing case. The diagnosis was confirmed by X-Ray, CT-scan and μ-CT scan. Therefore UF 755 from St. Pere – a male of more than 60 years old – can be confirmed as a femoral case of enchondroma, supported by evidence, in the paleopathological record.

1. Introduction Enchondromas are benign cartilaginous tumors located in the medullary cavity, most often in tubular bones. They are proliferative remnants of anachronistic growth plate chondrocytes that escape endochondral replacement by bone and so are most frequently located in the metaphysis of the phalanges of the hands, and secondary, in the long tubular bones of the arms and legs −namely that of the humerus and femur (Dahlin, 1981; Mirra, 1989; Schajowicz, 1982). The small bones of the hands often present enlargement of the affected bone accompanied by possible pain. These small bones occasionally will present a fracture causing a limiting or cessation of function of the affected phalanges. However, when the long tubular bones are affected they remain largely asymptomatic. Enchondromas account for approximately 10–25% of all benign bone tumors though it is hypothesized that this figure may be higher. Commonly enchondromas measure less than 3 cm and are rarely larger than 5 cm (Lucas and Bridge, 2013). The peak of prevalence occurs in the second to fourth decades of life but age profile for this neoplasm varies widely. There is no sexual predilection with regards to prevalence (Waldron, 2009; Dahlin, 1981; Fechner and Mills, 1993). The structure of the tumor in dry bone takes the form of rather dense, irregular masses, except in phalanges where they would be round. Due to endochondral ossification they are rigid. This rigidity in the form and structure of the tumor in dry bone would lead to an expectation that they would be preserved readily within the archaeological record. As shall be discussed later, this is however not the case.



Nevertheless, the sparsity within the archaeological record may be a result of the lack of external indications of enchondromas in long bones which masks their presence. They therefore go unobserved in osteological visual analysis, only to be detected if radiological tests are undertaken. Furthermore, the poor conservation of the small tubular bones of the hands likely results in enchondromas being lost from research. Regardless of the reasoning as to the infrequency of enchondromas in the archaeological and palaeopathological records, some cases have been described (Carter and Anderson, 1996; Charlier et al., 2012; Ciranni et al., 2006; Polo-Cerda and López-Flores, 2009) or cited (eg. some cases from Canarias Islands (Martín-Oval et al., 2008), Egypt (Baxarias, 2007), Nubia (Armelagos, 1969), or Russia [cit, at Ciranni et al., 2006]). There are also several cases that include enchondromas or related syndromes in the differential diagnosis (e.g. Kramar et al., 1995; Phillips and Verano, 2011) without a concluding etiology. This work presents an endomedullary mass compatible with enchondroma within the femoral diaphysis of an individual from the medieval necropolis of St. Pere de Terrassa. It will provide radiological information pertaining to this type of lesion, and discuss this diagnosis in the context of other cases published in the archaeological record. 2. Material and methods The site of St. Pere is a monumental archaeological complex, located in the city of Terrassa, 20 km North-West of Barcelona, Spain. It is comprised of three Romanic churches: Sta. Maria, St. Miquel and St.

Corresponding author at: Unitat d’Antropologia Biològica, Department BABVE, Facultat de Biociències, Universitat Autònoma de Barcelona, Barcelona, Spain.

http://dx.doi.org/10.1016/j.ijpp.2017.10.009 Received 31 May 2016; Received in revised form 19 October 2017; Accepted 27 October 2017 1879-9817/ © 2017 Published by Elsevier Inc.

Please cite this article as: McGlynn, H.K., International Journal of Paleopathology (2017), http://dx.doi.org/10.1016/j.ijpp.2017.10.009

