The Journal of Bone & Joint Surgery

The Journal of Bone & Joint Surgery, Volume 88, Issue 4

Scientific Articles | April 01, 2006

Morphological Changes of Collagen Fibrils in the Subsynovial Connective Tissue in Carpal Tunnel Syndrome

Jinrok Oh, MD¹; Chunfeng Zhao, MD¹; Mark E. Zobitz, MS¹; Lester E. Wold, MD¹; Kai-Nan An, PhD¹; Peter C. Amadio, MD¹

¹ Biomechanics Laboratory, Division of Orthopedic Research (J.O., C.Z., M.E.Z., K.-N.A., and P.C.A.), and the Department of Pathology (L.E.W.), Mayo Clinic, 200 First Street S.W., Rochester, MN 55905. E-mail address for P.C. Amadio: pamadio@mayo.edu

View Disclosures and Other Information

In support of their research for or preparation of this manuscript, one or more of the authors received grants or outside funding from the National Institutes of Health (NIAMS AR 49823) and the Mayo Foundation. None of the authors received payments or other benefits or a commitment or agreement to provide such benefits from a commercial entity. No commercial entity paid or directed, or agreed to pay or direct, any benefits to any research fund, foundation, educational institution, or other charitable or nonprofit organization with which the authors are affiliated or associated.

Investigation performed at the Biomechanics Laboratory, Division of Orthopedic Research, and the Department of Pathology, Mayo Clinic, Rochester, Minnesota

The Journal of Bone and Joint Surgery, Incorporated

J Bone Joint Surg Am, 2006 Apr 01;88(4):824-831. doi: 10.2106/JBJS.E.00377

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Abstract

Background: Pathologic changes occur commonly in the subsynovial connective tissue in patients with carpal tunnel syndrome. The purposes of this study were to investigate the ultrastructural changes of the subsynovial connective tissue in these patients and compare them with the findings in cadaver controls.

Methods: The diameter and density of collagen fibrils were measured by transmission electron microscopy in specimens of subsynovial connective tissue from ten patients with idiopathic carpal tunnel syndrome and from ten fresh-frozen cadavers of individuals without known symptoms of carpal tunnel syndrome.

Results: We noted deformed collagen fibrils with a spiraled appearance in the specimens from the patients. We also observed phagocytosis of elastin fibrils in all of those specimens. These changes were noted only rarely in the cadaver controls. The mean diameter (and standard deviation) of the collagen fibrils was 45.5 ± 8.0 nm in the control group and 54.8 ± 15.2 nm in the patient group (p < 0.05). The mean number of collagen fibrils per 0.04 µm² (density) was 201.38 ± 48.88 in the control group and 157.08 ± 54.38 in the patient group (p < 0.05).

Conclusions: These ultrastructural findings suggest that subsynovial collagen in patients with carpal tunnel syndrome is structurally different from that in individuals without carpal tunnel syndrome, but the processes resulting in that abnormal morphology remain to be elucidated.

Level of Evidence: Prognostic Level III. See Instructions to Authors for a complete description of levels of evidence.

Figures in this Article

The subsynovial connective tissue in the carpal tunnel is highly specialized for tendon gliding and tendon nutrition^1,2. In patients with carpal tunnel syndrome, commonly encountered pathologic findings in the subsynovial connective tissue include proliferation with thickening of the tendon sheath, fibrosis, and vascular lesions, including thickening of vessel walls, intimal hyperplasia, vascular proliferation, and thrombosis^3-9. These pathological changes are caused by interactions of cells and extracellular matrix components such as collagen, elastin, and proteoglycans^1,7,10,11. In general, fibrotic changes closely correlate with overproduction and structural changes of collagen^12-16. However, the ultrastructural changes of the collagen fibrils in the subsynovial connective tissue have not been reported. In this study, the morphological changes of the collagen fibrils in the subsynovial connective tissue of patients with idiopathic carpal tunnel syndrome were analyzed with use of transmission electron microscopy and were compared with the structure in cadaveric tissue from individuals with no history of carpal tunnel syndrome.

