Journal of Orthopaedic Research 4~452-457, Raven Press, New York 0 1986 Orthopaedic Research Society

Pathogenesis of Osteochondrosis Juvenilis Scheuermann

M. Aufdermaur and M. Spycher

Institute of Pathology, Lucerne, and Department of Pathology, University of Zurich, Zurich, Switzerland

Summary: In osteochondrosis juvenilis Scheuermann, foci of various sizes in the cartilaginous end plates of the vertebral bodies display a loosening or complete interruption of the collagen fibers. These findings, together with an alteration and occasional absence of the growth zone, may result in the typical deformation of the vertebral bodies. Electron micrographs of the areas with optically absent collagen fibers reveal collagen fibrils. They are arranged in an irregular pattern. We conclude that a disturbance of collagen or ground sub- stance biosynthesis is of importance in the pathogenesis of juvenile osteo- chondrosis. Key Words: Spine-Osteochondrosis-Scheuermann’s Disease -Vertebra- Electron microscopy- Collagen fibers- Collagen fibrils.

The most important sign of osteochondrosis ju- venilis (OJ) is an irregular course of the end plates of the affected vertebral bodies (4). There may also be interruptions of end plates with herniations into vertebral bodies, wedge-shaped vertebrae, and a thoracic kyphosis. In histological sections, the col- lagen fibers of the cartilaginous end plates are partly absent ( 1 - 3 3 ) . These areas were investi- gated by electron microscopy in order to establish whether collagen is present in these particular areas.

MATERIALS AND METHODS

One hundred vertebral columns were obtained at autopsy. At the time of death, the patients were 8-20 years old. Furthermore, 31 spines from neo- natal to 7-year-old children have been examined. The spines were sawed sagittally and lateral radio- graphs of both halves were made. The specimens were sectioned in planes parallel to the sagittal sur-

Address correspondence and reprint requests to Dr. M. Auf- dermaur at Institute of Pathology, CH-6004 Lucerne, Switzer- land.

Dedicated to Ruth Silberberg on the occasion of her 80th birthday.

face and decalcified in EDTA. For histologic exami- nation, the samples were fixed in formalin, em- bedded in paraplast or gelatine, and processed in accordance with routine methods. The stains used included haematoxylin and eosin, van Gieson, and silver and alcian blue. Samples of the end plates of vertebrae with distinct radiologic signs of OJ origi- nating from nine males aged 15-20 years were se- lected for the electron microscopic examination. The specimens were fixed with buffered glutaralde- hyde, decalcified in EDTA, and processed in accor- dance with routine methods.

RESULTS

Radiologic and Clinical Findings

Five of the hundred spines display striking radio- logic signs of OJ (Fig. 1). The end plates of the ver- tebrae protrude into the vertebral bodies. There are interruptions of end plates with prolapses of inter- vertebral disc tissue into the vertebral bodies. The adjoining vertebral bone is sclerosed. Clinically, one of these five patients was known to have suf- fered from back pain for 1 year (Fig. 1) . From the other individuals, results of clinical examination

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FIG. 1. Juvenile osteochondrosis. A: Lateral radiograph of the formalin fixed vertebral column from T 7 to L 1. Pin at T 718. lntervertebral spaces bulge into the vertebral bodies. Adjoining bone sclerosed. End plates discontinuous in places. 6 : Interver- tebral disc T 1011 1. Cartilage plates narrowed in the areas of bulging, collagen fibers lacking. van Gieson, x3. C: Same slide as B at higher magnification. Collagen fibers of the cartilaginous plate on the left side preserved, absent on the right. x43. D: lntervertebral disc T 12/L 1. Cartilage plates at the areas of bulging narrowed, but not interrupted; collagen fibers loosened and absent. van Gieson, x2.5. E: Same slide as Fig. 1D at higher magnification. Collagen fibers of the end plate on the left side preserved, in the middle loosened, on the right missing (male, 20 years) x30.

were not available. The spines of 17 patients repre- sented transitional radiographic forms between OJ and normal spines. The remaining vertebral columns showed no radiological evidence of OJ.

