We report on the paleopathological analysis of the partial skeleton of the late Pliocene hominin species Australopithecus africanus Stw 431 from Sterkfontein, South Africa. A previous study noted the presence of lesions on vertebral bodies diagnosed as spondylosis deformans due to trauma. Instead, we suggest that these lesions are pathological changes due to the initial phases of an infectious disease, brucellosis. The macroscopic, microscopic and radiological appearance of the lytic lesions of the lumbar vertebrae is consistent with brucellosis. The hypothesis of brucellosis (most often associated with the consumption of animal proteins) in a 2.4 to 2.8 million year old hominid has a host of important implications for human evolution. The consumption of meat has been regarded an important factor in supporting, directing or altering human evolution. Perhaps the earliest (up to 2.5 million years ago) paleontological evidence for meat eating consists of cut marks on animal remains and stone tools that could have made these marks. Now with the hypothesis of brucellosis in A. africanus, we may have evidence of occasional meat eating directly linked to a fossil hominin.
Citation: D'Anastasio R, Zipfel B, Moggi-Cecchi J, Stanyon R, Capasso L (2009) Possible Brucellosis in an Early Hominin Skeleton from Sterkfontein, South Africa. PLoS ONE 4(7): e6439. https://doi.org/10.1371/journal.pone.0006439
Editor: Virginia J. Vitzthum, Indiana University, United States of America
Received: February 12, 2009; Accepted: June 26, 2009; Published: July 30, 2009
Copyright: © 2009 D'Anastasio et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: Fondazione Cassa di Risparmio della Provinia di Chieti (www.fondazionecarichieti.it/) Grant numbers: 156/2006; 167/2007; 138/2008. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
The study of pathology in ancient human and pre-human populations can contribute to our knowledge of their life history and health status. Paleopathological investigations have the potential to yield particularly noteworthy results when the subjects of study are hominins. The documented array of pathological lesions affecting Australopithecus and early Homo consists of trauma, malformations, tumours, degenerative alterations associated with ageing and bipedal locomotion –. To date, there are no descriptions of infectious disease in early hominins and we could only speculate on what infectious organisms may have affected australopiths. Here we present the first possible case of an infectious pathology in an australopith (Stw 431) from the hominin site of Sterkfontein South Africa. Stw 431 was recovered in situ from Member 4, Bed B, of the Sterkfontein Formation . Member 4 was previously estimated to be 2.4–2.8 Ma –, while Berger et al.  later placed it at between 1.5–2.5 Ma. On grounds of provenance and compatible morphology, Stw 431 is attributed to Australopithecus africanus . The skeleton is that of an adult individual, probably male, and is comprised of eighteen mostly incomplete bones derived from the axial skeleton, pectoral girdle, upper limb, and the pelvic girdle. The vertebral column consists of nine consecutive thoracolumbar vertebrae, T9 to L5.
Lumbar vertebra L5 presents lytic lesions that Staps  described as spondylosis deformans resulting from a trauma. Here we discuss the possibility that these lytic lesions may be more consistent with pathological skeletal changes possibly due to brucellosis. Our findings support the hypothesis of a more complex diet of A. africanus that occasionally could have included meat to supplement its diet .
The fossil lumbar vertebrae L4 and L5, were examined with a stereomicroscope (Leica Wild M8) at the School of Anatomical Sciences at the University of the Witwatersrand. A mould of the lytic lesions of the anterior superior margin of the vertebral bodies of L4 and L5 was made using “President Plus Jet”, type 3, and “Elite H-D +”, Types 2 and 3. Casts were then produced and observed with a Scanning Electron Microscope (SEM) to examine the presence of osteoclastic and osteoblastic activity, which would suggest that inflammatory processes were in progress at the time of death of the individual. The SEM analyses were conducted in the Laboratories of the State University “G. d'Annunzio” in Chieti, Italy. Plain film radiographs were taken at the Helen Joseph Hospital in Johannesburg, South Africa.
A preliminary examination revealed the presence of some pathological lesions on the vertebral bodies. Lumbar vertebrae L4 and L5 have lytic lesions on the superior-anterior margin of the vertebral bodies; in particular L5 showed an excavation of the anterior-superior body with osteophytes. The position and gross morphology of the lesions were very similar to the pathological bone alterations observed in some infectious diseases in modern humans, such as in human zoonotic brucellosis .
