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Epidemiologic Study of Tumors in Dinosaurs

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Naturwissenschaften (2003) 90:495–500

DOI 10.1007/s00114-003-0473-9

SHORT COMMUNICATION

B. M. Rothschild · D. H. Tanke · M. Helbling ·


L. D. Martin

Epidemiologic study of tumors in dinosaurs

Received: 16 June 2003 / Accepted: 29 August 2003 / Published online: 14 October 2003
 Springer-Verlag 2003

Abstract Occasional reports in isolated fragments of of mummies), the confident diagnosis of pre-Cenozoic
dinosaur bones have suggested that tumors might repres- tumors has been elusive. Exceptions include examples of
ent a population phenomenon. Previous study of humans osteoma (a benign slow growing mass of lamellar bone)
has demonstrated that vertebral radiology is a powerful in mosasaurs (Moodie 1917) and hemangioma (a benign
diagnostic tool for population screening. The epidemiol- proliferation of vascular endothelium) and metastatic
ogy of tumors in dinosaurs was here investigated by cancer (a distant spread of malignant disease) in dinosaurs
fluoroscopically screening dinosaur vertebrae for evi- (Rothschild et al. 1998, 1999). The latter two were
dence of tumors. Computerized tomography (CT) and recognized only because chance sectioning of dinosaur
cross-sections were obtained where appropriate. Among bone revealed their presence.
more than 10,000 specimens x-rayed, tumors were only The absence of any external evidence of tumor
found in Cretaceous hadrosaurs (duck-billed dinosaurs). (Rothschild et al. 1998, 1999) has suggested that macro-
These included hemangiomas and metastatic cancer scopic examination is an insensitive technique for recog-
(previously identified in dinosaurs), desmoplastic fibro- nizing vertebral neoplasia (abnormal tissue growth or
ma, and osteoblastoma. The epidemiology of tumors in tumor). Systematic sectioning of vertebrae has been
dinosaurs seems to reflect a familial pattern. A genetic considered unacceptably destructive of valuable, non-
propensity or environmental mutagens are suspected. renewable resources. Because the previously noted hem-
angioma and metastatic cancer were recognizable on x-
rays (Rothschild et al. 1998, 1999), it seemed reasonable
Introduction to conduct a radiologic survey to assess the occurrence of
known dinosaurian vertebral tumors and the possible
Tumors are infrequently recognized in extreme antiquity. existence of any other varieties.
Limited to study of the skeleton (with the rare exception

