Embed Size (px)
Transcript of Vertebral Hiperostrosis
Vertebral Hyperostosis in Anteaters (Tamandua tetradactyla and Tamandua mexicana):Probable Hypervitaminosis A and/or DAuthor(s): Graham J. Crawshaw and Sergio E. OyarzunSource: Journal of Zoo and Wildlife Medicine, Vol. 27, No. 2 (Jun., 1996), pp. 158-169Published by: American Association of Zoo VeterinariansStable URL: http://www.jstor.org/stable/20095561Accessed: 25/01/2010 08:53
Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available athttp://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unlessyou have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and youmay use content in the JSTOR archive only for your personal, non-commercial use.
Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained athttp://www.jstor.org/action/showPublisher?publisherCode=aazv.
Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printedpage of such transmission.
JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range ofcontent in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new formsof scholarship. For more information about JSTOR, please contact [email protected].
American Association of Zoo Veterinarians is collaborating with JSTOR to digitize, preserve and extend accessto Journal of Zoo and Wildlife Medicine.
Journal of Zoo and Wildlife Medicine 27(2): 158-169, 1996
Copyright 1996 by American Association of Zoo Veterinarians
VERTEBRAL HYPEROSTOSIS IN ANTEATERS (TAMANDU? TETRADACTYLA AND TAMANDU? MEXICANA): PROBABLE HYPERVITAMINOSIS A AND/OR D
Graham J. Crawshaw, B.VeLMed., M.S., and Sergio E. Oyarzun, M.S.
Abstract: Hyperostosis of the thoracolumbar and coccygeal spine was seen in five captive ta
mand?as (Tamandu? tetradactyla and Tamandu? mexicana). Radiologie signs of the condition,
evident within the first year of captivity, progressed from a small subvertebral linear density to
massive vertebral hyperostosis and fusion. Clinical signs only developed in one tamandu? with
advanced hyperostosis. Soft tissue mineralization, observed during postmortem examination, is com
mon in tamand?as in other zoos. Plasma calcium levels were not significantly higher in captive tamand?as than in nine wild animals sampled. Plasma phosphorus, vitamin A, and vitamin D levels
were considered normal, but liver vitamin A levels were higher than levels in most normal domestic
animals. Vitamin levels in the diet were progressively reduced over 5 yr from a high of 57,000 IU/
kg vitamin A and 6,700 IU/kg vitamin D (dry matter basis) to 22,000 IU/kg and 1,900 IU/kg, respectively. Hyperostosis developed more slowly in animals fed diets containing the lower levels
of vitamins A and D, concentrations still considered excessive for this genus. The condition is most
likely caused by chronic hypervitaminoses A and/or D.
Key words: Anteater, Tamandu?, hyperostosis, spondylosis, hypervitaminosis.
Tamand?as (Tamandu? tetradactyla and
T. mexicana), are medium-sized arboreal
anteaters living in Central and South Amer
ica from Mexico to Paraguay.23 They have
been maintained in low numbers in captiv
ity for many years, but reproduction is un
common. Initial poor survivability in zoos
was likely related to their specialized di
The Metropolitan Toronto Zoo (MTZ)
acquired two female T. mexicana in 1981, and a male was received the following year. Each adjusted well to captivity and accept ed the diet offered. In 1987, the male de
veloped flaccid posterior paralysis and uri
nary retention. Radiography revealed exten
sive spondylosis and exostoses of the tho
racic, lumbar, and coccygeal vertebrae.
Minimal clinical improvement was seen
over the next few days, and the animal was
euthanized (animal 1). Survey radiographs of the two females (animals 2 and 3) re
vealed similar lesions in the axial skeleton,
although they showed no motor or other
neurologie deficits. One of these animals
(no. 2) died in 1989.
In December 1986, two additional ta
mand?as (T. tetradactyla), one male and
one female, were acquired. Both these new
er animals, normal when first examined,
also developed hyperostosis of the axial
skeleton (animals 4 and 5). Similar lesions
have been seen in tamand?as in other zoo
logical institutions (P. Wolff, Minnesota
Zoological Gardens; J. Ott-Joslin, Wood
land Park Zoo; J. Flanagan, Houston Zoo,
pers. comm.) and in the giant anteater (Myr
In this report, we describe the clinical,
radiographie, and pathologic findings in
these animals and the possible causes of
MATERIALS AND METHODS
All five tamand?as maintained at MTZ
were wild caught and were acquired from
commercial suppliers. Until 1985, the ani
mals were housed in a mixed-species public
exhibit, after which they were kept singly or
in pairs in hospital pens for breeding and
study purposes. Plasma calcium and phos
phorus levels from nine wild T. tetradactyla,
From the Metropolitan Toronto Zoo, 361A Old Finch
Avenue, Scarborough, Ontario M IB 5K7, Canada.
