Progressive and regressive changes in the nucleus pulposus. Part II. The adult

The spines of 28 cadavers were studied with magnetic resonance (MR) imaging, correlated with anatomic sections, to characterize the progressive and regressive changes in the nucleus pulposus. Four additional types of nucleus pulposus were identified in this study. The transitional type (type II) of childhood had fibrous tissue that developed near the anulus fibrosus anteriorly or posteriorly. MR images showed a notch of reduced signal intensity in the nucleus pulposus where the fiber was developing. The adult type (type III), which is predominant after age 30 years, had an indistinct boundary between the nucleus pulposus and anulus fibrosus. MR images showed the fibrocartilage in the nucleus pulposus and inner anulus fibrosus as areas of high signal intensity. Adult disks with a tear of the anulus fibrosus (type IIIB) had a lower signal intensity on MR images and slightly reduced disk heights. This type may represent an early stage of degeneration. Degenerated intervertebral disks (type IV) had either dense disorganized fibrous tissue or fluid replacing the normal fibrocartilaginous structure of the nucleus pulposus. MR images showed narrow intervertebral disk spaces with either reduced signal intensity if collagen was present or increased signal intensity if fluid was present. This study suggests that the nucleus pulposus may progress normally through types I, II, and III.     

Criteria for classifying normal and degenerated lumbar intervertebral disks

The purpose of this study was to develop criteria for distinguishing normal and degenerated lumbar intervertebral disks. Cryomicrotome sections from and magnetic resonance images of 31 cadavers were reviewed. The immature nucleus pulposus, found up to age 2 years; the transitional nucleus pulposus, found in teenagers; and the adult nucleus pulposus were associated with an intact anulus fibrosus without tears except for small concentric or transverse tears in the periphery of the anulus fibrosus. Discoloration of the nucleus pulposus, diminishing disk height, and diminishing signal intensity were associated consistently with a radial tear of the anulus fibrosus. The severely degenerated nucleus pulposus was associated also with a radial tear or complete disruption of the anulus fibrosus. The results suggest that intervertebral disk normally progresses from the immature to the transitional to the adult nucleus pulposus. When a radial tear develops in the anulus there is shrinkage and disorganization of fibrocartilage in the nucleus pulposus and replacement of the disk by dense fibrous tissue and cystic spaces.     

Comparison of MR and diskography in detecting radial tears of the anulus: a postmortem study

Radial tears of the anulus fibrosus, which anatomic studies suggest are a primary event in disk degeneration, can be detected by diskography or MR imaging. We compared the sensitivity of MR and diskography in the detection of anular tears. MR, diskography, and cryomicrotomy anatomic sectioning were performed in eight cadaver lumbar spines. Diskography demonstrated 15 radial tears in 36 intervertebral disks. MR demonstrated 10 of the 15, a sensitivity of 67%. MR (T2-weighted images) in each of the diskographically normal disks showed the high signal intensity characteristic of normal disks. Thirteen of 15 disks from which contrast medium extravasated at diskography had diminished signal intensity in MR images. We conclude that although MR may demonstrate some radial tears of the anulus, and associated changes in the disk, it cannot be used as effectively as diskography to visualize a radial tear.     

Canine intervertebral disks: correlation of anatomy and MR imaging

Because the structure, maturation, and degeneration of canine intervertebral disks resemble those of humans, the authors developed a model of acute intervertebral disk degeneration in dogs. Herniated disks of 18 dogs were examined with magnetic resonance (MR) imaging and then sectioned with a freezing microtome. On the basis of their morphologic appearance in the freezing microtome sections, most of the lumbar intervertebral disks could be categorized as one of six types. Each type has characteristic features and a distinctive appearance on MR images. Findings of this study--including decreased signal intensity from the intervertebral disk, altered signal intensity in contiguous bone marrow, bulging of the anulus fibrosus, herniation of the nucleus pulposus, and contrast enhancement after intravenous administration of gadolinium diethylenetriaminepentaacetic acid (DTPA)--resemble observations from human clinical studies. Classification of degenerating disks and identification of MR imaging characteristics of each type may improve the interpretation of MR images and recognition of early disk degeneration in humans.     

