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Chondrodysplastic Calves in Northeast Victoria
Chondrodysplastic Calves in Northeast Victoria
Abstract. Outbreaks of chondrodysplasia in calves occur sporadically every 10–15 years, particularly
following prolonged drought conditions, throughout Northeastern Victoria and the Southern Table-
lands of New South Wales, Australia. An outbreak spanning 2 calving seasons (2003–2004) involving
numerous losses through stillbirth, perinatal loss, and poor growth was investigated. Investigations of 4
representative cases are presented here with a definition of the gross and histopathologic defects and an
overview of epidemiologic data gathered from affected farms. Calves showed variable disproportionate
dwarfism without arthrogryposis. Long bones were shortened and showed axial rotation. Articular
surfaces were distorted with misshapen weight-bearing surfaces associated with variable thickness of
articular cartilage. Physes were distorted and variable in thickness with occasional foci of complete
closure. The major histologic abnormality in the physes was disorderly development of the zones of
cartilage hypertrophy, with reduced number and irregular arrangement of hypertrophic chondrocytes;
similar less severe changes were present in the zones of cartilage proliferation. Histochemical staining of
the cartilage matrix was variable in intensity, and there was evidence of abnormal resorption of cartilage
matrix at the level of the primary spongiosa. Osteoid formation and subsequent bone remodelling
seemed unaffected, and diaphyseal cortical bone appeared normal at the gross and light microscopic
level. No infectious agents were identified, and other known causes for chondrodysplasia in calves were
excluded. The most likely cause for the syndrome was considered to be congenital manganese deficiency.
Further surveys of tissue and blood manganese levels from cows and calves with and without clinical
signs from the region are planned.
Sporadic congenital deformities are expected in Congenital disease may result from genetic
the bovine population. Outbreaks of higher in- abnormality, infectious disease, or other in utero
cidence of congenital disease such as that described insults. ‘‘Chondrodysplasia’’ is a general term for
here may be associated with considerable losses of abnormalities of cartilage, usually caused by de-
animals and consequent financial loss. Across fective nutrition or metabolism of cartilage, which
Northeastern Victoria and the Southern Tablelands results in disproportionate dwarfism.19
of New South Wales (NSW), Australia, outbreaks Genetic chondrodysplastic syndromes are re-
of chondrodysplastic disease have been reported, ported in Holstein, Dexter, and several other
particularly in years following prolonged drought breeds of cattle. Beef breeds selected for short
conditions. Outbreaks occurring in 2 consecutive stocky phenotype have an increased prevalence of
spring calving seasons (July to November, 2003 brachycephalic calves, with longitudinal compres-
and 2004) and involving numerous losses through sion of the vertebrae and shortening of the distal
stillbirth, perinatal loss, and poor growth were long bones, believed to be hypochondroplasia
investigated to exclude potential infectious disease rather than a dysfunction of endochondral ossifi-
and to define the gross and histopathologic cation.19
defects. The cause of the syndrome is still un- There are many examples of toxic and nutrition-
resolved, although congenital manganese deficien- al causes of musculoskeletal deformity. Hypervita-
cy is suspected; despite marked improvement in the minosis A causes vertebral abnormalities and may
climatic conditions in this area, a lesser number of be compounded by protein-energy malnutrition.5
farms saw deformities among calves in a third ‘‘Crooked calves’’ are caused by ingestion of
consecutive calving season (2005). Investigations certain Lupinus sp. containing toxic concentrations
are ongoing. of the quinolizidine alkaloid, anagyrine, by the
342
Vet Pathol 44:3, 2007 Chondrodysplastic Calves in Northeast Victoria 343
dam, particularly between 40 and 70 days of abnormally short, stunted, or deformed calves with
gestation.23 This leads to arthrogryposis, spinal a spectrum of axial and appendicular skeletal
deformities, and disordered long bone growth, defects predominantly of reduced long bone/di-
possibly due to reduced intrauterine motility either aphysis length, angular rotations, irregular growth
through tonic contraction of the uterus or sup- plates, and articular cartilages, but without signif-
pressed motility and apparent sedation of the icant abnormality of cortical bone, born to dams
fetus,3 leading to a functional arthrogryposis without clinical signs in the area of Northeast
without identifiable histologic or histochemical Victoria and Southwest New South Wales.’’
