Spontaneous Spondylolisthesis in Embryonic and Adult Chick M.
A.
KHAN, N.
O.
O L S O N * AND D . O.
OVERMAN**
Department of Anatomy, Baltimore College of Dental Surgery, Dental School, University of Maryland, Baltimore, Maryland 21201 (Received for publication August 30, 1976)
POULTRY SCIENCE 56: 689-697,
LITERATURE REVIEW
S
PONTANEOUS spondylolisthesis in poultry is observed both in the embryo and the adult bird. (The term spondylolisthesis is derived from the Greek words: Spondylo, denoting spine and listhesis meaning to slip or slide.) A forward or ventral displacement of sixth thoracic vertebra was first described as "kinky-back" by Wise (1970) and later a similar condition was reported by Khan et al. (1973) as creeper syndrome. A similar condition has been reported in both dogs (Dueland, 1973) and man (Wiltse, 1962; MacEwen, 1973) but the condition is known to occur mainly in humans and chickens. MATERIALS AND METHODS Two flocks of adult breeders were secured
* Division of Animal and Veterinary Science, West Virginia University, Morgantown, West Virginia, 26506. ** Department of Anatomy, West Virginia University, Morgantown West Virginia, 26506. Published with the approval of the Agriculture Experiment Station as Scientific Paper 1443.
1977
for this investigation. Flock A was formed from birds obtained from commerical breeder flocks which had suffered three to seven percent mortality due to various forms of crippling anomalies. Over 90 percent of broiler hatches from these flocks were affected with crippling anomalies. Flock B birds were obtained by a similar process but using those birds which did not exhibit crippling conditions. Less than two percent of flock B's mortality was attributable to lameness. Day-old chicks obtained from each flock was identified as first generations—Flock A-G1 and B-G1. Subsequent generations were labeled as G2, G3 and G4. Breeders from each generation were selected by visual observation, back palpation and X-ray procedures. The back of each chicken was examined by holding the bird steady in its most natural standing position and palpating the back with the other hand. Radiographs of live chickens and excised vertebral column specimens were taken with industrial type M (8 x 10 inch Kodak ReadyPak) film. Live birds were exposed to 90 kv. X-rays at 20 ma. for 1 1/2 seconds and excised vertebral column specimens exposed
689
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ABSTRACT The incidence of spontaneous avian spondylopathy was maintained between 58 and 66% in the progeny of one flock (Flock A) and less than 40% in the progeny of another (Flock B), by proper selection and breeding for 4 generations. Spondylolisthesis, the major type of spondylopathy present, was observed at the first and sixth vertebral levels. Spondylolisthesis was progressive in nature and consisted of a ventrodorsal rotation of the 1st and/or 6th thoracic vertebrae leading to spinal cord injury and paraplegia or partial crippling in some birds. There was occasionally extensive muscle degeneration and connective tissue proliferation around the distorted vertebrae and the spinous ligaments bridging the defect were stretched and appeared heavier than normal. Spondylopathy was also observed in 20-day chick embryos. Spondylolisthesis was observed in 33% of the embryos examined from Flock A-G2 and the other conditions present consisted of scoliosis and abnormal lordosis and kyphosis. Using a grading scale of +1 (mild) to +3 (severe), all cases of embryonic spondylopathy were graded as + 1. The back defects present in Flock B-G2 embryos were entirely due to abnormal kyphosis.
690
M. A. KHAN, N . O. OLSON AND D. O. OVERMAN
Some selected sections were stained with 1, 9-dimethylmethyleneblue after Taylor and Jeffree (1969). Twenty day embryos from Flocks A-G2 and B-G2 were killed by quick chilling (8° C.) and examined immediately for gross skeletal abnormalities. Control embryos in this experiment were obtained from a commercial strain of White Rock chickens maintained at the West Virginia University Poultry Farm.
RESULTS The number of birds exhibiting spondylopathy in the parent stock (Flocks A and B) and subsequent generations is shown in Table 1. Spondylopathy was diagnosed in 66% of Flock A birds and by continuous selection and breeding the incidence of spondylopathy was maintained between 58 and 62% in the subsequent generations. Spondylolisthesis was diagnosed as the major type of spondylopathy in Flock A birds and their subsequent generations. The first and sixth thoracic vertebrae are the only movable vertebrae in the otherwise normally fused vertebral column of a chicken caudal to the cervical region. The first and sixth thoracic (Tl and T6) were also the sites where spondylolisthesis was diagnosed (Figs. 1, 2 and 3). The extent of ventrodorsal rotation
TABLE 1.—Vertebral column abnormalities in adult chickens bred from parents experiencing a high (Flock A) and low (Flock B) incidence of spondylopathy Type of flocks Abnormal flocks # of birds Age (days) Spondylopathy' Scoliosis' Spond/Scol 1 Others** 1 # Lame'
