The oldest case yet reported of osteoarthritis in a dog: an archaeological and radiological evaluation

[en] A century ago the remains of a dog skeleton were found in an archaeological double human burial, near Bonn-Oberkassel (Germany). Recent re-examination of the dog remains revealed that they were about 14,500 years old. Based on the growth plates, the animal was considered to be approximately 7·5 months old at the time of death. Based on the minimal humeral diameter, it was calculated that it was approximately 0·47 m tall at the shoulder and weighed approximately 15·7 kg. The right proximal ulna of this skeleton showed osteoarthritis, manifested by an osteophyte of 5×3×1·5 mm3 at its cranial edge, with no identified primary developmental causes for osteoarthritis. Osteochondritis dissecans, joint incongruity and trauma are possible aetiologies. The left ulna did not reveal any abnormalities. © 2016 British Small Animal Veterinary Association

Disciplines :

History
Archaeology

Author, co-author :

Janssens, L. A. A.; Clinic for Orthopaedic Surgery of Companion Animals, Rotterdam, Netherlands, Department of Archaeology, University of Leiden, Leiden, Netherlands

Street, M.; Monrepos Archaeological Research Centre and Museum for Human Behavioural Evolution, Neuwied, Germany

Miller, Rebecca ; Université de Liège - ULiège

Hazewinkel, H. A. W.; Department of Clinical Sciences of Companion Animals, Utrecht University, Utrecht, Netherlands

Giemsch, L.; Archäologisches Museum Frankfurt, Karmelitergasse 1D-60311 Frankfurt am Main, Germany

Schmitz, R.; LVR-Landesmuseum Bonn, Rheinisches Landesmuseum für Archäologie, Kunst- und Kulturgeschichte, Bachstraße 5, Bonn, Germany

Language :

English

Title :

The oldest case yet reported of osteoarthritis in a dog: an archaeological and radiological evaluation

Publication date :

2016

Journal title :

Journal of Small Animal Practice

ISSN :

0022-4510

eISSN :

1748-5827

Publisher :

Wiley, Oxford, United Kingdom

Volume :

Issue :

Pages :

568-574

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 08 June 2018

Statistics

Number of views

80 (1 by ULiège)