CRAWSHAW AND O Y ARZUN?HYPEROSTOSIS IN ANTEATERS 159
captured at Hato Masaguaral, Guarico, Ven
ezuela, in 1993, were used for comparisons.
For radiography and blood sampling, the
tamand?as were anesthetized with ketamine
(Ketaset, Ayerst, St. Laurent, Quebec H4R
1J6, Canada), 11 mg/kg, and xylazine
(Rompun, Bayvet, Etobicoke, Ontario
M9W 1G6, Canada), 0.8 mg/kg i.m. Blood was collected from the ventral coccygeal vessels into lithium-heparinized tubes. Plas
ma calcium and phosphorus were measured
using an Ektachem analyzer (Kodak Cana
da, Scarborough, Ontario M6M 1V3, Can
ada). Plasma was frozen in liquid nitrogen
prior to vitamin analysis. Plasma vitamin A
was measured by high-performance liquid
chromatography (HPLC).1 Vitamin D me
tabolites in plasma were measured by a
competitive protein-binding assay with rat
vitamin D-binding protein (25-OHD)21 or
HPLC (l-25(OH)2D).6 Bone fluoride con
centration was measured by neutron acti
vation analysis in the University of Toronto
Slowpoke-2 nuclear reactor. Results are
given as mean ? standard deviation, and
values were compared using Student's ?-test
modified for unequal sample numbers.20
Initially, the tamand?as were fed a mix
ture similar to that previously recommend
ed,9 consisting of evaporated milk, com
mercial dog food, powdered protein supple ment, multivitamins, and a small number of
mealworms and crickets. In 1983, the milk
and the protein supplement were eliminat
ed, and a small amount of orange was in
cluded. The dog food was gradually re
placed by the zoo's own horsemeat-based
carnivore ration, and the level of vitamin
supplementation was gradually reduced.
Between 1984 and 1986, commercial mon
key chow (Purina High-Protein, Ralston
Purina Canada, Woodstock, Ontario N4S
7K5, Canada) was included in the diet. Be
tween 1987, when the problem was first
identified, and 1994, each tamandu? was
fed the zoo's carnivore mixture (approxi
Table 1. Dietary vitamin levels (dry matter basis) fed to captive tamand?as over a 10-yr period.
Vitamin A Vitamin D Date (IU/kg) (IU/kg)
Jul 1984 48,730 5,760
Feb 1985 58,000 6,760
Dec 1985 46,700 5,300
Feb 1986 58,000 6,270
May 1986 26,000 3,320
Jan 1987 26,300 3,190 Mar 1987-1993 22,700 1,930
mately 300 g), Vi hard-boiled egg, Vi orange, and an additional 13 IU vitamin E daily.
Dietary calcium and phosphorus levels were approximately 1% and 0.7% dry mat
ter (DM), respectively. Between 1981 and
1986, vitamin supplementation was pro
gressively reduced. Calculated daily vita
min A intake, based on reported and ana
lyzed values of ingredients, decreased from a high of 7,600 IU per animal (58,000 IU/
kg DM) to 3,650 IU (26,000 IU/kg DM). Vitamin D intake was reduced from 1,050 IU (6,000 IU/kg DM) to 440 IU (3,100 IU/ kg DM). After 1987, the diet contained ap
proximately 22,000 IU/kg DM of vitamin A and 1,900 IU/kg DM of vitamin D, rep
resenting a daily intake of 2,080 IU vitamin A and 180 IU vitamin D. Changes in di
etary vitamin A and D levels over a 10-yr
period are shown in Table 1.
