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Prevalence of Facet Joint Degeneration in Association with Intervertebral Joint Degeneration in a Sample of Organ Donors Jun Li, 1 Carol Muehleman, 1 Yumiko Abe, 2 Koichi Masuda 3 1 Department of Biochemistry, Rush University Medical Center, Cohn Research Building, Room 506, 1753 W. Harrison Street, Chicago, Illinois 60612, 2 Department of Orthopedic Surgery, Rush University Medical Center, Chicago, Illinois 60612, 3 Department of Orthopaedic Surgery, School of Medicine, University of California, San Diego, California 92093-0630 Received 12 October 2010; accepted 24 January 2011 Published online 25 February 2011 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/jor.21387 ABSTRACT: Among the most common causes of low back pain are strain on the muscles and ligaments associated with the spine, degeneration of the intervertebral discs (IVDs), and osteoarthritis of the facet joints. It is not clear, however, how these latter two conditions are related to each other in terms of their development during a patient’s lifetime. The facet joint is the sole synovial joint of the spine but because it is difficult to image its degenerative history as well as its relationship to other degenerative factors within the spine remain elusive. We compared the gross and histologic characteristics of the lumbar spine from a sample of organ donors to the integrity of their associated IVDs as assessed through magnetic resonance imaging. In our study sample, we found that facet joint degeneration was common, occurring as early as 15 years of age, while the IVD could still remain intact. Facet degeneration was more severe at the L4/5 level and progressed along with IVD degeneration with age. Because such early degenerative changes in the facet joint are somewhat surprising, degeneration of this joint should not be overlooked when assessing OA of the spine and causes of lower back pain. ß 2011 Orthopaedic Research Society. Published by Wiley Periodicals, Inc. J Orthop Res 29:1267–1274, 2011 Keywords: facet joint; lower back; spine; osteoarthritis; intervertebral disc Low back pain is one of the most common reasons for physician office visits. It is generally believed that low back pain, as a result of lumbar degeneration, begins in the intervertebral disc (IVD), with ensuing mala- lignment of the spine followed by facet joint degener- ation. However, the actual sequence of events is not known and it is quite likely that both IVD and facet joints contribute to the initial degenerative process. The facet joint, as the only synovial joint of the spine, allows articulation between vertebrae, and pro- vides stability, control, and shock absorption for the back. Facet joints are specifically designed to block rotation in the axial plan along with forward sliding of the lumbar vertebrae. 1 It is because of this intimate relationship between the IVD and the facet joints on either side that any change in one of these elements will alter the mechanics of the spine and thus the integrity of the other elements at that, and other, levels, perhaps throughout the entire length of the spine. Although it has been suggested that pathology of the facet joint is associated with low back pain 2,3 the precise contribution of this joint to back pain as well as its relationship to IVD degeneration are largely unproven and the histological details of the aging facet articular surface have not been fully investigated. In an effort to elucidate the extent and morphology of degenerative changes within the facet joint, Tischer et al. 4 carried out a detailed gross morphological study in an elderly population. Swanepoel et al. 5 studied the prevalence of facet degeneration and its relation- ship to IVD degeneration in the upper lumbar levels by gross morphological assessment. The largest studies, comparing IVD degeneration and facet degeneration, have been carried out by Eubanks et al. 6,7 on an impressively large sample of skeletal remains which were graded on the degree of osteophy- tosis. Although osteophytosis is associated with the degree of cartilage degeneration, Tischer et al. have found that osteophytes were not as frequently found as cartilage defects. All of these studies, however, agree on some factors: lumbar facet degeneration increases with age, degeneration is more severe at the more caudal levels, and degeneration is seen even in young individuals. Most previous studies, however, have focused on older cadaveric specimens or patients, without accompanying study of the IVD, and often, without histological examination. The association between facet degeneration, on both the gross morphological and histological levels, and IVD degeneration as assessed through magnetic reson- ance imaging (MRI) has never been fully explored. Here we examine the level of cartilage degeneration and presence of osteophytes of the lumbar facet joints in a relatively young cadaveric human sample of organ bank donors in comparison to the level of degeneration within the associated IVDs. MATERIALS AND METHODS Specimens and Preparation A total of 57 (18 female and 39 male) cadaveric human spines were received from the Gift of Hope Organ and Tissue Donor Network, with Institutional Review Board approval. Ages of the donors ranged from 15 to 85 years (mean ¼ 59 years, 14.7). The spines were imaged sagittally using a T2-weighted fat- suppressed fast spin echo sequence on a 0.3-T imager (Airis II, version 4.0 A; Hitachi Medical Systems America, Inc., Twinsburg, OH) with a quadrature extremity coil receiver using the following parameters: Time-to-Repeat ¼ 3,100 ms, Time-to-Echo ¼ 125 ms, field of view ¼ 300 mm, slice thick- ness ¼ 4.5 mm, matrix ¼ 256 160 (phase oversampled). Correspondence to: Carol Muehleman (T: 312-942-6780; F: 312- 942-3053; E-mail: [email protected]) ß 2011 Orthopaedic Research Society. Published by Wiley Periodicals, Inc. JOURNAL OF ORTHOPAEDIC RESEARCH AUGUST 2011 1267