lesions in the bone or muscle.1 Many other plant- Portions of vertebrae and long bones from calf
associated toxins are implicated in skeletal disease, No. 1, a stillborn calf from a farm in Northern
for example teratogenic piperidine alkaloids in Victoria, were received fixed in 10% neutral
Astragalus sp., Oxytropis sp., and Nicotiana glauca, buffered formalin (NBF) and examined grossly
which may act in a similar manner.3 Fungal toxins and histopathologically. Calf No. 2, one live 21-
have been presumptively associated with outbreaks day-old calf from a second farm, and calves Nos. 3
of congenital spinal stenosis and disproportionate and 4, entire stillborn calves from a third farm,
dwarfism, leading to myelomalacia and posterior underwent full postmortem and histologic exami-
paralysis in 3 outbreaks in Western Canada, where nation using standard methods. Carcasses of calves
heavy growth of Penicillium sp. and Fusarium sp. in Nos. 2–4 were weighed, and skeletal components of
wet straw bales was also causally associated with calves Nos. 3 and 4 were recorded using standard
pruritus and mortality in dams.20 ‘‘Acorn calves,’’ measuring tapes. Radiographic analysis of intact
described in western regions of North America and demuscled limb bones and sections through verte-
also recorded in New Zealand and South Africa, brae were prepared using a band saw, after fixation
were associated in the original reports with in- but before decalcification, on calves Nos. 3 and 4
gestion of acorns.2,19 Affected calves showed joint (not presented).
laxity, varus, and valgus deformities, and dispro- Five-millimeter sections were taken from a wide
portionate dwarfism. More recent work has sug- range of axial and appendicular skeletal sites and
gested that some of these cases may be consistent fixed in 10% NBF for 24–48 hours before de-
with a deficiency in dietary intake of manganese, as calcification, using a standard aqueous solution of
supported by small feeding trials in cattle.6,7,10,22 18% formic acid and 3.5% sodium formate for
Infectious causes of skeletal deformities seen in approximately 1 week at room temperature with
cattle in Australia include bovine viral diarrhea continuous slow agitation. Following standard
virus (BVDV), Akabane and Aino viruses. These paraffin embedding, 4-mm sections were cut and
tend to cause arthrogrypotic deformity of the stained with hematoxylin and eosin (HE). Histo-
skeleton rather than chondrodysplasia. chemical stains used to evaluate cartilage and bone
Consideration and, to a large part, elimination of included Giemsa and Acid Giemsa, periodic acid–
these differential diagnoses combined with evalua- Schiff (PAS), Alcian blue, Alcian blue–PAS,
tion of the anatomic pathology of several cases led toluidine blue, safranin O/fast green,15 and Ver-
investigators to propose that deficiency of manga- hoeff elastic stain.
nese could be responsible for the abnormalities For comparison of bone measurements and
in this outbreak. Manganese deficiency was sus- histopathology, 20 femora of grossly normal young
pected, although not conclusively proven, in several calves randomly collected by staff at an abattoir in
previous field outbreaks of skeletal disease in an unaffected region were weighed and measured,
calves.24,28 and histologic sections were prepared from the
This article presents the gross and histopatho- distal physis of each. Age and sex matching was not
logic features of 2 outbreaks of congenital disease possible in this investigation.