Histological Findings

In the samples with characteristic radiographic changes of OJ, the end plates are bent toward the

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vertebral bodies. They are partly undulated (Fig. 1B and D) and partly straight (Fig. 2). In these parts, the collagen fibers of the cartilaginous end plates are partly or totally missing. The growth zone is narrowed or completely missing. At these places, collagen fibers of loosened cartilaginous areas pass into the fibers of the vertebral bone. The cartilage cells are preserved and so is the ground substance, stained with alcian blue. Areas without collagen fibers are seen, with one exception, in the spines without radiologic signs of OJ; their number and size is small in these cases.

Ultrastructural Findings

In histologically normal sites of the cartilaginous end plates, the matrix consists of collagen fibers and an electronlucent ground substance containing numerous proteoglycan granules (Fig. 3 ) . The fibers are composed of densely-packed collagen fi- brils varying in diameter (20-40 nm) and running predominantly parallel to the fiber axis. The fibrils reveal a periodic cross-banding of about 65 nm.

In histologically loosened areas, the collagen fibers are seen to taper off. Amorphous osmiophilic material often follows the collagen fibers, envel- oping the fibrils or arranged as dispersed interfibril- lary granular masses (Fig. 4). Outside of the fibers, collagen fibrils are arranged irregularly within the ground substance (Fig. 5) .

Even in areas with a complete lack of collagen fibers, however, collagen fibrils are also present in

FIG. 2. Juvenile osteochondrosis. lntervertebral disc T 9/10. Cartilage plates narrowed. At T 9 two Schmorl's nodes and at T 10 end plate displaced into the vertebral body; adjoining bone is sclerosed (male, 17 years). van Gieson, x 5.

all of the samples investigated (Fig. 6). In contrast to fiber areas they form a loose feltlike network. The fibrils exhibit the same characteristics as those of the fiber areas, although the accompanying dense interfibrillary masses are not observed. Pro- teoglycan granules, however, are present.

DISCUSSION

Defects of collagen fibers in cartilaginous tissue have only been observed in the cartilaginous end plates of human vertebral bodies. In numerous au- topsied individuals and in biopsies we have never

FIG. 3. Low-power micrograph with part of collagenous fiber in the cartilaginous end plate at the site of fiber interruption. The fiber is composed of parallel running collag- enous fibrils (F) and of granular interfibrillar osmiophilic masses. Bar = 1 pm, T 121L 1 (male, 18 years). x 10,400.

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FIG. 4. Terminal part of a collagenous fiber with parallel fibrils and some interfibrillar granular masses. Beyond the fiber col- lagenous fibrils run in any direction. At sites of fiber interruptions, tufted fibril formations are seen (arrows). Bar = 1 pm, T 12/L 1 (male, 18 years). x 13,400.

seen this alteration anywhere else, particularly not in the cartilage of any diarthric joint. However, areas without collagen fibers have been detected in 99 of the examined 100 spines. From the 8th year of age onwards, they can be seen almost in every ver- tebral column. Their number and size increase in

the thoracic spine in the craniocaudal direction. In the lumbar spine, they may also be conspicuous (1). Therefore, the lack of collagen fibers is not spe- cific for OJ. There is a striking quantitative differ- ence, however, as spines without radiological signs of OJ display only minor histological defects.

FIG. 5. Cartilage matrix at site of fiber inter- ruption with feltlike fibrillary network. Bar = 1 km, T 12/L 1 (male, 8 years). x 11,730.

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Moreover, there is a marked correlation between the radiologic signs of OJ and the number and size of the histological findings (1,3).