The lumbar vertebra L5 of Stw 431 has a destructive focus on the superior-anterior margin of the body, with clear signs of active bone reaction (Figure 1A). Scanning Electron Microscope (SEM) analysis of the trabeculae surrounding the walls of the lytic lesion revealed sheets of new bone formation and Howship's lacunae due to the osteoclastic and osteoblastic cell activity (demonstrating that the bone alteration occurred in vitam) (Figure 1E). The lateral radiograph shows the destructive lesion of the anterior vertebral body and a sclerosis limited to the affected area consistent with the Sign of Pedro-Pons ,  (Figure 1B).
Stereomicroscopic and radiographic studies of L5 (A, B), and L4 (C, D). Scanning Electron Microscope (SEM) analysis showing Howship's lacunae of L5 (E) and L4 (F).
The lumbar vertebra L4 of Stw 431 presented granulomatosic tissue in a clearly delimited region of the anterior rim of the body (Figure 1C). The SEM images revealed bone destruction mediated by osteoclasts (Figure 1F), whose activity may have been stimulated by pathogenic organisms. The radiographs of the sample also revealed a sclerotic repair of the lesion (Figure 1D).
The macroscopic, microscopic and radiological appearance of the lytic lesions of 4th and 5th lumbar vertebrae is consistent with all the skeletal characteristics of brucellosis. The remaining vertebrae and bones of this australopith skeleton did not show any other pathological lesions or degenerative changes.
We carefully considered alternative diagnoses of various infectious diseases including tuberculous and staphylococcic spondylitis, which in modern humans occasionally develop anterior epiphysitis of the vertebral body . Nevertheless these diseases seemed less likely to produce the complex of alterations we observed. For instance, unlike early brucellosis that frequently affects the lumbar column and particularly L4 and L5, these disease agents are usually not circumscribed and frequently involve other vertebrae . In general, tuberculosis of the spine results in collapse of the vertebral bodies and angular deformity – (Figure 2A, B ), conditions that are absent in the spine of Stw 431. We also considered Scheuermann's disease which in 1983 Cook et al.  diagnosed in the vertebral column, more specifically T8 of the australopith AL-288-1AG. However, this juvenile pathology, typically affecting the thoracic vertebrae, shows lesions that differ from brucellosis both morphologically and radiologically (Figure 2C).
Modern human L4 affected by tuberculosis: macroscopic (A) and radiographic picture (B)  (Courtesy of Capasso; adult female E58, Herculaneum, 79 AD, University Museum of Chieti). Scheuermann's disease in the vertebral column of a living 18 years old male: Radiographic analysis (C) (Courtesy of Zipfel; School of Anatomical Sciences at the University of the Witwatersrand). Modern human L4 affected by brucellosis: macroscopic (D) and radiographic picture (E)  (Courtesy of Capasso; adult female E50, Herculaneum, 79 AD, University Museum of Chieti).
We also evaluated the possibility that the marked epiphysitis observed in the L5 of Stw 431 may have resulted from degenerative processes due to aging and/or bipedal locomotion reported in early hominins. However, this possibility also seemed less likely because the paleopathological examination of the skeletal elements of Stw 431 did not show any other degenerative lesions that could be associated with age or mode of locomotion.
Staps  described the vertebral lesions in the Stw 431 individual as spondylosis deformans of L5 as a result of trauma. The lytic lesion of the superior-anterior margin of L5 may be interpreted as a lesion having resulted from an intrabody herniation of disc material (so-called Schmorl's node)  or as the sequela of a remote injury in an immature skeleton (limbus vertebrae) –. Trauma, directly or with possible consequent necrosis of the anterior epiphysis is a possible interpretation that cannot be completely ruled out. However trauma does not appear to fit well with the lesion in L4: the granulomatosic tissue in the delimited region of the anterior rim of the body was more likely the result of an acute inflammatory process rather than of a traumatic fracture of the superior-anterior margin of the vertebral body.
After carefully evaluating all reasonable alterative hypotheses we suggest that the position, gross morphology and the radiological appearance of the lesions observed in the vertebral elements L4 and L5 of Australopithecus africanus Stw 431seem to be more consistent with the pathological condition of early brucellosis .