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Page 1: Prevalence of facet joint degeneration in association with intervertebral joint degeneration in a sample of organ donors

Prevalence of Facet Joint Degeneration in Association withIntervertebral Joint Degeneration in a Sample of Organ Donors

Jun Li,1 Carol Muehleman,1 Yumiko Abe,2 Koichi Masuda3

1Department of Biochemistry, Rush University Medical Center, Cohn Research Building, Room 506, 1753 W. Harrison Street, Chicago, Illinois60612, 2Department of Orthopedic Surgery, Rush University Medical Center, Chicago, Illinois 60612, 3Department of Orthopaedic Surgery,School of Medicine, University of California, San Diego, California 92093-0630

Received 12 October 2010; accepted 24 January 2011

Published online 25 February 2011 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/jor.21387

ABSTRACT: Among the most common causes of low back pain are strain on the muscles and ligaments associated with the spine,degeneration of the intervertebral discs (IVDs), and osteoarthritis of the facet joints. It is not clear, however, how these latter twoconditions are related to each other in terms of their development during a patient’s lifetime. The facet joint is the sole synovial joint ofthe spine but because it is difficult to image its degenerative history as well as its relationship to other degenerative factors within thespine remain elusive. We compared the gross and histologic characteristics of the lumbar spine from a sample of organ donors to theintegrity of their associated IVDs as assessed through magnetic resonance imaging. In our study sample, we found that facet jointdegeneration was common, occurring as early as 15 years of age, while the IVD could still remain intact. Facet degeneration was moresevere at the L4/5 level and progressed along with IVD degeneration with age. Because such early degenerative changes in the facetjoint are somewhat surprising, degeneration of this joint should not be overlooked when assessing OA of the spine and causes of lowerback pain. � 2011 Orthopaedic Research Society. Published by Wiley Periodicals, Inc. J Orthop Res 29:1267–1274, 2011

Keywords: facet joint; lower back; spine; osteoarthritis; intervertebral disc

Low back pain is one of the most common reasons forphysician office visits. It is generally believed that lowback pain, as a result of lumbar degeneration, beginsin the intervertebral disc (IVD), with ensuing mala-lignment of the spine followed by facet joint degener-ation. However, the actual sequence of events is notknown and it is quite likely that both IVD and facetjoints contribute to the initial degenerative process.

