Congenital lordosis in three John W. Coates, Ronald C. McFee

This report describes the pathological findings in two Prior to the birth of the three swayback foals, both of three clinical cases of congenital thoracic lordosis Haflinger had previously been bred to the same observed in Haflinger foals over a three-year period . The dam of 1 has delivered a total of five and comments on the possible influence of heredity foals from this same stallion. These include two nor- in manifestation of the defect. mal colts and a , plus lordotic foals 1 and 3. From The Haflinger is described as a medium-sized, sure- time of purchase, the dam of lordotic foal 2 has also footed, robust , used originally as a pulling or produced three additional and twin colts, all packhorse in mountainous terrain in Europe. The normal. By 1991, the stallion had sired approximately name is derived from the small community of Hafling twelve purebred foals on this farm, including lordotic in South Tyrol, Austria. The modern Haflinger breed foals 1 and 2. No prior cases of congenital lordosis has been described as one of the most inbred equine or any other musculoskeletal anomalies had been breeds in the world (1). Inbreeding is the mating of observed by the owners. At that time, the stallion had related individuals; the greater the extent of inbreeding also sired approximately ten crossbred foals that were within a population, the lower the frequency of hetero- phenotypically normal. zygotes (2). As in purebred stock of any domestic Following euthanasia, foals 2 and 3 were submitted species, inbreeding increases the likelihood of expres- for necropsy with the intention of more precisely defin- sion of defects transmitted either as autosomal ing the nature of the spinal abnormality. In order to recessives or via the familial influence of multiple gene examine the spine of each animal, the entire vertebral (polygenic) inheritance (2). column from the atlas to the sacrum was dissected From a clinical viewpoint, lordosis in domestic from the rest of the cadaver. A heavy-gauge wire was animals refers to a ventral curvature of the spine, and drawn through the vertebral canal to maintain the in is usually associated with the thoracic seg- relative position of each vertebra. The vertebrae, ment of the vertebral column. In horses, lordosis together with the surrounding muscles and ligaments, (swayback) may be congenital or acquired, with vary- were boiled in water until all soft tissues could be ing degrees of severity (3,4). In one report listing all readily removed from the underlying bone. known congenital defects observed in foals, lordosis In foal 2, anomalous development was observed is considered to be rare and of unknown etiology (5). only in the cranial and caudal articular facets of the In 1989, a purebred Haflinger (Foal 1) presented mid-thoracic vertebrae. The caudal articular facets of with severe lordosis of the midthoracic spine, which thoracic vertebra six (T6) were found to be hypoplastic had been present since birth. A necropsy was not done in comparison to those of T5. Both cranial and caudal on this foal as it was considered to be an isolated inci- articular facets of T7, T8, T9, and TIO were severely dent. In 1991, a second Haflinger foal (Foal 2) with hypoplastic (Figure IA, B). This was in contrast to the severe midthoracic lordosis was born at the same farm articular facets observed on normally developed though from a different . Despite the swayback, thoracic vertebrae, such as T4 (Figure IC). The the filly was bright and alert and had a normal gait hypoplastic cranial articular facets of T7-T10 consisted and motor response. In 1992, a third lordotic foal, also of a thin bony outline barely elevated above the a filly, was born from the same mare that had pro- vertebral arch. Malformation of the cranial articular duced foal 1. The three lordotic foals were all sired processes was generally slightly more pronounced than by the same stallion. that of the caudal processes. Articular facets of T 11 The occurrence of three lordotic foals suggested that and the remaining thoracic vertebrae were normal. No the condition could be heritable, which was a concern other malformations of the affected thoracic vertebrae to the owners of these purebred animals. For this were observed. reason, detailed studies of the anatomical malforma- Foal 3 was necropsied at two months of age. tions of foals 2 and 3 and pedigree links between the Pathological changes were very similar to those that three foals were undertaken. had been observed in foal 2 the previous year. There The affected farm has five purebred brood mares, was moderate hypoplasia of the cranial and caudal together with the