Normal Flocks B-G2 B-G3
A*
A-Gl
A-G2
A-G3
A-G4
B*
B-Gl
29 77 66 0 7 0 48
223 180 62 13 78 0 5
117 210 43 9 6 0 10
102 112 41 15 4 2 14
78 112 32 6 1 17 12
5 77 0 0 0 0 0
124 180 23 15 0 0 1
1 Figures in percentage. * Parent stock. ** Abnormal kyphosis and lordosis.
79 210 16 6 1 0 1
86 112 40 19 2 8 5
B-G4 78 112 31 19 0 6 6
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for one second. Lateral and ventrodorsal radiographs of live chickens were taken by stretching out the wings and legs, and placing the bird above the film. Vertebral columns removed at necropsy were prepared for radiographs by cutting bilaterally adjacent to the vertebral bodies. A lateral view was taken of the columns showing spondylolisthesis and a ventrodorsal view of scoliotic columns. Birds not used for future breeding purposes were necropsied immediately following selection and the remaining birds were raised on floor under room isolation conditions. Flocks A and B and their subsequent generations were maintained separate at all times. Eggs from the breeder birds were collected daily for a 6-8 week period after which the breeder birds were also necropsied. The skin and viscera were removed during necropsy and the skeletal muscles and bony skeleton examined for gross lesions. The vertebral columns were separated from the rest of the body, fixed in 10% buffered formalin for 7 days and later processed through decalcifying solution containing 22% formic acid buffered with 9% sodium citrate. Following two weeks of decalcification, a midsagittal section of thoracic 5-7 region was removed from each column and processed for histology. For routine examination 10(x. paraffin sections were stained with hematoxylin and eosin.
691
SPONDYLOLISTHESIS
of T6 in Flock A birds affected with spondylolisthesis ranged from a slight rotation ( + 1 ) to a maximum of + 3 (Table 2). There was usually some local adjustment to check
TABLE 2.—Degree of spondylopathy
the progressive displacement of T6. Fibrocartilaginous tissue surrounded the defect (Fig. 4) and the spinous ligaments bridging the intervertebral gaps were stretched and
in Flock A and B, and their subsequent
generations
Degree of back defect* Number Number +2 +3 +1 examined normal Flock 24 4 8 10 A 29 12 85 88 13 A-Gl 223 5 46 17 A-G2 117 49 36 21 5 59 A-G3 102 4 33 24 16 A-G4 ^8 0 0 0 B 5 5 20 6 2 96 B-Gl 124 0 66 11 2 B-G2 79 2 27 5 B-G3 86 52 13 8 4 78 53 B-G4 * Grading scale for back defects. + 1 Subclinical spondylopathy. + 2 Spondylopathy resulting in stenosis of vertebral canal with some compression of the cord. + 3 Spondylopathy resulting in stenosis of vertebral canal and severe damage to the cord.
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FIG. 1. Radiograph showing spondylolisthesis in a seven-week Flock A-Gl bird. This bird was selected for breeding purposes by palpation of the back for abnormal hump formation (left arrow) and presence of spondylolisthesis at T5-7 region (right arrow) confirmed by radiographic procedures (kv. 90. ma. 20).
692
M. A. KHAN, N. O. OLSON AND D. O. OVERMAN
appeared heavier than normal. The pathological anatomy was not the same in very case, but appeared related to the severity and the age of the defect. The subclinical cases showed minor stretching of the spinous ligaments while the more severely deformed columns had extensive accumulations of fibrous tissue surrounding the defect. In some cases the extensive connective tissue proliferation at the cephalic and caudal aspects of T6 arrested its further rotation. Examination of histologic sections revealed slight stenosis of the vertebral canal due to extensive fibrocartilage growth but the spinal cord was not damaged. Examination of the skeletal muscles of the paraplegic birds revealed a bilateral degeneration of the coracobrachialis,
sartorius and gluteus. Actively phagocytic histiocytes and variable leucocytes were present in abundant numbers and in late stages of degeneration the muscle fibers were replaced by fibrotic tissue (Fig. 5). The progeny of Flock B birds was selected for normal back conformation but the incidence of spondylolisthesis in these birds did not approach zero. The condition was diagnosed in 15% of Flock B-Gl and 19% of Flock B-G4 birds examined (Table 1). However, examination of decalcified vertebral columns revealed only a slight degree of rotation of T6 in 9 of the 18 Flock B-Gl birds showing spondylolisthesis (Fig. 6). The minimum amount of spinal cord damage in these subclinical cases did not produce lame-
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FIG. 2. Radiographs of vertebral columns specimens (kv. 90, ma. 20). 1) Thoracolumbar region of a normal chicken. Arrow indicates the 6th thoracic vertebra. 2) Thoracolumbar region of a vertebral column specimen showing spondylolisthesis at T5 and 6 region. 3) Thoracolumbar region of a vertebral column showing spondylolisthesis at T6 and 7 region.