The facet joint, as the only synovial joint of thespine, allows articulation between vertebrae, and pro-vides stability, control, and shock absorption for theback. Facet joints are specifically designed to blockrotation in the axial plan along with forward sliding ofthe lumbar vertebrae.1 It is because of this intimaterelationship between the IVD and the facet joints oneither side that any change in one of these elementswill alter the mechanics of the spine and thus theintegrity of the other elements at that, and other,levels, perhaps throughout the entire length of thespine. Although it has been suggested that pathologyof the facet joint is associated with low back pain2,3

the precise contribution of this joint to back pain aswell as its relationship to IVD degeneration are largelyunproven and the histological details of the aging facetarticular surface have not been fully investigated.

In an effort to elucidate the extent and morphologyof degenerative changes within the facet joint, Tischeret al.4 carried out a detailed gross morphological studyin an elderly population. Swanepoel et al.5 studiedthe prevalence of facet degeneration and its relation-ship to IVD degeneration in the upper lumbar levelsby gross morphological assessment. The largest

studies, comparing IVD degeneration and facetdegeneration, have been carried out by Eubankset al.6,7 on an impressively large sample of skeletalremains which were graded on the degree of osteophy-tosis. Although osteophytosis is associated with thedegree of cartilage degeneration, Tischer et al. havefound that osteophytes were not as frequently foundas cartilage defects. All of these studies, however,agree on some factors: lumbar facet degenerationincreases with age, degeneration is more severe at themore caudal levels, and degeneration is seen even inyoung individuals. Most previous studies, however,have focused on older cadaveric specimens or patients,without accompanying study of the IVD, and often,without histological examination.

The association between facet degeneration, on boththe gross morphological and histological levels, andIVD degeneration as assessed through magnetic reson-ance imaging (MRI) has never been fully explored.Here we examine the level of cartilage degenerationand presence of osteophytes of the lumbar facet jointsin a relatively young cadaveric human sample of organbank donors in comparison to the level of degenerationwithin the associated IVDs.

MATERIALS AND METHODSSpecimens and PreparationA total of 57 (18 female and 39 male) cadaveric human spineswere received from the Gift of Hope Organ and Tissue DonorNetwork, with Institutional ReviewBoard approval. Ages of thedonors ranged from 15 to 85 years (mean ¼ 59 years, �14.7).The spines were imaged sagittally using a T2-weighted fat-suppressed fast spin echo sequence on a 0.3-T imager (AirisII, version 4.0 A; Hitachi Medical Systems America, Inc.,Twinsburg, OH) with a quadrature extremity coil receiverusing the following parameters: Time-to-Repeat ¼ 3,100 ms,Time-to-Echo ¼ 125 ms, field of view ¼ 300 mm, slice thick-ness ¼ 4.5 mm, matrix ¼ 256 � 160 (phase oversampled).

Correspondence to: Carol Muehleman (T: 312-942-6780; F: 312-942-3053; E-mail: [email protected])

� 2011 Orthopaedic Research Society. Published by Wiley Periodicals, Inc.

JOURNAL OF ORTHOPAEDIC RESEARCH AUGUST 2011 1267

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Each disc was graded in agreement by two orthopedic sur-geons (Y.A. and K.M.) using the Thompson grading scale8,9

as follows:

Grade 1: Nucleus pulposus (NP) is homogeneous bright;annulus fibrosus (AF) is homogeneous dark; endplate(EP) is a single dark line; vertebral body (VB) marginsare rounded.

Grade 2: NP has horizontal dark bands; AF has areas ofsignal intensity; EP has increased central concavity;VB has margin tapering.

Grade 3: NP has diminished signal intensity; AF is indis-tinguishable from AF; EP is less distinct; VB has smalldark projections from the margin.

Grade 4: NP has reduced gray signal and large bright anddark regions, and is indistinguishable from AF; AP hasfocal defects; VB has projections of <2 mm with thesame intensity as the marrow.

Grade 5: Displays a gross loss of disc height and brightand dark signals which are contiguous with AF; EPhas defects and thickened areas; VB has projections of>2 mm with the same intensity as the marrow.