B. M. Rothschild ()) · M. Helbling II Materials and methods


Arthritis Center of Northeast Ohio,
5500 Market Street, Youngstown, OH 44512, USA Given the logistical challenges of juxtaposing specimens, routine x-
e-mail: bmr@neoucom.edu ray equipment and film development facilities, an alternative
Tel.: +1-330-7835900 approach was considered. Fluoroscopy was chosen as the screening
Fax: +1-330-7835350 technique. Obviating the requirements for film and development
facilities allows time-effective population screening. The use of a
B. M. Rothschild fluoroscope permits recognition of alterations in real time, in
Northeastern Ohio Universities College of Medicine, contrast to film radiography with its inherent film delays for each
Rootstown, OH 44527, USA exposure. Real-time visualization also allows the overlying shad-
ows from protuberant processes and taphonomic damage to be
B. M. Rothschild clearly distinguished from true pathology. Because the film
Carnegie Museum of Natural History, technique requires problematic exposure times (with an associated
Pittsburgh, PA 15213, USA risk of destruction of the expensive cathode ray tube), film–screen
combinations are required. These are composed of phosphorescent
B. M. Rothschild · L. D. Martin sheets which magnify the effect of the x-ray photons. Therefore,
University of Kansas Museum of Natural History, shorter, more practical, exposures can be utilized, thus reducing the
Lawrence, KS 66045, USA risk of damaging the x-ray cathode ray tube. Fluoroscopy
overcomes these challenges. The fluoroscopic technique utilizes a
D. H. Tanke cathode ray tube, as in routine x-rays. The image is visualized with
Royal Tyrrell Museum of Palaeontology, an image intensifier and can be recorded digitally (Resnick 2002;
Drumheller, Alberta, T0J 0Y0, Canada Rothschild and Martin 1993), thereby eliminating the expense of x-
496
ray film and development and providing immediately interpretable
images. The shortcoming of the fluoroscopic technique utilized is
the C-arm size (the space between the cathode ray tube and the
image intensifier detection system). The latter can handle speci-
mens up to 28 cm in diameter.
Given the common involvement of vertebrae in neoplastic
processes (Resnick 2002; Rothschild and Martin 1993; Rothschild
and Rothschild 1995) and size prohibition for other skeletal
components in which neoplasia is commonly found in humans
(Rothschild and Rothschild 1995), the study was limited to
vertebrae less than 28 cm in diameter. The C-arm and portable
nature of the fluoroscope allowed in situ radiography of mounted
skeletons, as well as of separate elements. Size limitation, however, Fig. 1 Cross-section (a) and x-ray (b) views of Edmontosaurus
did preclude fluoroscopic examination of the largest adult sauropod (CM 12100) vertebra. a Trabeculae in right upper portion clearly
cervical, thoraco-lumbar, and proximal caudal vertebrae. different from surrounding trabecular pattern. b Radiologically
Systematic x-ray survey screening of dinosaur vertebrae in the lucent, very circumscribed lesion with sclerotic margin and fine
collections of the American Museum of Natural History, New York trabeculation at anterior superior aspect. Posterior superior density
(AMNH); Black Hills Institute, Black Hills, South Dakota (BHI); is matrix artifact
Brigham Young University, Provo, Utah (BYU); Carnegie Museum
of Natural History, Pittsburgh, Pennsylvania (CM); Denver Muse-
um of Science and Nature, Denver, Colorado (DNMH); Field Metastatic cancer was extremely rare, found in only 1
Museum of Natural History, Chicago, Illinois (FMNH); Los out of 548 (0.2%) Edmontosaurus vertebrae. Absence in
Angeles Museum of Natural History, Los Angeles, California other genera may simply reflect an inadequate sample,
(LACM); Museum of the Rockies, Bozeman, Montana (MOR);
National Museum of Ancient Life, Lehi, Utah (NMAL); Canadian rather than species specificity. However hemangiomas
Museum of Nature, Ottawa, Ontario, Canada (CMN, aka NMC); present in 669 Edmontosaurus at a frequency of 3% were
National Museum of Natural History, Washington, D.C. (NMNH); absent in 286 Corythosaurus (c2=7.307, P<0.004). The
Oklahoma Museum of Natural History, Norman, Oklahoma absence of hemangiomas in vertebrae of 7,475 sauropods,
(OMNH); Royal Ontario Museum, Toronto, Ontario, Canada ceratopsians, stegosaurs, theropoda, ornithomimids, and
(ROM); Royal Tyrrell Museum, Drumheller, Alberta, Canada
(RTM); Texas Tech Museum, Lubbock, Texas (TTM); University ankylosaurs was statistically significant (c2=, 4.14,
of Kansas Museum of Natural History, Lawrence, Kansas (KU); P<0.05). Osteoblastoma and desmoplastic fibroma were
University of Texas Museum, Austin, Texas (TMM); University of only found in hadrosaurs and were extremely rare; only
Utah, Salt Lake City, Utah (UMNH); Wyoming Dinosaur Center, one example of each was found.
Thermopolis, Wyoming (WDC); Yale Peabody Museum, New
Haven, Connecticut (YPM), and the private collection of Jack Radiologic examination of hemangioma revealed a
Henke, Danville, Kentucky was pursued utilizing the Xi-scan sharply defined, abnormal area completely enclosed by
fluoroscopic unit. This included 10,312 vertebrae and 700+ normal bone. The abnormal bone consisted of unidirec-
individuals (minimum number based on associated/articulated tionally thickened bone trabeculae, separated by wide