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Pere. The subject of this report is one of more than one hundred Carolingian (9th- 10thCenturies) burials that have been excavated in the Necropolis of the St. Pere Church intermittently from 1982 to 2007. These burials are typically decubito supine, in a Southwest-Northeast orientation and are simple graves with anthropomorphic form. In specific cases they are covered with slabs or wood (Garcia et al., 2009; Jordana et al., 2010). The case we present here corresponds to the skeleton UF 755 dated by C14 between 770AD and 1020AD (95.4%; LTL16803ACeDaD Code, Centro di Datazione e Diagnostica (CEDAD), Università de Salento).The entire individual presents an index of preservation of 73% (Armentano et al., 2012) with some taphonomic alterations of the cortical. The taphonomic damage of the right femur resulted in the loss of the cortical bone in the anterior distal diaphysis. Consequently, the internal region of the diaphysis was exposed displaying the presence of a rounded mass bound to the internal wall. The sex and age at death of the individual were determined by studying the auricular surface of the ilium using methods compiled by Ferembach et al. (1980) and Ubelaker (1989) concluding that the individual was a male more than 60 years old. UF 755 has a firm mass in the endomedullary cavity of the distal right femur (Fig. 1). An X-ray and CT scan were taken at the Hospital Universitari Sagrat Cor (Barcelona, Spain) (Fig. 2). X-ray of long bones and small bones of the hand were obtained. Later an additional μ-CT Scan of the damaged femur was acquired at CIRTEBEC (Università degli Studi di Sassari, Italy). In order to visualize the tangible aspects of the 3D structure of the tumour and cortical bone, μ-CT data were collected using a Bruker Skyscan 1172 high-resolution MicroCT system with a 5 μm focal spot size. Fig. 2. Frontal and lateral view of CT images of distal femur of UF 755 individual. Image B indicates the way in which the calcification is attached to the posterior wall.

3. Results partially exposed due to taphonomic damage in the distal diaphysis. Additionally, there is no observed cortical thickening or periosteal reaction. By X-ray, the image shows a flocculent and arc-and-ring pattern (Ragsdale, 1993; Greenspan and Borys, 2016). The CT image (Fig. 2) showed a disordered and dense mass approximately 7 × 2.8 cm, fused to the posterior internal diaphysis wall featuring sharp edges. The abnormal mass structurally differs from normal bone as is also seen in the μ-CT scan 3D images (Fig. 3). The location, ossification and appearance of the identified mass in the results of the X-ray and μ-CT scan support the diagnosis of enchondroma.

The individual UF 755 presented several common pathological conditions seen in aged individuals. Indicators of axial degeneration were documented by way of osteophyte activity on all lumbar vertebrae (L1-L5), Schmorl’s nodes on L3 and L4, and calcified flavum ligaments on most of the dorsal vertebrae. There were osteophytes and enthesophytes of the left radial tuberosity and also osteochondritis of the head of the left radius. The most intriguing pathological alteration is an endomedullary lesion in the right femur (Fig. 1). Macroscopically, the internal mass is distinct from normal surrounding cancellous bone. The sharp, rather circumscribed mass is

4. Discussion The differential diagnosis includes various osteoblastic bone lesions. A bone infarction (a pseudotumoral lesion) should be located within the medullary cavity as outlined by a peripheral shell of amorphous mineralization (Inagaki et al., 2015). These lesions are difficult to differentiate morphologically from other endotumoral cases; in UF 755 there is slight endosteal scalloping (less than 2/3 of the cortical thickness), but no sclerotic rim (Fig. 4). Intramedullary osteomas or enostomas are solid laminations of bone without cancellous structure (Campillo, 2001), which are certainly not present in this case. The differential diagnosis also includes other endomedullary tumors. Of these, the most frequent types are benign (osteoblastoma) and malignant (osteosarcoma, chondrosarcoma). A benign osteoblastoma could display spotted intralesional mineralizations, often associated with a cortical reaction. Bone fibroma conditions have a predilection for the distal femur and have sclerotic type IA border (Mehta et al., 2017). Loss of all unmineralized tumor tissue precludes differentiation of UF 755 from low grade chondrosarcoma by histological analysis. The area most commonly affected by low grade chondrosarcoma is the proximal femur (Schajowicz, 1982).The matrix of the enchondroma

Fig. 1. Image of calcified lesion located inside the medullar diaphysis of the distal right femur belonging to UF 755 individual from St. Pere de Terrassa medieval site.

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Fig. 3. Comparison of different 3D rotated images of a fragment of non-affected spongy tissue of the distal epiphysis of the same femur (A, B, C) and of enchondroma (D, E, F) obtained by μ-CT (Bruker Sky scan 1172 high-resolution μ-CT system with a 5 μm focal spot size was used). The differing densities can be observed between both tissues, the enchondroma particularly appears as a dense and irregular mass.