The facet joints from L1 to L5 (total ¼ 456 joints, 912articular surfaces) were then isolated by removing surround-ing soft tissue elements with a scalpel and bony elementswith an oscillating saw. Each facet joint was carefully openedwith a scalpel so that the superior and inferior halves couldbe examined and scored as described below for gross anatom-ical grading. The joints were then prepared further as out-lined below.

Gross Morphological GradingThe joint cartilage was scored by two graders in agreement(J.L. and C.M., without knowledge of donor demographics)for gross degenerative appearance (under �8 magnificationon a Nikon SMZ1000 dissection microscope) according tothe following scale: grade 0 ¼ normal-appearing cartilage;grade 1 ¼ early fibrillation, flaking, shallow pits or groovesand/or small blisters affecting the cartilage surface in theabsence of changes in articular surface geometry; grade2 ¼ deep fibrillation and fissuring, flaking, pitting and/orblistering; grade 3 ¼ 30% or less of the articular surfaceeroded down to subchondral bone; grade 4 ¼ more than 30%of the articular surface eroded down to subchondral bone.10

Osteophytes were graded based on Pathria’s criteria in whichgrade 1 ¼ no osteophytes, grade 2 ¼ mild osteophyte, grade3 ¼ moderate osteophyte(s), and grade 4 ¼ large and exten-sive osteophytes.11

Histology and Histopathological GradingThe superior and inferior halves of each facet joint were thenre-approximated and sharply cut with a #10 blade scalpel,rendering superior and inferior halves. One-half of each jointwas dehydrated and paraffin embedded so that 6 mm sectionswould be taken from its cut surface (the center of the joint).Sections were then processed for histology by first dehydrat-ing with increasing concentrations of ethanol and then stain-ing with Safranin O/Fast green.12 Stained sections wereexamined under 20�, 40�, and 100� magnification andgraded (CM in agreement with Shirley Dehn [a summerlaboratory assistant]; without knowledge of donor demo-graphics or gross morphological scores) for histopathologybased on a scale by Pritzker et al.13 Briefly, grade 0 surface

intact, cartilage morphology intact; grade 1 ¼ superficialfibrillation, cell clusters, hypertrophy, some loss of stain;grade 2 ¼ deep fibrillation, matrix depletion, clusters, hyper-trophy; grade 3 ¼ vertical fissures into mid-zone, staindepletion, cell clusters, hypertrophy; grade 4 ¼ cartilagematrix loss, delamination of superficial layer, mid layer cystformation, matrix loss in superficial and mid zone; grade5 ¼ denudation, sclerotic bone or reparative tissue; grade6 ¼ bone remodeling (more than osteophytes formation only).

Statistical AnalysesThe Spearman correlation and Chi-square distribution testswere performed.

RESULTS

Facet Articular Cartilage GradingAges of the donors and scores for the MRI of the inter-vertebral disc (IVD MRI), the gross morphology andthe histology, by decade, are shown in Table 1. For allfacet joints, we documented the most severe gross andhistological grade of both superior and inferior articu-lar surfaces as the grade for the entire joint. For alldecades combined, the mean scores for gross macro-scopic degeneration were: L1/L2 ¼ 2.0 (�0.17); L2/L3 ¼ 1.9 (�0.22); L3/L4 ¼ 2.0 (�0.37); L4/L5 ¼ 2.3(�0.29).

Data for facet joints of a spine level are reported asthe most severe grade of the right side or left sidesince there was no significant statistical differencebetween them (p ¼ 0.67). However, reporting on thegross examination of the right side and left side separ-ately (scale ¼ 0 through 4) revealed that the followingpercentage of joints displayed no cartilage degener-ation at all (grade 0): L1/2 ¼ 5% for left side, 0% forright side; L2/3 ¼ 2% for left side, 2% for right side;L3/4 ¼ 0% for left side, 0% for right side; L4/5 ¼ 2%for left side, 0% for right side.