Wide anulus rent appearance on axial MR imaging: a sign of postdiskectomy recurrent disk herniation

A band of high intensity extending from a hyperintense nucleus pulposus at the center of a lumbar disk toward the thecal sac is occasionally encountered on axial MR images with a long TR technique. A retrospective review of 195 patients who previously underwent surgery of the lumbar spine revealed eight instances of this wide anulus rent appearance. Four were confirmed to have recurrent disk herniation at re-operation, and the other four were clinically strongly suggestive. Wide anulus rent appearance is a useful sign of a postdiskectomy recurrent disk herniation.     

The intranuclear cleft of the intervertebral disk: magnetic resonance imaging

Three cadaver spines, 40 patients who were symptomatic for lumbar disk disease, and ten healthy subjects were examined by MR. T2 weighted spin echo images were used to evaluate the character of an intranuclear cleft. This cleft appears identical to annular tissue both on T2 weighted images and histologically. A 120 msec TE, 3 sec TR image was used to delimit the normal nucleus pulposus from the annulus. The incidence and age distribution of the cleft were calculated. An intranuclear cleft was present in all normal disks in both control and symptomatic subjects who were 30 years of age and older. If present in one disk, it was also present in 94% of the other disks in the same subject. This cleft represents a normal anatomic structure and appears to be a constant feature in subjects 30 years of age or older. Its absence, in the presence of an increased signal intensity within the disk, suggests a pathological process with a long T2 value, such as inflammation.     

Tears of the anulus fibrosus: correlation between MR and pathologic findings in cadavers

Tears of the anulus fibrosus, which have been implicated in back pain, have not been studied systematically with MR imaging. We correlated MR images with cryomicrotome sections to study the lumbar anulus fibrosus in 20 cadavers. Three distinct types of tears of the anulus were identified: concentric tears, characterized by fluid-filled spaces between adjacent lamellae; radial tears, characterized by a rupture of all layers in the anulus between the nucleus and the surface of the disk; and transverse tears, characterized by a rupture of Sharpey's fibers in the periphery of the anulus, near the ring apophysis. In each type, fluid or mucoid material was present in the tear. MR demonstrated the transverse and radial tears. We conclude that MR imaging provides an accurate means for investigating tears of the anulus.     

Degenerative lumbar disk disease: pitfalls and usefulness of MR imaging in detection of vacuum phenomenon

Magnetic resonance (MR) images of the lumbar spine from 150 patients were retrospectively reviewed. In 14 of these patients, at 18 disk levels, a vacuum phenomenon (VP) had been identified on plain radiographs and/or computed tomographic scans. The MR imaging appearance of these gas collections in 17 disks was an area without signal, best seen on spin-echo sequences with short repetition time and echo time in the sagittal view. MR imaging precisely located the VP in the anulus fibrosus, the nucleus pulposus, and Schmorl nodes. In all but one case, degeneration of the disk was complete and associated with adjacent changes in vertebral bone. Pitfalls of MR imaging detection of VP included chemical shift artifact, calcifications, and tears without gas in the disk.     

腰椎间盘早期退变的MRI与病理对照研究

目的：研究腰椎间盘早期退变的MRI征象和病理改变。材料和方法：对5具新鲜尸体的腰椎标本（共23个椎间盘）行MRI扫描，并与其病理对照研究。结果：所有椎间盘都有不同程度地退变。其中属早期退变的间盘16个。MR可以反映的病理改变主要包括：（1）T2加权像在低信号的纤维环中出现高信号是纤维环粘液样变性肿胀，软骨细胞增生地反映：（2）在高信号的椎间盘内出现与纤维环相连的低信号是纤维环内折地反映；（3）T1加权像椎间盘前部角形低信号伴T2加权像髓核前缘成角是纤维环外折地反映。结论：MRI信号强度地改变能真实地反映某些椎间盘早期退变的病理改变，有助于早期椎间盘退变诊断。     

Normal and disrupted lumbar longitudinal ligaments: correlative MR and anatomic study

The posterior and anterior longitudinal ligaments of the lumbar spine appear on magnetic resonance (MR) images as thin lines of very low signal intensity in all spin-echo sequences. They cover the periphery of the outer fibers of the anulus fibrosus on sagittal images. The lumbar spine of 17 patients with 19 disk herniations was prospectively evaluated with MR imaging, and these findings were correlated with surgical findings. At surgery the posterior ligament was found to be disrupted in eight cases and intact in 11. Absence of a low-signal peripheral line around the herniated nucleus pulposus (HNP) was the most reliable sign of ligament rupture (no false-negative or false-positive findings). The peripheral line appeared to be interrupted in four cases, two of which were falsely positive. The two false-positive cases were related to a chemical shift artifact between epidural fat and the HNP. Presence of a normal and continuous peripheral line outlining the HNP excluded ligament disruption. The overall sensitivity for detecting disruption was 100%, and the specificity was 78%.     

