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Vertebral Body Shape as a Predictor of Spinal Deformity in Osteogenesis Imperfecta*

SEIICHI ISHIKAWA, M.D., NIIGATA-SHI, S. JAY KUMAR, M.D., WILMINGTON, DELAWARE, HIDEAKI E. TAKAHASHI, M.D. and MASAFUMI HOMMA, M.D., NIIGATA-SHI, JAPAN

Investigation performed at the Department of Orthopaedic Surgery, Alfred I. duPont Institute, Wilmington, and the Department of Orthopaedic Surgery, Hamagumi Medical and Educational Center for Handicapped Children, Niigata-shi

	Abstract

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We analyzed forty-four patients who had osteogenesis imperfecta, in order to determine the prevalence of spinal deformities. At the time of the most recent follow-up, scoliosis was present in thirty patients (68 per cent) and kyphosis, in eighteen (41 per cent). According to the classification system of Falvo et al., scoliosis progressed rapidly with growth in twelve of fifteen patients who had the congenita type of osteogenesis imperfecta and in four of thirteen who had the tarda-I type. Curves that progressed before puberty did not always continue to progress after cessation of growth. Lateral roentgenograms made at the initial examination revealed four types of vertebral body deformities: biconcave, flattened, wedged, and unclassifiable vertebrae. Biconcave vertebrae were seen characteristically in patients who had the congenita type of osteogenesis imperfecta. The presence of six biconcave vertebrae or more before puberty indicated that severe scoliosis (more than 50 degrees) was likely to develop. Biconcave vertebrae did not appear to affect the severity of kyphosis. The other types of vertebral deformities were not useful for predicting progression of spinal deformity.

	Introduction

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Osteogenesis imperfecta is characterized by fragility of bones, blue sclerae, dentinogenesis imperfecta, and early loss of hearing. On the basis of abnormalities of collagen synthesis^17,18, osteogenesis imperfecta is currently considered a genetic and metabolic disorder that involves connective tissue. Since Fairbank's 1948 report of a patient who had spinal deformity with this disorder, there have been many reports of spinal deformity^{1-4,8,10,11,13-15,18,20}, with the prevalence ranging from 39 to 100 per cent. Seventeen (40 per cent) of forty-two patients reported on by Bauze et al., sixty-four (62 per cent) of 103 patients reported on by Benson et al.⁴, thirty-five (39 per cent) of ninety patients reported on by Falvo et al., thirty-eight (88 per cent) of forty-three patients reported on by Hanscom et al.¹¹, twenty-two (71 per cent) of thirty-one patients reported on by Moorefield and Miller, all twenty-two patients reported on by Norimatsu et al., and twenty-eight (52 per cent) of fifty-four patients reported on by Renshaw et al. had scoliosis. Other authors^1,3,10,18,20, after analyzing the literature, have reported similar numbers. However, only a few reports^3,4,11,15 have described the roentgenographic characteristics of vertebral deformities, and little is known about the relationship between vertebral shape and spinal deformities. The purpose of this study was to identify the different vertebral deformities seen in osteogenesis imperfecta and to determine if progression of the curve and deformity could be predicted on the basis of changes in vertebral bodies.

	Materials and Methods

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The study included forty-four patients who were seen for osteogenesis imperfecta between 1961 and 1992 and for whom posteroanterior and lateral roentgenograms of the spine were made, with them sitting or standing, at the initial and most recent follow-up visits. Twenty-one of these patients were seen at the Alfred I. duPont Institute and twenty-three, at the Hamagumi Medical and Educational Center for Handicapped Children. There were twenty-four male and twenty female patients, with a mean age of nine years (range, two to twenty-eight years) at the initial examination at our institutions and a mean age of twenty years (range, seven to forty-eight years) at the most recent examination. The mean period of follow-up was twelve years (range, two to thirty years). The medical records were reviewed for the family history, scleral color, quality of the teeth, loss of hearing, number of fractures, deformities of the chest, joint laxity, walking ability, and, in particular, spinal deformities (Table I). In most of the patients, spinal deformity was treated with either observation alone or a brace; only four patients had a spinal arthrodesis.

The mean age of the fifteen patients who had the congenita type was seven years (range, two to fifteen years) at the initial examination and seventeen years (range, seven to thirty-two years) at the most recent examination. Many of these patients were referred to our institutions from other institutions. A fracture of five long bones or more was documented in the charts of only eight of the fifteen patients at the time of the most recent follow-up. The information in the charts of the other seven patients was incomplete with regard to the number of fractures that had been sustained. The number of fractures ranged from five to fifty (mean, twenty-one). At the time of the most recent follow-up, eleven patients were unable to walk and used a wheelchair, three walked with crutches, and one patient was bedridden. Twelve patients had a spinal deformity, and three did not.