When considering the relationship of facet jointswithin individuals, it was observed that when thehighest grade of degeneration at any facet was a grossgrade of the highest level of degeneration (grossgrade 4; N ¼ 10 donors), only one donor had at leastone other facet joint with a grade less than 2 (i.e.,more than 1 grade of difference). In this donor thegrade 1 facet was located at a higher spinal level thanthe grade 4 facet. When the highest grade of degener-ation at any facet was a gross grade 3 (N ¼ 20 individ-ual donors), only two donors (10%) had at least oneother facet joint with a grade less than two (one facetdisplayed grade 1 at a higher spinal level than thegrade 3 facet and one was at a lower level than thegrade 3 facet). Seven donors had grade 4 facets at onlythe L4/5 level or both L3/4 and L4/5 levels, one hadgrade 4 at the L3/4 level only, and two had grade 4 atthe L1/2 level only.

Figure 1A and B shows the gross and histologicalscores of the facet joints as a function of age. Withincreasing age, there was a significant increase in facetdegeneration, as assessed gross morphologically andhistologically (Spearman rank correlation, r ¼ 0.33,

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p < 0.0001; r ¼ 0.12, p ¼ 0.01, respectively, for alllevels combined). Representative facet surfaces for grossmorphological grades and for the most representativehistological grades are shown in Figures 2 and 3,respectively. By the age of 40, nearly all donors dis-played a histopathological grade of at least 2 (deep fis-suring; an example of which is seen in Fig. 3C). By theage of 42 years, no donor displayed a facet articular

surface that was normal in appearance. Analysis of theassociation between the gross and histological gradesshowed a strong positive correlation (Chi-square 1008.5,contingency coefficient, 0.843, p < 0.0001).

Gross and Histological DescriptionMacroscopic and microscopic examination showed thatnearly all facet joints displayed diffuse cartilage

Table 1. Demographics of the Donor Pool with Mean Scores for IVD Integrity as Assessed through MRI, and MeanScores for Histological and Gross Morphologic Integrity of the Facet Joints

Decade

10–19(N ¼ 1)

20–29(N ¼ 2)

30–39(N ¼ 1)

40–49(N ¼ 7)

50–59(N ¼ 17)

60–69(N ¼ 13)

70–79(N ¼ 13)

80–89(N ¼ 3)

IVD mean scoreL1/2 1.0 1.0 (0) 2.0 2.0 (0.26) 2.5 (0.21) 2.8 (0.23) 3.0 (0.23) 3.0 (0.58)L2/3 1.0 2.0 (0) 2.0 1.9 (0.14) 2.6 (0.21) 2.6 (0.15) 3.6 (0.21) 3.3 (0.33)L3/4 1.0 2.0 (0) 2.0 2.0 (0.22) 2.8 (0.20) 2.6 (0.15) 3.5 (0.14) 3.0 (0)L4/5 1.0 2.0 (0) 2.0 2.7 (0.33) 2.9 (0.20) 3.1 (0.23) 3.6 (0.22) 3.0 (0)

Facet mean histology scoreL1/2 2.0 2.5 (0.50) 4.0 3.5 (0.50) 3.8 (0.24) 3.6 (0.31) 3.3 (0.21) 5.0 (0)L2/3 2.0 3.0 (0) 5.0 3.4 (0.53) 3.6 (0.24) 3.7 (0.37) 3.4 (0.18) 4.0 (0.58)L3/4 3.0 3.0 (1.0) 2.0 3.7 (0.47) 4.0 (0.22) 4.1 (0.31) 3.8 (0.22) 4.7 (0.33)L4/5 3.0 3.0 (1.0) 5.0 4.2 (0.31) 4.6 (0.25) 4.6 (0.27) 4.4 (0.22) 5.3 (0.67)