Materials and Methods

Materials and Methods | Results | Discussion | References

Ten specimens of subsynovial connective tissue were obtained from ten patients with idiopathic carpal tunnel syndrome during open carpal tunnel release, and ten specimens of subsynovial connective tissue were obtained from fresh-frozen cadavers. Ten consecutive patients who had a synovial biopsy during carpal tunnel surgery and who did not have a history of diabetes, thyroid disease, rheumatoid arthritis, osteoarthrosis, gout, hemodialysis, a body mass index of >30, sarcoidosis, amyloidosis, peripheral nerve disease, or traumatic injuries to the ipsilateral arm were selected. This was not a randomly selected group as, in each case, the surgeon decided to perform a synovectomy or synovial biopsy, usually to mobilize an adherent median nerve or to remove thickened synovium that was thought to affect tendon function. In some patients, a synovial biopsy was done to rule out amyloidosis or other conditions; such specimens were included if the conditions were indeed ruled out, leaving an idiopathic diagnosis. A review of available medical records for the selected cadavers was performed in order to exclude any cadavers of individuals with an antemortem diagnosis of carpal tunnel syndrome, as well as to confirm that they met the same exclusion criteria. The ages of the patients ranged from forty-nine to sixty-seven years (mean, 59.4 years), and the ages of the controls at the time of death ranged from sixty-eight to eighty-four years (mean, seventy-five years). The mean age of the patients was significantly (p < 0.05) less than that of the controls. This study was approved by our institutional review board.

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Figs. 1-A through 1-D: Subsynovial connective tissue from a patient with carpal tunnel syndrome. Fig. 1-A Phagocytosis. Note the variation in the fibril diameter in the cell (×50,000). CF = collagen fibrils, N = nucleus, LV = lysosomal vacuole, and ICM = intracellular microfibril. Fig. 1-B Elastolysis, with blunt margin and elastin debris in the vacuole inside the cell (×12,000). Fig. 1-C Higher magnification of Figure 1-B (×60,000). E = elastin, EL = elastolysis, C = cell, and ICM = intracellular microfibril. Fig. 1-D Normal elastin with sharp margin (×10,000).

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Figs. 2-A, 2-B, 2-C, and 2-D: Figs. 2-A and 2-B Normal subsynovial connective tissue from a cadaver specimen shows the uniform diameter of the collagen fibrils (×50,000). Fig. 2-A Longitudinal section. Fig. 2-B Transverse section. Figs 2-C and 2-D Subsynovial tissue from a patient with carpal tunnel syndrome shows the uneven thickness of the collagen fibrils (×50,000). Fig. 2-C Longitudinal section. Fig. 2-D Transverse section.

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Tissue Preparation for Transmission Electron Microscopy

Biopsy specimens were fixed overnight in 0.1% glutaraldehyde and 4% formaldehyde in 0.1-M phosphate buffer at pH 7.2. After primary fixation, tissues were rinsed in 0.1-M phosphate buffer, followed by postfixation in phosphate-buffered 1% osmium tetroxide. After rinsing in three changes of distilled water, the tissue was stained en bloc with 2% uranyl acetate at 60°C. The tissues were rinsed in distilled water, dehydrated in progressive concentrations of ethanol and propylene oxide, and embedded in Spurr resin¹⁷. The resin was polymerized at 65°C. Thin sections were mounted on copper grids for evaluation with a transmission electron microscope (JEOL 1200; JEOL USA, Peabody, Massachusetts).

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Figs. 3-A and 3-B: The diameter of the collagen fibrils in the specimens from each cadaver control and from each patient with carpal tunnel syndrome (CTS). The short line within the data points represents the mean value. The density of the collagen fibrils in the specimens from each cadaver control and from each patient with carpal tunnel syndrome. The short line within the data points represents the mean value.

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Figs. 4-A and 4-B: Distribution of the diameters of the collagen fibrils in the subsynovial connective tissue in specimens from the normal controls and from patients with carpal tunnel syndrome. Distribution of the density of the collagen fibrils in the subsynovial connective tissue in specimens from the normal controls and from patients with carpal tunnel syndrome.

Data Collection

For the ultrastructural study of the collagen fibrils, photographs were made of eight regions in which transversely cut collagen fibrils were visible at a magnification of 50,000 for each specimen grid. Each of three individuals, who were not otherwise associated with this study, selected one of the eight images per specimen for analysis, resulting in three of the eight images per specimen ultimately selected for analysis. As a result of the selection process, our two reviewers, an orthopaedic surgeon and a pathologist, who reviewed the images together, were blinded to the source of the images.

