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Osteomyelitis in Quaternary mammal from the Rio Grande do Norte State, Brazil
Quaternary International xxx (2013) 1e4
Contents lists available at SciVerse ScienceDirect
Quaternary International journal homepage: www.elsevier.com/locate/quaint
Osteomyelitis in Quaternary mammal from the Rio Grande do Norte State, Brazil Fernando Henrique de Souza Barbosa a, *, Kleberson de Oliveira Porpino b, Ana Bernadete Lima Fragoso b, Maria de Fátima Cavalcante Ferreira dos Santos c a
Centro de Tecnologia e Geociências, Departamento de Geologia, Universidade Federal de Pernambuco, Rua Acadêmico Hélio Ramos, S/N, Cidade Universitária, Recife, PE, Brazil Departamento de Ciências Biológicas, Laboratório de Sistemática e Ecologia Animal, Universidade do Estado do Rio Grande do Norte, Av. Professor Antônio Campos, S/N, Costa e Silva, Mossoró, RN, Brazil c Museu Câmara Cascudo, Universidade Federal do Rio Grande do Norte, Av. Hermes da Fonseca, 1398 Tirol, Natal, RN, Brazil b
a r t i c l e i n f o
a b s t r a c t
Article history: Available online xxx
The discovery, description and interpretation of paleopathologies in fossil materials are essential in answering several paleobiological questions. However, paleopathologies have been poorly studied in fossil vertebrates from the Quaternary deposits of Brazil. This paper describes a pathological lesion in a gomphothere humerus collected in a natural tank deposit from the late Pleistocene of Northeastern Brazil based on a macroscopic and radiological analysis. The lesion shows features indicative of osteomyelitis, such as a well-developed cloaca and abscesses, thus, it was possible to suggest tuberculosis as a potential source of the osteomyelitis, though a conclusive diagnosis is not feasible. Other putative causes such as pyogenic osteomyelitis can be discarded based on the evidence at hand. This is the first case of osteomyelitis reported for gomphotheres. Ó 2012 Elsevier Ltd and INQUA. All rights reserved.
1. Introduction
could leave diagnostic signals in bones. On the other, only a fraction of these diagnosable features is actually preserved (Waldron, 2009). Thus, in most paleontological cases it is not possible to establish a symptomatology or to follow the disease course (Pfeiffer, 1991). The only observable features in the bones are limited to those affecting the normal balance between growth and bone loss (Waldron, 2009), which are commonly evidenced by bone destruction, discontinuities, growth and density alterations (Ortner, 2003a). Inflammatory bone infections are among the most frequent paleopathologies in the fossil record. They commonly occur in three main types, depending on their initial focus location (Ortner, 2003a, 2008): periostitis (periosteum), osteomyelitis (bone marrow), and osteitis (soft tissues inside compact bone). There are two types of osteomyelitis: pyogenic and non-pyogenic. Pyogenic osteomyelitis is caused by pus-producing bacteria, such as Staphylococcus aureus. The non-pyogenic form is represented by tuberculosis-induced osteomyelitis, when caused by Mycobacterium tuberculosis or Mycobacterium bovis, besides others bacterial diseases, brucellosis and fungal disorders (Aufderheide and Rodríguez-Martin, 1998; Ortner, 2003b; Rothschild and Martin, 2006; Waldron, 2009). It is hard to determine the type of osteomyelitis based only in bone remains, particularly when studying isolated bone elements. However, the careful analysis of some diagnostic characters allows at least eliminating competing causes.
Paleopathological studies are pivotal for a deep appreciation of the paleobiology of fossil organisms, providing a basis for estimating crucial traits, such as the relative age of death, general behavior, diet, metabolic and nutritional disorders and disease evolution (Ferigolo, 2007). In addition, knowledge of paleopathology is important to avoid errors in systematic studies (Ferigolo, 2007) and to interpret taphonomic signatures, which eventually could be confused with bone pathologies. Finally, paleopathological studies can potentially enlighten the understanding of the causes of key paleobiological events. Ferigolo (1999), for instance, argued that the extinction of South American Pleistocene megafauna was triggered by the introduction of new pathogens (neoinfection) brought by North American immigrants during the Great American Biotic Interchange. Not surprisingly, the identification of paleopathological conditions in fossil vertebrates is strongly biased in favor of the analysis of bone alterations, as the soft tissues are rarely preserved (Waldron, 2009). This is obviously a limiting factor for paleopathological studies. On one hand, there are few pathologies that
* Corresponding author. E-mail address: [email protected] (F.H.S. Barbosa). 1040-6182/$ e see front matter Ó 2012 Elsevier Ltd and INQUA. All rights reserved. http://dx.doi.org/10.1016/j.quaint.2012.12.035
Please cite this article in press as: Barbosa, F.H.S., et al., Osteomyelitis in Quaternary mammal from the Rio Grande do Norte State, Brazil, Quaternary International (2013), http://dx.doi.org/10.1016/j.quaint.2012.12.035
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F.H.S. Barbosa et al. / Quaternary International xxx (2013) 1e4
