Department of Orthopaedic Surgery, Princess Margaret Rose Hospital, Frogston Road West, Edinburgh EH10 7ED and
1 Department of Pathology, University Medical School, Teviot Place, Edinburgh EH8 9AG, UK
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Abstract |
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Methods. The right sacroiliac joints of 15 adult patients were examined post-mortem. HOME (Highly Optimized Microscope Environment) microscopy was used to measure articular cartilage and subchondral bone end-plate thickness. Conventional morphometric techniques were employed to estimate cartilage cellularity and cancellous bone density.
Results. Sacral articular cartilage was thicker than iliac (1.81 vs 0.80 mm, P<0.001). Iliac cartilage cell density in all zones was higher than sacral. The overall mean was 31.19x10-3 vs 23.23x10-3/mm3, P<0.001. Superficial zones contained more cells than middle and deep zones but there were large differences between the cell numbers of the middle and deep zones of both sacral and iliac cartilages. Iliac subchondral bone end-plates were thicker than sacral (0.36 vs 0.23 mm, P<0.001). The thickness of these plates was related inversely to that of the overlying articular cartilages. Iliac subchondral cancellous bone was twice as dense as sacral (22.07 vs 12.05%, P<0.001), a ratio recognized anteriorly, centrally and posteriorly.
Conclusions. Adult human sacral cartilage is thick and of low cell density. It rests upon a thin bone end-plate supported by porous, cancellous bone. Iliac cartilage and bone display the converse proportions. The identification of these variables may assist understanding of normal sacroiliac joint function and the interpretation of tissue changes in the spondylarthropathies.
KEY WORDS: Sacroiliac joint, Cartilage, Bone, Morphometry, HOME microscopy, Laser scanning microscopy.
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Introduction |
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Measurements of the circumference, area and diameter of the bearing surfaces of normal human sacroiliac articulations can be made readily by the naked eye. They have been reported on several occasions [59]. Conspicuous differences between the thicknesses of the sacral and iliac cartilages have been recorded [511]. By contrast, there have been relatively few microscopic studies of normal SI joints [12]. As one consequence, records of the cellularity of the sacral and iliac articular cartilages [13] and of the thickness and density of subchondral sacral and iliac bones are rare. The present studies were made to remedy this deficiency. Some of the results have been presented in preliminary form [14, 15].
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Materials and methods |
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Dissection
The upper part of each left femur was divided transversely. The right innominate bone was transected 30 mm lateral to the right sacroiliac joint and the pelvis was excised by cutting through the L3L4 interface. The vertebral column was divided sagittally. Four to 11 slab blocks were cut at right angles to this plane of section, the number varying with the size of the individual. The blocks were fixed in buffered formalin at pH 7.0 before decalcification in EDTA (ethylenediamine tetraacetic acid). From each block, semiserial sections were prepared and stained differentially with haematoxylin and eosin, toluidine blue, picro-Sirius red, phosphotungstic acid/haematoxylin, Martius scarlet blue and alkaline Congo red. The mean anteroposterior length of the 15 SI joints was 23.40±11.72 mm.
Cartilage thickness
The thickness of the sacral and iliac articular cartilages was measured with a Zeiss Highly Optimised Microscope Environment (HOME) system in 66 sections. Cartilage thickness (the distance from the bearing surface to the chondro-osseous junction) was recorded at 11 equidistant points along the anteroposterior axis of the sacral and iliac cartilages, giving a total of 1452 measurements. Integration of the measurements at points 1, 2 and 3; at 5, 6 and 7; and at 9, 10 and 11 allowed direct comparison with those of cartilage thickness.
Section thickness
Section thickness was measured with a Zeiss LSM laser confocal scanning microscope and x40 water-immersion objective lens. The precision of the microscope measurements was tested against a Mitutoyo metal block standard. Measurements were made in the z-axis mode, using an argon ion laser. Brightness (blue) and contrast (red) were balanced. Observer error was assessed by repetitive measurements at single sites. From each case, slides representing five different staining techniques were taken. A total of 750 determinations was made. The mean thickness of 75 sections was 11.002±4.38 µm (SD).
Cell numbers
The numbers of cells, nuclei and empty chondrocyte lacunae were recorded by conventional light microscope and eyepiece graticule in 62 sections of sacral and iliac cartilage. The number of empty lacunae (on average 0.3 per field) had no influence on any analysis and was discarded. Differences between nuclear and cellular counts were minimal. Only counts of whole cell numbers were therefore considered.
Sections were divided into three equal superficial, middle and deep cartilage zones and subdivided into nine equal anteroposterior segments. Cell counts were made in each of these areas. From these 27 areas, 3348 measurements were therefore obtained. The results were adjusted for section thickness and expressed as cellsx10-3/mm3.
Bone thickness
Sacral and iliac bone end-plate thickness was measured at the 11 points selected for assessing cartilage thickness. Sites were chosen where marrow cavities lay closest to the deepest aspects of the articular cartilage. The areas delineated by the tide-line and by the bone margin were included in the counting procedure. A total of 1452 bone thickness measurements was recorded and expressed in millimetres.