Number of downloads

0 (0 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Altuna, J.g, Baldeon, A. & Mariezkurrena, K. (1984) Dépôts rituels magdaléniens de la grotte d'Erralla (Pays Basque). Munibe. Sociedad de Ciencias Naturales Aranzadi (San Sebastian) 36, 3-10
Anderson, J. F., Hall-Martin, A. & Russell, D. A. (1985) Long-bone circumference and weight in mammals, birds, and dinosaurs. Journal of Zoology 207, 53-61
Anyonge, W. (1993) Body mass in large extant and extinct carnivores. Journal of Zoology 231, 339-350
Aranbarri, J., González-Sampériz, P., Valero-Garcés, B., et al. (2014) Rapid climatic changes and resilient vegetation during the Lateglacial and Holocene in a continental region of south-western Europe. Global and Planetary Change 114, 50-65
Bell, S., Carter, S. & Bennett, D. (1991) Canine distemper viral antigens and antibodies in dogs with rheumatoid arthritis. Research in Veterinary Science 50, 64-68
Benecke, N. (1987) Studies on early dog remains from Northern Europe. Journal of Archaeological Science 14, 31-49
Benecke, N. (1994) Archäozoologische Studien zur Entwicklung der Haustierhaltung. Akademie Verlag Schriften zur Ur- und Frühgeschichte 46, 21-49
Bennett, D. & Taylor, D. (1988) Bacterial infective arthritis in the dog. Journal of Small Animal Practice 29, 207-230
Bennett, D., Duff, S., Kene, R., et al. (1981) Osteochondritis dissecans and fragmentation of the coronoid process in the elbow joint of the dog. The Veterinary Record 109, 329-336
Binois, M., Wardius, C., Rio, P., et al. (2014) A dog's life: multiple trauma and potential abuse in a medieval dog from Guimps (Charente, France). International Journal of Paleopathology 3, 39-47
Blom, A. B., van Lent, P. L., Holthuysen, A. E., et al. (2004) Synovial lining macrophages mediate osteophyte formation during experimental OA. Osteoarthritis and Cartilage 12, 627-635
Boitani, L., Francisci, F., Ciucci, P., et al. (1995) Population biology and ecology of feral dogs in central Italy. In: The Domestic Dog: Its Evolution, Behavior, and Interactions with People. Ed J. Serpell. Cambridge University Press, Cambridge, UK. pp 217-244
Bookstein, F. L. (1997) Morphometric Tools for Landmark Data: Geometry and Biology. Cambridge University Press, Cambridge, UK
Boudadi-Maligne, M. & Escarguel, G. (2014) A biometric re-evaluation of recent claims for Early Upper Palaeolithic wolf domestication in Eurasia. Journal of Archaeological Science 45, 80-89
Boudadi-Maligne, M., Mallye, J.-B., Langlais, M., et al. (2012) Des restes de chiens magdaléniens à l'abri du Morin (Gironde, France). Implications socio-économiques d'une innovation zootechnique. Revue d'archéologie Préhistorique 23, 39-54
Célérier, G. (1994) L'abri sous roche de Pont d'Ambon à Bourdeilles (Dordogne): présentation. Gallia Préhistoire 36, 65-144
Célérier, G., Tisnerat, N. & Valladas, H. (1999) Données nouvelles sur l'âge des vestiges de chien à Pont d'Ambon, Bourdeilles (Dordogne)/New data on the age of Canis remains at Pont d'Ambon, Bourdeilles (Dordogne, France). Revue d'archéologie Préhistorique 11, 163-165
Chaix, L. (2000) A preboreal dog from the northern Alps (Savoie, France). BAR International Series 889, 49-60
Chrószcz, A., Janeczek, M., Pasicka, E., et al. (2014) Paleopathology of brown bears (Ursus arctos, L. 1758) from Liptovská Mara, Northern Slovakia. Research Opinions in Animal and Veterinary Sciences 4, 35-39
Clutton-Brock, J. (1962) Near Eastern canids and the affinities of the Natufian dogs. Zeitschrift für Tierzüchtung und Züchtungsbiologie 76, 326-333
Clutton-Brock, J. (2012) Animals as domesticates: a world view through history. Michigan University Press, East Lansing, Michigan, USA.
Cross, E. (1940) Arthritis among wolves. Canadian Field-Naturalist 54, 2-4
Drake, A. G. (2011) Dispelling dog dogma: an investigation of heterochrony in dogs using 3D geometric morphometric analysis of skull shape. Evolution & Development 13, 204-213
Drake, A. G., Coquerelle, M. & Colombeau, G. (2015) 3D morphometric analysis of fossil canid skulls contradicts the suggested domestication of dogs during the late Paleolithic. Scientific Reports 5, 1-8
Druzhkova, A. S., Thalmann, O., Trifonov, V. A., et al. (2013) Ancient DNA analysis affirms the canid from Altai as a primitive dog. PLoS One 8, e57754
Duleba, A., Skonieczna, K., Bogdanowicz, W., et al. (2015) Complete mitochondrial genome database and standardized classification system for Canis lupus familiaris. Forensic Science International: Genetics 19, 123-129