Paleopathological studies are scarce for the Brazilian Quaternary, and they are almost restricted to human skeletal remains (Souza, 2011). There are few paleopathology cases reported for the Pleistocene megafauna from Brazil, although they include a fair number of different pathologies, such as degenerative articular lesions and Scheuermann disease in megatheriid ground sloth vertebra (Ferigolo, 1985, 1992), congenital deformation and overload and senility-related injuries in mylodontid ground sloth (Cabral and Henriques, 2006) and enamel hypoplasy in toxodontids (Melo et al., 2010). Concerning infectious lesions, Ferigolo et al. (2005) reported chronic osteomyelitis and infectious arthritis in a ground sloth and Cabral and Henriques (2007) identified infectious lesions in Lestodon armatus. This paper describes, for the first time, a paleopathological lesion for a gomphotherid Proboscidean from Brazil. The aim is to improve the knowledge of paleopathology in fossil materials associated with the megafauna from the late Pleistocene of Brazil. 2. Materials and methods The analyzed specimen was collected in a lag formed by the coalescence of several natural tank deposits located at Fazenda Lagoa da Cruz site in Nova Cruz municipality, Rio Grande do Norte state, northeastern Brazil (Fig. 1). Tanks are natural elliptic to rounded depressions, with steep walls, generated by weathering of fractures in basement rocks (Mabesoone et al., 1990; Bergqvist et al., 1997; Santos, 2002). The vertebrate fossil assemblages of tanks are traditionally assigned to late Pleistocene based on its
taxonomic composition (Cartelle, 1999). Recently, some age estimations based on Electron Spin Resonance of fossil vertebrates collected in tanks from Paraíba (Kinoshita et al., 2005), Pernambuco (Oliveira et al., 2009), Alagoas (Silva, 2009) and Sergipe (Dantas et al., 2011), show that these fossils are between 60 and 10 ka. DGEO 829 was found in association with other megafauna fossils including Megatheriidae and Toxodontidae (Oliveira and Damasceno, 1987). It is housed in the paleontological collection of the paleontology laboratory of Departamento de Geologia of Universidade Federal do Rio Grande do Norte, in Natal, Rio Grande do Norte State. The specimen is a fragmentary left humerus (DGEO 829, Fig. 2) nearly 55 cm in proximodistal length, originally assigned by Oliveira and Damasceno (1987) to the species Haplomastodon waringi (¼Notiomastodon platensis Ameghino, 1888; see Mothé et al. (2011) for revision of South American gomphotheres) lacking the proximal and distal epiphyses due to taphonomic processes. Macroscopical analysis of the external features was conducted, along with an internal analysis of this humerus based on radiographic examination with X-Ray apparatus Siemens Heliophoes 4 S, 500 Ma, 125 Kv. 3. Results and discussion The macroscopic and radiological analyses of DGEO 829 revealed an extensive lesion in the proximal half of the bone. Internally, this lesion extends proximodistally for 200 mm through the medular canal and is roughly divided into three segments
Fig. 1. Location map of Lagoa da Cruz site in Nova Cruz municipality, Rio Grande do Norte state, Brazil.
Please cite this article in press as: Barbosa, F.H.S., et al., Osteomyelitis in Quaternary mammal from the Rio Grande do Norte State, Brazil, Quaternary International (2013), http://dx.doi.org/10.1016/j.quaint.2012.12.035
F.H.S. Barbosa et al. / Quaternary International xxx (2013) 1e4
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Fig. 2. Fragmented humerus of Notiomastodon platensis (DGEO 829) in cranial view. right, detail showing the crests and tuberosities (arrows) surrounding the cloaca. Scale bar ¼ 6 cm.
delimited by crests of sclerotic bone tissue. Distally, it curves laterally reaching the cortical bone and opens cranially into an elliptic rounded-edge cloaca (proximodistal length ¼ 130 mm, width ¼ 22 mm) on the external surface, just below the distal basis of the greater tuberosity. The area surrounding the cloaca is characterized by several small crests and tubercles (Fig. 2). Reactive bone sclerosis is present in the borders of the cortical and medular portions of this lesion, indicated by whitened areas with enhanced radiopacity (Fig. 3). The lesion was likely caused by a chronic infection, because acute diseases commonly lead to the death of the individual before any bone alterations can be produced. The segments dividing the internal portion of the lesion may represent the initial foci that later coalesced with the progress of the infection. The described features are suggestive of osteomyelitis. Both chronic and acute osteomyelitis may occur as a posttraumatic infection (Lovell, 1997; Ortner, 2003b), due, for instance, to an open fracture (Lovell, 1997). Another common situation is the occurrence of fractures generated by bone weakening resulting from osteomyelitis (Ferigolo, 2007). There was no macroscopic or radiological evidence of fracture in the area affected by the lesion in DGEO 829 or in other preserved portions of the bone. However, the implications of such an absence are hard to evaluate, as the studied specimen is fragmentary and no other skeletal element assignable to the same individual was collected. It could be problematic to distinguish among the different subtypes of osteomyelitis, as they can produce similar alterations (Watts et al., 1996; Vorha et al., 1997). To diagnose pyogenic osteomyelitis through differential analysis, it would be necessary to observe three features (Rothschild and Martin, 2006; Ferigolo, 2007; Waldron, 2009): cloaca (pus drainage canal), sequestrum (bone necrosis located in the infection focus) and involucrum (a sheath of new bone which originates from the periostium and growths around the sequestrum). As mentioned above, a cloaca was observed and correspond to the external aperture of the lesion in the bone surface. There is slight evidence of reactive bone formation represented by very small bone crests and tubercles surrounding the cloaca but there is no sign of a real involucrum. There is no observed evidence of sequestrum. Nonetheless, the absence of sequestrum in fossil material is problematic, as it represents a dead bone fragment inside
Fig. 3. Radiograph of the fragmented humerus of Notiomastodon platensis (DGEO 829) a) craniocaudal plane: thick arrows indicate crests of sclerotic bone tissue that separate the lesion into segments and thin arrows indicate bone sclerosis in the borders of the lesion; b) lateromedial plane: arrow indicates the cloacal aperture; abbreviations: S1e S3, internal segments of the lesion; Ca, cloaca.