Brucellosis in humans is currently comparatively rare in developed countries . Many recent cases come from areas such as North Africa and the Middle East. The disease in humans occurs as a chronic infection of the lungs and other organs. In a number of cases, the skeleton becomes infected by the hematogenous route . Skeletal involvement varies from 2% to 70% of the cases  and 20% to 80% of patients with brucellosis experience osteoarticular symptoms . In historical times adult human males are affected much more frequently than females, independently from the species of Brucella involved . The most common skeletal lesion occurs in the spine or the sacroiliac joint , . Ganado and Craig  observed 130 instances of spondylitis in 6300 patients with brucellosis. Long bones were rarely involved . Kelly et al.  observed in 36 cases the following distribution: spine, 47,2%; humerus, 8,3%; femur, 5,6%; ilium, 2,8%; hand, 2,8% and foot, 2,8%. The spinal lesions involved the vertebral bodies, especially of the lower thoracic, lumbar and lumbosacral areas , , . The early skeletal signs of brucellar diseases are characterised by the epiphysitis of the anterior-superior angle of the lumbar vertebrae, radiographically showing a selective sclerosis in the antero-superior angle of the vertebra. This radiographic expression is known as the Sign of Pedro-Pons and represents a characteristic aspect of the early stage of brucellar disease in ancient human remains , , –. Brucellar lesions on vertebral bodies were observed also in human skeletal remains from archaeological sites , , – (Figure 2D, E).
In humans, Brucella melitensis is the main etiological agent of brucellosis and its diffusion is linked to the consumption of milk and dairy products such as unpasteurised cheese; yet other bacterial species such as Brucella abortus, may be transmitted to humans and other primates . B. abortus usually leads to abortion in the host and the infection is transmitted through contact with foetal membranes, post parturient discharges and milk . In recent times B. abortus has been isolated from several South African species of wildlife such as zebra (Equus burchellii), eland (Taurotragus oryx), waterbuck (Kobus ellipsiprymnus) and impala (Aepyceros melampus) .
Given this background, it seems reasonable to suggest that some species of Brucella (possibly even B. abortus) could have been the infective agent in this Australopithecus africanus individual, through contact with (or consumption of ) infected tissues of other mammals, such as parturient discharges, foetal membranes or meat of young antelopes or other Ungulata. Occasional meat eating is well documented among baboons and chimpanzees – and therefore similar dietary behaviour in australopith from South Africa seems likely . Our hypothesis is supported by the results of stable carbon isotope analysis of A. africanus from Makapansgat Limeworks, South Africa, that suggest a diet based not only on fruit and leaves, but also on large quantities of carbon-13-enriched foods such as grasses and sedges or animals that ate these plants, or both , .
In conclusion, we feel that the type and distribution of the lytic lesions observed in the lumbar vertebrae L4 and L5 of the Stw 431 individual are most consistent with early brucellosis. Consequently, this paleopathological case may represent the first example of an infectious disease in an australopith and, in particular, suggests that mammal tissues could have been an important but perhaps highly variable part of the australopith diet. However, even in light of this compelling evidence we strike a cautionary note as we cannot completely rule out that these lesions result from other infectious diseases such as echinococcosis and fungal diseases  or even an unusual form of trauma.
The hypothesis of brucellosis (most often associated with the consumption of animal proteins) in a Pliocene hominin has important implications for human evolution. The consumption of meat has been regarded an important factor in supporting, directing or altering human evolution –.
Perhaps the earliest paleontological evidence (up to 2.5 m.y. BP) for meat eating consists of cut marks on animal remains and stone tools that could have made these marks –. Now with the hypothesis of brucellosis in A. africanus we may have evidence of occasional meat eating directly linked to a fossil hominin.
We thank J. Limbachia and E. Joseph of the Helen Joseph Hospital for help with radiography, A. Traini for the Scanning Electron Microscope (SEM) analysis and C. G. Menter for assistance. We are grateful to the University of the Witwatersrand for access to the fossil material. Comments from the Editor and the reviewers helped to improve the paper.