The thirteen patients who had the tarda-I type of osteogenesis imperfecta were a mean of nine years old (range, two to nineteen years old) at the initial examination and twenty-one years old (range, ten to thirty-nine years old) at the most recent examination. All thirteen patients sustained fractures of the long bones, but the number was recorded for only eight patients. Those eight patients had three to twenty-three fractures (mean, nine fractures). The patients who had the tarda-I type of osteogenesis imperfecta appeared to have sustained fractures of long bones less frequently than those who had the congenita type. Seven patients were able to walk independently, and the other six walked with aids such as crutches at the time of the most recent follow-up.

The mean age of the sixteen patients who had the tarda-II type of osteogenesis imperfecta was ten years (range, two to twenty-eight years) at the initial examination and twenty-three years (range, nine to forty-eight years) at the most recent examination. Fractures of long bones were clearly documented in the charts of only eleven patients, who had two to thirteen fractures (mean, seven fractures). Fifteen patients were able to walk independently, and one patient walked with crutches at the time of the most recent follow-up.

All patients were followed with roentgenograms of the spine, made with them sitting or standing, and the spinal deformities were measured with the Cobb method on posteroanterior or lateral roentgenograms. If two curves were present, the greater curve was used for analysis of data. The vertebral deformities in the thoracic and lumbar spine were identified on lateral roentgenograms made at the initial examination and were classified as biconcave, flattened, wedged, or unclassifiable vertebrae (Figs. 1-A, 1-B, 1-C through 1-D). The unclassifiable vertebrae did not have a definite shape and had a variety of abnormalities. Biconcave vertebrae were defined as ones in which the height of the mid-portion of the vertebral body was 70 per cent or less of the mean height at the anterior and posterior borders of the vertebral body. These vertebrae are also known as codfish vertebrae. The levels and distribution of the vertebral deformities also were recorded.

View larger version (143K): [in this window] [in a new window]   Figs. 1-A through 1-D: Vertebral deformities (arrows) seen on lateral roentgenograms at the initial examination. Fig. 1-A: Biconcave (so-called codfish) vertebrae with widening of the disc space.

View larger version (139K): [in this window] [in a new window]   Fig. 1-B: Flattened vertebrae.

View larger version (128K): [in this window] [in a new window]   Fig. 1-C: Wedged vertebrae.

View larger version (129K): [in this window] [in a new window]   Fig. 1-D: Unclassifiable vertebrae.

	Results

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Scoliosis
Scoliosis was classified into three groups: severe (more than 50 degrees), moderate (between 30 and 50 degrees), and mild (less than 30 degrees)¹⁵. Progression of the curve was documented as rapid when the curve had increased 4 degrees or more per year and as slow when it had increased 3 degrees or less per year. A curve was considered to be non-progressive when it had not changed. Nineteen (43 per cent) of the forty-four patients had scoliosis, with a mean curve of 29 degrees (range, 6 to 86 degrees), at the initial examination. Scoliosis was documented in ten of the fifteen patients who had the congenita type of osteogenesis imperfecta, seven of the thirteen who had the tarda-I type, and two of the sixteen who had the tarda-II type.

The ten patients who had the congenita type of disorder and scoliosis at the initial examination had a mean age of eight years (range, two to fifteen years) and a mean curve of 33 degrees (range, 7 to 86 degrees) at that time. Two other patients had no scoliosis at the initial examination, but a curve developed at the age of eight years in one and thirteen years in the other. At the most recent follow-up examination, the scoliosis in these twelve patients measured a mean of 79 degrees (range, 47 to 115 degrees) and the mean age was eighteen years (range, seven to thirty-two years). The twelve patients all had a rapidly progressive curve. One (Case 15), who was followed to the age of thirty years, had more than 100 degrees of scoliosis by the age of twenty-three years but only mild progression after that age. In two patients (Cases 11 and 13), the curve did not progress after the ages of eighteen and twenty-one years, respectively, despite rapid progression before those ages. These two patients used a wheelchair and, even though the curve did not worsen, their ability to perform activities of daily living appeared to deteriorate with age.