the cloaca that could be easily expelled by the flux of purulent material or be lost after death due to taphonomic processes or even during collection and preparation (Ferigolo, 2007). Bone alterations caused by tuberculosis are typically lithic lesions. The affected specimen shows bone remodeling areas, slight or no reactive bone formation and absence of sequestrum (Rothschild and Martin, 2006). In DGEO 829, there is slight evidence of reactive bone reaction, and the most remarkable bone alterations are the cloaca and the internal coalescent lithic lesions. Similar features are also found in bones affected by fungal infections (Aufderheide and Rodrígues-Martin, 1998). However, in tuberculosis the lithic lesions frequently coalesce, as in the studied specimen (Fig. 3), unlike in fungal lesion (Hershkovitz et al., 1998). Moreover, tuberculosis affects predominantly joints, but they can also occur in diaphysis, as in DGEO 829 (Rothschild and Martin, 2006). Fungal disease in contrast occurs mainly in bone metaphysis and on the top of skull (Resnick, 2002; Rothschild and Martin, 2006). Gomphotheres, together with megatheriid ground sloths, glyptodonts and toxodontids, are among the most common megamammals preserved in fossil assemblages of natural tanks as well as in other late Pleistocene South American deposits. Ferigolo (1999) argued that the osteomyelitis frequency, in addition to other kinds of evidence (e.g. preserved pathogens in coprolites, hypoplasia), would function as a test for his South American megafauna extinction hypothesis according to which the extinction was caused by neoinfection(s) brought by Holarctic immigrants. However, an isolated single case, as that reported here, although an important initial step, is far from representing compelling evidence for Ferigolo’s or any other extinction hypothesis (e.g. Cartelle, 1999;
Please cite this article in press as: Barbosa, F.H.S., et al., Osteomyelitis in Quaternary mammal from the Rio Grande do Norte State, Brazil, Quaternary International (2013), http://dx.doi.org/10.1016/j.quaint.2012.12.035
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Cione et al., 2003). Therefore, paleontologists working with South American megafauna are urged to pay attention to evidence of osteomyelitis and other pathologies in fossils of gomphotheres and other megamammals they are investigating. 4. Conclusions The gomphothere humerus from Rio Grande do Norte analyzed here shows bone alterations, such as cloaca and small abscesses, suggestive of osteomyelitis. The alterations observed indicate a chronic infectious process, more compatible with tuberculosis osteomyelitis, although a conclusive diagnosis is not feasible. There is no evidence of posttraumatic or secondary fracture in the studied specimen. Pyogenic osteomyelitis disease can be discarded as the cause of the observed alterations. This is the first record of osteomyelitis in fossil gomphotheres and represents an important piece of evidence for the compilation of a data base to test hypotheses on megafaunal extinction in South America. Acknowledgments We would like to thank Dr. Fernando José Vieira de Sousa (Clínica de Raios-X e Ultra-Som) for the X-Ray analysis, Departamento de Geologia da Universidade Federal do Rio Grande do Norte (UFRN) for allowing the study of DGEO 829 and also Dr. Edison Vicente Oliveira (UFPE) for comments on a early draft of this manuscript, and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for financial support for the first author. References Aufderheide, A.C., Rodrígues-Martin, C., 1998. The Cambridge Encyclopedia of Human Paleopathology. Cambridge University Press, Cambridge, 478 pp. Bergqvist, L.P., Gomide, M., Cartelle, C., Capilla, R., 1997. Faunas locais de mamíferos pleistocênicos de Itapipoca/Ceará, Taperoá/Paraíba e Campina Grande/Paraíba. Estudo comparativo, bioestratinômico e paleoambiental. Revista Geociências, 23e62. Cabral, U.G., Henriques, D.D.R., 2006. Estudo de caso ánatomo-patológico e tafonômico de material pertencente ao gênero Lestodon Gervais, 