Animals 1 and 3 showed severe hyper ostosis when first examined radiographical ly. There was massive hyperostosis ventral to the lumbar and thoracic vertebrae, up to
10 mm in depth, equivalent to the depth of
the vertebral body itself. Fusion of osteo
phytes had, in effect, consolidated the spine into one bone (Figs. 1, 2). Hyperostosis was
almost entirely limited to the ventral and
lateral aspects of the vertebral bodies, with
minimal ossification dorsally along the neu
ral canal, vertebral facets, or the spinous
processes. Disc space, although radiograph
160 JOURNAL OF ZOO AND WILDLIFE MEDICINE
Figure 1. Radiograph of a severe case of vertebral hyperostosis in a tamandu? (T. mexicana) (animal 3),
showing massive deposition of bone along the ventral surface of the lumbar spine and the resulting kyphosis.
ically obscured by overlying bone, ap
peared to be well maintained in most lo
cations. Individual thoracic vertebrae ap
peared triangular because of r?sorption of
the cranial and caudal margins.
Hyperostosis also occurred in the cranial
portion of the tail; the individual vertebrae
became united (Fig. 3). Changes were less
marked in the distal half of the tail. The
cervical spine appeared remarkably unaf
fected despite the severity of the changes in
the thoracolumbar and coccygeal regions
(Fig. 2). No extravertebral bony changes were seen, but in one of the animals (no.
1), mineralization of the tracheobronchial
tree was apparent.
Animal 2 had a less advanced radiograph ie stage of the disease when first examined.
Osteophytes at the cranial and caudal mar
gins of the thoracolumbar vertebral bodies
had developed into pointed excrescences be
neath the vertebral discs. Bridging of these
exostoses gave the ventral surface of the
spine an undulating appearance (Fig. 4). Over the next 2 yr, the hyperostosis became
temporarily denser and more aggressive ra
diographically, with loss of integrity of the
ventral portion of the bodies of the verte
brae. Four years later, fusion was complete
but the lesion had a more benign appear ance, similar to that in animals 1 and 3.
Following the identification of vertebral le
sions in the three original tamand?as, the two
new animals (nos. 4 and 5) were monitored
radiographically for skeletal changes. Initial
ly, these animals showed no abnormalities, but radiographs taken 18 mo later demon
strated early vertebral lesions. The earliest ev
idence was a small linear radiodensity, 1 mm
in height, in the soft tissue approximately 2
mm ventral to the lumbosacral joint. Over the
next 4 yr, progressive development of radio
graphic lesions was similar in both animals.
Fifteen months later, the initial density had
enlarged to 3 mm in height and abutted the
adjacent vertebrae. Similar discrete linear or
CRAWSHAW AND OYARZUN?HYPEROSTOSIS IN ANTEATERS 161
Figure 2. Dorsoventral view of the cranial half of the spine of a tamandu? (T. mexicana) (animal 3), showing extensive hyperostosis of the thoracic vertebrae but an absence of bony changes in the neck.
162 JOURNAL OF ZOO AND WILDLIFE MEDICINE
Figure 3. Radiograph of the cranial half of the tail of a tamandu? (T. mexicana) (animal 1), showing extensive
ventral hyperostosis and adjacent soft tissue mineralization.
triangular radiodensities were visible ventral to most of the thoracic and lumbar interver
tebral joints (Fig. 5). Roughening, with small
osteophytes, was evident at the ventral mar
gins of several vertebral bodies. Linear soft
tissue calcification also developed lateral to
the coccygeal vertebrae. A progressive in crease in the size and density of the subver tebral foci, moderate lysis and remodelling of
the vertebral margins, and growth of the os
teophytes on the vertebral bodies were seen
over the next 2 yr. However, in these two
animals, no bridging of vertebral joints oc
curred as long as 5 yr after the initial exam
Examination of radiographs and reports from other institutions have documented similar lesions in other tamand?as (J. Flan
agan, Houston Zoo; J. Ott-Joslin, Woodland
Park Zoo, pers. comm.).
Clinical findings Clinical signs were evident only in the
presence of severe vertebral hyperostosis.
The most severely affected animal (no. 1) showed rear limb paresis and urinary reten
tion, which progressed to complete flaccid
paralysis within 2 wk of the initial presen tation. Animal 2 showed no evidence of neu
rologic deficit, although death may have re
sulted from a fall due to reduced ability to
climb. The third severely affected animal
(no. 3) continues to move slowly and stiffly but is otherwise mobile and able to climb.
All three of these tamand?as had kyphosis, which is typical of the normal posture of the
species but could not be straightened under
anesthesia. No signs have been seen to date
in the other two animals, despite moderate
radiologie evidence of hyperostosis.