skeletons). Vertebrae from incomplete specimens were identified
to genus or family on the basis of the monospecific bone beds from zones of matrix. There was no evidence of bone
which they were derived. Additionally, the bone of the previously expansion. Desmoplastic fibroma was recognized on the
suggested case of chondrosarcoma in an Allosaurus/Torvosaurus basis of the characteristic trabeculated radiolucent defect.
humerus (BYUVP 5009; Taylor 1992) was also examined macro-
scopically and radiologically.
Further radiologic examination of identified abnormal vertebrae
was performed with a triple-phase generator at 30 kV and Occurrence of osteoblastoma
190 milliamp-seconds (mAs) utilizing the high resolution Kodak-
2000 system. Computerized tomographic (CT) x-rays (General Specimen Carnegie Museum (CM 12100) was collected
Electric, Sytec-i 3000) were obtained using both 1 and 3 mm thick by J. Leroy Kay in 1937 from Location 2488: Fred
slices. The images were photographed digitally (Mavica, Sony and
GRj-DVM90, JVC) and analyzed for disruption of trabecular Townsend’s Ranch, Carter County, Montana (Late Cre-
patterns. taceous). Currently classified as Edmontosaurus, the
specimen consists of caudal vertebrae, 6 ribs, 3 chevrons,
pubes, left ischium, and skin impressions. Osteoblastoma
Results in this individual was recognized in one vertebra on the
basis of a radiologically lytic, very circumscribed, lesion
Epidemiology of tumors with sclerotic margin and very fine trabeculae (see
Fig. 1).
Radiologic evidence of neoplasia was limited to one
family, Hadrosauridae (Table 1). Within that family, only
Brachylophosaurus, Gilmoreosaurus, Bactrosaurus, and Comments on specimen
Edmontosaurus were affected and only caudal vertebrae BYUVP 5009 Allosaurus/Torvosaurus
were attacked. Hemangiomas were found in all of these
taxa. Desmoplastic fibroma (benign tumor of fibroblast Examination of an Allosaurus/Torvosaurus humerus
cells), osteoblastoma (benign tumor of bone cells), and (BYUVP 5009) with a cauliflower-like growth (Taylor
metastatic cancer were found in Edmontosaurus. 1992) revealed no evidence of cancer. The shape of the
humerus had been altered, with acute angulation midshaft.
The area of angulation was surrounded by reactive (not
497
Table 1 Evaluation of dinosaur Minimum no. No. of No. of individuals
vertebrae for presence of neo- of individuals vertebrae with tumors
plasia
Hadrosauran dinosaurs
Lambeosaurine
Bactrosaurus 2 94 3Ha
Corythosaurus 13 286
Eolambia 9 16
Hypacrosaurus 2 117
Lambeosaurus 5+ 518
Parasaurolophus 3 86
Lambeosaurid 3 21
Hadrosaurine
Brachylophosaurus 2+ 175 6Ha
Cheneosaurus 1 2
Edmontosaurus 16+ 669 15Ha
1Ma
1Da
1Ba
Gryposaurus 1 9
Hadrosaurus 6 67
Kritosaurus 10 90
Maiasaura 5 317
Prosaurolophus 5 172
Saurolophus 4 81
Edmontosaurid 6 36
Non-lambeosaurine/hadrosaurine
Gilmoreosaurus 1 49 2Ha
Non-specific 3 32
TOTAL HADROSAURS 97 2,837 29a
Non-hadrosauran dinosaurs
Order Saurischia
Suborder Sauropodomorpha 3 38
Titanosauridae
Alamosaurus 2 20
Titanosaurus 3 59
Diplodocidae
Apatosaurus 21+ 254
Barosaurus 8 30
Diplodocus 30+ 327
Camarasauridae
Camarasaurus 60+ 434
Anchisauridae
Plateosaurus 3 94
Cetiosauridae
Haplocanthosaurus 32 45
Brachiosauridae
Astrodon 57 58
Marshosaurus/Stokesaurus ? 234
Non-speciated sauropods 13 48
Suborder Theropoda
Podokesauridae
Coelophysis 2 43
Ornithomimidae
Struthiomimus 2 25
Archaeornithomimus 9 118
Dromiceiomimus 1 1
Ovoraptosauridae
Chirostenotes 3 50
Dromaeosauridae
Deinonychus 7 67
Saurornitholestes 2+ 130
Utahraptor 1 58
Troodonidae
Troodon 3+ 47
Megalosauridae
Carcharodontosaurus 4 4
Allosauridae
Allosaurus 39+ 1,091
Spinosauridae
Spinosaurus 5 6
Acrocanthosaurus 6 38
498
Table 1 (continued) Minimum no. No. of No. of individuals
of individuals vertebrae with tumors
Ceratosauridae
Ceratosaurus 4 38
Dryptosauridae
Dryptosaurus 2 2
Tyrannosauridae
Tyrannosaurus 4 58
Gorgosaurus 5 46
Daspletosaurus 4 47
Albertosaurus 6 56
Albertosaurid 1 6
Tyrannosaurid 18 130
Non-specific small theropods ? 36
Order Ornithischia
Suborder Ornithopoda
Hypsilophodontidae
Tenontosaurus 39 614
Orodromeus 2 50
Thescelosaurus 6 77
Othnielia 1 22
Non-speciated 2+ 50
Iguanodontidae
Camptosaurus 33 348
Non-specific 2 13
Dryosauridae
Dryosaurus 5 86
Suborder Ceratopsia
Psittacosauridae
Psittacosaurus 4 66
Protoceratopsidae
Protoceratops 6 104
Leptoceratops 2 25
Ceratopsidae
Brachyceratops 3 98
Centrosaurus 5 206
Monoclonius b 5 64
Chasmosaurus 7 150
Triceratops 27 195
Pachyrhinosaurus ? 180
Pentaceratops 1 9
Styracosaurus 1 23
Einiosaurus 2 32
Achelousaurus 3 35
Non-specific ceratopsian 13 48
Suborder Ankylosauria
Nodosauridae
Edmontonia 5 16
Sauropelta 13 199
Silvisaurus 1 8
Non-specific 2+ 102
Ankylosauridae
Ankylosaurus 1 22
Euplocephalus 12 87
Anodontosaurus (=Euplocephalus) 1 1
Non-speciated Ankylosauria 4 23
Suborder Pachycephalosauria
Pachycephalosauridae
Pachycephalosaurus ? 46
Suborder Stegosauria
Stegosauridae
Stegosaurus 43+ 738
TOTAL NON-HADROSAURAN 611 7,475
a
Number indicates number of individuals of that genus with each variety of tumor, if any; B =
osteoblastoma; D= desmoplastic; H = hemangioma; M = metastatic cancer
b
While Monoclonius is now classified as Centrosaurus, the horn bases in these individuals differed
from that of classic Centrosaurus
499