1855, Coletado no Estado de São Paulo e depositado na coleção do Museu Nacional/UFRJ. Anuário do Instituto de Geociências-UFRJ, 252 pp. Cabral, U.G., Henriques, D.D.R., 2007. Estudos ánatomo-patológico e tafonômico de exemplares de Lestodon armatus Gervais, 1855, provenientes do Estado do Rio Grande do Sul, Brasil. In: Carvalho, I.S. (Ed.), Paleontologia: Cenários da Vida, vol. 2. Interciência, Rio de Janeiro, pp. 309e317. Cartelle, C., 1999. Pleistocene mammals of the Cerrado and Caatinga of Brazil. In: Eisenberg, J.F., Redford, K.H. (Eds.), Mammals of the Neotropics. The University of Chicago Press, pp. 27e46. Cione, A.L., Tonni, E.P., Soibelzon, L., 2003. The broken zig-zag: late Cenozoic large mammals and tortoise extinction in South America. Revista do Museu Argentino de Ciencias Naturais 5 (1), 1e19. Dantas, M.A.T., Porpino, K.O., Bauermann, S.G., Prata, A.P.N., Cozzuol, M.A., Kinoshita, A., Barbosa, J.H.O., Baffa, O., 2011. Megafauna do Pleistoceno Superior de Sergipe, Brasil: Registros taxonômicos e cronológicos. Revista Brasileira de Paleontologia, 311e320. Ferigolo, J., 1985. Paleopatologia em preguiças terrícolas. Artrose. In: Congresso Brasileiro de Paleontologia, Coletânea de Trabalhos paleontológicos, sér. Geologia. DNPM, Rio de Janeiro, pp. 43e49. Ferigolo, J., 1992. Non-human vertebrate paleopathology of some Brazilian Pleistocene mammals. In: Araújo, A.J.G., Ferreira, L.F. (Eds.), Paleopatologia, Paleo-
epidemiologia. Estudos Multidisciplinares. Panorama. Escola Nacional de Saúde Pública, Fundação Oswaldo Cruz, Rio de Janeiro, pp. 213e234. Ferigolo, J., 1999. Late Pleistocene South American land-mammal extinction: the infection hypothesis. Quaternary of South America and Antarctic Peninsula, 279e310. Ferigolo, J., Negri, F.R., Buchmann, F.S., 2005. Chronic osteomyelitis and infections arthritis in a ground sloth (Mammalia, Mylodontidae) from upper Pleistocene of Rio Grande do Sul State, Brazil. In: 1st Paleopathology Association Meeting in South America, Human Migrations and Diseases, Rio de Janeiro. Abstracts. Paleopathology Association Meeting in South America 2005, Rio de Janeiro, p. 42. Ferigolo, J., 2007. Paleopatologia em Mamíferos. In: Carvalho, I.S., Fernandes, A.C.S. (Eds.), Icnologia, 1st ed. Sociedade Brasileira de Geologia, São Paulo, pp. 88e107. Hershkovitz, I., Rothschield, B.M., Dutour, O., Greenwald, C., 1998. Clues to recognition of fungal origin of lytic skeletal lesions. American Journal of Physical Anthropology 106, 47e60. Kinoshita, A., Barreto, A.M.F., Almeida, J.A.C., Figueiredo, A.M., Nicolucci, P., Graeff, C.F.O., Baffa, O., 2005. ESR dating at K and X band of northeastern Brazilian megafauna. Applied Radiation and Isotopes 62, 225e229. Lovell, N.C., 1997. Trauma analysis in paleopathology. Yearbook of Physical Anthropology 40, 139e170. Mabesoone, J.M., Oliveira, L.D.D., Damasceno, J.M., 1990. Desenvolvimento dos tanques fossilíferos no semiárido norte-rio-grandense. In: Congresso Brasileiro de Geologia, vol. 36. Anais, Natal, UFRN, pp. 733e741. Melo, D.J., Henriques, D.D.R., Carvalho, C.R., 2010. Ocorrência de defeitos de esmalte em materiais de Toxodon na coleção do Museu Nacional/UFRJ, uma perspectiva paleoepidemiológica. In: Carvalho, I.S. (Ed.), Paleontologia: Cenários da Vida. Interciência, Rio de Janeiro, pp. 745e756. Mothé, D., Avilla, L.S., Cozzuol, M., Winck, G.R., 2011. Taxonomic revision of the Quaternary gomphoteres (Mammalia: Proboscidea: Gomphotheriidae) from the South American lowlands. Quaternary International 276e277, 2e7. Oliveira, L.D.D., Damasceno, J.M., 1987. Registro de novos espécimes de mamíferos fósseis em Lagoa da Cruz-Nova Cruz (RN). In: Congresso Brasileiro de Paleontologia 10. Oliveira, E.V., Barreto, A.M.F., Alves, R. da S., 2009. Aspectos sistemáticos, paleobiogeográficos e paleoclimáticos dos mamíferos Quaternários de Fazenda Nova, PE, Nordeste do Brasil. Gaea 5 (2), 75e85. Ortner, D.J., 2003a. Methods used in the analyses of skeletal lesions. In: Ortner, D.J. (Ed.), Identification of Pathological Conditions in Human Skeletal Remains. Academic