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Spondarthritis in the Triassic
Juan Carlos Cisneros
1
*, Uiara Gomes Cabral
2
, Frikkie de Beer
3
, Ross Damiani
4
, Daniel Costa Fortier
5
1Centro de Cie
ˆncias da Natureza, Universidade Federal do Piauı
´, Teresina, Brazil, 2Departamento de Geologia e Paleontologia, Museu Nacional, Universidade Federal do
Rio de Janeiro, Rio de Janeiro, Brazil, 3Nuclear Technology Division, South African Nuclear Energy Corporation, Pretoria, South Africa, 4Staatliches Museum fu
¨r
Naturkunde Stuttgart, Stuttgart, Germany, 5Departamento de Paleontologia e Estratigrafia, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil
Abstract
Background:
The evidence of several forms of arthritis has been well documented in the fossil record. However, for pre-
Cenozoic vertebrates, especially regarding reptiles, this record is rather scarce. In this work we present a case report of
spondarthritis found in a vertebral series that belonged to a carnivorous archosaurian reptile from the Lower Triassic (,245
million years old) of the South African Karoo.
Methodology/Principal Findings:
Neutron tomography confirmed macroscopic data, revealing the ossification of the entire
intervertebral disc space (both annulus fibrosus and nucleus pulposus), which supports the diagnosis of spondarthritis.
Conclusions/Significance:
The presence of spondarthritis in the new specimen represents by far the earliest evidence of
any form of arthritis in the fossil record. The present find is nearly 100 million years older than the previous oldest report of
this pathology, based on a Late Jurassic dinosaur. Spondarthritis may have indirectly contributed to the death of the animal
under study.
Citation: Cisneros JC, Gomes Cabral U, de Beer F, Damiani R, Costa Fortier D (2010) Spondarthritis in the Triassic. PLoS ONE 5(10): e13425. doi:10.1371/
journal.pone.0013425
Editor: Gian Paolo Fadini, University of Padova, Italy
Received June 16, 2010; Accepted September 24, 2010; Published October 14, 2010
Copyright: ß2010 Cisneros 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: Palaeontological Scientific Trust, PAST, South Africa (www.past.org.za). South African Nuclear Energy Corporation, NECSA, South Africa (www.necsa.co.
za). NECSA participated in study design, data collection and analysis of the authors’ study. The funders had no role in decision to publish, or preparation of the
manuscript.
Competing Interests: One of the co-authors is employed at NECSA, one of the funders of the present study. This, however, does not alter the authors’
adherence to all the PLoS ONE policies on sharing data and materials.
* E-mail: juan.cisneros@ufpi.edu.br
Introduction
The Karoo Basin, comprising South Africa and neighboring
countries, has produced an unparalleled wealth of past life, being
notable for its detailed record of fossil vertebrates that highlight the
Permo-Triassic biotic crisis [1]. In this contribution, we analyze
the vertebral remains of a carnivorous reptile from the Lower
Triassic of South Africa, a specimen that shows macroscopic signs
of a severe bone pathology. The condition is here identified as
spondarthritis, which encompasses a diverse group of related
inflammatory arthritides that share multiple clinical features as
well as common genetic predisposing factors [2], and it represents
the oldest instance of this pathology hitherto known.
Materials and Methods
Specimen BP-1-5796 (stored at the Bernard Price Institute for
Palaeontological Research, Johannesburg) consists of three
articulated anterior caudal vertebrae of a large, basal archosaurian
reptile (Figure 1). The specimen was collected at Driefontein
District, Free State Province, South Africa. This locality produces
a fauna that is considered to represent the lower portion of the
Cynognathus Zone (Cynognathus subzone A), of late Early Triassic age
(Olenekian, ,245 Ma) [3,4,5].
Neutron tomography, a nondestructive technique, was em-
ployed in order to examine the internal structure of the specimen.