Conceived and designed the experiments: RD LC. Performed the experiments: RD BZ JMC. Analyzed the data: RD BZ JMC RS LC. Contributed reagents/materials/analysis tools: RD. Wrote the paper: RD BZ. Acquired the data and the Scanning Electron Microscope analysis and contributed to the interpretation of data: RD. Described the anthropological characteristics of A. africanus Stw 431 and the main geological features of the paleontological site: BZ. Produced the mould of the vertebrae of Stw 431, contributed to the interpretation of data and to the writing of the article: JMC. Contributed to the interpretation of data and the writing of the article: RS LC.
- 1. Tobias PV (1974) Aspects of pathology and death among early hominids. The Leech 44: 119–124.PV Tobias1974Aspects of pathology and death among early hominids.The Leech44119124
- 2. Trinkaus E, Zimmerman MR (1982) Trauma among the Shanidar Neandertals. Am J Phys Anthropol 57: 61–76.E. TrinkausMR Zimmerman1982Trauma among the Shanidar Neandertals.Am J Phys Anthropol576176
- 3. Cook DC, Buikstra JE, DeRousseau CJ, Johanson DC (1983) Vertebral pathology in the Afar australopithecines. Am J Phys Anthropol 60: 83–101.DC CookJE BuikstraCJ DeRousseauDC Johanson1983Vertebral pathology in the Afar australopithecines.Am J Phys Anthropol6083101
- 4. Lovell NC (1991) An evolutionary framework for assessing illness and injury in nonhuman primates. Am J Phys Anthropol 34: 117–155.NC Lovell1991An evolutionary framework for assessing illness and injury in nonhuman primates.Am J Phys Anthropol34117155
- 5. Fisk GR, Macho GA (1992) Evidence of a healed compression fracture in a Plio-Pleistocene hominid talus from Sterkfontein, South Africa. Int J Osteoarch 2: 325–332.GR FiskGA Macho1992Evidence of a healed compression fracture in a Plio-Pleistocene hominid talus from Sterkfontein, South Africa.Int J Osteoarch2325332
- 6. Tobias PV (1994) The Pathology of the Kanam Mandible. Journal of Paleopathology 6: 125–128.PV Tobias1994The Pathology of the Kanam Mandible.Journal of Paleopathology6125128
- 7. Toussaint M, Macho GA, Tobias PV, Partridge TC, Hughes AR (2003) The third partial skeleton of a late Pliocene hominin (Stw 431) from Sterkfontein, South Africa. South African Journal of Science 99: 215–223.M. ToussaintGA MachoPV TobiasTC PartridgeAR Hughes2003The third partial skeleton of a late Pliocene hominin (Stw 431) from Sterkfontein, South Africa.South African Journal of Science99215223
- 8. Vrba ES (1985) Early hominids in southern Africa: updated observations on chronological and ecological background. In: Tobias PV, editor. Hominid evolution: past, present and future. New York: Alan R Liss. pp. 195–200.ES Vrba1985Early hominids in southern Africa: updated observations on chronological and ecological background.PV TobiasHominid evolution: past, present and futureNew YorkAlan R Liss195200
- 9. Delson E (1988) Chronology of South African australopiths site units. In: Grine FE, editor. Evolutionary history of the robust australopithecines. New York: Aldine de Gruyter. pp. 317–325.E. Delson1988Chronology of South African australopiths site units.FE GrineEvolutionary history of the robust australopithecinesNew YorkAldine de Gruyter317325
- 10. McKee JK, Thackeray JF, Berger LR (1995) Faunal assemblage serration of Southern African Pliocene and Pleistocene fossil deposits. Am J Phys Anthropol 106: 235–250.JK McKeeJF ThackerayLR Berger1995Faunal assemblage serration of Southern African Pliocene and Pleistocene fossil deposits.Am J Phys Anthropol106235250