The bending segments may be discontinuous. At these places intervertebral disc tissue is prolapsed into the vertebral bone marrow. The amount of the herniated disc material is variable. Prolapses may be microscopic or even detectable as single or mul- tiple by the naked eye (Figs. 1B and 2). Some end plates are regularly bulging but not discontinuous, particularly in the lowest thoracic and upper lumbar spine (Fig. 1D). Radiologically, the finding is described as Schmorl’s nodules. Yet, histologi- cally it does not always present as nuclear prolapse but, without exception, as areas with deficient or even lacking collagen fibers (Fig. 1D and E). The irregular course of the end plates in radiographs is particularly due to their indentations into the ver- tebral bodies.

Chondrocytes and the acid proteoglycans of the ground substance are present in the areas without collagen fibers. Chondrocytes with shadows and pycnoses of nuclei are of no significance as these findings are also to be observed from the 7th and 8th year of life in persons without signs of OJ. By silver staining, irregularly arranged delicate fibrils may be demonstrated. Electron micrographs reveal

FIG. 6. High-power micrograph of the same region as shown in Fig. 4. The characteristic banding of the collagenous fibrils is clearly visible (arrows). Bar = 1 km, T 12/L 1 (male, 18 years). ~28,140.

the presence of irregularly arranged collagen fibrils. Recently, Ippolito et al. (6) described similar obser- vations made in biopsy specimens obtained from seven 14- 16?h-year-old patients with OJ. These findings suggest that a defect may exist in collagen biosynthesis (2).

The abnormal cartilage matrix contains abundant acid proteoglycans (1 3, histochemically scanty glycoproteins, collagen, and basic proteins (5). These histochemical reactions are different from those in the areas containing collagen fibers. The suggestion of a local disturbance in the biosynthesis of matrix components restricted to the cartilaginous end plates of the human vertebrae is confirmed by these findings.

Areas without or with very few collagen fibers may occur in segments that are not bent into the vertebral body, whereas a bulging of the end plate is only to be seen at sites with few or no collagen fibers. Moreover, prolapses of intervertebral disc tissue into vertebral bodies occur only in places with a narrow end plate where collagen fibers are absent (Figs. 1B, 2). The strength of hyaline carti- lage tissue is based on the presence of collagen fibers (7,8). Their partial or complete absence and their compensation by irregularly arranged fibrils result in a reduced mechanical strength of the carti-

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lage. The weakening of the end plates permits her- niations of nuclear tissue into the bone marrow of the vertebral bodies.

2. Aufdermaur M: Pathologische Anatomie und Pathogenese der Scheuermann-Kyphose. In: Die Wirbelsbule in For- schung und Praxis, ed by H Junghanns. Stuttgart, Hip- uokrates, 1976. 60:55-65

The growth zone adjoining an abnormal area of the vertebral end plate is of irregular structure or even absent (I -33). Thus, the enchondral ossifica- tion is altered in these areas and the growth of the vertebrae appears to be stunted. The height of vertebral bodies is totally or locally diminished (Fig. 2).

All these findings may be of importance in the pathogenesis of OJ, whereas the cause is unknown.

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REFERENCES 8.

1. Aufdermaur M: Zur Pathogenese der Scheuermannschen Krankheit. Dtsch Med Wschr 89:73-76, 1964

Aufdermaur M: Juvenile Kyphosis (Scheuermann's dis- ease): radiology, histology, and pathogenesis. Clin Orthop

Epstein B: The Spine, 4rh ed., Philadelphia, Lea & Febiger,

Ippolito E, Ponseti IV: Juvenile kyphosis. J Bone Joint Surg [Am] 63:175-182, 1981 Ippolito E, Bellocci M, Montanaro A, Ascani 6, Ponseti IV: Juvenile kyphosis: An ultrastructural study. J Pediatr Orthop 5:315-322, 1985 Pauwels F: Gesammelte Abhandlungen zur funktionellen Anatomie des Bewegungsapparates. Springer, Berlin Hei- delberg New York, 1969, pp 424-479 Sokoloff L: The Biology of Degenerative Joint Disease. Chicago, London, University of Chicago Press, 1969, pp 31-44

154:166-174, 1981

1976, pp 611-616

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