Inheritance of tibial hemimelia in Galloway cattle1

By H. W. LEIPOLD, G. SAPERSTEIN, R. SWANSON, M. M. GUFFY and R. SCHALLES

Ms. received 10. 4. 1977

Tibial hemimelia, a congenital syndrome in Galloway calves, may include these defects : nonfusion of the Mullarian ducts in female calves, cryptorchidism in male calves, and in both sexes cranioschisis, meningocele, internal hydrocephalus, bilateral agenesis or shortening of the tibia, bilateral agenesis of the patella, and an open pelvic symphy- sis. Most commonly Galloway calves affected with tibial hemimelia are stillborn or die shortly after birth. The syndrome has been described in one calf of unspecified breed in Scotland (YOUNG 1951) and in Galloway calves in the United States (OJO et al. 1974). Tibial agenesis also occurs in man (CLARK 1975) dog (BAKER and LEWIS 1974), and goat (GIDDINGS 1977). In this paper we describe pathologic changes of tibial hemimelia and report results of a breeding trial.

Materials and methods

For the breeding trial, part of a long-term study of the nature, frequency, cause and effect of congenital defects of cattle (LEIPOLD et al. 1972), in 1973 we purchased from a rancher in Southeast Kansas eight open Galloway COWS (I,,, I,,, I,,, I,,, I,,, I,,, I,,, and I,,, fig. 1) that previously had given birth to affected calves and one Galloway bull (bull E, Fig. 1) known to have sired affected calves. The animals were trans- ported to Kansas State University and were placed on pasture and allowed to breed naturally. In addition, bull E was bred to a Chianina cow. All abnormal calves born during the breeding trial were radiographed. All abnormal calves and three dams (cows I,,, I,,, and I,, in Fig. 1) were necropsied and organs examined grossly and histologically. Ratios of normal to abnormal calves were tested.

Results

During the breeding trial, 16 Galloway calves were born, ten calves were clinically normal and 6 calves were affected with tibial hemimelia. The Chianina cow bred to the Galloway bull (not included in Fig. 1) produced a clinically normal calf. All affected calves except one were stillborn, that one which lived only several days (Figs 2, 3 and 4). Of the affected calves four were females and one was a male, and the sex of one was not determined due to severe postmortem autolysis. Of the normal calves, six were females and four males.

Cont. Nos. 443-j, 222-j, and 528-j, respectively, Department of Pathology, Department of Surgery and Medicine, Department of Animal Science, Kansas Agricultural Experiment Station, Manhattan, Kansas, USA, 66506.

%. Tierzuchrg. Zuchtgsbiol. 94 (1977/78) 291-295 (0 1978 Verlag Paul Parcy, Hamburg und Berlin ISSN 004C3581/ASThbCodcn: ZTZBAS

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294 H. W . Le$old, G. .Taperstein, R . Swanson, M . M. Guffy and R . Schalles

Gross, radiographic, and histologic lesions in affected calves (Table) were con- sistent with our previous report (OJO et al. 1974). Cow I, and cow I,, showed no lesions. Internal hydrocephalus caused by a prolapsed vermis, was present in cow I,.

Discussion

Hemimelia is defined as agenesis of any part of the limb (as seen in adactyly, meromelia, or phocomelia) as opposed to amelia or absence of an entire limb. Agenesis of the tibial side of the lower limb has been reported in man as an autosomal dominant trait (CLARK 1975). Studies reported here and previously (OJO et al. 1974) revealed that expressivity on the tibial and femoral structures varies. In the slightest degree tibias were shorter than normal, and there was agenesis of the patella, and the distal joint surface of the femur carried only a single trochlea without subdivision into medial and lateral. Severely affected calves had bilateral agenesis of the tibia, and their femurs had one distal trochlea and the patella was absent. In addition, the skeleton of each calf had defects in the pelvic girdle and the cranium. The symphysis oft he pelvis remained open in all calves, including those having a short tibia. With one documented exception, all calves had cranioschisis ranging from an opening of .25 cm to 1.0 cm in diameter.

Other pleiotropic effects of the genes causing tibial hemimelia in Galloway calves included meningoceles (Table). The brains had moderate to marked internal hydroce- phalus. In addition, their reproductive systems and abdominal muscles had various changes. All calves with tibial hemimelia have ventral abdominal hernia. Defects of the reproductive system included cryptordichism in males and persistence of the Mullerian ducts in females.