In the seven patients who had the tarda-I type of osteogenesis imperfecta and scoliosis at the initial examination, the curve measured a mean of 25 degrees (range, 6 to 60 degrees) and the mean age was twelve years (range, six to nineteen years) at that time. Scoliosis developed later, at a mean age of fourteen years (range, seven to twenty-one years), in the remaining six patients. At the most recent follow-up examination, the scoliosis in these thirteen patients averaged 35 degrees (range, 5 to 86 degrees) and the mean age was twenty-one years (range, ten to thirty-nine years). The curve had increased in ten of these patients, and it had not changed since the initial examination in the other three. Two patients (Cases 18 and 23) had rapid progression of the curve, to 70 degrees by the age of fourteen years in one and to 56 degrees by the age of sixteen years in the other. They were followed until the age of twenty-seven and twenty-three years, respectively, and the curves progressed only slowly after that age. Both patients were able to walk independently, and the disabilities did not appear to increase with age. Another patient (Case 24) had rapid progression of the curve, to 86 degrees, before the age of thirteen years but no progression after that age. This patient walked with crutches, and this function did not appear to deteriorate with age. Nine patients had a slowly progressive curve before puberty, and three of them had no progression after puberty. The scoliosis in these three patients was 15, 17, and 19 degrees at the time of the most recent follow-up (Table I).

The two patients (Cases 37 and 44) who had the tarda-II type of osteogenesis imperfecta and scoliosis at the initial examination were nine and twenty-eight years old and had curves measuring 10 and 27 degrees at that time. Scoliosis developed later, at the ages of fifteen, seventeen, and twenty-seven years, in three patients (Cases 33, 34, and 39). At the time of the most recent follow-up, the scoliosis in these five patients averaged 19 degrees (range, 6 to 40 degrees) and the mean age was twenty-five years (range, fifteen to forty-eight years). The curve had increased since the initial examination in four of these five patients, and it had not changed in one. No patient in this group had a rapidly progressive curve, and eleven patients had no scoliosis (Table I).

Kyphosis
Kyphosis in association with scoliosis was noted as being present in either the thoracic or the thoracolumbar spine. Kyphosis in the thoracolumbar spine was seen only in patients who had the congenita type of osteogenesis imperfecta. Thoracic kyphosis was defined as a Cobb angle of 40 degrees or more⁹. Kyphosis was seen in four (9 per cent) of the forty-four patients at the initial examination and in eighteen (41 per cent) at the most recent examination.

At the time of the most recent follow-up, kyphosis was seen in twelve patients who had the congenita type of osteogenesis imperfecta. Seven of the curves were thoracic (mean, 60 degrees; range, 40 to 100 degrees), and the mean age of the seven patients was twenty-one years (range, thirteen to thirty-two years). Thoracolumbar kyphosis (mean, 48 degrees; range, 35 to 70 degrees) was seen in the other five patients, who had a mean age of fifteen years (range, seven to twenty-four years). Four patients with the tarda-I type of osteogenesis imperfecta had thoracic kyphosis at the time of the most recent follow-up. They had a mean curve of 47 degrees (range, 40 to 55 degrees) and a mean age of twenty-six years (range, fifteen to thirty-nine years). At the time of the most recent follow-up, three patients who had the tarda-II type of osteogenesis imperfecta had thoracic kyphosis, with curves of 40, 64, and 69 degrees and mean ages of eighteen, thirty-four, and twenty-seven years, respectively.

Vertebral Deformities
Vertebral deformities were seen in thirty-three patients (75 per cent) on lateral roentgenograms made at the initial examination. These patients included the fifteen who had the congenita type, nine who had the tarda-I type, and nine who had the tarda-II type of osteogenesis imperfecta (Table I). Most of the biconcave vertebrae were seen at the mid-thoracic to lumbar levels. The flattened, wedged, and unclassifiable vertebrae tended to be seen at the mid-thoracic to thoracolumbar levels.

Relationship between Progression of Curves and Vertebral Deformities
Severe scoliosis (more than 50 degrees) was seen at the time of the most recent follow-up in eleven of the fifteen patients who had the congenita type of osteogenesis imperfecta (Table I). Initial roentgenograms demonstrated biconcave vertebrae in all eleven (Figs. 2-A, 2-B and 2-C). Ten of these patients had at least eight biconcave vertebrae, and one had three. Six of the eleven patients who had severe scoliosis at the time of the most recent follow-up and biconcave vertebrae on the initial roentgenograms had wedged vertebrae, involving a mean of two vertebral segments, and four had flattened vertebrae, also involving a mean of two vertebral segments. A 47-degree (moderate) scoliosis was seen in one patient (Case 1) at the time of the most recent follow-up, when she was nine years old. The initial roentgenogram of the spine, made at the age of two years, revealed fourteen biconcave vertebrae, one flattened vertebra, and one wedged vertebra. As this patient was still premenarchal and had had a 34-degree progression of the curve over a period of seven years, the curve was likely to progress further. No patient with the congenita type of osteogenesis imperfecta had mild scoliosis (a curve of less than 30 degrees) at the time of the most recent follow-up.