Fahy, N., de Vries-Van Melle, M., Lehman, J., et al. (2014) Human osteoarthritic synovium impacts chondrogenic differentiation os mesenchymal stem cells via mach rophage polarisation state. Osteoarthritis and Cartilage 22, 1167-1175
Freedman, A. H., Gronau, I., Schweizer, R. M., et al. (2014) Genome sequencing highlights the dynamic early history of dogs. PLoS Genetics 10, e1004016
Fritts, S. H., Stephenson, R. O., Hayes, R. D., et al. (2003) Wolves and humans. In: Wolves: Behavior, Ecology and Conservation. Eds L. D. Mech and L. Boitani. The University of Chicago Press, Chicago, IL, USA and London, UK. pp 289-316
Frost-Christensen, L., Mastbergen, S., Vianen, M., et al. (2008) Degeneration, inflammation, regeneration, and pain/disability in dogs following destabilization or articular cartilage grooving of the stifle joint. Osteoarthritis and Cartilage 16, 1327-1335
Germonpré, M., Sablin, M. V., Stevens, R. E., et al. (2009) Fossil dogs and wolves from Palaeolithic sites in Belgium, the Ukraine and Russia: osteometry, ancient DNA and stable isotopes. Journal of Archaeological Science 36, 473-490
Germonpré, M., Lázničková-Galetová, M., Sablin & M. V. (2012) Palaeolithic dog skulls at the Gravettian Předmostí site, the Czech Republic. Journal of Archaeological Science 39, 184-202
Germonpré, M., Sablin, M., Després V., et al. (2013) Palaeolithic dogs and the early domestication of the wolf: a reply to the comments of Journal of Crockford and Kuzmin. Archaeological Science 40, 786-792
Gräslund, A.-S. (2004) Dogs in graves-a question of symbolism? In: Pecus. Man and Animal in Antiquity. Ed B. S. Frizell. The Swedish Institute in Rome, Rome, Italy. pp 167-176
Greer, M., Greer, J. & Gillingham, J. (1977) OA in selected wild mammals. Proceedings of the Oklahoma Academy of Science 57, 39-43
Grøndalen, J. & Grøndalen, T. (1981) Arthrosis in the elbow joint of young rapidly growing dogs. V. A pathoanatomical investigation. Nordisk Veterinaermedicin 33, 1-16
Harcourt, R. A. (1974) The Dog in Prehistoric and Early Historic Britain. Journal of Archaeological Science 1, 151-175
Hewitt, G. M. (1999) Post-glacial re-colonization of European biota. Biological Journal of the Linnean Society 68, 87-112
Ho, S. Y., Phillips, M. J., Cooper, A., et al. (2005) Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Molecular Biology and Evolution 22, 1561-1568
Housley, R. A., Gamble, C. S., Street, M., et al. (1997) Radiocarbon evidence for the Lateglacial human recolonisation of northern Europe. Proceedings of the Prehistoric Society 63, 25-54
Jalut, G., Marti, J. M., Fontugne, M., et al. (1992) Glacial to interglacial vegetation changes in the northern and southern Pyrenees: deglaciation, vegetation cover and chronology. Quaternary Science Reviews 11, 449-480
Janssens, L. A., De Meurichy, W. & Janssens, D. L. (1994) Surgical correction of patellar luxation in a cheetah (Acinonyx jubatus). Journal of Zoo and Wildlife Medicine 25, 466-471
Jordan, P. A., Shelton, P. C. & Allen, D. L. (1967) Numbers, turnover, and social structure of the Isle Royale wolf population. American Zoologist 7, 233-252
Kirberger, R. & Fourie, S. (1998) Elbow dysplasia in the dog: pathophysiology, diagnosis and control: review article. Journal of the South African Veterinary Association 69, 43-54
Kurtén, B. (1968) Pleistocene Mammals of Europe. Weindefield and Nicolson, London
Langlais, M., Costamagno, S., Laroulandie, V., et al. (2012) The evolution of Magdalenian societies in South-West France between 18,000 and 14,000 calBP: changing environments, changing tool kits. Quaternary International 272, 138-149
Larson, G. & Burger, J. (2013) A population genetics view of animal domestication. Trends in Genetics 29, 197-205
Larsson, L. (1990) Dogs in fraction–symbols in action. In: Contributions to the Mesolithic in Europe, Vol. 5. Eds P. M. Vermeersch and P. van Peer. Leuven University Press, Leuven, Belgium. pp 153-160
Lau, S., Wolschrijn, C., Hazewinkel, H., et al. (2013) The early development of medial coronoid disease in growing Labrador retrievers: radiographic, computed tomographic, necropsy and micro-computed tomographic findings. The Veterinary Journal 197, 724-730
Lawing, A. M. & Polly, P. D. (2010) Geometric morphometrics: recent applications to the study of evolution and development. Journal of Zoology 280, 1-7
Leesch, D., Müller, W., Nielsen, E., et al. (2012) The Magdalenian in Switzerland: re-colonization of a newly accessible landscape. Quaternary International 272, 191-208