MR imaging of marrow changes adjacent to end plates in degenerative lumbar disk disease

MR studies of the lumbar spine in 41 patients were analyzed at 203 disk interspaces to assess the appearance and frequency of bone marrow signal changes in the vertebral bodies adjacent to normal and degenerated disks. Degenerative changes were found at 58 interspaces; an abnormal bone marrow signal was identified in 29 (50%) of these. On spin-echo pulse sequences with short and long repetition times (TRs) and echo times (TEs), an area of relative increased signal intensity was seen in the vertebral body adjacent to the disk in 24 cases (17 were bandlike on both sides of the disk, four were focal on one side of the disk, and three were bandlike and focal on one or both sides of the disk). In one patient decreased signal was noted on both short and long TR/TE imaging. In the other four patients decreased signal was noted on short TR/TE pulse sequences and increased signal was evident on long TR/TE. These marrow changes were not present adjacent to normal disks. The relatively high signal intensity on both short and long TR/TE pulse sequences suggests that the increased signal resulted from the conversion of normal hemopoietic bone marrow to fatty marrow. We conclude that bandlike or focal areas of high signal intensity in the bone marrow adjacent to degenerated intervertebral disks occur commonly on MR images of the spine and must not be confused with signal changes from tumors or infections involving the disk space and adjacent vertebral end plates.     

Effect of degeneration of the intervertebral disk on the process of diffusion.

PURPOSETo test the hypothesis that diffusion of contrast medium into the intervertebral disk is affected by the integrity of the nucleus pulposus and annulus fibrosus.METHODSIn canine intervertebral disks, defects were made in the annulus fibrosus and nuclear material was removed from the disk with a nucleotome. MR imaging was performed with intravenous contrast medium at 15, 30, 60, and 90 days after the procedure. The diffusion of contrast medium in the intervertebral disk was studied by visual inspection and by measuring changes in signal intensity. The intervertebral disk were classified at each MR study as normal or abnormal on the basis of the signal intensity on T2-weighted images.RESULTSIn untreated disks after intravenous injection of contrast medium, a band of increased signal intensity was observed near the endplates that became wider with time and approached the center of the disk. In six of the 12 treated disks, the band of increased signal intensity was visibly diminished or less discrete compared with that in the control disks. Weeks later, these treated disks showed diminished signal intensity on T2-weighted images and bulging of the annulus fibrosus.CONCLUSIONSIntervertebral disks with defects in the annulus fibrosus and reduced cartilage content were characterized by abnormal diffusion of contrast medium into the disk, and changes characteristic of early disk degeneration were detected subsequently.     

Fibrous structure in the intervertebral disk: correlation of MR appearance with anatomic sections

To correlate the MR appearance of the disk with its fibrous structure, we studied the lumbar intervertebral disks in 10 cadavers with MR, CT, cryomicrotome anatomic sections, and, in selected disks, with histologic and dried sections. In MR images the predominantly fibrous tissues such as Sharpey's fibers had a low signal intensity while the fibrocartilagenous tissues with a mucoid matrix in the intervertebral disk had a high signal intensity. In the equator of the adult disk was a well-defined fibrous plate that contained collagenous, elastic, and reticular fibers with little ground substance. This plate appeared to develop progressively from the periphery of the nucleus toward the center, starting in the second decade of life. The fibrous plate was also distinguished as a lower signal intensity in the MR images.     

MR imaging of peripheral cholangiocarcinoma.

A prospective study was performed to compare MR spin-echo (SE) sequences [repetition time/echo time (TR/TE) 2,000/80, 500/44 ms], unenhanced CT, and rapid intravenous contrast enhanced CT in eight consecutive patients with peripheral cholangiocarcinoma. All the tumors (ranging from 5 to 9.6 cm in size) were detected with all four techniques. Tumor contrast, however, was qualitatively greatest on long TR/TE SE images. With long TR/TE SE images, tumors were demonstrated as well-demarcated homogeneous regions of high signal intensity, and the anatomic relations between tumors and intrahepatic blood vessels were easily perceived. Detection of small intrahepatic metastatic foci was best on long TR/TE images. Tumor invasion of the portal vein's branches was also best seen on long TR/TE SE images. These results indicate that long TR/TE SE sequence is the most effective initial screening method in demonstrating the presence and determining resectability of peripheral cholangiocarcinoma.     