693
SPONDYLOLISTHESIS
ness in the affected birds. The degree of spondylopathy in Flock B and subsequent generations is shown in Table 2. A normal 20-day chick embryo usually shows slight lumbosacral kyphosis and lower thoracic lordosis, thus care was taken to distinguish these normal curvatures from abnormal lordosis and kyphosis. Abnormal back conformations were observed in 33% of embryos from breeder birds in Flock A-G2 (Table 3). Abnormal kyphosis was the major
type of back abnormality present in these embryos. The other conditions observed consisted of lordosis, scoliosis and spondylolisthesis. Presence of scoliosis and spondylolisthesis in embryos was determined by examining the location of adjacent ribs. In embryos with scoliosis the 4th, 5th and 6th intercostal spaces were narrower on the concave side of the curvature than on the convex side. This comparison was considered an ideal indicator of scoliotic vertebral columns,
TABLE 3.—Spontaneous cases of spondylopathy in 20 day chick embryos from flocks with either a low (Flock B-G2) or a high (Flock A-G2) incidence of hack defects Spondylopathy
A-G2 B-G2 White Rock*
#of embryos
Age (days)
Small body size
116 58 54
20 20 20
21 4 2
SpondyloLordosis Kyphosis Scoliosis listhesis 5 0 0
21 2 3
4 0 0
8 0 0
Limb defects 12 1 0
* Chick embryos obtained from a commercial strain of White Rock birds maintained at West Virginia University Poultry Farm.
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FIG. 3. 1) Radiograph of vertebral column of a chicken showing spondylolisthesis at Tl (arrow). 2) Similar region as in 1. but from a chicken with normal back.
694
M. A. KHAN, N. O. OLSON AND D. O. OVERMAN
"'^f-^Y- ff^*-
since in the control embryos the intercostal spaces were usually evenly spaced thoughout. On a scale of +1 (mild) to +3 (severe), all cases of embryonic scoliosis were graded as + 1 . In embryos with spondylolisthesis (Table 3) the 7th pair of ribs was usually displaced dorsally and there was a bilateral decrease in the width of the 6th intercostal spaces. Mild cases of spondylolisthesis were also distinguished from scoliosis since in the latter case there was unilateral narrowing of the intercostal spaces. All cases of spondylolisthesis in embryos were graded as + 1 . Twelve of the 116 Flock A-Gl embryos examined had limb defects such as enlarged hock joints and abnormally curved toes. The enlargement of hock joints was due to excessive accumulation of synovial fluid which. however, appeared clear and showed no signs of infection. The back defects in embryos
from White Rock and Flock B-G2 were entirely due to abnormal kyphosis (Table 3). DISCUSSION Spondylopathy, as described in this study, includes any abnormal conformation of the vertebral column of a chicken. The two major types of back defects observed in adult chickens and in chick embryos are spondylolisthesis and scoliosis. Both conditions can be progressive, leading to spinal cord injury and motor disturbances. The damage to the spinal cord resulting from the lateral displacement of the vertebral column in scoliosis and from the ventrodorsal rotation of Tl or T6 in spondylolisthesis, is usually mild. Stenosis of the vertebral canal usually does not appear in the subclinical cases, but if present, there are often adhesions in between
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FIG. 4. Intervertebral region between 5th and 6th thoracic vertebrae. Note the fibrocartilage (A) and enlarged dorsal spinal ligament (B). (1, 9-dimethylmethyleneblue x 105).
695
SPONDYLOLISTHESIS
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the meninges and between the dura mater and periosteum. In about 2-10% of cases, the distortion of the vertebrae resulting from spondylopathy causes a marked stenosis of the vertebral canal in the general area of the defect. Injuries to the spinal cord in such cases are due chiefly to the physical stresses to which the spinal cord is subjected and partly to impedence to the blood supply of that segment of the spinal cord. Cumulative injury may occur, especially in cases of severe spondylolisthesis when continued pressure on the spinal cord due to stenosis of the vertebral canal or stretching of the spinal cord over bony prominences causes intermittent ischemia. However, in this study, the spinal cord was never transected, or found to contain large blood clots in the epidural space. Thus, vertebral dislocation due to
fracture was ruled out as a possible cause of spinal cord injury. Furthermore, there was no histologic evidence in the present study indicating that the vertebral defects and spinal cord injury were related to an inflammatory process. Deformities of the vertebral column among vertebrates have been attributed to a variety of causes, such as lack of exercise, inadequate diet, extensive inbreeding and drugs. Recent reports, however, emphasize nutrition, abnormal physical stress and genetic factors as possible causes of spondylopathy (Osbaldiston and Wise, 1967; Rigdon and Mack, 1968a,b; Riddell and Howell, 1972; Wise, 1973; Khan et al., 1973). In the present study birds were not selected for scoliosis, but the condition did appear in a small percent of cases (Table 1). Attempts to cull birds
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FIG. 5. A paraffin section of the sartorius from a paraplegic bird. The tissue shows edema, and degeneration of muscle fibers, (hematoxylin and eosin x 375).