Leonard, J. A., Wayne, R. K., Wheeler, J., et al. (2002) Ancient DNA evidence for Old World origin of New World dogs. Science 298, 1613-1616
Losey, R. J., Garvie-Lok, S., Leonard, J. A., et al. (2013) Burying dogs in ancient cis-Baikal, Siberia: temporal trends and relationships with human diet and subsistence practices. PLoS One 8, e63740
MacKinnon, M. (2010) ‘Sick as a dog’: zooarchaeological evidence for pet dog health and welfare in the Roman world. World Archaeology 42, 290-309
May, C., Carter, S., Bell, S., et al. (1994) Immune responses to canine distemper virus in joint diseases of dogs. Rheumatology 33, 27-31
Miller, R. (2012) Mapping the expansion of the Northwest Magdalenian. Quaternary International 279-280, 209-230
Morey, D. F. (1986) Studies on Amerindian dogs: taxonomic analysis of canid crania from the Northern Plains. Journal of Archaeological Science 13, 119-145
Morey, D. F. (1992) Size, shape and development in the evolution of the domestic dog. Journal of Archaeological Science 19, 181-204
Morey, D. F. (2006) Burying key evidence: the social bond between dogs and people. Journal of Archaeological Science 33, 158-175
Morey, D. (2010) Dogs: Domestication and the Development of a Social Bond. Cambridge University Press, Cambridge, UK
Morey, D. F. (2014) In search of paleolithic dogs: a quest with mixed results. Journal of Archaeological Science 52, 300-307
Morey, D. & Wiant, M. (1992) Early holocene domestic dog burials from the North American midwest. Current Anthropology 33, 224-229
Moskowitz, R. W. (1972) Experimental models of degenerative joint disease. Seminars in Arthritis and Rheumatism 1, 95-116
Muller, W. (2005) The domestication of the wolf-the inevitable first? In: The first steps of animal domestication. Eds J.-D. Vigne, J. Peters and D. Helmer. Oxbow Books, Oxford, UK. pp 34-40
Napierala, H. & Uerpmann, H. P. (2012) A ‘new’ palaeolithic dog from Central Europe. International Journal of Osteoarchaeology 22, 127-137
Nehring, A. (1888) Zur Abstammung der Hunde-Rassen. In: Zoologische Jahrbücher Abtheilung Für Systematik, Geographie ind Biologie der Thiere. Ed G. Spengel. Verlag Gustav Fischer, Jena, Germany. pp 51-59
Nobis, G. (1979) Der älteste haushund lebte vor 14,000 Jahren. Umschau 79, 610
Nobis, G. (1981) Aus bonn: das älteste haustier des menschen. Unterkiefer eines hundes aus dem magdaleniengrab von bonn-oberkassel. Das Reinische Landesmuseum Bonn:Berichte aus der Arbeit des Museums 81, 49-50
Olsen, S. J. & Olsen, J. W. (1977) The Chinese wolf, ancestor of New World dogs. Science 197, 533-535
Onar, V. & Belli, O. (2005) Estimation of shoulder height from long bone measurements on dogs unearthed from the Van-Yoncatepe early iron age necropolis in Eastern Anatolia. Revue de Médecine Vétérinaire 156, 53-60
O'Regan, H. & Kitchener, A. C. (2005) The effects of captivity on the morphology of captive, domesticated and feral mammals. Mammal Review 35, 215-230
Ovodov, N. D., Crockford, S. J., Kuzmin, Y. V., et al. (2011) A 33,000-year-old incipient dog from the Altai Mountains of Siberia: Evidence of the earliest domestication disrupted by the Last Glacial Maximum. PLoS One 6, e22821
Pionnier-Capitan, M. (2010) La domestication du chien en Eurasie: étude de la diversité passée, approches ostéoarchéologiques, morphométriques et paléogénétiques. Ph.D. Dissertation, Ecole Normale Superieure, Lyon, France
Pionnier-Capitan, M., Bemilli, C., Bodu, P., et al. (2011) New evidence for Upper Palaeolithic small domestic dogs in South-Western Europe. Journal of Archaeological Science 38, 2123-2140
Räikkönen, J., Bignert, A., Mortensen, P., et al. (2006) Congenital defects in a highly inbred wild wolf population (Canis lupus). Mammalian Biology-Zeitschrift für Säugetierkunde 71, 65-73
Räikkönen, J., Vucetich, J. A., Peterson, R. O., et al. (2009) Congenital bone deformities and the inbred wolves (Canis lupus) of Isle Royale. Biological Conservation 142, 1025-1031
Rütimeyer, L. (1861) Die Fauna der Pfahlbauten der Schweiz. Geschichte der Wilden und der Haus-Saugetiere. Neue Denkschrift der Algemeinne Schweizerische Geselschaft der ges. Naturwissenschaft, 19, Basel, Switzerland. 1-235s
Savolainen, P., Zhang, Y.-P., Luo, J., et al. (2002) Genetic evidence for an East Asian origin of domestic dogs. Science 298, 1610-1613
Savolainen, P., Leitner, T., Wilton, A. N., et al. (2004) A detailed picture of the origin of the Australian dingo, obtained from the study of mitochondrial DNA. Proceedings of the National Academy of Sciences of the United States of America 101, 12387-12390