Painful sickle cell crisis: bone marrow patterns observed with MR imaging

Eleven patients with homozygous sickle cell anemia (SCA) undergoing painful crisis were studied with magnetic resonance (MR) imaging. The signal intensity of bone marrow was diffusely decreased in the axial and peripheral skeleton on short repetition time (TR)/echo time (TE) images and long TR/TE images, which suggested hematopoietic marrow hyperplasia and was confirmed by isotope marrow scans in five patients. Focal areas of further decrease in signal intensity were seen on short TR/TE images in 12 of the 14 (86%) painful joints and three of the five (60%) painless joints. In the painful joints, these focal areas converted to high signal intensity on long TR/TE images, presumably due to edema, which suggested acute marrow infarction. In the painless joints, these low-intensity focal areas remained as low signal on long TR/TE images, which suggested absence of edema and thus areas of old infarction or fibrosis. These results indicate that MR imaging may enable differentiation between acute and chronic marrow infarcts in patients with SCA and serve as a useful guide in monitoring and directing therapy.     

Clinical significance of the intranuclear cleft of the lumbar intervertebral disk on MRI

MR studies of the lumbar spine in 111 patients were analyzed at 469 disks to assess the prevalence of intranuclear cleft (INC) in the lumbar intervertebral disk. MR studies were performed on either 0.1-tesla (T) magnet (69 patients) or 0.22-T magnet (42 patients). The pulse sequences reviewed were saturation recovery (SR; TR = 0.5 sec), short TR, TE spin echo (S-SE; TR = 0.5 sec, TE = 34 msec) and long TR, TE spin echo (L-SE; TR = 1.5 sec, TE = 68,80 msec). All study were done in a sagittal plane with 10 mm slice thickness. The conclusions were as follows: 1) On a 80 msec TE, 1.5 sec TR image, INCs were detected in more than 80% of disks in patients over 30 years old but in only 13.3% of disks in patients under 20 years old. 2) In both imaging system, L-SE showed INCs more frequently than SR and S-SE. 3) INCs were less frequently demonstrated in the disk with decreased signal intensity on 0.1-T magnet as compared with 0.22-T magnet. 4) On SR and S-SE, there is an increase in the prevalence of INC in the disk with decreased signal intensity. We suggest that the INC will be a good landmark of the pathological process of the lumbar disk, such as degeneration.     

Distinguishing between scar and recurrent herniated disk in postoperative patients: value of contrast-enhanced CT and MR imaging

Twenty patients with failed back surgery syndrome were analyzed prospectively with MR imaging. In addition, 10 of these patients were analyzed with high-dose contrast-enhanced CT or gadopentetate dimeglumine-enhanced MR imaging. Imaging results were compared with surgical and pathologic findings in all cases. In the 10-patient subset, abnormal epidural soft-tissue specimens were also assessed with light and electron microscopy for vascular density, size of the extracellular space, and collagen orientation and thickness. The average vascular density of epidural fibrosis on light microscopy was found to be 1.19%; the average size of the extracellular space on electron microscopy was 4.29%. Scar 4 months of age or less had a larger extracellular space than did older scar; high- (grade 4 or 5) intensity scar had a larger extracellular space than did less intense scar on long TR/short TE images. Scar 1 year old or less enhanced more intensely on CT than did older scar. The MR signal intensity and CT enhancement characteristics of epidural scar were also found to differ according to epidural location. The percentage of scar that was hyperintense on long TR/TE images was as follows: anterior, 82%; lateral recess, 70%; lateral, 47%; and posterior, 20%. However, no relationship was found between the degree of CT enhancement of scar and vascular density. Gap junction status and extracellular space size, therefore, are more important than vascular density in predicting the degree of enhancement. The accuracy of contrast-enhanced CT and unenhanced MR in separating scar from herniated nucleus pulposus is 80%. This accuracy is related to the partial overlap in imaging characteristics of scar and recurrent herniated nucleus pulposus.     