- 11. Kuman K, Clarke RJ (2000) Stratigraphy, artifact industries and hominid associations for Sterkfontein, Member 5. J Hum Evol 38: 827–847.K. KumanRJ Clarke2000Stratigraphy, artifact industries and hominid associations for Sterkfontein, Member 5.J Hum Evol38827847
- 12. Berger LR, Lacruz R, de Ruiter DJ (2002) Brief communication: Revised age estimates of Australopithecus-bearing deposits at Sterkfontein, South Africa. Am J Phys Anthropol 119: 192–197.LR BergerR. LacruzDJ de Ruiter2002Brief communication: Revised age estimates of Australopithecus-bearing deposits at Sterkfontein, South Africa.Am J Phys Anthropol119192197
- 13. Staps D (2002) The first documented occurrence of spondylosis deformans in an early hominin. Am J Phys Anthropol Suppl 34: 146.D. Staps2002The first documented occurrence of spondylosis deformans in an early hominin.Am J Phys Anthropol Suppl34146
- 14. Ungar SP (2007) Evolution of the human diet: the known, the unknown, and the unknowable. Oxford: Oxford University Press. 413 p.SP Ungar2007Evolution of the human diet: the known, the unknown, and the unknowable.OxfordOxford University Press413
- 15. Etxeberria F (1994) Vertebral epiphysitis: early signs of brucellar disease. Journal of Paleopathology 6: 41–49.F. Etxeberria1994Vertebral epiphysitis: early signs of brucellar disease.Journal of Paleopathology64149
- 16. Pedro-Pons A, Farreras P (1944) La Brucelosis Humana. Barcelona: Ed Salvat. 251 p.A. Pedro-PonsP. Farreras1944La Brucelosis Humana.BarcelonaEd Salvat251
- 17. Alberola I (1986) Clinica de la brucelosis humana. Revista Sanitaria del Servicio Vasco de Salud 0: 38–43.I. Alberola1986Clinica de la brucelosis humana.Revista Sanitaria del Servicio Vasco de Salud03843
- 18. Capasso L (2001) I fuggiaschi di Ercolano. Roma: L'Erma di Bretschneider. L. Capasso2001I fuggiaschi di Ercolano.RomaL'Erma di Bretschneider
- 19. Ortner JD (2003) Identification of Pathological Conditions in Human Skeletal Remains. San Diego USA: Academic Press. 645 p.JD Ortner2003Identification of Pathological Conditions in Human Skeletal Remains.San Diego USAAcademic Press645
- 20. Reinhart M (1932) Die Fälle von Spondylitis in der Aargauischen Heilstätte Baemelweid aus den Jahren 1912-1930. Beiträge zur Klinik der Tuberkulose 79: 745–749.M. Reinhart1932Die Fälle von Spondylitis in der Aargauischen Heilstätte Baemelweid aus den Jahren 1912-1930.Beiträge zur Klinik der Tuberkulose79745749
- 21. Girdlestone G (1965) Tuberculosis of Bone and Joint. London ENG: Oxford University Press. 220 p.G. Girdlestone1965Tuberculosis of Bone and Joint.London ENGOxford University Press220
- 22. Madkour MM, Sharif HS (1989) Bone and joint imaging. In: Madkour M, editor. Brucellosis. London: Butterworths. pp. 105–115.MM MadkourHS Sharif1989Bone and joint imaging.M. MadkourBrucellosisLondonButterworths105115
- 23. Mays S (2007) Lysis at the anterior vertebral body margin: evidence for brucellar spondylitis? Int J Osteoarch 17: 107–118.S. Mays2007Lysis at the anterior vertebral body margin: evidence for brucellar spondylitis?Int J Osteoarch17107118
- 24. Ghelman B, Freiberger RH (1976) The limbus vertebra: an anterior disc herniation demonstrated by discography. Am J Roentgenol 127: 854–855.B. GhelmanRH Freiberger1976The limbus vertebra: an anterior disc herniation demonstrated by discography.Am J Roentgenol127854855
- 25. Henales V, Hervás JA, López P, Martínez JM, Ramos R, et al. (1993) Intervertebral disc herniations (limbus vertebrae) in pediatric patients: report of 15 cases. Pediatr Radiol 23: 608–610.V. HenalesJA HervásP. LópezJM MartínezR. Ramos1993Intervertebral disc herniations (limbus vertebrae) in pediatric patients: report of 15 cases.Pediatr Radiol23608610