in calves, defines the disease, and discusses the Fresh frozen liver was collected from calves
potential relationship with manganese deficiency. Nos. 3 and 4. Glutathione peroxidase was analyzed
using an enzymatic method according to the
Methods
Standing Committee on Agriculture, Common-
Veterinary field staff and epidemiologists per- wealth Scientific and Industrial Research Organ,
formed clinical investigations with visits to numer- Australia, 1993. Vitamin B12 was analyzed spec-
ous affected farms and epidemiologic data collec- trophotometrically with competitive binding assay,
tion through analysis of questionnaires completed and copper was analyzed by atomic absorption
by farmers. The case definition formulated among spectrophotometry. Manganese concentration was
the investigative group was as follows: ‘‘Birth of determined following wet combustion in perchlo-
344 McLaren, Cave, Parker, and Slocombe Vet Pathol 44:3, 2007
ric/nitric acid solution and dilution in dilute of calves; given economic conditions in this region
hydrochloric acid to correct volume by flame that had suffered severe drought for several years,
atomic absorption spectrophotometry at 279.5 nm unreported losses were expected to approximate
on an AAnalayst 300 Spectrometer (PerkinElmer, 1,000 calves.
Waltham, MA). The reference ranges available for Dams of all age groups produced deformed
concentration of each of these elements are based calves. Affected calves appeared to be clustered in
on adult cattle, and no reference range for neonates management cohort groups rather than showing
was available at the start of the study. a pattern of spread expected with an infectious
Agar gel immunodiffusion was performed on agent. The groups of dams giving birth to affected
serum samples from calves Nos. 2–4 and several calves had predominantly been at pasture on hilly
dams and live calves from affected farms to detect granitic country that had been extremely dry over
BVDV and Akabane virus antigen. Virus neutral- the majority of each gestation period, although not
ization was performed to detect Aino virus antigen. all dams were in poor body condition. No toxic
The National Arbovirus Monitoring Program of plants were found on repeated examination of the
Animal Health Australia was consulted to assess grazing areas or reported during careful question-
presence of insect vectors and serologic evidence of ing of farmers. Some farms had been blanketed in
arboviruses in the region during the periods of heavy bushfire smoke during the first gestation
gestation (www.namp.com.au/reports/report_0203. period (2003), but there did not appear to be an
pdf, 2005). association between density of smoke and the
affected cohort groups.
Results
Common supplemental food, medication, or
Many farms across Northeastern Victoria expe- management procedures, and genetic links were
rienced births of deformed calves during the spring not identified during clinical investigation and
(July to November) of 2003 and 2004, common epidemiologic study. The calves affected were
calving periods for this region. Although some a range of beef breeds and crosses, including
farms reported births of marginally increased Murray Grey, Hereford, and Angus. Numerous
numbers of mildly chondrodysplastic calves in sires were involved, and cows giving birth to
preceding years, exceeding the expected number deformed calves had previously produced normal
of sporadic cases, the outbreaks in 2003–2004 were calves and, in many cases, went on to produce
widespread with significant portions (#90%) of normal calves in the following season. One mildly
cohort groups affected. The spectrum of severity affected heifer calf was observed to produce
ranged from stillbirths and perinatal deaths (due to a normal calf at her first calving.
inability to stand and respiratory compromise) to
calves deformed but able to suckle and follow the Gross pathology
dam. Less-affected calves were vigorous and External examination of the calves revealed
seemed to show some clinical reduction of defor- similar deformities in all calves presented intact.
mities over time. Total reported losses due to high All had low body weight (Table 1) and short
morbidity and mortality numbered into hundreds stature, with moderate-to-marked limb-trunk dis-
Table 1. Selected individual and average measurements of skeletal elements of calves Nos. 2–4.