MR signal intensity of parathyroid adenomas: correlation with histopathology

Recent experience has shown that parathyroid adenomas vary in their MR signal intensity, which raises the question of whether the signal intensity is related to different histologic characteristics. In order to address this question, 10 patients who had MR imaging studies (four at 0.35 T, six at 1.5 T) showing large- to medium-sized parathyroid adenomas and who subsequently underwent surgery with histologic proof of the lesion were evaluated. The MR appearance was compared with histologic characteristics. The adenomas were classified into three groups according to the MR appearance: group I, low signal intensity on short TR/TE images, high signal intensity on long TR/TE images (n = 5); group II, low signal intensity on short and long TR/TE images (n = 3); group III, high signal intensity on short and long TR/TE images (n = 2). Histologic analysis revealed that the major features of each group were different. High cellularity without degeneration or fibrosis was observed for all five adenomas from group I. In group II, all three adenomas showed cellular degenerative changes, old hemorrhage with hemosiderin-loaded macrophages, and/or fibrosis. In group III, both adenomas showed evidence of acute hemorrhage without significant degenerative or fibrotic changes. These data suggest that the signal intensity of parathyroid adenomas on T1- and T2-weighted images corresponds at least in part to differences in histologic composition.     

Lumbar disk herniation: correlation of histologic findings with marrow signal intensity changes in vertebral endplates at MR imaging

PURPOSE: To compare findings at preoperative magnetic resonance (MR) imaging with data for tissue composition of herniated disks in patients after microsurgical removal of herniated material. MATERIALS AND METHODS: Fifty-one patients underwent MR imaging before microsurgical removal of extruded lumbar disk herniation material. Marrow signal intensity changes along the cartilaginous endplates were classified according to Modic types 1-3. Severity of changes was evaluated with respect to extension along the endplate in the anteroposterior diameter (0%, <33%, 33%-66%, >66%). The existence of a dorsal vertebral corner defect was evaluated in relation to the existence of hyaline cartilage in the disk extrusion material. RESULTS: Mean tissue composition of herniated material in all patients was 63% anulus fibrosus, 30% nucleus pulposus, and 8% cartilaginous endplate. Twenty-five of the 51 patients had hyaline cartilaginous material in the extrusion (range, 5%-50%). Patients without marrow signal intensity changes along the cartilaginous endplate showed significantly less cartilaginous material in the extruded disk (P =.023, Fisher exact test). Mean percentage hyaline cartilage in patients without changes was 2% +/- 4 (SD) (Modic type 1, 16% +/- 15; type 2, 10% +/- 12). When the changes extended 33% of the vertebral endplate, there was cartilaginous endplate material in the extruded disk (P =.006). Cartilage from the endplate was present in the extruded disk material in 40% (16 of 40) of patients without a vertebral corner defect and in 82% (nine of 11) of patients with a vertebral corner defect (P =.019). CONCLUSION: Avulsion-type disk herniation seems to be common, and vertebral endplate marrow signal intensity changes on MR images are indicative of cartilaginous material in the extruded disk herniation material.     

Peripheral focal low signal intensity areas in the degenerated annulus fibrosus on T2-weighted fast spin echo MR images: correlation with macroscopic and microscopic findings in elderly cadavers

Objective. To correlate the peripheral focal low signal intensity areas in the degenerated annulus fibrosus on T2-weighted fast spin echo MR images with the macroscopic and microscopic findings in cadavers derived from elderly subjects. Design. Twenty-eight intervertebral disks (16 lumbar and 12 cervical) derived from four nonembalmed cadavers were examined with T1-weighted spin echo and proton density-weighted and T2-weighted fast spin echo MR imaging. The signal intensities of the annulus fibrosus were evaluated on sagittal MR images and correlated with the findings on corresponding sagittal anatomic sections. The MR imaging-histologic correlation was then studied. Results. Peripheral focal low signal intensity areas and adjacent regions of high signal intensity were found in five lumbar intervertebral disks. Peripheral focal low signal intensity regions consisted of disorganized compact annular fibers, tiny fissures, and dense fibrosis. The high signal intensity regions, adjacent to the areas of low signal intensity, consisted of mucoid degeneration, tiny fissures, and chondroid metaplasia. Conclusions. Awareness of the histologic findings in regions that reveal peripheral focal low signal intensity with adjacent regions of high signal intensity in the degenerated annulus fibrosus on T2-weighted images may facilitate effective interpretation of clinical MR images of the spine. Received: 11 November 1998 Accepted: 20 January 1999