distinctive arc and ting pattern. In summary, the various alternatives do not fit this femoral lesion. After a comprehensive examination, it is concluded that the case of St. Pere necropolis is compatible with a calcifying EC. World Health Organization classifies a chondroma as a benign bone tumor (Lucas and Brigde, 2013), characterized by neoplastic cartilage formation with benign cellularity. An EC should be central. It could also be multiple in the context of a systemic disease such as Ollier’s disease and Maffucci syndrome. After the bones of the fingers, the most frequently affected location is the femur, according to the largest series of solitary enchondromas analyzed (9.28% out of 334 cases from Campanacci, 1999; 16.3% out of a 166 cases from Dahlin, 1981; 1.01% out of a 825 cases from Mirra, 1989; and 6.9% of proximal or distal cases of femur out of 466 cases from Schajowicz, 1982). In the Mirra and Campanacci series, the area of the femur most frequently affected by EC was the proximal metaphysis. Dahlin’s results favor the distal diaphysis as being more commonly affected than the proximal end, which is the location of the mass of this report. Taking into account all the characteristics of the internal mass of UF 755’s femur (location, X-ray, CT images and μ-CT scan) and comparing them with various bone tumors and bone infarction, the most likely diagnosis is EC. Prior to the discovery of the EC of St. Pere there were few published cases of possible EC in the archaeological literature and even less described (Table 1).The limited number of examples in the archaeological record may be a consequence of difficulties in the identification of the lesion in the skeleton that could only be found by systematic X-ray analysis of all bones of subject cases. Review of these reports finds lack of photographs or X-rays, dubious X-rays, and vague descriptions that are insufficient to support the diagnosis in the majority. The most complete and detailed information backing the diagnosis of EC is only provided in the cases of Auricarro (Ciranni et al., 2006) and d’Arcis-sur-Aube (Charlier et al., 2012). The case of St. Pere de Terrassa increase the list of clear cases of enchondroma of the paleopathological literature.

Fig. 4. Transversal slide of the enchondroma CT showing the lack of pathological scalloping at endosteal cortical bone (arrow), adjacent to the lesion.

(EC), when it is benign, contains chondroid with variable amorphous mineralization substance (Wu and Hochman, 2012); and thus, in dry bone, it is very difficult to ascertain which type of histological pattern our individual presents. It must be remembered that the broken bone was directly in contact with the ground and, in all likelihood, some mineral substances (like dust or sand) are attached to the lesion. Some scholars argue that x-ray examination does not give, with accuracy, a diagnosis between EC and low-grade chondrosarcoma (Geirnaerdt et al., 1997; Crim and Seeger, 1993). Other authors consider there are some radiological patterns that can facilitate differential diagnosis between EC and low-grade chondrosarcoma (Murphey et al., 1998; Flemming and Murphey, 2000). These patterns include: endosteal scalloping, widening of the bone contour, and/or periosteal reaction (McCarthy and Tyler, 2001; Ragsdale et al., 2017), pathological fracture, and mineralization of the lesion matrix. The lesion observed in UF 755 does not feature most of these changes. Radiologically the endosteal scalloping is not larger than 2/3 of the thickness from surrounding cortical bone (Wu and Hochman, 2012). UF 755 also has a more solid matrix −than expected in a chondrosarcoma- creating the 3

4

> 45

> 60

33–46

36–40

35–45

Male

Male

Female

Male

Male

Male

Male

Nécropole d’Arcissur-Aube, Ardenne, France

St. Pere, Terrassa, Spain

Necrópolis de El Salón, Ecija, Spain Huelva, Spain

St Gregory’s Priory, Canterbury, England

Auricarro, Puglia, Italy

Valencia City, Valencia, Spain

25–35

40–45

Age (years)

Sex

Case

Middle third of the right first metatarsal and the distal region of the second right metatarsal.

Diaphysis of the 2ndleft metacarpal bone and 1 st and 2nd phalanx

Medial and distal diaphysis of the proximal phalanx of the third finger of the left hand. Medial diaphysis, left fifth metacarpal

Distal diaphysis, left third and fourth metatarsals

Distal diaphysis, right femur

Metaphyseal-Diaphyseal junction, left humerus

Bone

Napoleonic War (1808)

Medieval (11th–14th centuries)

Yes

Yes



Medieval



Yes



Islamic Period (11th–12th centuries)

Yes

Yes



Islamic Period

1 st phalanx: 3 cm of diameter, 2nd phalanx: 1,5 × 1 cm.

Yes

7 × 3 cm

Increased translucency involving the distal shaft and metaphysis. The defect has a narrow zone of transition and a reasonably well-defined margin; there is expansion of the bone and thinning of the overlying cortex Fusiform swelling of metacarpal diaphysis and asymmetrical neoformation on the palmar surface of the 1 st phalanx and ovoid neoformation on the lateral surface of 2nd phalanx Tumor

Yes

3,2 × 2,7 cm

Strongly calcified, partially ossified, irregular but well-limited mass developed at diaphyso-epiphyseal junction. It is adhered in some points to the deep surface of the cortex. A dense, mottled irregular mass in the diaphysis. It is fused to the posterior cortical. Bilateral tumor that affects the interdigital space between the third and fourth left metatarsals Tumor growth.