Femoral Length
No. of Calves Mean Range
20 20.6 18.7–23.0
Measurement Range
Body weight (kg)* 31–33 41–43 53–63
Mean (SD)
Head length (cm)* 25.9 (0.89) 27.4 (0.85) 29.7 (1.46)
Poll–anus length (cm)* 90.3 (2.16) 94.3 (2.81) 107.1 (3.5)
Mean (range)
Metacarpal total length/ 6.25 (4.7–7.5)
diaphyseal diameter{
* 5 from Mee 199518
{ 5 from Tyler et al. 196125
abundant osteoclasts. Trabeculae within the pri- Sections of many long bones examined from all
mary spongiosa were short and irregular; a low cases showed variable osteopenia, with a reduced
proportion showed evidence of fracture close to the quantity of trabecular bone in the epiphysis and
physis, with osteoclasts present at the blunt distal medulla. Cortical lamellar bone was normal in
ends of trabeculae (Fig. 7). histologic appearance as was the perichondrial
The abnormalities of the cartilage matrix were collar, a lamellar plate of bone surrounding the
most clearly demonstrated by variable granular physis.
Alcian blue staining, compared with that of Sections of vertebrae examined from each animal
controls (Figs. 10, 11). showed irregular outlines of the cranial and caudal
The epiphyseal surface of the physis of the long physes due to variation in depth of both cranial
bones examined in calf No. 1 showed development and caudal aspects of the zones of hypertrophy and
of a band of mature bone horizontal and adjacent mineralization (Fig. 13).
to the physis (terminal plate), indicating closure of Sections of mandible demonstrated decreased
the growth plate (Fig. 12). The fused epiphyseal medullary trabecular bone, but lamellar cortical
and articular cartilages were apparently less affect- bone was within normal limits. The bones lining
ed. Horizontal metaphyseal trabeculae of bone the nasal cavity and turbinates were composed of
(growth-arrest lines suggesting periods of reduced fine irregular spicules of bone showing high
dam nutritional status) were found running parallel cellularity, numerous irregular growth-arrest lines,
to and at a short distance from the physes of some and irregular scalloped surfaces lined with reduced
bones in all cases (Fig. 5). osteoblast populations.
In calf No. 1, the atlas showed a pathologic in
utero fracture of a focus of ectopic cartilage,
disorderly proliferation of new bone, and cartilage
Table 4. Liver manganese, copper, cobalt, and selenium analysis from calves Nos. 3 and 4.
No. Manganese* Copper{ Cobalt (as vitamin B12){ Selenium (as glutathione peroxidase){
3 22 1.48 330 8.8
4 24 1.37 305 6.9
Reference 46–109 0.08–2.09 200–1,500 3.0–25.0
* mmol/kg wet weight.
{ mmol/kg wet weight.
{ U/g wet weight.
Vet Pathol 44:3, 2007 Chondrodysplastic Calves in Northeast Victoria 351
The literature on manganese metabolism and dietary manganese retained after intestinal absorp-
deficiency has been thoroughly reviewed.9,14,26,27 tion according to the concentration of the element
Deficiency of manganese has been associated in the food and in response to deficiency.12
experimentally and clinically with reduced repro- Manganese concentration in tissues has been
ductive performance7,22 and skeletal abnormali- shown to change rapidly after birth and onset of
ties7,10,22,24,28 in calves and laboratory animals and suckling in calves if there is high manganese
with ataxia associated with abnormal development concentration in the diet, as indicated by radioac-
of the otoliths in laboratory rodents but not cattle.13 tive isotope studies of manganese metabolism.4
Young calves are able to rapidly incorporate
Manganese bioavailability supplemental manganese from oral and intrave-
Concentrations of manganese in plants vary. nous administration into tissues, and the percent-
Grasses are richer than legumes, and straw and age retained varies according to the dietary and
corn silage have particularly low concentrations.9 whole body concentrations of the element at the
Uptake of bivalent manganese by plants is more time of administration of manganese.4 Once
efficient than that of the trivalent or tetravalent suckling commences, it is probable that the
forms present in highest concentrations in soil. Low manganese concentration in liver rises rapidly and
pH soils have a relatively high proportion of more markedly than in other tissues. This is
bivalent manganese. attributed to the liver’s role in manganese homeo-
Discussion with nutritionists in this investigation stasis through storage in mitochondria and excre-
led to a suggestion that rumen pH may have tion in bile. Higher manganese concentrations were
a similar effect on bioavailability of manganese. At found more often in suckled affected calves of a few
the time of writing, investigations were being days old (data not presented) than in neonatal
undertaken to review the current knowledge of unsuckled affected calves in this outbreak. Results
this interaction and determine whether manipula- suggested that within a few days, the liver
tion of rumen pH rather than direct supple- concentration of manganese in affected calves
mentation of manganese may aid in improving approached normal levels despite the low concen-
manganese absorption (T. Parker, personal com- tration of manganese found in milk.