696
M. A. KHAN, N. O. OLSON AND D. O. OVERMAN
with scoliosis did not eliminate the condition in the subsequent generations. These results are in agreement with those reported by Rigdon and Mack (1968a) and Taylor (1971). From the results reported in this study it appears that there are multiple factors contributing to the etiology of spondylolisthesis. Abnormal degrees of lordosis, kyphosis, and spondylolisthesis were observed in 17 to 20-day embryos (Table 3). It was further observed that these abnormal embryos were the progeny of birds with typical lesions of spondylolisthesis. Since various forms of avian spondylopathy are progressive, it is reasonable to assume that embryonic spondylopathy might precipitate various back conditions observed soon after hatching. These observations are, however, not in ac-
cordance with the results reported by Wise (1973), who was unable to observe spondylopathy at the time of hatching. Selection experiments were conducted to determine whether the incidence of spondylolisthesis could be increased by a process of random mating in an isolated flock. The results show that the incidence of spondylolisthesis was maintained at a considerably higher level than that found in an ordinary commerical flock by a well planned breeding and selection program (Table 1). Spondylolisthesis appeared to be self-limiting. Some birds with severely malformed vertebral columns were extremely crippled and obviously unable to breed. This lack of breeding ability was the main reason for the lower incidence of spondylolisthesis in Flock A-G4 birds. From the
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FIG. 6. This section of T5-7 region was removed from a normal back (Flock B-Gl) seven-week old chicken. The unstained decalcified specimen shows a slight rotation of T6, (arrow) but no injury to the spinal cord.
697
SPONDYLOLISTHESIS
instances, the connective tissue adjustments appeared to counteract the hereditary w e a k n e s s at the T6 level of the vertebral column. REFERENCES Dueland, R., 1973. Spinal fusion and dorsal laminectomy for midcervical spondylolisthesis in a dog. J. Am. Vet. Med. Ass. 162: 366-369. Khan, M. A., N. O. Olson and R. Weiss, 1973. Spondylopathy in broilers. Case reports. Poultry Sci. 52: 1847-1852. MacEwen, G. D., 1973. Experimental scoliosis. Clinical Orthopedics, 93: 69-74. Osbaldiston, G. W., and D. R. Wise. 1967. Spondylolisthesis and leg weakness in the chicken—a common etiology. Vet. Rec. 80: 320-322. Riddell, C , and J. Howell. 1972. Spondylolisthesis (Kinky Back) in broiler chickens in Western Canada. Avian Dis. 16: 444-452. Rigdon, R. H., and J. Mack. 1968a. Spontaneous occurrence of scoliosis in the chicken. Avian Dis. 12: 530-543. Rigdon, R. H., and J. Mack. 1968b. Spontaneously occurring scoliosis in the White Pekin duck (Anas platyrhynchos). Am. J. Vet. Res. 29: 1081-1087. Taylor, K. B., and G. M. Jeffree. 1969. A new basic metachromatic dye 1:9-dimethylmethyleneblue. Histochemical J. 1: 199-204. Taylor, L. W., 1971. Kyphoscoliosis in a long-term selection experiment with chickens. Avian Dis. 15: 376-390. Wiltse, L. L., 1962. The etiology of spondylolisthesis. J. Bone Joint Surgery, 44A: 539-560. Wise, D. R., 1970. Spondylolisthesis (kinky back) in broiler chickens. Res. Vet. Sci. 11: 447-451. Wise, D. R., 1973. The incidence and aetiology of avian spondylolisthesis (kinky back). Res. Vet. Sci. 14: 1-10.
NEWS AND NOTES (Continued from page 688) tions for the annual fellowships are solicited each year from land-grant universities., AMERICAN MOTORS CONSERVATION AWARDS Dr. Gary E. Duke and Dr. Patrick Redig, College of veterinary medicine, University of Minnesota, St.
Paul, Minnesota, received a joint American Motors Conservation Award in November. The presentations were made at the Fall Awards Convocation of the Veterinary College, held in the new Animal ScienceVeterinary Medicine Building. Duke and Redig are among 17 men and 5 women from 17 states named to receive 1976 Conservation
(Continued on page 700)
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number of generations of birds observed and from the work reported on chick e m b r y o s in this study, it was concluded that heredity is an important contributing factor in the etiology of spondylolisthesis. A mild form of the condition is present in the e m b r y o and occasionally becomes manifested shortly after hatching. In many c a s e s , of e m b r y o n i c spondylolisthesis, the condition remains subclinical even after hatching and during adult life. Because of its unique anatomic position in the vertebral column of a chicken, the sixth thoracic vertebra is vulnerable to extrinsic physical force of strain or tension. Other than the local distortion of the vertebrae involved and the injury to the spinal cord, the only other responses p r e s e n t at the site of t h e defect are muscle degeneration and general h y p e r t r o p h y of the connective tissue. Muscle degeneration was only observed in some paraplegic birds. T h e pathologic changes in muscles described previously, plus the presence of degenerated nerve filaments in some muscles indicated a progressive motor denervation. T h e rotation of the malformed vertebrae stretched the dorsal spinal ligaments and t h e gaps t h u s created were later filled with an abnormal fibrocartilaginous material. T h e connective tissue h y p e r t r o p h y is a local r e s p o n s e to affect stability and arrest further rotation and displacement of the malformed v e r t e b r a e . Since these changes were observed in subclinical cases of spondylolisthesis in at least some
A.