- 26. Mupparapu M, Vuppalapati A, Mozaffari E (2002) Radiographic diagnosis of Limbus vertebra on a lateral cephalometric film: report of a case. Dentomaxillofac Radiol 31: 328–330.M. MupparapuA. VuppalapatiE. Mozaffari2002Radiographic diagnosis of Limbus vertebra on a lateral cephalometric film: report of a case.Dentomaxillofac Radiol31328330
- 27. Norden C, Gillespie WJ, Nade S (1994) Infections in bones and joints. Boston: Blackwell Scientific Publications. 438 p.C. NordenWJ GillespieS. Nade1994Infections in bones and joints.BostonBlackwell Scientific Publications438
- 28. Spink W (1956) The Nature of Brucellosis. Minneapolis: University of Minnesota Press. 446 p.W. Spink1956The Nature of Brucellosis.MinneapolisUniversity of Minnesota Press446
- 29. Jaffe H (1972) Metabolic, Degenerative, and Inflammatory Disease of Bones and Joints. Philadelphia: Lea and Febiger. 1101 p.H. Jaffe1972Metabolic, Degenerative, and Inflammatory Disease of Bones and Joints.PhiladelphiaLea and Febiger1101
- 30. Mikolich DJ, Boyce JM (1989) Brucella species. In: Mandell GL, Douglas RG, Benner JE, editors. Principles and practice of infectious diseases. New York: Churchill Livingstone. pp. 1735–1742.DJ MikolichJM Boyce1989Brucella species.GL MandellRG DouglasJE BennerPrinciples and practice of infectious diseasesNew YorkChurchill Livingstone17351742
- 31. Glasgow M (1976) Brucellosis of the spine. British Journal of Surgery 63: 283–288.M. Glasgow1976Brucellosis of the spine.British Journal of Surgery63283288
- 32. Rajapakse C (1995) Bacterial infections: Osteoarticular brucellosis. Bailliere's Clinical Rheumatology 9: 161–177.C. Rajapakse1995Bacterial infections: Osteoarticular brucellosis.Bailliere's Clinical Rheumatology9161177
- 33. Ganado W, Craig A (1958) Brucellosis myelopathy. Journal of Bone and Joint Surgery 40A: 1380–1387.W. GanadoA. Craig1958Brucellosis myelopathy.Journal of Bone and Joint Surgery40A13801387
- 34. Kelly P, Martin W, Schieger A, Weed L (1960) Brucellosis of the bones and joints: Experience with 36 patients. Journal of the American Medical Association 174: 347–353.P. KellyW. MartinA. SchiegerL. Weed1960Brucellosis of the bones and joints: Experience with 36 patients.Journal of the American Medical Association174347353
- 35. Lowbeer L (1948) Brucellotic osteomyelitis of the spinal column in man. American Journal of Pathology 24: 723–724.L. Lowbeer1948Brucellotic osteomyelitis of the spinal column in man.American Journal of Pathology24723724
- 36. Lowbeer L (1949) Brucellotic osteomyelitis of man and animal. Proceeding of Staff Meeting of Hillcrest Memorial Hospital 6: 1–36.L. Lowbeer1949Brucellotic osteomyelitis of man and animal.Proceeding of Staff Meeting of Hillcrest Memorial Hospital6136
- 37. Mousa AR, Muhtaseb SA, Almudallal DS, Khodeir SM, Marafie AA (1987) Osteoarticular complications of brucellosis: a study of 169 cases. Rev Infect Dis 9: 531–543.AR MousaSA MuhtasebDS AlmudallalSM KhodeirAA Marafie1987Osteoarticular complications of brucellosis: a study of 169 cases.Rev Infect Dis9531543
- 38. Bahar RH, Al-Suhaili AR, Mousa AM, Nawaz MK, Kaddah N, et al. (1988) Brucellosis: appearance on skeletal imaging. Clin Nucl Med 13: 102–106.RH BaharAR Al-SuhailiAM MousaMK NawazN. Kaddah1988Brucellosis: appearance on skeletal imaging.Clin Nucl Med13102106
- 39. Madkour MM, Sharif HS, Abed MY, Al-Fayez MA (1988) Osteoarticular brucellosis: results of bone scintigraphy in 140 patients. Am J Roentgenol 150: 1101–1105.MM MadkourHS SharifMY AbedMA Al-Fayez1988Osteoarticular brucellosis: results of bone scintigraphy in 140 patients.Am J Roentgenol15011011105