Imperial Roman (IIIth–IVth centuries B.C.).

Carolingian (770AD–1020AD)

Photography

Measurements

Article’s Description

Antiquity

Table 1 Proposed cases of enchondroma in the archaeological record. The list include the cases with description, image or complementary diagnostic tests.

No

Yes

Yes

No

No

Yes

Yes

X-ray

No

No

No

No

No

Yes

No

CT Scan

No

No

No

No

No

Yes

No

Other analysis

Polo-Cerda and López-Flores (2009)

Ciranni et al. (2006)

Carter and Anderson (1996)

Polo-Cerda and López-Flores (2009) Polo-Cerda and López-Flores (2009)

Present work

Charlier et al. (2012)

Reference

H.K.M. McGlynn et al.

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Acknowledgements This work is a result of research undertaken as a part of the Masters in Biological Anthropology at the Universitat Autònoma de Barcelona and the Universitat de Barcelona. We would like to thank to A. Moro for allowing us to study the skeletal remains of St. Pere de Terrassa and to J. Puigarnau and S.Nebot from HUSC de Barcelona that completed the radiological images. This research is partially supported by Autonomous Region of Sardinia (LR3/2008-R.Cervelli, S.Politiche), with the research project titled: “Archaeometric and physico-chemical investigation using a multi-technique approach on archaeological, anthropological and paleontological materials from the Mediterranean area and Sardinia.” AI and AM are part of GREAB, research group from Generalitat de Catalunya (2014 SGR 1420). References Armelagos, G.J., 1969. Disease in ancient nubia. Science 163, 255–259. Armentano, N., Esteve, X., Nociarová, D., Malgosa, A., 2012. Taphonomical study of the anthropological remains from Cova Des Pas (Minorca). Quat. Int. 275, 112–119. Baxarias, J., 2007. Estudio Paleopatológico Preliminar de los Restos Humanos Exhumados en la Tumba de Monthemhat (El Asasif, Egypt). Revista Internacional d'Humanitats 12, 27–41. Campanacci, M., 1999. Bone & Soft Tissue Tumours: Clinical Features, Imaging, Pathology and Treatment, second ed. Springer, Vienna, New York. Campillo, D., 2001. Introducción a la Paleopatología. Ediciones Bellaterra, Barcelona. Carter, A.R., Anderson, T., 1996. The first archaeological example of enchondroma? Int. J. Osteoarchaeol. 6, 411–413. Charlier, P., Paresys, C., Brun, L., Huynh-Charlier, I., 2012. Un Enchondrome Humeral Vieux de 1700 ans. Ann. Pathol. 32 (3), 239–241. Ciranni, R., Tempestini, R., Sublimi Saponetti, S., Laraspata, L., Scattarella, V., Fornaciari, G., 2006. Enchondromas in a medieval skeleton from Southern Italy. An ancient benign tumor of the bones. Paleopathol. Newsl. 134, 24–27. Crim, J.R., Seeger, L.I., 1993. Diagnosis of low-grade chondrosarcoma. Radiology 189 (2), 503–504. Dahlin, D.C., 1981. Tumores Oseos, second ed. Ediciones Toray, Barcelona. Fechner, R.E., Mills, S.E., 1993. Tumors of the Bones and Joints Atlas of Tumor Pathology. Armed Forces Institute of Pathology, Washington D.C. Ferembach, D., Schwidetzky, I., Stloukal, M., 1980. Recommendations for age and sex diagnosis of skeletons. J. Hum. Evol. 9, 517–549. Flemming, D.J., Murphey, M.D., 2000. Enchondroma and chondrosarcoma. Semin. Musculoskelet. Radiol. 4 (1), 59–71. Garcia, M.G., Moro, A., Tuset, F., 2009. La Seu Episcopal d’Ègara. Arqueologia d’un Conjunt Cristià del Segle IV al IX. Institut Català d’Arqueologia Clàssica, Documenta 8, Tarragona. Geirnaerdt, M.J.A., Hermans, J., Bloem, J.L., Kroon, H.M., Pope, T.L., Taminiau, A.H., Hogendoorn, P.C., 1997. Usefulness of radiology in differentiating enchondroma

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