Plasma calcium level (x ? SD) in 31
samples taken from five captive animals over 5 yr, concurrent with the development of bony lesions, was 2.6 ? 0.4 mmol/L
(range, 1.7-3.6 mmol/L) (Table 2). Four
CRAWSHAW AND OYARZUN?HYPEROSTOSIS IN ANTEATERS 163
Figure 4. Lateral radiograph of the thoracic spine of an affected tamandu? (T. mexicana) (animal 2) at an
intermediate stage in the development of hyperostosis. Exostoses on the vertebral margins are enlarged and
fused, giving an undulating appearance to the ventral border of the spine.
samples taken from animals 3, 4, and 5 in
1989 were >:3.0 mmol/L, as were three
samples taken from animal 5 in 1990. Both
samples taken from animals within 1 mo of
arrival (animal 3 in 1981 and animal 4 in
1986) showed calcium levels <2 mmol/L.
Plasma phosphorus level in 28 samples from the same five animals over the same
5-yr period was 1.4 ? 0.6 mmol/L (range, 0.7-2.1 mmol/L). Calcium and phosphorus levels in nine wild tamand?as were 1.9 ?
0.4 and 1.6 ? 0.7 mmol/L, respectively (Ta ble 3), but these values did not differ sig
nificantly from the corresponding values in
the captive tamand?as (?-test). The 1,25-dihydroxyvitamin D level in 18
plasma samples from five captive taman
d?as was 49 ? 31 pmol/L. One animal (no.
2) showed higher levels (193 ? 29 pmol/L in three samples). The 25-hydroxyvitamin
D level in 18 samples from five animals was 55 ? 28 nmol/L.
Plasma vitamin A level in 14 samples from four captive tamand?as was 0.8 ?
0.18 |xmol/L. Serum vitamin A in two other
animals from the Woodland Park Zoo
showed even higher levels (2.2 and 3.3
|xmol/L). The mean liver vitamin A level in two samples taken from the one tamandu?
tested was 1,299 jxg/g. An affected female
tamandu? from Woodland Park Zoo had a
liver vitamin A level of 3,981 u,g/g. The
postmortem bone fluoride level in one ani
mal was 6.0 mM fluorine/M calcium.
Animal 1 was euthanized due to posterior
paralysis, consistent with a direct effect of
the vertebral changes impinging on the spi nal cord. Necropsy findings included atro
phy of the limb musculature and a greatly distended bladder. The vertebral column
from the thoracic inlet to the tail had very little flexibility. Most vertebrae had multi
164 JOURNAL OF ZOO AND WILDLIFE MEDICINE
Figure 5. An early stage in the development of vertebral hyperostosis in a tamandu? (T. tetradactyla) (animal
4), showing development of linear and triangular densities (arrows) ventral to the lumbar inter vertebral joints.
pie exostoses and were incorporated into a
solid bony mass (Fig. 6). Ankylosis was
primarily ventral to the vertebral bodies, al
though some fusion of exostoses had oc
curred more dorsally around the vertebral
facets. The most dramatic changes were
present in the thoracic vertebrae. Extensive
localized lysis of one vertebra had led to
complete degeneration of the vertebral body and collapse of the adjacent intervertebral
Histologically, the vertebral lesions con
sisted of irregular areas of cartilage, fibro
cartilage, dense collagenous fibrous tissue, and occasionally woven bone. In some sec
tions, adjacent to these exostoses there were
masses of eosinophilic necrotic debris.
Small foci of soft tissue calcification were
evident on the myocardium and on the sur
face of the spleen. Focal mineralization was
also present in the tunica media of the aorta
and some smaller vessels. Occasional renal
medullary tubules were mineralized.
In animal 2, death was a result of hem
orrhagic shock from a ruptured liver, which was likely a sequel to congestive heart fail ure. There was extensive exostosis and an
kylosis of the vertebral bodies from the tho
racic inlet to the tail, with fusion of the ver
tebral column between these points.
Histologically, there was hepatic conges tion and hemorrhage, and myocardial de
generation with focal mineralization. Mem
branoproliferative glomerulopathy was
present with scattered glomerular mineral
ization and occasional mineralized tubular
casts. Mineralization of the bronchiolar car
tilage was also noted. The normal ventral
borders of the vertebrae were obscured by
compact acellular swirling osteoid with nu
merous metabolic arrest lines and large amounts of hemopoietic marrow. Within
this matrix were small islands of degenerate
hypereosinophilic cartilage and osteoid.
The dorsal and lateral aspects of the verte
brae were minimally affected.