- 40. Cordero M, Sanchez I (1991) Brucellar and tuberculous spondylitis. A comparative study of their clinical features. Journal of Bone and Joint Surgery 73: 100–103.M. CorderoI. Sanchez1991Brucellar and tuberculous spondylitis. A comparative study of their clinical features.Journal of Bone and Joint Surgery73100103
- 41. el-Desouki M (1991) Skeletal brucellosis: assessment with bone scintigraphy. Radiology 81: 415–418.M. el-Desouki1991Skeletal brucellosis: assessment with bone scintigraphy.Radiology81415418
- 42. Ozgocmen S, Ardicoglu A, Kocakoc E, Kiris A, Ardicoglu O (2001) Paravertebral abscess formation due to brucellosis in a patient with ankylosing spondylitis. Joint Bone Spine 68: 521–524.S. OzgocmenA. ArdicogluE. KocakocA. KirisO. Ardicoglu2001Paravertebral abscess formation due to brucellosis in a patient with ankylosing spondylitis.Joint Bone Spine68521524
- 43. Geyik MF, Gür A, Nas K, Cevik R, Saraç J, et al. (2002) Musculoskeletal involvement of brucellosis in different age groups: a study of 195 cases. Swiss Med Wkly 132: 98–105.MF GeyikA. GürK. NasR. CevikJ. Saraç2002Musculoskeletal involvement of brucellosis in different age groups: a study of 195 cases.Swiss Med Wkly13298105
- 44. Capasso L (1999) Brucellosis at Herculaneum. Int J Osteoarch 9: 277–288.L. Capasso1999Brucellosis at Herculaneum.Int J Osteoarch9277288
- 45. Ortner DJ, Frohlich B (2007) The EB IA tombs and burials of Bab edh-Dhra, Jordan: A bioarchaeological perspective on the people. Int J Osteoarch 17: 358–368.DJ OrtnerB. Frohlich2007The EB IA tombs and burials of Bab edh-Dhra, Jordan: A bioarchaeological perspective on the people.Int J Osteoarch17358368
- 46. Rashidi JS, Ortner DJ, Frohlich B, Jonsdottir B (2001) Brucellosis in early Bronze Age Jordan and Bahrain: an analysis of possible cases of Brucella spondylitis. Am J Phys Anthr 114: 122.JS RashidiDJ OrtnerB. FrohlichB. Jonsdottir2001Brucellosis in early Bronze Age Jordan and Bahrain: an analysis of possible cases of Brucella spondylitis.Am J Phys Anthr114122
- 47. Curate F (2006) Two possible cases of brucellosis from a Clarist monastery in Alcácer do Sal, southern Portugal. Int J Osteoarch 16: 453–458.F. Curate2006Two possible cases of brucellosis from a Clarist monastery in Alcácer do Sal, southern Portugal.Int J Osteoarch16453458
- 48. Schlabritz-Loutsevitch NE, Whatmore AM, Quance CR, Koylass MS, Cummins LB, Dick EJ, Snider CL, Cappelli D, Ebersole JL, Nathanielsz PW, Hubbard GB (2009) A novel Brucella isolate in association with two cases of stillbirth in non-human primates - first report. Journal of medical primatology 38(1): 70–3.NE Schlabritz-LoutsevitchAM WhatmoreCR QuanceMS KoylassLB CumminsEJ DickCL SniderD. CappelliJL EbersolePW NathanielszGB Hubbard2009A novel Brucella isolate in association with two cases of stillbirth in non-human primates - first report.Journal of medical primatology38(1)703
- 49. Godfroid J (2002) Brucellosis in wildlife. Rev sci tech Off int Epiz 21: 277–286.J. Godfroid2002Brucellosis in wildlife.Rev sci tech Off int Epiz21277286
- 50. Pfeiffer JE (1969) The Emergence of Man. New York: Harper and Row. 477 p.JE Pfeiffer1969The Emergence of Man.New YorkHarper and Row477
- 51. Rhine RJ, Norton GW, Wynn GM, Wynn RD, Rhine HB (1986) Insect and meat eating among infant and adult baboons (Papio cynocephalus) of Mikumi National Park, Tanzania. Am J Phys Anthropol 70: 105–118.RJ RhineGW NortonGM WynnRD WynnHB Rhine1986Insect and meat eating among infant and adult baboons (Papio cynocephalus) of Mikumi National Park, Tanzania.Am J Phys Anthropol70105118