Skoglund, P., Götherström, A. & Jakobsson, M. (2011) Estimation of population divergence times from non-overlapping genomic sequences: examples from dogs and wolves. Molecular Biology and Evolution 28, 1505-1517
Stockhaus, K. (1965) Metrische Untersuchungen an Schädeln von Wölfen und Hunden. Journal of Zoological Systematics and Evolutionary Research 3, 157-258
Street, M. (2002) Ein wiedersehen mit dem hund von Bonn-Oberkassel. Bonner Zoologische Beitrage 50, 269-290
Street, M. & Jöris, O. (2014) Das Alter der Funde von Bonn-Oberkassel. In: Eiszeitjäger. Leben im Paradies. Europa vör 15 000 Jahren Ed LVR LandesMuseum. Nünnerich-Asmus-Verlag, Mainz, Germany. pp 182-189
Street, M. & Jöris, O. (2015) The age of the Oberkassel burial in the context of climate, environment and the late glacial settlement history of the Rhineland. In: Oberkassel 1914 – 2014. 100 Years of Research on the Late Glacial Burial. Eds L. Giemsch and R. Schmitz. Rheinische Ausgrabungen, Bonn, Germany. pp 72-83
Street, M., Jöris, O. & Turner, E. (2012) Magdalenian settlement in the German Rhineland–An update. Quaternary International 272, 231-250
Studer, T. (1901) Die prähistorischen Hunde in ihrer Beziehung zu den gegenwärtig lebenden Rassen. In: Die Prähistorischen Hunde in Ihrer Beziehung zu den Gegenwärtig Lebenden Rassen. Zurcher und Furrer, Zurich, Switzerland. pp 1-136c
Suminński, P. (1975) Morphologische Unterscheidungsmerkmale zwischen Wolfs-(Canis lupus L.) und Hundeschädel (Canis familiaris L.) Zeitschrift für Jagdwissenschaft 21, 227-232
Sumner-Smith, G. (1966) Observations on epiphyseal fusion of the canine appendicular skeleton. Journal of Small Animal Practice 7, 303-311
Temwichitr, J., Leegwater, P. A. & Hazewinkel, H. A. (2010) Fragmented coronoid process in the dog: a heritable disease. The Veterinary Journal 185, 123-129
Thalmann, O., Shapiro, B., Cui, P., et al. (2013) Complete mitochondrial genomes of ancient canids suggest a European origin of domestic dogs. Science 342, 871-874
Tirgari, M. (1974) Clinical radiographical and pathological aspects of arthritis of the elbow joint in dogs. Journal of Small Animal Practice 15, 671-679
Tsuda, K., Kikkawa, Y., Yonekawa, H., et al. (1997) Extensive interbreeding occurred among multiple matriarchal ancestors during the domestication of dogs: evidence from inter-and intra-species polymorphisms in the D-loop region of mitochondrial DNA between dogs and wolves. Genes & Genetic Systems 72, 229-238
Utumo, L., van Osch, G., Verhaar, J., et al. (2015) Macrophage phenotype modulation to control synovial inflammation. Osteoarthritis and Cartilage 23, 226-237
Verworn, M., Steinmann, G. & Bonnet, R. (1919) Der diluviale Menschenfund von Obsercassel bei Bonn. JF Bergmann Verlag, Wiesbaden, Germany
Vescovi, E., Ravazzi, C., Arpenti, E., et al. (2007) Interactions between climate and vegetation during the Lateglacial Period as recorded by lake and mire sediment archives in Northern Italy and Southern Switzerland. Quaternary Science Reviews 26, 1650-1669
Vigne, J.-D. (2005) L'humérus de chien magdalénien de Erralla (Gipuzkoa, Espagne) et la domestication tardiglaciaire du loup en Europe. Munibe. Sociedad de Ciencias Naturales Aranzadi (San Sebastian) 57, 279-287
Vilà, C., Savolainen, P., Maldonado, J. E., et al. (1997) Multiple and ancient origins of the domestic dog. Science 276, 1687-1689
Von Den Driesch, A. (1976) A Guide to the Measurement of Animal Bones from Archaeological Sites: As Developed by the Institut für Palaeoanatomie, Domestikationsforschung und Geschichte der Tiermedizin of the University of Munich. Peabody Museum Press, Cambridge, MA
Vonholdt, B., Pollinger, J. P., Lohmueller, K. E., et al. (2010) Genome-wide SNP and haplotype analyses reveal a rich history underlying dog domestication. Nature 464, 898-902
Wayne, R. K. & Ostrander, E. A. (1999) Origin, genetic diversity, and genome structure of the domestic dog. BioEssays 21, 247-257
Wobeser, G. (1992) Traumatic, degenerative, and developmental lesions in wolves and coyotes from Saskatchewan. Journal of Wildlife Diseases 28, 268-275
Wolfgram, A. (1894) Die Einwerkung der Gefangenschaft auf die Gestaltung des Wolfschädels. Zoologisches Jahrbuch (Abteilung fur Systematik) 7, 773-822
Wroe, S., Myers, T. J., Wells, R. T., et al. (1990) Estimating the weight of the Pleistocene marsupial lion, Thylacoleo carnifex (Thylacoleonidae: Marsupialia): implications for the ecomorphology of a marsupial super-predator and hypotheses of impoverishment of Australian marsupial carnivore faunas. Australian Journal of Zoology 47, 489-498