This was performed through the SANRAD tomography facility at
the SAFARI-1 nuclear research reactor operated by the South
African Nuclear Energy Corporation (NECSA) in Pretoria. The
reactor has a design power of 20MW and provides a neutron flux
of 1.26107 n.cm-2.s-1 at beam port no-2 at the object under
investigation. For detailed specifications of the SANRAD
tomography facility see [6,7]. The specimen was placed on top
of a rotating desk, on which a total of 180 projections in 180
angular degrees were made (Video S1). The image reconstruction
procedure was performed on IDL based GSECARS Tomography
Processing Software [8]. VGStudio MAX 2.1 software from
Volume-Graphics was used for 3D rendering, segmentation and
slicing of the images obtained.
Results
The specimen here studied is composed by three nearly
complete, fused vertebral bodies and partial zygapophyses
(Figure 1). The vertebrae are almost complete, except for the
missing distal portions of the neural spines. Judging from the size
of these vertebrae, it is assumed that they belonged to a large,
probably old individual. These are overall well preserved and show
no signs of taphonomical alteration. As the vertebrae are fused, it
is not possible to provide the length of each vertebra, the total
length of the specimen being 116 mm.
The osseous reactions in all three vertebrae are very similar,
however, the two posterior vertebrae are visibly more affected
(Figures 1A–C and 2A–D). In these vertebrae, the lateral and
ventral surfaces of the vertebral bodies exhibit an exuberant
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osseous overgrowth, being located below the left and right
transverse processes. This osseous growth precludes the visualiza-
tion of intervertebral limits. Neither zygapophyses or neural arcs
were affected, due to this, they are not fused, and the space
between these structures is filled with sediment.
The neutron tomography (Figure 2) revealed no traces of
fracture or trauma in the vertebral series. Through the
tomography we observed that the intervertebral disc spaces (both
annulus fibrosus and nucleus pulposus) are totally ossified,
producing the complete ankylosis of the vertebrae (Figure 2F
and G, Video S2 and S4). In this way, it is not possible to
distinguish the limits of each vertebral element. No evidence of
zygapophyseal ankylosis, however, was found through the
tomography (Figure 2E and H, Video S1, S3 and S4), thus,
confirming what was recognized by the external exam of the
specimen. Neutron images also showed that in the innermost layer
of the vertebral bodies the trabecular bone forms trabecular
bridges that follow a regular pattern across the ankylosed areas
(Figure 2G, Video S4). The absence of an irregular pattern of
trabecular bone allows to discard the hypothesis of an infectious
process or tumor [9,10].
Differential diagnosis
There are developmental anomalies that can lead to similar
vertebral ankyloses to the one observed in the vertebrae here
studied. This is the case of congenital vertebral synostosis, which
can occur both by an alteration of the secondary embrionary
segmentation or due to absence of intervertebral discs [11]. It is
not common, however, that bones affected solely by this anomaly
bear an external osseous protuberance such as the one found in
our specimen.
Regarding non-congenital pathologies, there is a variety of
processes that can affect, directly or indirectly, leading to vertebral
ankylosis. Fractures on articular surfaces may result in the damage
and osseous ankylosis of these articulations. This problem is
related to cominutive fractures, where more than one articular
surface is involved with the fibrocartilage callus, fusing two or
more bones [12]. In vertebrae, ankylosis is a common sequel to
fractures by compression of one or more vertebral bodies, this
occurs through a mechanism of fibrocartilage callus production
that extends to one or more adjacent vertebrae [12]. In cases of
ankylosis resulting from trauma, evidence of one or more fracture
lines often remains, allowing recognition of this process. However,
there is no evidence that the ankylosis in the vertebrae here studied
was the result of a traumatic process. There is neither presence of
immature bone nor evidence of fracture lines.
Rheumatoid arthritis of the vertebral column, an illness that
may also lead to vertebral ankylosis, is characterized by
progressive synostosis of the following elements: anterior and
posterior ligaments, capsules and small intervertebral articulations,
and intervertebral ligaments [11]. However, intervertebral discs
are not affected, being a pathological condition that is contradicted
by the specimen under study. Furthermore, the bone reaction in
rheumatoid arthritis is minimal or absent [13].