neoplastic) new bone. A malaligned infected fracture was unique to hadrosaurs (Barrett and Upchurch 2001; Krauss
actually responsible for the cauliflower-like growth. 2001). Hadrosaur physiology might also differ from that
of other dinosaurs. Chinsamy (Chinsamy 1994; Chinsamy
and Dodson 1995) noted that hadrosaurs show bone
Discussion structure that she felt was suggestive of endothermic
metabolism. These structures were demonstrated by
While tumors have previously been recognized in Chinsamy not to exist in a wide variety of other dinosaurs,
dinosaurs (Rothschild et al. 1998, 1999), their epidemi- including theropods.
ology has been unclear. This radio-epidemiologic study
documents the apparent restriction of tumor occurrence to
hadrosaurs. While Wade Miller at Brigham Young Diagnosis of tumors
University and Leon Goldman at the San Diego Naval
Hospital have suggested that a “cauliflower-like” growth Hemangiomas have an almost pathognomonic x-ray
on a 135–150-million-year-old theropod (probably Al- appearance: coarse vertical (cephalad–caudad) striations
losaurus or Torvosaurus) humerus might represent a type (thick trabecular struts), separated by relatively lucent
of cartilage cancer called a chondrosarcoma (Taylor zones, replacing normal trabeculae (Boye et al. 2001;
1992),personal examination of the specimen revealed that Chew 1997; Mohan et al. 1981; Resnick 2002; Rothschild
it was simply an infected fracture. Such lesions are not and Martin 1993; Schmorl and Junghanns 1971; Sherman
uncommon in the fossil record (Molnar 2001). and Wilner 1961; Yochum et al. 1993). The permeative
Although samples sizes are small for most species of edges of metastatic cancer are also easily recognizable.
dinosaurs, the combined sample is large and a relatively In addition to hemangiomas and metastatic cancer, two
high occurrence of hemangiomas in hadrosaurs, coupled additional types of tumor have been discovered in
with their absence in other kinds of dinosaurs, warrants an dinosaurs in this study: osteoblastoma and desmoplastic
explanation. It may, of course, be a genetic predilection fibroma. Osteoblastomas are radiologically lytic (radio-
towards hemangioma. If so, it would be basic to the lucent), very circumscribed lesions with sclerotic margins
hadrosaurs, as it is present in both flat-headed and crested and very fine trabeculae. Desmoplastic fibroma was
forms. recognized on the basis of the characteristic trabeculated
radiolucent defect. Desmoplastic fibromas are radiologi-
cally lucent lesions with honeycomb/soap-bubble patterns
Hypothetical considerations associated with endosteal erosion (Resnick 2002; Roth-
schild and Martin 1993). They are typically isolated
Causality of tumors is a contentious subject, even in phenomena. They are recognized radiologically in hu-
humans. The implications of the restriction of this type of mans, but only minimally alter vertebral shape/contour
pathology to a very narrow subset of the dinosaur and thus are usually not recognizable on macroscopic
radiation deserve an explanation. One of the features of examination of intact bones. Thus, radiologic examination
hadrosaur biology that might be considered is their diet. is essential for their detection.
Stomach contents of Edmontosaurus, known from the Because the appearances of these tumors are unique,
famous “mummies,” include conifers. This diet may be alternative diagnostic possibilities (see Table 2) are