- 52. Stanford CB, Wallis J, Matama H, Goodall J (1994) Patterns of predation by chimpanzees on red colobus monkeys in Gombe National Park, Tanzania, 1982-1991. Am J Phys Anthropol 94: 213–228.CB StanfordJ. WallisH. MatamaJ. Goodall1994Patterns of predation by chimpanzees on red colobus monkeys in Gombe National Park, Tanzania, 1982-1991.Am J Phys Anthropol94213228
- 53. Stanford CB, Wallis J, Mpongo E, Goodall J (1994) Hunting decisions in wild chimpanzees. Behaviour 131: 1–20.CB StanfordJ. WallisE. MpongoJ. Goodall1994Hunting decisions in wild chimpanzees.Behaviour131120
- 54. Speth JD (1989) Early hominid hunting and scavenging: the role of meat as an energy source. J Hum Evol 18: 329–343.JD Speth1989Early hominid hunting and scavenging: the role of meat as an energy source.J Hum Evol18329343
- 55. Sponheimer M, Lee-Thorp JA (1999) Isotopic Evidence for the Diet of an Early Hominid, Australopithecus africanus. Science 283: 368–370.M. SponheimerJA Lee-Thorp1999Isotopic Evidence for the Diet of an Early Hominid, Australopithecus africanus.Science283368370
- 56. Sponheimer M, Passey BH, de Ruiter DJ, Guatelli-Steimberg D, Cerling TE, et al. (2006) Isotopic Evidence for Dietary Variability in the Early Hominin Paranthropus robustus. Science 314: 980–882.M. SponheimerBH PasseyDJ de RuiterD. Guatelli-SteimbergTE Cerling2006Isotopic Evidence for Dietary Variability in the Early Hominin Paranthropus robustus.Science314980882
- 57. Ungar PS (2007) Evolution of the Human Diet The Known, the Unknown, and the Unknowable. Oxford: University Press. 413 p.PS Ungar2007Evolution of the Human Diet The Known, the Unknown, and the Unknowable.OxfordUniversity Press413
- 58. Stanford CB, Bunn HT (2001) Meat-Eating and Human Evolution. Oxford: University Press. 370 p.CB StanfordHT Bunn2001Meat-Eating and Human Evolution.OxfordUniversity Press370
- 59. Stanford CB, Bunn HT (1999) Meat Eating and Hominid Evolution. Current Anthropology 40: 726–728.CB StanfordHT Bunn1999Meat Eating and Hominid Evolution.Current Anthropology40726728
- 60. Milton K (1999) A hypothesis to explain the role of meat-eating in human evolution. Evolutionary Anthropology 8: 11–21.K. Milton1999A hypothesis to explain the role of meat-eating in human evolution.Evolutionary Anthropology81121
- 61. Rose L, Marshall F (1996) Meat Eating, Hominid Sociality, and Home Bases Revisited. Current Anthropology 37: 307–338.L. RoseF. Marshall1996Meat Eating, Hominid Sociality, and Home Bases Revisited.Current Anthropology37307338
- 62. Pobiner BL, Rogers MJ, Monahan CM, John WK, Harris JWK (2008) New evidence for hominin carcass processing strategies at 1.5 Ma, Koobi Fora, Kenya. J Hum Evol 55: 103–130.BL PobinerMJ RogersCM MonahanWK JohnJWK Harris2008New evidence for hominin carcass processing strategies at 1.5 Ma, Koobi Fora, Kenya.J Hum Evol55103130
- 63. Clark JD, Beyene Y, Gabriel GW, Hart WK, Renne PR, et al. (2003) Stratigraphic, chronological and behavioural contexts of Pleistocene Homo sapiens from Middle Awash, Ethiopia. Nature 423: 747–752.JD ClarkY. BeyeneGW GabrielWK HartPR Renne2003Stratigraphic, chronological and behavioural contexts of Pleistocene Homo sapiens from Middle Awash, Ethiopia.Nature423747752
- 64. Bunn HT (1994) Early Pleistocene hominid foraging strategies along the ancestral Omo River at Koobi Fora, Kenya. J Hum Evol 27: 247–266.HT Bunn1994Early Pleistocene hominid foraging strategies along the ancestral Omo River at Koobi Fora, Kenya.J Hum Evol27247266
- 65. Shipman P (1986) Studies of hominid—Faunal interactions at Olduvai George. J Hum Evol 15: 691–706.P. Shipman1986Studies of hominid—Faunal interactions at Olduvai George.J Hum Evol15691706