Multinuclear NMR and MRI studies of the maturation of pig articular cartilage

Abstract

The maturation of pig articular cartilage was followed by 2 H in-phase double quantum filtered (IP-DQF) spectroscopic MRI, 1 H T 2 MRI, and 23 Na DQF and triple quantum filtered MRS. The results all lead to the conclusion that the order and density of the collagen fibers in articular cartilage increase from birth to maturity. At birth, both 2 H IP-DQF signal and 1 H T 2 were homogeneous throughout the cartilage and their values independent of the orientation of the plug relative to the magnetic field. At maturation, the 2 H IP-DQF spectrum near the bone is composed of two pairs of quadrupolar split satellites and the 1 H T 2 relaxation is biexponential, indicating the presence of two groups of collagen fibers. Maturation of cartilage plays an important role in human development from birth to adulthood. Furthermore, the integrity of articular cartilage is an essential factor for the preservation of the quality of life. Thus, a noninvasive technique that will allow follow-up of changes in the microstructure of cartilage is highly desirable.Previous studies indicate that the maturation process of articular cartilage is associated with dramatic structural and chemical composition changes. With age, the proteoglycan content progressively decreases (1-3), the collagen content significantly increases (1-4), and cellularity diminishes (1,5), as does the cartilage thickness (1,2,5). Moreover, scanning electron microscopy (SEM) studies have shown that in newborns the collagen fibers are randomly oriented (6,7), while for mature cartilage, the fibers in the deep and radial zones are well ordered with an orientation perpendicular to the surface (8,9).T 2 and T 1 have been shown to be related to the architecture of the collagen fibers and the integrity of the cartilage matrix (10 -15). The effect of maturation on the MRI appearance of articular cartilage was studied in humans, pigs, calves, and rats (5,16 -18). A progressive and significant decrease in global T 2 values with maturation was observed in rat articular cartilage (16). In another work, a decrease of T 2 -weighted signal intensity within the weight-bearing region was seen during normal development of children (17). For newborn piglets, hip cartilage was homogeneous on T 1 -and T 2 -weighted images, while from 2 weeks of age a distinct trilaminar appearance was observed on T 2 -weighted images (5). Similar results were found for 3-month-old bovine calves (18). The laminar appearance in young articular cartilage was sensitive to the place of origin within a joint (19).We have shown that 2 H double quantum filtered (DQF) spectroscopic MRI gives very detailed information about the density and orientation of the collagen fibers in articular cartilage (20). Using this method, we studied the changes in the architecture of collagen fibers when cartilage is under load (21) and when the cartilage is detached from the bone (22).In the present work, the gradual ordering of the collagen fibers, from birth to adulthood, was followed by 2 H IP-DQF (23,24) spectroscopic MRI, prot...

Effect of multislice acquisition on T1 and T2 measurements of articular cartilage at 3T

“…Although it is difficult to get the "true" T 2 value with the MSE sequence, there is the advantage of reduced scan time. In principle, the decay of T 2 for articular cartilage has been reported to be best fitted to a double-exponential fit (29). Although a monoexponential curve fit had to be used for our clinical in vivo study because of the practical limitations of measurement, it should be noted that it is difficult to get the true T 2 value even if single-spin-echo sequence with monoexponential curve fit is used for calculation of T 2 .…”

“…A total of 10 knees were involved in the T 1 measurement study (three men, two women), and the other 10 knees were involved in the T 2 measurement study (three men, two women). Mean age at time of imaging was 31.8 Ϯ 3.9 years [25][26][27][28][29][30][31][32][33][34][35][36] (values are given throughout as mean Ϯ SD [range]) for the T 1 measurement study and 29.5 Ϯ 4.9 years [24 -36] for the T 2 measurement study. Exclusion criteria were history of knee pain or abnormality or trauma of the knee joint requiring medical treatment.…”

Monitoring Tissue Engineering Using Magnetic Resonance Imaging

“…An example of the changes in T 2 observed is shown in Figure 4 Progress in monitoring tissue-engineered cartilage in vivo -MRI techniques have also been used in vivo to characterize the development of tissue engineered cartilage (58], [59,60). In a study by Watrin-Pinzano and coworkers (58), MR was used to generate T 2 maps during the repair of a focal patellar cartilage defect in a rat.…”

“…In a related multinuclear NMR and MRI study by Keinan-Adamsky and associates (59) at 8.5 T using a pig model, the authors found that the order and the density of collagen fibers in articular cartilage increased from birth to maturity. This conclusion was derived from the bi-exponential nature of T 2 relaxation in mature cartilage, as well as its orientational dependence derived from NMR spectral splittings (59). Finally, a recent study by Ramaswamy and coworkers (60, 61) used T 2 relaxation data to assess the regrowth of cartilage in full-thickness chondral defects (surgically created) in rabbits.…”

Monitoring Cartilage Tissue Engineering Using Magnetic Resonance Spectroscopy, Imaging, and Elastography

“…77,[83][84][85] However, in engineered cartilage, sodium NMR has been primarily used for quantification of the order or preferred orientation of collagen fibers. 15,63,86 For example, KeinanAdamsky et al 86 have used multiquantum coherence spectroscopy in pig articular cartilage samples from birth to 39 months of age to obtain the average quadrupolar coupling, which provides information about collagen fiber orientation order. Using 1 H T 2 MRI and 23 Na double-and triple-quantum filtered NMR spectroscopy, they concluded that the collagen fibril order and the density of the collagen fibers increased from birth to maturation in the pig articular cartilage.…”