munication). The percentage of dietary manganese absorbed
Overall bioavailability from ingested plant mat- in adults is relatively constant. Manganese is
ter is low, with ,1% intestinal absorption in cattle. largely removed from first-pass portal circulation
It appears from some studies that high dietary by the liver, and peripheral blood has a very low
levels of iron, copper, zinc, sulphur, and, to a lesser concentration of manganese bound to a-2-macro-
extent, calcium and phosphorus lead to further globulin.
reduction in manganese bioavailability.8,9 Although The apparent difference in manganese absorp-
the soil in the affected area is high in granite, which tion may reflect the incorporation of the majority
usually has a high level of manganese, the bio- of dietary manganese into ruminal micro-organ-
availability of the manganese may be reduced by isms in adults, as evidenced by more efficient
high dietary intake of other elements in soil such as cellulose digestion by micro-organisms in the
copper, cobalt, calcium, phosphorus, and iron, presence of supplemental manganese.17 The reason
which show significant interference with manga- adult cows are unable to enhance retention of
nese.26 Under severe drought conditions, cows may manganese if deficient is unclear.
ingest a high volume of soil and dust, leading to Feeding of silage alone through winter in
altered dietary mineral balance. northern latitudes has been identified as a risk
Manganese has been shown in rats and sheep to factor for a condition known as congenital
be preferentially sequestered by the placenta in joint laxity and dwarfism, which has some similar-
conditions of manganese deficiency of the dam, but ities to experimental manganese deficiency.21 It is
this sequestration is insufficient to return the fetal postulated by some authors that this may relate in
manganese concentration to normal.11 Unlike part to manganese deficiency indirectly through
neonates, fetuses are not able to preferentially reduced bioavailability of manganese present in
concentrate manganese in the liver.14 It is believed silage.10
that manganese concentrations in the liver of In this outbreak, drought conditions may have
neonatal presuckled calves represent the manga- led to rumen content with a high percentage of dry
nese status of the dam.26 matter and thus a relatively high pH. Under these
Retention of absorbed manganese varies with conditions, it is postulated that manganese is
age; calves may apparently alter the percentage of present within the rumen mostly as poorly bio-
Vet Pathol 44:3, 2007 Chondrodysplastic Calves in Northeast Victoria 353
available forms and thus absorption may be acknowledged for his investigations into the effect of
reduced. One potential avenue of investigation at rumen pH on bioavailability of manganese, and his
present is analysis of the effects of rumen pH on assistance in planning therapeutic strategies. Staff at
manganese absorption; alterations of rumen pH Primary Industries Research Victoria for further path-
may be more readily achieved through the use of ologic investigations, including mineral analysis and
virology studies; Gribbles Veterinary Pathology for
supplemental grain feeding or dietary cation- serological and mineral analysis; and Regional Labora-
anion–deficit rations without the need to supple- tory Services Benalla for mineral analysis are gratefully
ment manganese directly. acknowledged.
Conclusion References
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4 Carter JC Jr, Miller WJ, Neathery MW, Gentry RP,
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Stake PE, Blackmon DM: Manganese metabolism
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Request reprints from Dr. P. J. McLaren, Gribbles Veterinary Pathology, 1868 Dandenong Road, Clayton, Victoria
3168 (Australia). E-mail: philippa.mclaren@gribbles.com.au.