The data suggested tibial hemimelia in Galloway calves is caused by recessive inheritance involving one locus. The expected phenotypic ratio would be: 4 affected and 12 normal calves. We observed 6 affected and 10 normal calves, that gave a chi- square value of 1.3 and a probability of 0.28 of having this amount or more deviation from the expected ratio. This probability supports the hypothesis of recessive inhe- ritance. Based on our breeding trial, we concluded that tibial hemimelia is a hereditary disease and that the mode of inheritance is simple autosomal recessive.

Three calves from one cow (1%) were affected. That cow had hydrocephalus typical of tibial hemimelia, however other signs were not present. Two other cows that had given birth to tibial hemimelia calves were normal upon necropsy. The remaining 5 cows and bull were not necropsied.

Other types of inheritance considered included dominance, incomplete dominance, sex-linked recessive and polygenic influence. If the defect had been caused by a domi- nant gene, either the dams or the sire would have been affected. They were clinically normal and at least two of the dams were normal upon necropsy. If the bull had been affected and was homozygous dominant, all of his offspring would have been affected. They were not. If he were heterozygous, one would expect half of his offspring to be affected. They were not. A 3 : 1 ratio fits the data better than a 1 : 1 ratio does.

Incomplete dominant inheritance would require the bull and cows to be heterozy- gous and to show some signs toward producing affected calves. At least 2 cows had no abnormalities. Sex-linked recessive inheritance was not likely. If the bull had the recessive gene, he would have been affected, if he did not have the gene all of the female offspring would have been normal.

Polygenic inheritance is always difficult to rule out. However, it is difficult to believe that all of the experimental cows could have had the correct genetic combina- tion to match those of the bull and to produce so many affected offspring.

Inheritance of tibial hemimelia in Gallaway cattle 295

In conclusion, our breeding trial indicated that tibial hemimelia in Galloway cattle is caused by homozygosity of a single autosomal recessive gene with variable expressivity upon the tibial structure (usually bilateral agenesis) and pleiotropic effects upon central nervous, reproductive, skeletal and muscular systems.

Summary

In a breeding trial conducted with selected Galloway cattle, tibial hemimelia in calves was produced. In describing thc calves it was concluded that tibial hemimelia in Galloway calves is a hereditary disease, most likely due to a simple autosomal gene with variable expressivity and pleiotropic effect on various body systems.

Resumen

1.a herencia de hemimelia tibial en la raza Galhwag

En un experiment0 fueron apareados animales seleccionados de la raza Galloway para producir terneros con hemimelia tibial. La descripcirin de 10s terneros indica que la hemimelia tibial en la raza Galloway es una enfermedad hereditaria, probablemente debida a un gen simple autosomal con expresividad variable y efectos pleiotrbpicos sobre varios sistemas del cuerpo.

Zusammenfassung

Vererbung tibialer Hemimelie bei Galloway Kindern

Tibiale Hemimelie konnte in einem Paarungsversuch mit Elterntieren produziert werden, die schon fehlerhafte Nachkommen gezeugt hatten. Tibiale Hemimelie bei Galloway-Rindern zeigt sich als eine Erbkrankheit, die wahrscheinlich einfach autosomal bedingt ist, aber variable Expressivitat und pleiotrope Wirkung auf verschiedene Kiirpersysteme zeigt.

References

BAKER, J.R.; LEWIS, D.G., 1974: Congenital absence of the tibia in a dog. Vet. Rec. 96,64. CLARK, M.W., 1975: Autosomal dominant inheritance of tibial meromelia. Report of a Kindred.

GIDDINGS, R.F., 1977: Tibial agenesis in a Toggenburg kid. J.A.V.M.A. 169, 1306. LEIPOLD, H.W.; DENNIS, S.M.; HUSTON, K., 1972: Congenital defects in cattle: Nature, cause and

OJO, S . A . ; GUFFY, M.M.; SAPERSTEIN, G.; LEIPOLD, H.W., 1974: Tibial hemimelia in Galloway

YOUNG, G.B., 1951 : A case of tibial hemimelia in cattle. Brit. Vet. J. 107, 23.

Authors address:

J. Bone Jt . Surg. 57-A, 262.

effect. Adv. Vet. Sci. Comp. Med. 16, 103.

calves. J. A. V.M.A. 165, 548.

Department of Pathology, Kansas State University, Manhattan, Kansas 66506, USA