Press, San Diego, pp. 45e64. Ortner, D.J., 2003b. Infectious diseases: introduction, biology, osteomyelitis, periostitis, brucellosis, glanders, and septic arthritis. In: Ortner, D.J. (Ed.), Identification of Pathological Conditions in Human Skeletal Remains. Academic Press, San Diego, pp. 179e226. Ortner, D.J., 2008. Differential diagnosis of skeletal lesions in infectious disease. In: Pinhasi, R., Mays, S. (Eds.), Advances in Human Palaeopathology. Wiley, pp. 191e214. Pfeiffer, S., 1991. Is paleopathology a relevant predictor of contemporary health patterns? In: Ortner, D.J., Aufderheide, A.C. (Eds.), Human Paleopathology: Current Synthesis and Future Options. Smithsonian Institution Press, Washington and London, pp. 12e17. Resnick, D., 2002. Diagnosis of Bone and Joint Disorders. Saunders, Philadelphia. Rothschild, B.M., Martin, L.D., 2006. Skeletal Impact of Disease. Albuquerque. Santos, M.F.C.F., 2002. Geologia e paleontologia de depósitos fossilíferos pleistocênicos do Rio Grande do Norte. Dissertação de Mestrado, Programa de PósGraduação em Geodinâmica e Geofísica, Centro de Ciências Exatas e da Terra, Universidade Federal do Rio Grande do Norte, Brasil. Silva, J.L.L., 2009. Reconstituição paleoambiental baseada no estudo de mamíferos pleistocênicos de Maravilha e Poço das Trincheiras, Alagoas, Nordeste do Brasil. Programa de Pós-Graduação em Geociências, Universidade Federal de Pernambuco, Tese de Doutorado, 244 pp. Souza, S.M., 2011. A paleopatologia no Brasil: crânios, parasitos e doenças no passado. In: Ferreira, L.F., Reinhard, K.J., Araújo, A. (Eds.), Fundamentos da Paleoparasitologia. Editora Fio Cruz, pp. 69e92. Vorha, R., Kang, H.S., Dogra, S., Saggar, R.R., Sharma, R., 1997. Tuberculous osteomyelitis. The Journal of bone and joint surgery 79-B, 562e566. Waldron, T., 2009. Palaeopathology. Cambridge University Press, New York, 298 pp. Watts, H.G., Lifeso, R.M., 1996. Tuberculosis of bones and joints. The Journal of bone and joint surgery 78-A, 288e298.
Please cite this article in press as: Barbosa, F.H.S., et al., Osteomyelitis in Quaternary mammal from the Rio Grande do Norte State, Brazil, Quaternary International (2013), http://dx.doi.org/10.1016/j.quaint.2012.12.035
Contents lists available at SciVerse ScienceDirect
Quaternary International journal homepage: www.elsevier.com/locate/quaint
Osteomyelitis in Quaternary mammal from the Rio Grande do Norte State, Brazil Fernando Henrique de Souza Barbosa a, *, Kleberson de Oliveira Porpino b, Ana Bernadete Lima Fragoso b, Maria de Fátima Cavalcante Ferreira dos Santos c a
Centro de Tecnologia e Geociências, Departamento de Geologia, Universidade Federal de Pernambuco, Rua Acadêmico Hélio Ramos, S/N, Cidade Universitária, Recife, PE, Brazil Departamento de Ciências Biológicas, Laboratório de Sistemática e Ecologia Animal, Universidade do Estado do Rio Grande do Norte, Av. Professor Antônio Campos, S/N, Costa e Silva, Mossoró, RN, Brazil c Museu Câmara Cascudo, Universidade Federal do Rio Grande do Norte, Av. Hermes da Fonseca, 1398 Tirol, Natal, RN, Brazil b
a r t i c l e i n f o
a b s t r a c t
Article history: Available online xxx
The discovery, description and interpretation of paleopathologies in fossil materials are essential in answering several paleobiological questions. However, paleopathologies have been poorly studied in fossil vertebrates from the Quaternary deposits of Brazil. This paper describes a pathological lesion in a gomphothere humerus collected in a natural tank deposit from the late Pleistocene of Northeastern Brazil based on a macroscopic and radiological analysis. The lesion shows features indicative of osteomyelitis, such as a well-developed cloaca and abscesses, thus, it was possible to suggest tuberculosis as a potential source of the osteomyelitis, though a conclusive diagnosis is not feasible. Other putative causes such as pyogenic osteomyelitis can be discarded based on the evidence at hand. This is the first case of osteomyelitis reported for gomphotheres. Ó 2012 Elsevier Ltd and INQUA. All rights reserved.