CRAWSHAW AND OYARZUN?HYPEROSTOSIS IN ANTEATERS 165
Table 2. Plasma calcium, phosphorus, 1,25-dihydroxy vitamin D, 25-hydroxyvitamin D, and vitamin A levels
in five captive tamand?as.
Ca P l,25(OH)2D3 25,(OH)2D3 Vit A Animal no. Date (mmol/L) (mmol/L) (pmol/L) (nmol/L) (|xmol/L)
1 Mar 87 3.4 1.3 8 58 2 Aug 88 2.1 1.6 172 38 Dec 88 1.9 1.4 204 37 1.2 Oct 89 2.4 4.1
3 Oct 81 2.1 2.2 43 36
Jan 82 2.1 2.0 79 136
Mar 87 2.2 1.8 16 23 Nov 89 3.0 1.1 0.9 Dec 89 3.2 1.4
Sep 90 2.3 60 46 0.6 Oct 90 2.3 1.4 39 65 1.1 Feb 92 2.4 1.7
4 Dec 86 1.8 2.1 50 4
Jan 87 2.5 1.4 12
Aug 88 2.3 1.0 26 32 1.0 Nov 89 3.5 1.3 0.7
Sep 90 2.4 53 66 0.8 Oct 90 2.2 1.6 100 66 0.7
Mar 92 2.4 1.6
5 Jan 87 2.2 1.2 86 80
Aug 88 2.4 1.1 18 49 0.6 Nov 89 3.6 0.8 0.7
May 90 3.0 0.9 102 61 0.7
May 90 3.0 0.8
Jun 90 2.6 0.7 0.8 Jul90 2.6 1.1 26 71
Aug 90 3.0 0.8
Sep 90 2.3 70 0.8 Oct 90 2.7 1.4 60 67 0.8
Nov 90 2.8 1.0
Mar 92 2.5 1.4
x 2.6 1.4 49 55 0.8
SD 0.4 0.6 31 28 0.18
n 31 28 18 18 14
The nature, history, and distribution of
the bony lesions in the tamand?as at MTZ
and the occurrence of cases in other insti
tutions point to a common etiology. The ra
diologie and pathologic findings strongly
suggest a nutritional cause related to calci um metabolism. Hyperostosis of the axial
skeleton is the predominant characteristic.
Soft tissue calcification in the necropsied animals was extensive and considered part of the syndrome.
Despite extensive vertebral hyperostosis,
kyphosis, and reduction in mobility, neu
rologic signs were limited. Rear limb pa resis was seen in only one animal in an ad
vanced stage of the disease, indicating that
spinal cord and segmental nerve function are not compromised until hyperostosis be comes extensive. Focal dorsoventral flatten
ing of the spinal cord was seen, but only one small bony spicule in the dorsolateral
part of the canal was evident. New bone
formation was predominantly ventral, as
seen in the prepared specimen (Fig. 6). The
location of the early radiographie lesion
166 JOURNAL OF ZOO AND WILDLIFE MEDICINE
Table 3. Plasma calcium and phosphorus levels in
nine wild tamand?as (T. tetradactyl?).
Ca P Animal no. (mmol/L) (mmol/L)
6 1.6 1.2
7 1.4 1.6
8 1.3 1.0
13 1.9 3.0
15 2.2 2.3
16 2.2 1.3
17 2.5 1.6
18 2.2 0.9
20 2.2 1.7
x 1.9 1.6
SD 0.4 0.7
suggests that calcification first develops in
the ventral longitudinal spinal ligament. The myocardial degeneration, glomerulo
pathy, and soft tissue mineralization prob
ably relate to the age of the animals and to
chronic hypercalcemia. The pathologic changes were suggestive
of hypervitaminosis A or D. Excessive vi
tamin A intake has been incriminated in cases of deforming spondylosis of the cer
vical vertebrae in domestic cats.19 There are,
however, some differences between the
changes seen in cats and those in the ta
mand?as. In feline hypervitaminosis A, ex
ostoses develop principally on the dorsal
and lateral aspects of the cervical vertebrae,
rarely ventrally, and proliferations will
readily impinge on the intervertebral foram
ina to affect the segmental nerves. The tho
racic vertebrae, ribs, and axial skeleton may also be affected. In contrast, the ventral as
pect of the thoracolumbar spine is the pri
mary site in the tamand?as. Periosteal cal
cification and skeletal hyperostosis are also seen in adult humans as a feature of vitamin
A toxicosis, although the spine is rarely in
volved.4-17 The histopathology was similar
to that in cats with hypervitaminosis A.