View larger version (128K): [in this window] [in a new window]   Figs. 2-A, 2-B, and 2-C: Case 13, who had the congenita type of osteogenesis imperfecta. Figs. 2-A and 2-B: Anteroposterior and lateral roentgenograms made when the child was twelve years old. There was moderate scoliosis, and the lateral roentgenogram shows a number of biconcave vertebrae.

View larger version (125K): [in this window] [in a new window]   Figs. 2-A, 2-B, and 2-C: Case 13, who had the congenita type of osteogenesis imperfecta. Figs. 2-A and 2-B: Anteroposterior and lateral roentgenograms made when the child was twelve years old. There was moderate scoliosis, and the lateral roentgenogram shows a number of biconcave vertebrae.

View larger version (139K): [in this window] [in a new window]   By the age of twenty-four years, a marked scoliosis was apparent.

Two patients with the tarda-I type of osteogenesis imperfecta had moderate scoliosis. One (Case 16) had two biconcave vertebrae in the lumbar spine and nine flattened vertebrae in the thoracic spine at the initial examination. At the time of the most recent follow-up, when the patient was fourteen years old, the scoliosis measured 45 degrees. The other patient (Case 21) had no biconcave vertebrae but had two wedged vertebrae at the initial examination. The scoliosis in this patient measured 30 degrees at the time of the most recent follow-up, at the age of sixteen years. Seven patients with the tarda-I type of osteogenesis imperfecta had mild scoliosis. One (Case 20) had two biconcave vertebrae at the initial examination and 5 degrees of scoliosis at the time of the most recent follow-up, at the age of fifteen years. Four patients who had mild scoliosis had no vertebral deformities. Severe scoliosis was seen less frequently in the patients who had the tarda-I type of osteogenesis imperfecta than in those who had the congenita type. Scoliosis may progress to a severe degree in the absence of biconcave vertebrae. However, if six biconcave vertebrae or more are present, severe scoliosis almost certainly develops, as illustrated by Cases 18 and 24.

None of the sixteen patients who had the tarda-II type of osteogenesis had a severe curve (Table I), and only one (Case 37) had a moderate one. This patient, who was nineteen years old at the most recent examination, had no biconcave vertebrae but had three flattened and three wedged vertebrae. Four patients had mild scoliosis. Another patient (Case 42) had three biconcave vertebrae, and thoracic kyphosis instead of scoliosis developed. Seven patients had no vertebral deformities. Thus, scoliosis was moderate or mild and progression of scoliosis was not common in patients who had the tarda-II type of osteogenesis imperfecta. No patient had more than three biconcave vertebrae.

Ten of the eleven patients with the congenita type and two of the four with the tarda-I type of osteogenesis imperfecta as well as severe scoliosis had at least six biconcave vertebrae (Table I). On the basis of this finding, we believe that the presence of at least six biconcave vertebrae may influence the severity of the scoliosis.

Thoracic and thoracolumbar kyphosis at the most recent examination was also classified into three groups: severe (80 degrees or more), moderate (between 60 and 79 degrees), and mild (between 40 and 59 degrees). Of the seven patients who had the congenita type of osteogenesis imperfecta and thoracic kyphosis at the time of the most recent follow-up, two had a severe kyphosis. Of these two patients, one (Case 11) had fourteen biconcave vertebrae at the initial examination. The other patient (Case 14) had only three biconcave vertebrae at the initial examination. In addition, this patient had two flattened, one wedged, and eleven unclassifiable vertebrae. Moderate thoracic kyphosis was seen in one patient (Case 15) at the time of the most recent follow-up. This patient had fourteen biconcave vertebrae at the initial examination. Four patients had mild thoracic kyphosis. They had a mean of thirteen biconcave vertebrae (range, eleven to sixteen vertebrae) at the initial examination.

The five patients with the congenita type of osteogenesis imperfecta who had thoracolumbar kyphosis had a mean of eleven biconcave vertebrae (range, eight to fourteen vertebrae) at the initial examination. The kyphosis progressed only moderately, and only one patient had a 70-degree kyphosis at skeletal maturity.

All four of the patients with the tarda-I type of osteogenesis imperfecta who had thoracic kyphosis at the time of the most recent follow-up had a mild curve. They had a mean of five biconcave vertebrae (range, zero to thirteen vertebrae) at the initial examination.