1. Introduction
could leave diagnostic signals in bones. On the other, only a fraction of these diagnosable features is actually preserved (Waldron, 2009). Thus, in most paleontological cases it is not possible to establish a symptomatology or to follow the disease course (Pfeiffer, 1991). The only observable features in the bones are limited to those affecting the normal balance between growth and bone loss (Waldron, 2009), which are commonly evidenced by bone destruction, discontinuities, growth and density alterations (Ortner, 2003a). Inflammatory bone infections are among the most frequent paleopathologies in the fossil record. They commonly occur in three main types, depending on their initial focus location (Ortner, 2003a, 2008): periostitis (periosteum), osteomyelitis (bone marrow), and osteitis (soft tissues inside compact bone). There are two types of osteomyelitis: pyogenic and non-pyogenic. Pyogenic osteomyelitis is caused by pus-producing bacteria, such as Staphylococcus aureus. The non-pyogenic form is represented by tuberculosis-induced osteomyelitis, when caused by Mycobacterium tuberculosis or Mycobacterium bovis, besides others bacterial diseases, brucellosis and fungal disorders (Aufderheide and Rodríguez-Martin, 1998; Ortner, 2003b; Rothschild and Martin, 2006; Waldron, 2009). It is hard to determine the type of osteomyelitis based only in bone remains, particularly when studying isolated bone elements. However, the careful analysis of some diagnostic characters allows at least eliminating competing causes.
Paleopathological studies are pivotal for a deep appreciation of the paleobiology of fossil organisms, providing a basis for estimating crucial traits, such as the relative age of death, general behavior, diet, metabolic and nutritional disorders and disease evolution (Ferigolo, 2007). In addition, knowledge of paleopathology is important to avoid errors in systematic studies (Ferigolo, 2007) and to interpret taphonomic signatures, which eventually could be confused with bone pathologies. Finally, paleopathological studies can potentially enlighten the understanding of the causes of key paleobiological events. Ferigolo (1999), for instance, argued that the extinction of South American Pleistocene megafauna was triggered by the introduction of new pathogens (neoinfection) brought by North American immigrants during the Great American Biotic Interchange. Not surprisingly, the identification of paleopathological conditions in fossil vertebrates is strongly biased in favor of the analysis of bone alterations, as the soft tissues are rarely preserved (Waldron, 2009). This is obviously a limiting factor for paleopathological studies. On one hand, there are few pathologies that
* Corresponding author. E-mail address: [email protected] (F.H.S. Barbosa). 1040-6182/$ e see front matter Ó 2012 Elsevier Ltd and INQUA. All rights reserved. http://dx.doi.org/10.1016/j.quaint.2012.12.035
Please cite this article in press as: Barbosa, F.H.S., et al., Osteomyelitis in Quaternary mammal from the Rio Grande do Norte State, Brazil, Quaternary International (2013), http://dx.doi.org/10.1016/j.quaint.2012.12.035
2
F.H.S. Barbosa et al. / Quaternary International xxx (2013) 1e4
Paleopathological studies are scarce for the Brazilian Quaternary, and they are almost restricted to human skeletal remains (Souza, 2011). There are few paleopathology cases reported for the Pleistocene megafauna from Brazil, although they include a fair number of different pathologies, such as degenerative articular lesions and Scheuermann disease in megatheriid ground sloth vertebra (Ferigolo, 1985, 1992), congenital deformation and overload and senility-related injuries in mylodontid ground sloth (Cabral and Henriques, 2006) and enamel hypoplasy in toxodontids (Melo et al., 2010). Concerning infectious lesions, Ferigolo et al. (2005) reported chronic osteomyelitis and infectious arthritis in a ground sloth and Cabral and Henriques (2007) identified infectious lesions in Lestodon armatus. This paper describes, for the first time, a paleopathological lesion for a gomphotherid Proboscidean from Brazil. The aim is to improve the knowledge of paleopathology in fossil materials associated with the megafauna from the late Pleistocene of Brazil. 2. Materials and methods The analyzed specimen was collected in a lag formed by the coalescence of several natural tank deposits located at Fazenda Lagoa da Cruz site in Nova Cruz municipality, Rio Grande do Norte state, northeastern Brazil (Fig. 1). Tanks are natural elliptic to rounded depressions, with steep walls, generated by weathering of fractures in basement rocks (Mabesoone et al., 1990; Bergqvist et al., 1997; Santos, 2002). The vertebrate fossil assemblages of tanks are traditionally assigned to late Pleistocene based on its
taxonomic composition (Cartelle, 1999). Recently, some age estimations based on Electron Spin Resonance of fossil vertebrates collected in tanks from Paraíba (Kinoshita et al., 2005), Pernambuco (Oliveira et al., 2009), Alagoas (Silva, 2009) and Sergipe (Dantas et al., 2011), show that these fossils are between 60 and 10 ka. DGEO 829 was found in association with other megafauna fossils including Megatheriidae and Toxodontidae (Oliveira and Damasceno, 1987). It is housed in the paleontological collection of the paleontology laboratory of Departamento de Geologia of Universidade Federal do Rio Grande do Norte, in Natal, Rio Grande do Norte State. The specimen is a fragmentary left humerus (DGEO 829, Fig. 2) nearly 55 cm in proximodistal length, originally assigned by Oliveira and Damasceno (1987) to the species Haplomastodon waringi (¼Notiomastodon platensis Ameghino, 1888; see Mothé et al. (2011) for revision of South American gomphotheres) lacking the proximal and distal epiphyses due to taphonomic processes. Macroscopical analysis of the external features was conducted, along with an internal analysis of this humerus based on radiographic examination with X-Ray apparatus Siemens Heliophoes 4 S, 500 Ma, 125 Kv. 3. Results and discussion The macroscopic and radiological analyses of DGEO 829 revealed an extensive lesion in the proximal half of the bone. Internally, this lesion extends proximodistally for 200 mm through the medular canal and is roughly divided into three segments
Fig. 1. Location map of Lagoa da Cruz site in Nova Cruz municipality, Rio Grande do Norte state, Brazil.