Plasma vitamin A levels in the taman
d?as were at the lower end of the ranges
Figure 6. Prepared specimen of the lumbar spine of an affected tamandu? (T. mexicana) (animal 2), showing ventral and lateral hyperostosis and fusion. Note that the apophyseal joints are unaffected.
CRAWSHAW AND OYARZUN?HYPEROSTOSIS IN ANTEATERS 167
considered normal in other species (rat =
1.5 |xmol/L; human = 0.7-1.0 |xmol/L; cat = 0.7-2.8 |xmol/L) and did not approach the levels usually considered toxic (>3.5
Ixmol/L).11-12'19 However, there may be little
correlation between plasma vitamin A lev
els and liver stores.12 The liver vitamin A
stores were higher than the normal levels
usually seen in other species, although they were still well below the values associated
with hypervitaminosis A in cats (8,500
40,000 |xg/g).81119 Standard mammalian liv
er vitamin A concentrations are 50-300 |xg/
g, but polar bear livers may contain as
much as 30,000 |xg/g.812 The upper safe limit for dietary admin
istration of vitamin A in other species is
about 10 times the normal daily require ment, i.e., 20,000 and 100,000 IU/kg diet.12
The initial dietary vitamin A levels were
potentially toxic for some domestic species. After 1987, the dietary level of approxi
mately 22,000 IU/kg is consistent with that
provided to many carnivorous species, al
though still several times the daily require ment for most mammalian species.8
In humans, hypercalcemia occurs in a
minority of cases of vitamin A intoxica
tion.3417 In feline hypervitaminosis A, hy
percalcemia does not appear to be present, and the levels of calcium and phosphorus in the diet have little influence on the de
velopment of exostoses in the cat.2-5 A few
of the individual plasma calcium values
from the affected tamand?as would be con
sidered hypercalcemia in other species, but
the overall mean is comparable with that of
other mammals, including the limited num
ber of reports for captive anteaters.7 22
reported values were obtained from captive animals fed similar diets. Samples taken
from nine wild T. tetradactyla in 1993 had
a mean plasma calcium value of only 1.95
mmol/L (Table 3), but this value was not
significantly different (i-test) from that of
the captive animals. The levels found in an
imals soon after arrival were lower than
those measured later. The levels found in
the long-term captive animals could repre
sent hypercalcemia in this species, which
would be supported by the presence and
distribution of the soft tissue mineraliza
tion. The tamandua's diet of invertebrates
suggests a low calcium intake.1415 Further
studies are in progress to evaluate normal
calcium levels in this species. Levels of vitamin D metabolites were
within the normal ranges for humans and do
mestic animals, except for animal 2, which
showed elevated levels of l,25(OH)2D and
normal serum calcium and is the only result
suggesting hypervitaminosis D. One sample taken from one animal (no. 4) shortly after
arrival was considered to be deficient in vi
tamin D, but interpretation of these blood val
ues is hampered by a lack of knowledge of
normal values for these animals. Normal lev
els of 25-hydroxyvitamin D in other mam
mals are between 25 and 80 nmol/L (10-30
ng/ml), increasing to 500-1000 nmol/L in
toxic states. Normal 1,25-dihydroxyvitamin D levels are between 25 and 100 pmol/L
Very little information exists on the max
imum safe dietary level for chronic expo sure to vitamin D in any species, although it is generally accepted that disorders of
metabolism and increases in serum vitamin
D metabolites will occur at intakes of 20
times the daily requirement, which in most
animal species is in the range of 200-1,200
IU/kg diet.12 Based on studies in other spe
cies, chronically ingested levels below
2,200 IU/kg DM should be safe, but there
is considerable species variability. The vi
tamin D levels initially fed to the taman
d?as (6,000 IU/kg) would have been poten
tially toxic for other species, and even the
reduced level fed since 1987 (2,000 IU/kg) is 2-10 times the requirement for other
mammals and is at the high end of the safe
Most of the effects of hypervitaminosis D are due to chronic hypercalcemia, result
ing in metastatic calcification, particularly in the major arteries, gastric vessels, and
renal tubules. Mineralization of the bron
chial cartilage, alveoli, and bronchial sub
168 JOURNAL OF ZOO AND WILDLIFE MEDICINE
mucosa may also be seen.13 Although cor
tical thickening and bone sclerosis also oc
cur in vitamin D toxicosis, typically with
the production of abundant basophilic ma
trix and obliteration of the medullary cav
ities of the long bones, proliferative bone
disease as seen in the tamand?as is not a
feature of vitamin D intoxication in other
species, including humans.1317 In the taman
d?as at MTZ, soft tissue mineralization was
present in both necropsy specimens at many of these typical locations. Postmortem re
cords from other institutions indicate that
soft tissue calcification occurred quite fre
quently, but vertebral hyperostosis was seen
(P. Wolff, J. Letcher, J. Flanagan, and J. Ott
Joslin, pers. comm.). Variations in vitamin
A and vitamin D supplementation between
institutions probably account for the differ
ences in presentation.