KHAN, N.
O.
O L S O N * AND D . O.
OVERMAN**
Department of Anatomy, Baltimore College of Dental Surgery, Dental School, University of Maryland, Baltimore, Maryland 21201 (Received for publication August 30, 1976)
POULTRY SCIENCE 56: 689-697,
LITERATURE REVIEW
S
PONTANEOUS spondylolisthesis in poultry is observed both in the embryo and the adult bird. (The term spondylolisthesis is derived from the Greek words: Spondylo, denoting spine and listhesis meaning to slip or slide.) A forward or ventral displacement of sixth thoracic vertebra was first described as "kinky-back" by Wise (1970) and later a similar condition was reported by Khan et al. (1973) as creeper syndrome. A similar condition has been reported in both dogs (Dueland, 1973) and man (Wiltse, 1962; MacEwen, 1973) but the condition is known to occur mainly in humans and chickens. MATERIALS AND METHODS Two flocks of adult breeders were secured
* Division of Animal and Veterinary Science, West Virginia University, Morgantown, West Virginia, 26506. ** Department of Anatomy, West Virginia University, Morgantown West Virginia, 26506. Published with the approval of the Agriculture Experiment Station as Scientific Paper 1443.
1977
for this investigation. Flock A was formed from birds obtained from commerical breeder flocks which had suffered three to seven percent mortality due to various forms of crippling anomalies. Over 90 percent of broiler hatches from these flocks were affected with crippling anomalies. Flock B birds were obtained by a similar process but using those birds which did not exhibit crippling conditions. Less than two percent of flock B's mortality was attributable to lameness. Day-old chicks obtained from each flock was identified as first generations—Flock A-G1 and B-G1. Subsequent generations were labeled as G2, G3 and G4. Breeders from each generation were selected by visual observation, back palpation and X-ray procedures. The back of each chicken was examined by holding the bird steady in its most natural standing position and palpating the back with the other hand. Radiographs of live chickens and excised vertebral column specimens were taken with industrial type M (8 x 10 inch Kodak ReadyPak) film. Live birds were exposed to 90 kv. X-rays at 20 ma. for 1 1/2 seconds and excised vertebral column specimens exposed
689
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ABSTRACT The incidence of spontaneous avian spondylopathy was maintained between 58 and 66% in the progeny of one flock (Flock A) and less than 40% in the progeny of another (Flock B), by proper selection and breeding for 4 generations. Spondylolisthesis, the major type of spondylopathy present, was observed at the first and sixth vertebral levels. Spondylolisthesis was progressive in nature and consisted of a ventrodorsal rotation of the 1st and/or 6th thoracic vertebrae leading to spinal cord injury and paraplegia or partial crippling in some birds. There was occasionally extensive muscle degeneration and connective tissue proliferation around the distorted vertebrae and the spinous ligaments bridging the defect were stretched and appeared heavier than normal. Spondylopathy was also observed in 20-day chick embryos. Spondylolisthesis was observed in 33% of the embryos examined from Flock A-G2 and the other conditions present consisted of scoliosis and abnormal lordosis and kyphosis. Using a grading scale of +1 (mild) to +3 (severe), all cases of embryonic spondylopathy were graded as + 1. The back defects present in Flock B-G2 embryos were entirely due to abnormal kyphosis.
690
M. A. KHAN, N . O. OLSON AND D. O. OVERMAN
Some selected sections were stained with 1, 9-dimethylmethyleneblue after Taylor and Jeffree (1969). Twenty day embryos from Flocks A-G2 and B-G2 were killed by quick chilling (8° C.) and examined immediately for gross skeletal abnormalities. Control embryos in this experiment were obtained from a commercial strain of White Rock chickens maintained at the West Virginia University Poultry Farm.
RESULTS The number of birds exhibiting spondylopathy in the parent stock (Flocks A and B) and subsequent generations is shown in Table 1. Spondylopathy was diagnosed in 66% of Flock A birds and by continuous selection and breeding the incidence of spondylopathy was maintained between 58 and 62% in the subsequent generations. Spondylolisthesis was diagnosed as the major type of spondylopathy in Flock A birds and their subsequent generations. The first and sixth thoracic vertebrae are the only movable vertebrae in the otherwise normally fused vertebral column of a chicken caudal to the cervical region. The first and sixth thoracic (Tl and T6) were also the sites where spondylolisthesis was diagnosed (Figs. 1, 2 and 3). The extent of ventrodorsal rotation
TABLE 1.—Vertebral column abnormalities in adult chickens bred from parents experiencing a high (Flock A) and low (Flock B) incidence of spondylopathy Type of flocks Abnormal flocks # of birds Age (days) Spondylopathy' Scoliosis' Spond/Scol 1 Others** 1 # Lame'