Please cite this article in press as: Barbosa, F.H.S., et al., Osteomyelitis in Quaternary mammal from the Rio Grande do Norte State, Brazil, Quaternary International (2013), http://dx.doi.org/10.1016/j.quaint.2012.12.035
F.H.S. Barbosa et al. / Quaternary International xxx (2013) 1e4
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Fig. 2. Fragmented humerus of Notiomastodon platensis (DGEO 829) in cranial view. right, detail showing the crests and tuberosities (arrows) surrounding the cloaca. Scale bar ¼ 6 cm.
delimited by crests of sclerotic bone tissue. Distally, it curves laterally reaching the cortical bone and opens cranially into an elliptic rounded-edge cloaca (proximodistal length ¼ 130 mm, width ¼ 22 mm) on the external surface, just below the distal basis of the greater tuberosity. The area surrounding the cloaca is characterized by several small crests and tubercles (Fig. 2). Reactive bone sclerosis is present in the borders of the cortical and medular portions of this lesion, indicated by whitened areas with enhanced radiopacity (Fig. 3). The lesion was likely caused by a chronic infection, because acute diseases commonly lead to the death of the individual before any bone alterations can be produced. The segments dividing the internal portion of the lesion may represent the initial foci that later coalesced with the progress of the infection. The described features are suggestive of osteomyelitis. Both chronic and acute osteomyelitis may occur as a posttraumatic infection (Lovell, 1997; Ortner, 2003b), due, for instance, to an open fracture (Lovell, 1997). Another common situation is the occurrence of fractures generated by bone weakening resulting from osteomyelitis (Ferigolo, 2007). There was no macroscopic or radiological evidence of fracture in the area affected by the lesion in DGEO 829 or in other preserved portions of the bone. However, the implications of such an absence are hard to evaluate, as the studied specimen is fragmentary and no other skeletal element assignable to the same individual was collected. It could be problematic to distinguish among the different subtypes of osteomyelitis, as they can produce similar alterations (Watts et al., 1996; Vorha et al., 1997). To diagnose pyogenic osteomyelitis through differential analysis, it would be necessary to observe three features (Rothschild and Martin, 2006; Ferigolo, 2007; Waldron, 2009): cloaca (pus drainage canal), sequestrum (bone necrosis located in the infection focus) and involucrum (a sheath of new bone which originates from the periostium and growths around the sequestrum). As mentioned above, a cloaca was observed and correspond to the external aperture of the lesion in the bone surface. There is slight evidence of reactive bone formation represented by very small bone crests and tubercles surrounding the cloaca but there is no sign of a real involucrum. There is no observed evidence of sequestrum. Nonetheless, the absence of sequestrum in fossil material is problematic, as it represents a dead bone fragment inside
Fig. 3. Radiograph of the fragmented humerus of Notiomastodon platensis (DGEO 829) a) craniocaudal plane: thick arrows indicate crests of sclerotic bone tissue that separate the lesion into segments and thin arrows indicate bone sclerosis in the borders of the lesion; b) lateromedial plane: arrow indicates the cloacal aperture; abbreviations: S1e S3, internal segments of the lesion; Ca, cloaca.