stallion, and has raised foals for articular facets of T7, severe hypoplasia of the cranial abQut eight years. The stallion, and the two mares that and caudal articular facets of T8, T9, and TIO, and produced the lordotic foals were clinically normal, as moderate hypoplasia of Tl 1. were the other mares. Although lordosis is recognized clinically by veteri- nary practitioners as a ventral curvature of the spine, Can Vet J 1993; 34: 496-498 the actual mechanics of the condition are related to the extent of motility and extension (dorsiflexion) per- Animal Health Centre, Ministry of Agriculture, Fisheries and mitted by hypoplastic vertebral articular processes (4). Food, 1874 Gladwin Road, P.O. Box 100, Abbotsford, Because spinal overextension rather than overflexion British Columbia V2S 4N8 (Coates); Greenbelt Veterinary occurs with hypoplasia of the vertebral articulations, Services Ltd, 8810 Young Road South, Chilliwack, British the force developed by the dorsal back muscles such Columbia V2P 4P5 (McFee). as the longissimus dorsi must be greater than that 496 Can Vet J Volume 34, August 1993 I

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U Figure 1. Lordotic Haflinger foal 2, aged two months. A) Severely hypoplastic cranial articular processes of thoracic vertebra seven (T7) (arrows). Similar lesions were observed on T8-T1O. B) Hypoplasia of caudal articular processes of T7 (arrows). Similar lesions were observed on T8-T10. C) Normal cranial articular processes of T4 (arrows). exerted by the ventral vertebral muscles. In these foals, An examination of the environment in which the as in previously reported cases of equine swayback, brood mares and stallion were kept did not reveal any no lateral deviation of the spine, or scoliosis, was potential teratogens to which the animals may previ- observed (4). ously have been exposed. However, since the processes In horses, gravity is not a primary contributing fac- leading to vertebral malformation occur early in mor- tor to congenital lordosis. Previous reports have linked phogenesis, the possibility of detecting a specific envi- the pathogenesis of equine congenital lordosis with ronmental teratogen following the birth of an hypoplasia of the intervertebral articulations and con- anomalous foal becomes remote. Substances within the sequent instability of the spine in utero. These factors, maternal or external environment that are harmful to combined with normally developing muscle tone, are a developing fetus usually produce a range or variation thought to produce the lordotic curvatures observed of teratogenic effects, from very mild to lethal, clinically at birth (3,4). As in other congenital depending upon dosage (10). Gradation in anomalous anomalies, the relevant biochemical changes induced development was not seen in these lordotic foals. in developing embryonic systems at the molecular or The physical condition of all the mares and the subcellular level are difficult to discern (6). stallion was good. The nutritional quality of the ration There is no known effective treatment of equine fed to the animals was adequate and satisfactory. lordosis. The condition does not appear to cause pain It is unlikely that chromosomal aberrations such as unless dorsal vertebral spines override (7). trisomy would produce a solitary, specific vertebral In one survey of 443 cases involving disorders of the lesion as seen in these foals. Aberrations in chromo- thoracolumbar spine of the horse, only 15 (2.9%) some number arise from errors in nondisjunction dur- vertebral malformations involved lordosis, scoliosis, ing meiosis and tend to be sporadic in occurrence. or kyphosis (8). Another report described a mid- Because each chromosome carries genetic information thoracic lordosis in a six-month-old filly important to several metabolic and developmental and six cases of lordosis of the middle to caudal pathways, phenotypic abnormalities associated with thoracic region in adult horses, but there was confu- changes in number usually involve several body sys- sion as to whether the lordosis observed in some of tems the animals was congenital or acquired (8). It is cer- (11). tainly possible that there may be overlapping in these The role of heredity in equine lordosis is poorly categories in the equine species, because hereditary and defined and generally considered unknown, probably structural factors, or other induced stressors in com- because of the rarity of the condition and the small bination, may result in the expression of lordosis not number of cases in which accurate breeding records only at birth but at later stages of development. have been kept or made available for examination Congenital defects are abnormalities