Another disorder that can produce vertebral ankylosis is the
diffuse idiopathic skeletal hyperostosis (DISH). DISH describes a
phenomenon characterized by calcification and ossification of
entheseal sites. The ossification and calcification of the anterolat-
eral aspect of the thoracic spine are regarded as a hallmark of the
disease, however, it is not limited to the spine, as it has often been
reported to involve peripheral sites as well [14]. It is important to
note that DISH should not be considered merely as an isolated
spinal condition but rather a systemic disease. DISH should be
regarded as an extensive proliferative musculoskeletal disease with
clinical and metabolic derangements [14]. Resnick and Niwayama
[15] defined the classification criterion that is currently used:
involvement of at least four contiguous thoracic vertebral
segments, preservation of intervertebral disc spaces, and the
absence of apophyseal joint degeneration or sacroiliac inflamma-
Figure 1. External views of vertebrae BP-1-5796. A. Left lateral
view. B. Right lateral view. C. Posterior view. D. Schematic drawing of a
basal archosaurian reptile, showing the likely placement of the vertebral
series within the caudal region of the column. Scale bars represent
10 mm for (A–B), and 1 m for (D).
doi:10.1371/journal.pone.0013425.g001
Spondarthritis in the Triassic
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tory changes. The condition is recognized radiographically by the
presence of ‘‘flowing’’ ossification along the anterolateral margins
of the vertebrae and the absence of changes of spondyloarthrop-
athy or degenerative spondylosis [16].
Osteoarthritis is a non-erosive type of arthritis, in which the
primary sites of tissue injury are the cartilage of the joint and the
subchondral bone, directly underlying and supporting it [13]. In
osteoarthritis, overgrowth of bone (osteophytes) do occur, but not
bone resorption. Vertebral phenomena, however, are usually not a
result of osteoarthritis. The term osteoarthritis is properly
restricted in application to diarthrodial joints, thus, excluding the
disk spaces [17]. The only form of spine disease accurately referred
to as osteoarthritis is that producing osseous overgrowth
(osteophytes) of the zygapophyseal joints [10].
The term ‘‘spondyloarthropathy’’ is still frequently employed in
the literature (both medical and paleopathological), however, it is
recommended the use of the term ‘‘spondarthritis’’ (or ‘‘spondy-
loarthritis’’), because the suffix ‘‘arthropathy’’ is too ambiguous
and does not indicate the inflammatory nature of the condition
[18,19,20]. The spondarthrites are characterized by axial and
Figure 2. Neutron tomographies of vertebrae BP-1-5796. A. First (anterior to posterior direction) preserved vertebrae. B. Second vertebrae. C–
D. Third vertebrae. A–C. Transversal slices, in anterior view, at level of anterior border of the transverse process. D. Transversal slice, in anterior view, at
level of maximum thickness of inflammation. E–F. Coronal slices of the vertebral series in dorsal view, (E) at level of the neural canal, (F) at level of the
centrae, anterior to the left. G. Sagittal slice of the vertebral series in right view. H. Raw neutron image in right lateral view. Scale bar represents
10 mm.
doi:10.1371/journal.pone.0013425.g002
Spondarthritis in the Triassic
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peripheral arthritis, absence of rheumatoid factor, increased
frequency of HLA-B27, overlapping syndromes, familial aggrega-
tion, and mutual association within patients and families [20]. The
following diagnostic criteria have been employed in skeletal
analyses: evidence of zygapophyseal or sacroiliac joint erosion or
ankylosis; asymmetrical arthritis patterns; reactive new bone
formation; syndesmophytes (being either marginals or calcifica-
tions/ossifications within the annulus fibrosus); or, peripheral joint
ankylosis [17,21]. Zygapophyseal joint erosion or ankylosis and
ossification within annulus fibrosus are pathognomonic signals
[17]. In addition, Golding [22] reports that a more florid type of
periosteal reaction occurs in the spondarthritis group of arthritic
disorders, such as Reiter’s disease and psoriatic arthritis.