the cloaca that could be easily expelled by the flux of purulent material or be lost after death due to taphonomic processes or even during collection and preparation (Ferigolo, 2007). Bone alterations caused by tuberculosis are typically lithic lesions. The affected specimen shows bone remodeling areas, slight or no reactive bone formation and absence of sequestrum (Rothschild and Martin, 2006). In DGEO 829, there is slight evidence of reactive bone reaction, and the most remarkable bone alterations are the cloaca and the internal coalescent lithic lesions. Similar features are also found in bones affected by fungal infections (Aufderheide and Rodrígues-Martin, 1998). However, in tuberculosis the lithic lesions frequently coalesce, as in the studied specimen (Fig. 3), unlike in fungal lesion (Hershkovitz et al., 1998). Moreover, tuberculosis affects predominantly joints, but they can also occur in diaphysis, as in DGEO 829 (Rothschild and Martin, 2006). Fungal disease in contrast occurs mainly in bone metaphysis and on the top of skull (Resnick, 2002; Rothschild and Martin, 2006). Gomphotheres, together with megatheriid ground sloths, glyptodonts and toxodontids, are among the most common megamammals preserved in fossil assemblages of natural tanks as well as in other late Pleistocene South American deposits. Ferigolo (1999) argued that the osteomyelitis frequency, in addition to other kinds of evidence (e.g. preserved pathogens in coprolites, hypoplasia), would function as a test for his South American megafauna extinction hypothesis according to which the extinction was caused by neoinfection(s) brought by Holarctic immigrants. However, an isolated single case, as that reported here, although an important initial step, is far from representing compelling evidence for Ferigolo’s or any other extinction hypothesis (e.g. Cartelle, 1999;
Please cite this article in press as: Barbosa, F.H.S., et al., Osteomyelitis in Quaternary mammal from the Rio Grande do Norte State, Brazil, Quaternary International (2013), http://dx.doi.org/10.1016/j.quaint.2012.12.035
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Cione et al., 2003). Therefore, paleontologists working with South American megafauna are urged to pay attention to evidence of osteomyelitis and other pathologies in fossils of gomphotheres and other megamammals they are investigating. 4. Conclusions The gomphothere humerus from Rio Grande do Norte analyzed here shows bone alterations, such as cloaca and small abscesses, suggestive of osteomyelitis. The alterations observed indicate a chronic infectious process, more compatible with tuberculosis osteomyelitis, although a conclusive diagnosis is not feasible. There is no evidence of posttraumatic or secondary fracture in the studied specimen. Pyogenic osteomyelitis disease can be discarded as the cause of the observed alterations. This is the first record of osteomyelitis in fossil gomphotheres and represents an important piece of evidence for the compilation of a data base to test hypotheses on megafaunal extinction in South America. Acknowledgments We would like to thank Dr. Fernando José Vieira de Sousa (Clínica de Raios-X e Ultra-Som) for the X-Ray analysis, Departamento de Geologia da Universidade Federal do Rio Grande do Norte (UFRN) for allowing the study of DGEO 829 and also Dr. Edison Vicente Oliveira (UFPE) for comments on a early draft of this manuscript, and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for financial support for the first author. References Aufderheide, A.C., Rodrígues-Martin, C., 1998. The Cambridge Encyclopedia of Human Paleopathology. Cambridge University Press, Cambridge, 478 pp. Bergqvist, L.P., Gomide, M., Cartelle, C., Capilla, R., 1997. Faunas locais de mamíferos pleistocênicos de Itapipoca/Ceará, Taperoá/Paraíba e Campina Grande/Paraíba. Estudo comparativo, bioestratinômico e paleoambiental. Revista Geociências, 23e62. Cabral, U.G., Henriques, D.D.R., 2006. Estudo de caso ánatomo-patológico e tafonômico de material pertencente ao gênero Lestodon Gervais, 1855, Coletado no Estado de São Paulo e depositado na coleção do Museu Nacional/UFRJ. Anuário do Instituto de Geociências-UFRJ, 252 pp. Cabral, U.G., Henriques, D.D.R., 2007. Estudos ánatomo-patológico e tafonômico de exemplares de Lestodon armatus Gervais, 1855, provenientes do Estado do Rio Grande do Sul, Brasil. In: Carvalho, I.S. (Ed.), Paleontologia: Cenários da Vida, vol. 2. Interciência, Rio de Janeiro, pp. 309e317. Cartelle, C., 1999. Pleistocene mammals of the Cerrado and Caatinga of Brazil. In: Eisenberg, J.F., Redford, K.H. (Eds.), Mammals of the Neotropics. The University of Chicago Press, pp. 27e46. Cione, A.L., Tonni, E.P., Soibelzon, L., 2003. The broken zig-zag: late Cenozoic large mammals and tortoise extinction in South America. Revista do Museu Argentino de Ciencias Naturais 5 (1), 1e19. Dantas, M.A.T., Porpino, K.O., Bauermann, S.G., Prata, A.P.N., Cozzuol, M.A., Kinoshita, A., Barbosa, J.H.O., Baffa, O., 2011. Megafauna do Pleistoceno Superior de Sergipe, Brasil: Registros taxonômicos e cronológicos. Revista Brasileira de Paleontologia, 311e320. Ferigolo, J., 1985. Paleopatologia em preguiças terrícolas. Artrose. In: Congresso Brasileiro de Paleontologia, Coletânea de Trabalhos paleontológicos, sér. Geologia. DNPM, Rio de Janeiro, pp. 43e49. Ferigolo, J., 1992. Non-human vertebrate paleopathology of some Brazilian Pleistocene mammals. In: Araújo, A.J.G., Ferreira, L.F. (Eds.), Paleopatologia, Paleo-
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Please cite this article in press as: Barbosa, F.H.S., et al., Osteomyelitis in Quaternary mammal from the Rio Grande do Norte State, Brazil, Quaternary International (2013), http://dx.doi.org/10.1016/j.quaint.2012.12.035