Normal Flocks B-G2 B-G3
A*
A-Gl
A-G2
A-G3
A-G4
B*
B-Gl
29 77 66 0 7 0 48
223 180 62 13 78 0 5
117 210 43 9 6 0 10
102 112 41 15 4 2 14
78 112 32 6 1 17 12
5 77 0 0 0 0 0
124 180 23 15 0 0 1
1 Figures in percentage. * Parent stock. ** Abnormal kyphosis and lordosis.
79 210 16 6 1 0 1
86 112 40 19 2 8 5
B-G4 78 112 31 19 0 6 6
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for one second. Lateral and ventrodorsal radiographs of live chickens were taken by stretching out the wings and legs, and placing the bird above the film. Vertebral columns removed at necropsy were prepared for radiographs by cutting bilaterally adjacent to the vertebral bodies. A lateral view was taken of the columns showing spondylolisthesis and a ventrodorsal view of scoliotic columns. Birds not used for future breeding purposes were necropsied immediately following selection and the remaining birds were raised on floor under room isolation conditions. Flocks A and B and their subsequent generations were maintained separate at all times. Eggs from the breeder birds were collected daily for a 6-8 week period after which the breeder birds were also necropsied. The skin and viscera were removed during necropsy and the skeletal muscles and bony skeleton examined for gross lesions. The vertebral columns were separated from the rest of the body, fixed in 10% buffered formalin for 7 days and later processed through decalcifying solution containing 22% formic acid buffered with 9% sodium citrate. Following two weeks of decalcification, a midsagittal section of thoracic 5-7 region was removed from each column and processed for histology. For routine examination 10(x. paraffin sections were stained with hematoxylin and eosin.
691
SPONDYLOLISTHESIS
of T6 in Flock A birds affected with spondylolisthesis ranged from a slight rotation ( + 1 ) to a maximum of + 3 (Table 2). There was usually some local adjustment to check
TABLE 2.—Degree of spondylopathy
the progressive displacement of T6. Fibrocartilaginous tissue surrounded the defect (Fig. 4) and the spinous ligaments bridging the intervertebral gaps were stretched and
in Flock A and B, and their subsequent
generations
Degree of back defect* Number Number +2 +3 +1 examined normal Flock 24 4 8 10 A 29 12 85 88 13 A-Gl 223 5 46 17 A-G2 117 49 36 21 5 59 A-G3 102 4 33 24 16 A-G4 ^8 0 0 0 B 5 5 20 6 2 96 B-Gl 124 0 66 11 2 B-G2 79 2 27 5 B-G3 86 52 13 8 4 78 53 B-G4 * Grading scale for back defects. + 1 Subclinical spondylopathy. + 2 Spondylopathy resulting in stenosis of vertebral canal with some compression of the cord. + 3 Spondylopathy resulting in stenosis of vertebral canal and severe damage to the cord.
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FIG. 1. Radiograph showing spondylolisthesis in a seven-week Flock A-Gl bird. This bird was selected for breeding purposes by palpation of the back for abnormal hump formation (left arrow) and presence of spondylolisthesis at T5-7 region (right arrow) confirmed by radiographic procedures (kv. 90. ma. 20).
692
M. A. KHAN, N. O. OLSON AND D. O. OVERMAN
appeared heavier than normal. The pathological anatomy was not the same in very case, but appeared related to the severity and the age of the defect. The subclinical cases showed minor stretching of the spinous ligaments while the more severely deformed columns had extensive accumulations of fibrous tissue surrounding the defect. In some cases the extensive connective tissue proliferation at the cephalic and caudal aspects of T6 arrested its further rotation. Examination of histologic sections revealed slight stenosis of the vertebral canal due to extensive fibrocartilage growth but the spinal cord was not damaged. Examination of the skeletal muscles of the paraplegic birds revealed a bilateral degeneration of the coracobrachialis,
sartorius and gluteus. Actively phagocytic histiocytes and variable leucocytes were present in abundant numbers and in late stages of degeneration the muscle fibers were replaced by fibrotic tissue (Fig. 5). The progeny of Flock B birds was selected for normal back conformation but the incidence of spondylolisthesis in these birds did not approach zero. The condition was diagnosed in 15% of Flock B-Gl and 19% of Flock B-G4 birds examined (Table 1). However, examination of decalcified vertebral columns revealed only a slight degree of rotation of T6 in 9 of the 18 Flock B-Gl birds showing spondylolisthesis (Fig. 6). The minimum amount of spinal cord damage in these subclinical cases did not produce lame-
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FIG. 2. Radiographs of vertebral columns specimens (kv. 90, ma. 20). 1) Thoracolumbar region of a normal chicken. Arrow indicates the 6th thoracic vertebra. 2) Thoracolumbar region of a vertebral column specimen showing spondylolisthesis at T5 and 6 region. 3) Thoracolumbar region of a vertebral column showing spondylolisthesis at T6 and 7 region.