The diameter of the collagen fibrils was measured with use of Adobe Photoshop (version 6.0; Adobe Systems, San Jose, California). The digital image was placed in a Photoshop window and was overlapped by a dotted grid composed of ten columns and ten rows to randomly select collagen fibrils to be measured. The number of collagen fibrils per unit area was then calculated from the resulting images. The results per specimen were averaged for statistical analysis.

Statistical Analysis

The information was entered into a database, and statistical analysis was done with the SSPS software program (version 10.0 for Windows; SPSS, Chicago, Illinois). The data on the subjects were compared with use of t tests for continuous variables. All statistical tests were two-sided and p values of <0.05 were considered significant. The results are reported as the mean and the standard deviation unless otherwise indicated.

Results

Materials and Methods | Results | Discussion | References

Findings on Transmission Electron Microscopy

Two kinds of cells were observed in the subsynovial connective tissue: fibroblast-like cells and macrophage-like cells. The macrophage-like cells had many vacuoles, especially in the specimens from the patients with carpal tunnel syndrome. Intracellular microfibrils were observed in the vacuoles in the specimens from the patients, suggesting phagocytosis (Fig. 1-A). We also noted elastin within the cells in the patient group, suggesting elastolysis (Figs. 1-B, 1-C, and 1-D).

In the extracellular space of the control specimens, there were collagen bundles with characteristic periodic, striped collagen fibrils and microfibrils spanning the extracellular space (Fig. 2-A). Transversely sectioned collagen bundles were round in shape, with a clear margin (Fig. 2-B). Longitudinally sectioned collagen bundles showed an even diameter, without any distortion of the fibrillar stripe pattern (Fig. 2-A). However, in the patient group, abnormal collagen bundles, uneven in diameter and thickness, were observed (Figs. 2-C and 2-D). These collagen bundles were quite similar to the so-called spiraled collagen described by Ghadially¹⁸, with an irregular margin in transverse section and variable thickness in longitudinal section. Abnormal collagen in a spiral shape was found in all ten samples from the patients with carpal tunnel syndrome but only rarely in the cadaver specimens. The diameter of the collagen fibrils had a wider range in the patients than in the controls.

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Quantitative Analysis of Collagen Diameter

Thirty randomly selected photographs were analyzed in each group. There were 2029 collagen fibrils measured in the control group and 2180 collagen fibrils measured in the patient group. The mean diameter of the collagen fibrils was 45.5 ± 8.0 nm in the control group and 54.8 ± 15.2 nm in the patient group. The diameter of the collagen fibrils was significantly larger in the patients than in the controls (p < 0.05). Although the mode of diameter distribution in both groups was approximately 45 to 50 nm, the distribution graph for the patient group skewed to a larger mean diameter compared with that of the control group (Figs. 3-A and 4-A).

Quantitative Analysis of Collagen Density

Ninety randomly cropped photographs in each group were analyzed. The mean number of collagen fibrils per 0.04 µm² (density) was 201.38 ± 48.88 in the control group and 157.08 ± 54.38 in the patient group. The mean collagen density in the patient group was significantly lower than that in the control group (p < 0.05). The modal density in the control group was approximately 250 to 260 collagen fibrils per 0.04 µm². However, in the patient group, the distribution was bimodal, with peaks at approximately 100 to 110 and 120 to 130 collagen fibrils per 0.04 µm² (Figs. 3-B and 4-B).

Discussion

Materials and Methods | Results | Discussion | References

The extracellular matrix of human subsynovial connective tissue contains collagen types I, III, IV, V, and VI as well as proteoglycans^1,3,17 and elastin⁷. Collagen types I and III are co-distributed within the subsynovial connective tissue. Collagen type VI is primarily located in microfibrillar structures between collagen bundles, between elastin and collagen bundles, and between collagen bundles and cells⁷. Collagen type IV is most likely present in the basement membrane of vessels in the subsynovial connective tissue^2,19. Collagen type V is involved in controlling the lateral growth of collagen type-I fibrils and matrix assembly^20,21.