Bone density
A Weibel eyepiece graticule engraved with 42 lines [16] was used within a Leitz Orthoplan microscope. The graticule was positioned so that its inner edge lay immediately beyond the outermost margin of the subchondral bone end-plate. Care was taken to avoid dense, cortical bone. In each of 69 sections, linear intercept counts were made of sacral and iliac bone. Fields encompassed the anterior, middle and posterior parts of the subarticular, cancellous bone. A total of 414 fields was therefore counted. The results were expressed as the mean percentage of the fields occupied by bone trabeculae.
Statistics
There was an asymmetrical, non-normal distribution of data (Fig. 1). The MannWhitney procedure was therefore used, within Minitab v. 12, to test the significance of differences between samples. In searching for the possible influences of age, sex and location, regression analysis was employed to take account of unequal replication and missing values. Statistical significance was accepted at the 5% level.
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Results |
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Chondrocyte numbers
Iliac cartilage was more cellular than sacral (Table 1; Fig. 3
). Cell numbers of superficial zones of both sacral and iliac cartilage were greater than those of the corresponding middle and deep zones. The cellularity of each of the three iliac cartilage zones (superficial, middle and deep) was greater than that of the corresponding sacral zone. Cell density declined from the superficial to the deep zone. However, the degree of this difference varied. There was a smaller reduction in cellularity from the surface downwards in iliac cartilage than in sacral cartilage. There was no demonstrable relationship between age or the anteroposterior or superoinferior position of the sample within the joint and the cellularity of sacral or iliac cartilage.
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Bone end-plate thickness
End-plate iliac bone was thicker than end-plate sacral bone (Table 1). Male iliac bone end-plates were thicker than female iliac end-plates. There was no demonstrable relationship between end-plate bone thickness and age or between the anteroposterior or superoinferior position of the sample within the joint and this variable. An inverse relationship between bone end-plate thickness and overlying cartilage thickness was observed consistently.
Bone density
Subchondral, iliac cancellous bone density was greater than sacral (Table 1). This relationship was confirmed at each of the anterior, central and posterior parts of the joint. However, differences between the three parts of the individual sacral and iliac bones did not reach acceptable levels of significance.
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Discussion |
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Understanding of the structure and function of the human SI joints has progressed slowly, over many years. Meckel [17] first described the articulations in 1816. Although their diarthrodial nature was claimed by Luschka in 1854 [18], their synovial character remained contentious until modern times. The unusual shape and size of the paired joints was recognized more than a century ago [19]. Early workers recorded the most obvious anatomical features of the joints: their oblique position, the boomerang shape of the load-bearing surfaces, and the distinct appearances and unequal thickness of the sacral and iliac bearing surfaces. Inequalities of sacral and iliac cartilage thickness were detected early in life and the contrasting dimensions of embryonic and infantile sacral and iliac cartilages were established [8, 12]. Age-related structural divergences persisted and increased. In children and young adults, the sacral cartilage was 46 mm in thickness; it was greater anteriorly than posteriorly [20]. By contrast, the iliac cartilage was no more than 2 mm in thickness. This ratio continued into the second decade [21], during which sacral and iliac measurements of 23 and 1.5 mm [22] or 14 and 0.52 mm [20] were described, respectively. By 6069 yr of age, these figures became 23 and <1.0 mm respectively, while in those aged more than 70 yr they were 1.5 and 0.5 mm [22].
The thicker sacral cartilage closely resembles that of the large limb joints [23]. The thinner iliac cartilage is quite different. It is less rich in proteoglycan and is interspersed with dense, tangential and perpendicular collagen bundles that often extend to the bone end-plate. The differential features of male and female joints have been documented [24], as have those of some racial and ethnic groups [25]. Generally, however, evidence of anatomical distinctions between male and female SI joints is still inconclusive. In the present study, the influence of sex on cartilage thickness could not be substantiated, possibly because the numbers of cases studied was small. Because of incomplete data, it has not been possible to apply correction factors for body mass or stature.
Conventional radiology has been used extensively in the clinical analysis of diseased SI joints [26, 27] but reveals limited structural detail and then only long after the onset of symptoms. The advent of non-invasive magnetic resonance imaging (MRI) [28, 29] has offered new scope for early diagnosis and has made it increasingly possible to correlate structure and function. Braun et al. [30] have employed dynamic MRI with fast imaging. The technique offers a clear advantage over CT scanning in the evaluation of cartilage disease, although the precise measurement of joint space and cartilage thickness has proved difficult. In a MRI study of 114 children with no clinical evidence of sacroiliitis, Bollow et al. [28] have shown that the width of the adolescent SI joint is, on average, 4 mm, a figure closely similar to that obtained in adult joints. In this investigation, the sacral cartilage is reported as approximately 3 mm in thickness, the iliac cartilage approximately 1 mm.