Table 2 Distinguishing charac- Consideration Differential finding Osteoblastoma Desmoplastic fibroma


teristics of osteoblastoma and
desmoplastic fibroma from oth- Osteoporosis Thin trabeculae Thick trabeculae Thick trabeculae
er bone pathologiesa Giant cell tumor Thin trabeculae Thick trabeculae Thick trabeculae
Aneurysmal bone cyst Thin trabeculae Thick trabeculae Thick trabeculae
Cystic angiomatosis Sclerotic margin Non-sclerotic margin Non-sclerotic margin
Hemangioendothelioma Thin trabeculae Thick trabeculae Thick trabeculae
Ill-defined margin Sharply defined margin Sharply defined margin
Hemangiopericytoma Thin trabeculae Thick trabeculae Thick trabeculae
Paget’s disease Coarse trabecular Thickened individual Thickened individual
pattern trabeculae trabeculae
Fronts of resorption No resorptive sites No resorptive sites
Woven bone Lamellar bone Lamellar bone
Metastatic disease Ill-defined margin Sharply defined margin Sharply defined margin
Thin trabeculae Thick trabeculae Thick trabeculae
Chondromyxoid fibroma Endosteal sclerosis Non-sclerotic margin Non-sclerotic margin
Coarse trabecular Thickened individual Thickened individual
pattern trabeculae trabeculae
a
Derived from Chew (1997), Resnick (2002), Rothschild et al. (1999), Rothschild and Martin (1993)
500

limited (Boye et al. 2001; Chew 1997; Mohan et al. 1981; Acknowledgements Appreciation is expressed to Allison A. Smith,
Schmorl and Junghanns 1971; Sherman and Wilner 1961; J.D. Stewart, Peter and Neal Larson, Burkhard Pohl, Richard
Cifelli, Kevin Seymour, Sankar Chatterjee, Nick Czaplewski, Ray
Yochum et al 1993). Differential diagnosis includes DiVasto, Mark Norrell, Pamela Owen, Juan Langston, Bill
osteoporosis, giant cell tumor, aneurysmal bone cyst, Simpson, Robert Purdy, Lorrie McWinnery, Ken Carpenter, Dave
“brown tumor” of hyperparathyroidism, cystic angioma- Berman, Mary Dawson, Richard Harrington, Elizabeth Hill, Jack
tosis, hemangioendothelioma, hemangiopericytoma, Hanke, Mary Ann Turner, Kyle Davies, Hans-Dieter Sues, Kyle S
McQuilkin, Kieran Shepherd, Margaret Feuerstack, Jack Horner,
metastatic disease, Paget’s disease, and pseudotumors Mary Flynn, Cliff Miles, Ken Stadtman, and Scott Sampson for
related to intra-osseous bleeding in hemophilia (Boye et assistance in accessing the collections they curate, and to Virginia
al. 2001; Chew 1997; Mohan et al. 1981; Resnick 2002; Naples, Margery Coombs and an anonymous reviewer for cogent
Rothschild and Martin 1993; Schmorl and Junghanns manuscript review.
1971; Sherman and Wilner 1961; Yochum et al 1993).
Osteoporosis is characterized by a thinning, rather than
a thickening, of the trabeculae. Giant cell tumors, References
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