of structure or (3,5). In earlier reports, hereditary considerations are function present at birth, resulting from disruptive often only briefly discussed. In one instance a mare events during embryogenesis (5,9). Congenital defects produced three consecutive lordotic foals; unfor- may originate at the gene or chromosome level, or they tunately, the mare had been pasture bred and an may result from the influence of environmental factors accurate determination of the stallion(s) involved was acting as teratogens, including those created by man. not possible (3). Congenital anomalies may also be caused by inter- All three lordotic or swayback foals in this report action between the genotype of the fetus and the envi- were sired by the same purebred Haflinger stallion. ronment, a multifactorial etiology (2,6,10). The Foals 1 and 3 were out of the same mare. Pedigree etiology and pathogenesis of congenital defects in analysis (Figure 2) revealed the two mares that pro- animals and man are frequently complex, and the duced these lordotic foals were half-sisters, with a origins of many are still unknown (2,3,6,9,10). common sire. Because the mares were half-sisters, the Can Vet J Volume 34, August 1993 497 ditions (2). Individual foals are either completely affected or normal. For these reasons, we suspect that the congenital lordosis described in these three Haflinger foals is caused by a single gene defect consistent with an autosomal recessive form of inheritance. As the pedigrees of other congenitally lordotic foals in the Haflinger breed become available for examination, further definition of this suspected hereditary influence 1 2 3 4 5 6 7 8 9 10 11 may evolve. Acknowledgments Figure 2. Diagram depicting pedigree relationships of We thank Dr Sheila Schmutz, Department of eleven Haflinger foals, their dams, sire and grand-sire (three Animal and Poultry Science, University of Saskatch- generations). Squares represent males, females are ovals. ewan, for her constructive comments and the prepa- Lordotic foal 1 is colt 2, lordotic foal 2 is filly 10, and lordotic ration of the pedigree diagram. cvi foal 3 is filly 5. References 1. Schweisgut 0. Haflinger Horses. New English ed. Munich, possibility that they carried the same allele in a het- Germany: BLV Verlagsgesellschaft mbH, 1988: 24-25, 64-65, erozygous state was increased (2). 76, 132-137. We believe the occurrence of three cases of con- 2. Nicholas FW. Veterinary Genetics. Oxford: Clarendon Press, genital lordosis within a small group of related 1986: 98-215. 3. Rooney JR. Congenital equine scoliosis and lordosis. Clin purebred animals is more than mere coincidence. We Orthop 1969; 62: 25-30. suspect a hereditary influence in these three Haflinger 4. Rooney JR, Prickett ME. Congenital lordosis of the horse. foals, because there are close familial links in their Cornell Vet 1967; 57: 417-428. pedigrees and an incidence of the anomaly that is sig- 5. Huston R, Saperstein G, Leipold HW. Congenital defects in nificantly higher than that foals. J Equine Med Surg 1977; 1: 146-161. previously reported in the 6. Fraser FC. Relation of animal studies to the problem in man. equine species (5,8). In: Wilson JG, Fraser FC, eds. Handbook of Teratology. An autosomal dominant method of inheritance is Vol. 1. New York and London: Plenum Press, 1977: 75-96. unlikely in these cases as both mares and the stallion 7. Mansmann RA, McAllister ES, eds. Equine Medicine and appeared clinically normal. Because a male and two Surgery. 3rd ed. Vol. 2. Santa Barbara, California: American Veterinary Publications, 1982: 1146-1147. female foals were lordotic, sex-linked inheritance is 8. Jeffcott LB. Disorders of the thoracolumbar spine of the horse also unlikely. There was no gradation in the lesions - a survey of 443 cases. Equine Vet J 1980; 12: 197-210. observed, as would be anticipated in a familial disorder 9. Shupe JL, James LF. Teratogenic plants. Vet Hum Toxicol in which the increasing severity of a defect is directly 1983; 25: 415-422. to 10. Wilson JG. Current status of teratology. In: Wilson JG, Fraser proportional the number of genes present that con- FC, eds. Handbook of Teratology. Vol 1. New York and tribute to its expression (2). We think it is noteworthy London: Plenum Press, 1977: 47-74. that the vertebral lesions observed in the foals were 11. Coates JW, Schmutz SM, Rousseaux CG. A survey of almost identical not only in location but also in malformed aborted bovine fetuses, stillbirths and nonviable severity, which is typical of autosomal recessive con- neonates for abnormal karyotypes. Can J Vet Res 1988; 52: 258-263.

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498 Can Vet J Volume 34, August 1993