Braun et al. [30] are careful to emphasize that, in the clinic, confirmatory morphological evidence of phenomena observed by MRI is not yet available; there is a lack of direct correlation between histological and scanning results and no gold standard [28]. There are several reasons for this deficiency. First, very few controlled microscopic analyses of sacroiliac joint structure have been made [4]. Secondly, it is difficult to obtain the necessary post-mortem material. The SI joints cannot easily be examined directly in the living patient. Much of the evidence rests upon autopsy enquiries. Thirdly, although many needle biopsy investigations of SI joint synovia have been made, sacroiliac joint surgery is uncommon and cartilaginous tissue is rarely sampled. Fourthly, it is unethical to undertake contrast-enhanced MRI studies of the sacroiliac joints in entirely normal individuals or even in patients with unrelated diseases, such as cancer [28].
A serious problem in the use of MRI for the measurement of SI joint cartilage thickness remains the limited resolution of MRI scanners. In the majority of cases, a 3 mm slice is required to yield a resolution of 11.5 mm. The resolution of scanners varies but is determined principally by the filling factor of the detector coil [L. Hall, personal communication]. This factor is high in relation to small joints, such as those of a finger, and low in relation to large joints, such as those of the hip and pelvis. Whereas the best plane resolution in a 1-mm slice of distal interphalangeal joint is 75 µm and that of a 1-mm slice of knee joint
300 µm, the resolution of a 1-mm slice of hip joint may be no more than
1500 µm. This constraint contrasts with the much higher resolution of the light microscope lenses used in the present study, in which, in theory, the physical limit is that of the wavelength of the light source. This limit is
300 nm, the diameter of a staphylococcus.
To a small but encouraging extent, it has been shown that the horizons of conventional MRI can be extended but, so far, only in the laboratory. Xia et al. [31] have demonstrated that, by scaling down the receiver coil of a Bruker AMX 300 NMR (nuclear magnetic resonance) microscope equipped with a 7-tesla/89-mm vertical-bore superconducting magnet and microimaging accessory, they can obtain a pixel resolution of 10 µm. Xia et al. describe the technique variously as NMR microscopy, microscopic MRI or µMRI. Using this technique, they have made an in vitro analysis of canine humeral cartilage. Comparing their µMRI results with those of polarized light microscopy, they have shown that articular cartilage zones are statistically equivalent to cartilage collagen fibre orientation assessed by polarized light microscopy. To what extent the possibilities raised by this investigation can be applied clinically is a matter for further research.
The SI joints play a crucial role in the pathogenesis of the spondyloarthropathies, in particular of AS, and it is to be hoped that the methods of morphometry may contribute to further understanding of the microscopic properties of the joint components. In an investigation of the structural changes in AS [4], active, peripheral and central cartilage destruction and severe basal cartilage injury were recognized with greater frequency in affected patients than in control subjects. Although observed and graded subjectively, the cartilage changes in the diseased tissues could not be measured adequately. There were two reasons. Only three patients with AS had a disease duration of less than 3 yr and many other abnormalities, including in particular chondroid fusion, made attempts at cartilage morphometry technically difficult.
Full understanding of the structure and function of the normal SI joints is still incomplete. For example, there is only a single account of the chemical composition of the sacral and iliac cartilages [10]. The sacral and iliac moieties are parts of a complex shock-absorbing system that protects the mammalian brain and spinal cord against diurnal static and impact forces. The congruent nature of the articulation, with each opposed bearing surface wholly in contact with the other, suggests strongly that forces derived from a sacral direction are transmitted equally and uniformly to the iliac cartilage surfaces. The evidence presented in this report highlights the paradoxical nature of SI joint structure: if the forces applied to both bearing surfaces are identical, why is their structure so different? One explanation for this enigma may lie in postulating differential responses by the sacrum and ilium. The open, porous, bone of the former contrasts with the immensely strong, dense bone of the latter. The deformable sacrum can be viewed as a cushion in a sacroiliac shock-absorbing system, transmitting loads but not absorbing them. The non-deformable (elastic) ilium, by contrast, is responsible for absorbing the forces imposed by the weight of the upper half of the body in all upright and semi-upright positions, and for transmitting these forces to the legs and feet.
In conclusion, investigations of the SI joints should now be extended by taking advantage of continued advances in the techniques of imaging and microscopy. By these means, and by the investigation, in parallel, of non-human mammals, it should prove possible to analyse the components of the SI joints in greater detail and to extend to their understanding new micromechanical, immunohistochemical, cytogenetic and molecular biological techniques. The correlation of the biological properties of the extracellular matrix components of the SI joints with the selective distribution and nature of individual cells is likely to permit a fuller understanding of the role of these structures in modulating compressive and shear forces at the junction between the vertebrae and the pelvis and in explaining their disorganization in diseases such as AS. Investigations to fulfil these aims are in progress.
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Acknowledgments |
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Notes |
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Correspondence to: D. L. Gardner.
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References |
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