The condition in these anteaters is similar
to diffuse idiopathic skeletal hyperostosis (DISH) in humans. DISH is a discrete skel
etal disorder of middle-aged and older peo
ple manifested by a number of clinical and
radiographie criteria, including the presence of flowing calcification and ossification
along the anteroventral (in human termi
nology) aspect of at least four contiguous vertebral bodies, particularly in the thoracic
spine, in the absence of other evidence of
inflammatory disease or degenerative disc
disease.18 A similar condition has been re
ported in a dog.10 In many cases, extraspinal
calcification and exostoses are also seen.
The predominant, and likely initial, lesion
in DISH is calcification or ossification of
the anterior (ventral in animals) longitudi nal ligament of the spine, in some cases in
the absence of vertebral lesions, hence the
earlier terminology spondylitis deformans
ligamentosa. This is also the location of the
earliest visible lesion in the tamand?as. The causes of DISH are unknown, although ge netic factors may be involved.
Chronic fluorine intoxication or fluorosis
may also be characterized by vertebral os
teophytosis as part of a syndrome of mul
tifocal periosteal proliferation.16 Vertebral
hyperostosis in fluorosis develops at several
locations on the vertebrae, including the
spinous processes and the posterior (dorsal) intervertebral ligament, and is more likely to cause neurologic impairment. Periosteal
proliferation will also be seen in the appen dicular skeleton. The bone fluoride level in
the one tamandu? tested was within the nor
mal range for humans and domestic animals
(K. Pritzker, Univ. Toronto, pers. comm.).
The slow progression and limited radio
graphic changes in the newer animals over a 5-yr period contrasts strongly with the
massive hyperostosis and soft tissue calci
fication that occurred in the original ani
mals over a similar period, suggesting that
the reduced amount of vitamin supplemen tation since 1987 is safer than that offered
previously but still produces toxic levels.
The original animals were a different spe cies from the newer animals, but the differ ences between the two species are limited to minor anatomical variation and are not
considered significant factors.
A survey of diets fed to giant anteaters
(Myrmecophaga tridactyla) in zoos re
vealed a wide variation in calculated nutri
ent values (R. Patton, pers. comm.). Vita
min A levels were 1,900-60,000 IU/kg, vi
tamin D levels were 308-7,260 IU/kg, cal
cium was 0.7-2.0% DM, and phosphorus was 0.37-1.1% DM.
The bony and soft tissue lesions in the
tamand?as probably were due to excessive
intake of vitamin A, perhaps compounded
by a higher than necessary intake of vitamin
D. We recommend that levels of vitamin A
and vitamin D in anteater diets be restricted to less than 8,000 IU/kg DM and 800 IU/
kg, respectively, and the level of calcium
should be restricted to 1.0% or less. Studies are currently being undertaken on the nutri ent intake of these species in the wild.
Acknowledgments: We thank Drs. Sandie
Black and Virginia Honeyman for the pathologic examinations; Drs. Ken Pritzker and Reinhold
Vieth for fluorine and vitamin D analyses, re
spectively, and for their advice; Dr. Carlos
Bosque, Maribel Hernandez, and the staff of the
CRAWSHAW AND OYARZUN?HYPEROSTOSIS IN ANTEATERS 169
Fundaci?n Nacional de Parques Zool?gicos y
Aquarios in Venezuela for their cooperation in
the collection of the blood samples from wild
animals; and Mr. Tomas Blohm for providing
facilities at Hato Masaguaral. Drs. Janis Ott-Jos
lin, James Letcher, and Joe Flanagan provided
data from the Woodland Park, Lincoln Park, and
Houston zoos, respectively.
1. Brubacher, G., W. Muller-Mulot, and D. A. T.
Southgate. 1985. Methods for the Determination of
Vitamins in Food. Elsevier, New York, New York.