693
SPONDYLOLISTHESIS
ness in the affected birds. The degree of spondylopathy in Flock B and subsequent generations is shown in Table 2. A normal 20-day chick embryo usually shows slight lumbosacral kyphosis and lower thoracic lordosis, thus care was taken to distinguish these normal curvatures from abnormal lordosis and kyphosis. Abnormal back conformations were observed in 33% of embryos from breeder birds in Flock A-G2 (Table 3). Abnormal kyphosis was the major
type of back abnormality present in these embryos. The other conditions observed consisted of lordosis, scoliosis and spondylolisthesis. Presence of scoliosis and spondylolisthesis in embryos was determined by examining the location of adjacent ribs. In embryos with scoliosis the 4th, 5th and 6th intercostal spaces were narrower on the concave side of the curvature than on the convex side. This comparison was considered an ideal indicator of scoliotic vertebral columns,
TABLE 3.—Spontaneous cases of spondylopathy in 20 day chick embryos from flocks with either a low (Flock B-G2) or a high (Flock A-G2) incidence of hack defects Spondylopathy
A-G2 B-G2 White Rock*
#of embryos
Age (days)
Small body size
116 58 54
20 20 20
21 4 2
SpondyloLordosis Kyphosis Scoliosis listhesis 5 0 0
21 2 3
4 0 0
8 0 0
Limb defects 12 1 0
* Chick embryos obtained from a commercial strain of White Rock birds maintained at West Virginia University Poultry Farm.
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FIG. 3. 1) Radiograph of vertebral column of a chicken showing spondylolisthesis at Tl (arrow). 2) Similar region as in 1. but from a chicken with normal back.
694
M. A. KHAN, N. O. OLSON AND D. O. OVERMAN
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since in the control embryos the intercostal spaces were usually evenly spaced thoughout. On a scale of +1 (mild) to +3 (severe), all cases of embryonic scoliosis were graded as + 1 . In embryos with spondylolisthesis (Table 3) the 7th pair of ribs was usually displaced dorsally and there was a bilateral decrease in the width of the 6th intercostal spaces. Mild cases of spondylolisthesis were also distinguished from scoliosis since in the latter case there was unilateral narrowing of the intercostal spaces. All cases of spondylolisthesis in embryos were graded as + 1 . Twelve of the 116 Flock A-Gl embryos examined had limb defects such as enlarged hock joints and abnormally curved toes. The enlargement of hock joints was due to excessive accumulation of synovial fluid which. however, appeared clear and showed no signs of infection. The back defects in embryos
from White Rock and Flock B-G2 were entirely due to abnormal kyphosis (Table 3). DISCUSSION Spondylopathy, as described in this study, includes any abnormal conformation of the vertebral column of a chicken. The two major types of back defects observed in adult chickens and in chick embryos are spondylolisthesis and scoliosis. Both conditions can be progressive, leading to spinal cord injury and motor disturbances. The damage to the spinal cord resulting from the lateral displacement of the vertebral column in scoliosis and from the ventrodorsal rotation of Tl or T6 in spondylolisthesis, is usually mild. Stenosis of the vertebral canal usually does not appear in the subclinical cases, but if present, there are often adhesions in between
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FIG. 4. Intervertebral region between 5th and 6th thoracic vertebrae. Note the fibrocartilage (A) and enlarged dorsal spinal ligament (B). (1, 9-dimethylmethyleneblue x 105).
695
SPONDYLOLISTHESIS
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the meninges and between the dura mater and periosteum. In about 2-10% of cases, the distortion of the vertebrae resulting from spondylopathy causes a marked stenosis of the vertebral canal in the general area of the defect. Injuries to the spinal cord in such cases are due chiefly to the physical stresses to which the spinal cord is subjected and partly to impedence to the blood supply of that segment of the spinal cord. Cumulative injury may occur, especially in cases of severe spondylolisthesis when continued pressure on the spinal cord due to stenosis of the vertebral canal or stretching of the spinal cord over bony prominences causes intermittent ischemia. However, in this study, the spinal cord was never transected, or found to contain large blood clots in the epidural space. Thus, vertebral dislocation due to
fracture was ruled out as a possible cause of spinal cord injury. Furthermore, there was no histologic evidence in the present study indicating that the vertebral defects and spinal cord injury were related to an inflammatory process. Deformities of the vertebral column among vertebrates have been attributed to a variety of causes, such as lack of exercise, inadequate diet, extensive inbreeding and drugs. Recent reports, however, emphasize nutrition, abnormal physical stress and genetic factors as possible causes of spondylopathy (Osbaldiston and Wise, 1967; Rigdon and Mack, 1968a,b; Riddell and Howell, 1972; Wise, 1973; Khan et al., 1973). In the present study birds were not selected for scoliosis, but the condition did appear in a small percent of cases (Table 1). Attempts to cull birds
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FIG. 5. A paraffin section of the sartorius from a paraplegic bird. The tissue shows edema, and degeneration of muscle fibers, (hematoxylin and eosin x 375).