While we did not type the collagen fibrils in this study, we showed that the collagen fibrils in the extracellular matrix of subsynovial connective tissue in carpal tunnel syndrome were morphologically different from fibrils in normal subsynovial connective tissue. The abnormal morphology was similar to the collagen fibril abnormalities seen in conditions such as Ehlers-Danlos syndrome^22-24, pseudoxanthoma elasticum²⁵, and amyloid kidney²⁶ among others. This so-called spiraled collagen, which characteristically has an irregular margin in cross-section, was also described as flower-like or moth-eaten by Ghadially¹⁸. To the best of our knowledge, the present study is the first report of this collagen morphology in patients with carpal tunnel syndrome. While we can only speculate as to the etiology of the spiral deformity of the collagen shape in carpal tunnel syndrome, it is associated with remodeling and phagocytosis. Ishikawa et al. reported that a hemodynamic force such as shear stress might cause vascular wall remodeling leading to a spiraled collagen appearance²⁷. Sato et al. studied human fibrotic liver using electron microscopy and found abnormal elastin fibers in large amounts also with so-called spiraled collagen²⁸. Hicks et al. found that diabetes was associated significantly (p = 0.003) with the presence of spiraled collagen²⁹, but none of our patients or cadaver donors had diabetes, as the presence of diabetes was an exclusion criterion for this study. Whatever the cause, it seems likely that the presence of this spiraled collagen is evidence of injury of the synovium in patients with carpal tunnel syndrome, which is not present as a result of normal aging.

We observed two types of cells in the subsynovial connective tissue⁷. One cell type resembles a macrophage, with numerous lysosomes, vesicles, phagocytic vacuoles, and pseudopods. The other cell type resembles a fibroblast, with abundant rough endoplasmic reticulum and few vesicles, vacuoles, or lysosomes. In our specimens from patients with carpal tunnel syndrome, we could see similar macrophage-like cells, with many pseudopods surrounding deformed collagen bundles. The importance of these findings remains to be elucidated.

A weakness of our study was the use of cadaver controls, which we chose as a result of ethical concerns in opening the carpal tunnel in normal, age-matched volunteers. Yet, we think it is unlikely that the normal aging process would result in less rather than more evidence of collagen fibril damage in the cadaver specimens, which is what we observed³⁰. While not reported in the present study, we recently observed the collagen morphology in cadavers of individuals with an antemortem history of carpal tunnel syndrome, which showed changes similar to those seen in the patients with carpal tunnel syndrome.

Another weakness of this study is that it was focused on the morphological changes of the collagen fibrils in the subsynovial connective tissue. We did not assess collagen type, which would have required immunohistochemistry, nor did we study other matrix components or intracellular organelles in detail. We also did not compare our findings with those seen on light microscopy of specimens from the same patients, but the findings on light microscopy of specimens from patients with carpal tunnel syndrome have been well described elsewhere^3,4,8,31,32. Finally, our patients and controls were not selected randomly. However, the findings in our patients with carpal tunnel syndrome were similar to those seen with light microscopy of specimens from patients with carpal tunnel syndrome in the past, and the findings in our cadaver controls were similar to those described for normal synovial tissue and were clearly different from the findings in the patients.

In conclusion, there are significant changes in the collagen fiber morphology in the subsynovial connective tissue of patients with carpal tunnel syndrome, including increased collagen fibril diameter and decreased collagen density, compared with the subsynovial connective tissue of control cadavers without carpal tunnel syndrome. In addition, we noted deformation of collagen fibrils and phagocytosis of aberrant collagen fibrils and elastin in the tissue from patients with carpal tunnel syndrome. Future studies are necessary to determine the relationship between these morphological changes and the alterations in absorptive function³³, interstitial pressure³⁴, and ischemia^32,35,36, which are known to be present in patients with carpal tunnel syndrome. ?

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Topics

carpal tunnel syndrome ; cadaver ; collagen ; connective tissue ; microscopes, transmission electron

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Jinrok Oh, Chunfeng Zhao, Mark E. Zobitz, Lester E. Wold, Kai-Nan An, Peter C. Amadio; Morphological Changes of Collagen Fibrils in the Subsynovial Connective Tissue in Carpal Tunnel Syndrome. The Journal of Bone & Joint Surgery. 2006 Apr;88(4):824-831.

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