2. Clark, L., A. A. Seawright, and J. Hrdlicka.
1970. Exostoses in hypervitaminotic A cats with op timal calcium-phosphorus intakes. J. Small Anim.
Pract. 11: 553-561.
3. Fisher, G., and P. G. Skillern. 1974. Hypercal cemia due to hypervitaminosis A. J. Am. Med. Assoc.
4. Frame, B., C. E. Jackson, W. A. Reynolds, and
J. E. Umphrey. 1974. Hypercalcemia and skeletal ef
fects in chronic hypervitaminosis A. Ann. Intern. Med.
5. Goldman, A. L. 1992. Hypervitaminosis A in a
cat. J. Am. Vet. Med. Assoc. 200: 1970-1972.
6. Hollis, B. W? and T. Kilbo. 1988. The assay of
circulating l,25(OH)2D using non-end-capped C18 sil
ica: performance and validation. In: Norman, A. W.,
K. Schaefer, H.-G. Grigoleit, and D. Herrath (eds.).
Vitamin D. Molecular, Cellular and Clinical Endocri
nology. deGruyter, Berlin, Germany. Pp. 710-719.
7. ISIS. 1987. Normal values for hematology and
biochemistry for zoo species. International Species In
ventory System, Apple Valley, Minnesota.
8. McDowell, L. R. 1989. Vitamins in Animal Nu
trition. Academic Press, San Diego, California.
9. Meritt, D. A. 1976. The lesser anteater in cap
tivity. Int. Zoo Yearb. 16: 41-45.
10. Morgan, J. P., and M. Stavenborn. 1991. Dis
seminated idiopathic skeletal hyperostosis (DISH) in a
dog. Vet. Radiol. 32: 65-70.
11. National Research Council. 1986. Nutrient Re
quirements of Cats. National Academy of Sciences,
Washington, D.C. Pp. 21-22.
12. National Research Council Subcommittee on
Vitamin Tolerance. 1986. Vitamin Tolerance of Ani
mals. National Academy of Sciences, Washington, D.C. Pp. 3-9.
13. Palmer, N. 1993. Bones and joints. In: Jubb,
K. V. E, P. C. Kennedy, and N. Palmer (eds.). Pathol
ogy of Domestic Animals, 4th ed., vol. 1. Academic
Press, San Diego, California. Pp. 81-88.
14. Redford, K. H. 1984. Nutritional value of in
vertebrates. J. Zool. 203: 385-395.
15. Redford, K. H. 1985. Feeding and food pref erence in captive and wild giant anteaters. J. Zool. 205:
16. Resnick, D. 1988. Disorders due to medica
tions and other chemical agents. In: Resnick, D., and
G. Niwayama (eds.). Diagnosis of Bone and Joint Dis
orders. W. B. Saunders Co., Philadelphia, Pennsylva nia. Pp. 3080-3090.
17. Resnick, D. 1988. Hypervitaminosis and hy
povitaminosis. In: Resnick, D., and G. Niwayama
(eds.). Diagnosis of Bone and Joint Disorders. W. B.
Saunders Co., Philadelphia, Pennsylvania. Pp. 3091
18. Resnick, D., and G. Niwayama. 1988. Diffuse
idiopathic skeletal hyperostosis (DISH). In: Resnick,
D., and G. Niwayama (eds.). Diagnosis of Bone and
Joint Disorders. W. B. Saunders Co., Philadelphia,
Pennsylvania. Pp. 1563-1600.
19. Seawright, A. A., P. B. English, and R. J. W.
Gartner. 1967. Hypervitaminosis A and deforming cervical spondylosis of the cat. J. Comp. Pathol. 77:
20. Snedecor, G. W., and W. G. Cochran. 1992.
Statistical Methods. Iowa State Univ., Ames, Iowa. Pp. 96-97.
21. Vieth, R., M. J. Kessler, and K. P. Pritzker.
1990. Species differences in the binding kinetics of
25-hydroxyvitamin D3 to vitamin D binding protein. Can. J. Physiol. Pharmacol. 68: 1368-1371.
22. Wallach, J., and W. J. Boever. 1983. Diseases
of Exotic Animals. W. B. Saunders Co., Philadelphia,
Pennsylvania. Pp. 613-629.
23. Wetzel, R. M. 1975. The species of Tamandu?
Gray (Edentata, Myrmecophagidae). Proc. Biol. Soc.
Wash. 88: 95-112.
Received for publication 1 March 1994