Furthermore, the presence of annulus fibrosus ossification in
combination with typical syndesmophytes, allows to discard the
diagnosis for DISH, discarthrosis and infectious spondylitis [19].
The diagnosis for some diseases is defined based on the presence
of characteristic features in certain bones or in a group of them.
For this reason, the study of pathologies on isolated bones may
become a delicate question. However, despite of the obstacles that
are inherent to diagnosing isolated bones, these instances of
pathologies do have their own value, specially in relation to
behavior and habitat. In perspective, they reinforce through
understanding the population that they represent [17]. Through
the differential diagnosis of the features found in the vertebral
series, it is possible to discard in our specimen the possibility of
congenital anomaly, fracture, tumor, rheumatoid arthritis, DISH,
or osteoarthritis. Based on the present analysis, the most probable
explanation, supported both by the elimination of other hypothesis
and by the observed characteristics, is that the vertebral ankylosis
was generated by a process of spondarthritis.
Discussion
It is not always feasible to identify the variety of spondarthritis
recorded. Not even clinically, when it is possible to actually talk with an
afflicted human. The presence of ancillary body system involvement
(e.g., dermatologic, genito-urinary symptom) allows spondarthrites to
be distinguished clinically, but discrimination among them may not be
possible when only the skeleton is available for analysis [13].
The present find constitutes the oldest instance of spondarthritis
in the fossil record. The previous oldest evidence of this pathology
was found on vertebrae from the dinosaur Camarasaurus from Utah,
USA [23] of latest Jurassic age (Tithonian, ,147 Ma). Thus, our
find extends the presence of spondarthritis in the fossil record by
nearly one hundred million years, back to the Early Triassic.
The vertebrae under study constitute the remnants of a large,
and presumably old, carnivorous reptile. Being affected by this
pathology, the individual would suffer an increasing constraint of
the movements of its axial skeleton that slowly would hamper its
faculty of locomotion. Such condition was surely disadvantageous
in a number of activities that may require great physical effort,
such as praying and territory defense. By gradually imposing
restrictions in activities that are vital to the individual (i.e.
acquisition of food items) the development of spondarthritis may
have indirectly contributed to the death of this individual.
Conclusions
A severe pathology was recognized in a caudal vertebral series
of a basal archosaurian reptile from the Lower Triassic of the
South African Karoo. Both macroscopic examination and neutron
tomography data revealed features that are diagnostic of
spondarthritis. As such, the present find represents the earliest
example of this pathology in the fossil record. The disease was
likely an indirect cause of the death of the animal.
Supporting Information
Video S1 Rotation of vertebrae BP-1-5796, made from 180
neutron images in 180 angular degrees.
Found at: doi:10.1371/journal.pone.0013425.s001 (3.13 MB
MPG)
Video S2 Parasagittal slices of vertebrae BP-1-5796, from left to
right.
Found at: doi:10.1371/journal.pone.0013425.s002 (1.04 MB
MP4)
Video S3 Transversal slices of vertebrae BP-1-5796, in posterior
to anterior direction.
Found at: doi:10.1371/journal.pone.0013425.s003 (2.21 MB
MP4)
Video S4 Coronal slices of vertebrae BP-1-5796, in ventral to
dorsal direction.
Found at: doi:10.1371/journal.pone.0013425.s004 (1.17 MB
MP4)
Acknowledgments
We are in debt to John Hancox (BPI Palaeontology, Johannesburg) for
collecting the specimen and to Bruce Rothschild (University of Kansas) for
valuable discussion. Editor Gian Paolo Fadini and three anonymous
reviewers are kindly acknowledged.
Author Contributions
Conceived and designed the experiments: JCC FdB RD. Performed the
experiments: FdB. Analyzed the data: JCC UGC. Contributed reagents/
materials/analysis tools: FdB. Wrote the paper: JCC UGC. Processed
images: DCF.
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