Of the three patients with the tarda-II type of osteogenesis imperfecta who had thoracic kyphosis at the most recent follow-up examination, two had a moderate curve. One of these two patients had three biconcave vertebrae and the other had no biconcave vertebrae at the initial examination. The third patient, who had mild kyphosis, had no biconcave vertebrae but had six wedged vertebrae at the initial examination. The kyphosis in this patient did not change.

In the whole group of forty-four patients, only two (Cases 11 and 14) had a severe kyphosis and only one (Case 11) had biconcave vertebrae involving a large number of segments (fourteen). Kyphotic and scoliotic curves were unrelated. Fifteen patients (eleven with the congenita type and four with the tarda-I type of osteogenesis imperfecta) had severe scoliosis, but only two of them had severe kyphosis. Biconcave vertebrae do not seem to influence kyphosis to the same extent as they do scoliosis.

	Discussion

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The prevalence of scoliosis in patients who have osteogenesis imperfecta is high, with a range of 39 to 100 per cent depending on the report^{1-4,8,10,11,13-15,18,20}. Scoliosis is recognized to be progressive, especially in patients who have the congenita type of osteogenesis imperfecta. Other investigators have reported that the curve is progressive and is associated with fractures of long bones, deformities of the chest, and the inability to walk^3-5,10,13-15. In the literature, little reference has been made to the behavior of the curve after the late teen-age years, and little is known concerning the prevalence and progression of kyphotic curves.

The pathogenesis of spinal deformities in osteogenesis imperfecta is still unknown, but in general spinal curvature and its progression are thought to be caused primarily by a combination of vertebral microfractures due to the fragility of the bones and injury to the vertebral growth plate. Ligamentous laxity, limb-length discrepancy, pelvic obliquity, and abnormalities of the discs are secondary factors^4,14,15. Changes in the vertebral bodies due to the fragility of the bones cause four different types of vertebral deformities. Biconcave vertebrae are probably caused by the pressure of the elastic nucleus pulposus on the brittle vertebral body. Wedged vertebrae may develop secondary to compression fractures. Flattened vertebrae may be caused by a combination of microfractures and the pressure of the disc, and unclassifiable vertebrae may be due to a combination of these factors^3,4,15.

In our series, the prevalence of scoliosis at the time of the most recent follow-up was high (68 per cent; thirty of forty-four patients). The natural history of scoliosis was generally consistent with that reported previously^{4,10,11,13-15,20}. Three patients (Cases 11, 13, and 15) who had a severe curve resulting from rapid progression before puberty and who were followed into adulthood had little or no progression of the scoliosis after puberty. As they had a severe curve, one reason for this phenomenon could be that the rib cage was close to the pelvis and thus prevented additional progression. Three patients with the congenita type of osteogenesis imperfecta had a severe spinal deformity, an unsatisfactory appearance, and deformities of the extremities, while three patients who had the tarda-I type of osteogenesis imperfecta had few or no deformities of the extremities, despite severe spinal deformity and an unsatisfactory appearance. This was probably because the latter patients had sustained fewer fractures during their years of growth.

Eighteen (41 per cent) of the forty-four patients had kyphosis at the time of the most recent follow-up. The kyphosis progressed with growth and mostly paralleled the progression of the scoliosis, although the severity of the kyphosis did not appear to be related to that of the scoliosis.

Previous reports have mentioned that biconcave vertebrae are a common feature in patients who have the congenita type of osteogenesis imperfecta^4,11,14. Biconcave vertebrae were commonly seen in the patients who had severe scoliosis in our series as well and were accompanied by marked widening of the disc space. In addition, severe scoliosis (a Cobb angle of more than 50 degrees) developed in all patients who had at least six biconcave vertebrae, except for a nine-year-old patient who had a 47-degree curve at the time of the most recent follow-up. As this patient was premenarchal and had had a 34-degree progression over a period of seven years, she was likely to have additional progression. The other vertebral deformities did not consistently affect the progression of scoliotic deformities as much as biconcave vertebrae did. Patients who had thoracolumbar kyphosis tended to have more biconcave vertebrae than those who had thoracic kyphosis. The presence of biconcave vertebrae did not appear to be related to the severity of the kyphosis to the same extent that it was related to the severity of the scoliosis.

	Footnotes

 
*No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. No funds were received in support of this study.

Department of Orthopaedic Surgery, Niigata University School of Medicine, Asahimachi-dori 1, Niigata-shi 951, Japan.

Department of Orthopaedic Surgery, Alfred I. duPont Institute, 1600 Rockland Road, P.O. Box 269, Wilmington, Delaware 19899.

Department of Orthopaedic Surgery, Hamagumi Medical and Educational Center for Handicapped Children, Suidocho 1-5932, Niigata-shi 951, Japan.

	References

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