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M. A. KHAN, N. O. OLSON AND D. O. OVERMAN
with scoliosis did not eliminate the condition in the subsequent generations. These results are in agreement with those reported by Rigdon and Mack (1968a) and Taylor (1971). From the results reported in this study it appears that there are multiple factors contributing to the etiology of spondylolisthesis. Abnormal degrees of lordosis, kyphosis, and spondylolisthesis were observed in 17 to 20-day embryos (Table 3). It was further observed that these abnormal embryos were the progeny of birds with typical lesions of spondylolisthesis. Since various forms of avian spondylopathy are progressive, it is reasonable to assume that embryonic spondylopathy might precipitate various back conditions observed soon after hatching. These observations are, however, not in ac-
cordance with the results reported by Wise (1973), who was unable to observe spondylopathy at the time of hatching. Selection experiments were conducted to determine whether the incidence of spondylolisthesis could be increased by a process of random mating in an isolated flock. The results show that the incidence of spondylolisthesis was maintained at a considerably higher level than that found in an ordinary commerical flock by a well planned breeding and selection program (Table 1). Spondylolisthesis appeared to be self-limiting. Some birds with severely malformed vertebral columns were extremely crippled and obviously unable to breed. This lack of breeding ability was the main reason for the lower incidence of spondylolisthesis in Flock A-G4 birds. From the
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FIG. 6. This section of T5-7 region was removed from a normal back (Flock B-Gl) seven-week old chicken. The unstained decalcified specimen shows a slight rotation of T6, (arrow) but no injury to the spinal cord.
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SPONDYLOLISTHESIS
instances, the connective tissue adjustments appeared to counteract the hereditary w e a k n e s s at the T6 level of the vertebral column. REFERENCES Dueland, R., 1973. Spinal fusion and dorsal laminectomy for midcervical spondylolisthesis in a dog. J. Am. Vet. Med. Ass. 162: 366-369. Khan, M. A., N. O. Olson and R. Weiss, 1973. Spondylopathy in broilers. Case reports. Poultry Sci. 52: 1847-1852. MacEwen, G. D., 1973. Experimental scoliosis. Clinical Orthopedics, 93: 69-74. Osbaldiston, G. W., and D. R. Wise. 1967. Spondylolisthesis and leg weakness in the chicken—a common etiology. Vet. Rec. 80: 320-322. Riddell, C , and J. Howell. 1972. Spondylolisthesis (Kinky Back) in broiler chickens in Western Canada. Avian Dis. 16: 444-452. Rigdon, R. H., and J. Mack. 1968a. Spontaneous occurrence of scoliosis in the chicken. Avian Dis. 12: 530-543. Rigdon, R. H., and J. Mack. 1968b. Spontaneously occurring scoliosis in the White Pekin duck (Anas platyrhynchos). Am. J. Vet. Res. 29: 1081-1087. Taylor, K. B., and G. M. Jeffree. 1969. A new basic metachromatic dye 1:9-dimethylmethyleneblue. Histochemical J. 1: 199-204. Taylor, L. W., 1971. Kyphoscoliosis in a long-term selection experiment with chickens. Avian Dis. 15: 376-390. Wiltse, L. L., 1962. The etiology of spondylolisthesis. J. Bone Joint Surgery, 44A: 539-560. Wise, D. R., 1970. Spondylolisthesis (kinky back) in broiler chickens. Res. Vet. Sci. 11: 447-451. Wise, D. R., 1973. The incidence and aetiology of avian spondylolisthesis (kinky back). Res. Vet. Sci. 14: 1-10.
NEWS AND NOTES (Continued from page 688) tions for the annual fellowships are solicited each year from land-grant universities., AMERICAN MOTORS CONSERVATION AWARDS Dr. Gary E. Duke and Dr. Patrick Redig, College of veterinary medicine, University of Minnesota, St.
Paul, Minnesota, received a joint American Motors Conservation Award in November. The presentations were made at the Fall Awards Convocation of the Veterinary College, held in the new Animal ScienceVeterinary Medicine Building. Duke and Redig are among 17 men and 5 women from 17 states named to receive 1976 Conservation
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number of generations of birds observed and from the work reported on chick e m b r y o s in this study, it was concluded that heredity is an important contributing factor in the etiology of spondylolisthesis. A mild form of the condition is present in the e m b r y o and occasionally becomes manifested shortly after hatching. In many c a s e s , of e m b r y o n i c spondylolisthesis, the condition remains subclinical even after hatching and during adult life. Because of its unique anatomic position in the vertebral column of a chicken, the sixth thoracic vertebra is vulnerable to extrinsic physical force of strain or tension. Other than the local distortion of the vertebrae involved and the injury to the spinal cord, the only other responses p r e s e n t at the site of t h e defect are muscle degeneration and general h y p e r t r o p h y of the connective tissue. Muscle degeneration was only observed in some paraplegic birds. T h e pathologic changes in muscles described previously, plus the presence of degenerated nerve filaments in some muscles indicated a progressive motor denervation. T h e rotation of the malformed vertebrae stretched the dorsal spinal ligaments and t h e gaps t h u s created were later filled with an abnormal fibrocartilaginous material. T h e connective tissue h y p e r t r o p h y is a local r e s p o n s e to affect stability and arrest further rotation and displacement of the malformed v e r t e b r a e . Since these changes were observed in subclinical cases of spondylolisthesis in at least some