Facet mean gross scoreL1/2 1.0 1.5 (0.50) 2.0 1.7 (0.33) 2.4 (0.17) 2.4 (0.20) 2.2 (0.12) 3.0 (0)L2/3 1.0 1.5 (0.50) 3.0 2.0 (0.31) 2.2 (0.13) 2.3 (0.20) 2.2 (0.10) 2.3 (0.33)L3/4 1.0 1.5 (0.50) 1.0 2.3 (0.36) 2.2 (0.16) 2.3 (0.24) 2.2 (0.15) 3.0 (0.58)L4/5 1.0 1.5 (0.50) 3.0 2.3 (0.21) 2.5 (0.23) 2.6 (0.20) 2.6 (0.22) 3.3 (0.67)

The mean number is followed by the standard error of the mean in parentheses. The IVD scale ranges from 1 to 4, the histology scoreranges from 0 to 6, and the gross score ranges from 0 to 4. The highest score in each of the three categories is shown in bold font.

Figure 1. Graphs showing the relationship between the age of the donor and the level of degeneration of the facet joint as visualizedgross morphologically (A) and microscopically, after Safranin O/Fast green staining (B) for each level of the lumbar spine. Facetdegeneration increased with age at all levels.

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degeneration across the superior and inferior articularsurfaces even at early stages. There did not appear tobe any particular articular region which was prone tosevere degeneration while other sites were completelyspared, and no particular region that appeared to becompletely protected from degeneration, even at ear-lier stages. The articular regions that showed lessdegeneration as compared to surrounding areas variedsomewhat among specimens. However, degenerationwas always most severe along the articular borders.

IVD MRI GradeOnly two spines (from 15- and 44-year-old males)showed no signs of IVD degeneration, as assessedthrough MRI, but both donors showed early fibrillation(grade 1 on the macroscopic and histopathology scales)on the facet articular surfaces.

With increase in age, there was a significantincrease in IVD MRI grade through the 8th decade(Spearman rank correlation; r ¼ 0.50 for L1/2,

r ¼ 0.62 for L2/3, r ¼ 0.57 for L3/4, r ¼ 0.47 for L4/5;p < 0.001 for all levels). Although there was a slightdecrease in degeneration score in the 9th decade, thelow sample number should be noted. The L4/5 leveldisplayed consistently worse MRI scores with age. Theearliest age at which severe degeneration at the L4/5IVD was found was in a 45-year-old male who dis-played only moderate degeneration at the other spinelevels. Severe degeneration at the L4/5 IVD was alsofound in three donors in their 50s.

When the relationship between the IVD MRI gradeand gross and histological grades was examined, a sig-nificant positive correlation was observed (MRI vs.gross grade: Chi-square 130.7, contingency coefficient,0.503, p < 0.0001, Fig. 4A; MRI vs. histological grade:Chi-square, 117.054, contingency coefficient, 0.482,p < 0.0001, Fig. 4B).

Importantly, even in the group displaying an IVDMRI grade 2 (fairly early degeneration), the majorityof facet joints exhibited grade 2 or higher cartilagedegeneration (gross grade, 88% were grade 2; histo-logical grade, 89% were grade 2). With an increase inIVD MRI grade, the grade of facet cartilage degener-ation steadily increased.

OsteophytesOsteophyte scores significantly increased with agewith Spearman’s r ¼ 0.355, p < 0.0001. Osteophyteswere found primarily on the dorso-lateral margin ofthe superior facet, the location of the attachment ofthe dorsal capsule. Osteophyte formation wasstrongly correlated to the gross grade (data notshown. Chi-square 40.4, contingency coefficient, 0.098,p < 0.0001). The prevalence of osteophytes as a com-ponent of the facet joint was as follows: grade 1 (noosteophyte) ¼ 48%; grade 2 ¼ 27%; grade 3 ¼ 20%,grade 4 ¼ 5%.

The majority of osteophytes were associated withsome level of cartilage degeneration. Only two facetshad osteophytes but no cartilage degeneration; fourfacets had cartilage degeneration but no osteophytes.The youngest age at which osteophytes were foundwas in a 24-year-old male whose facets, at all spinelevels, displayed osteophytes on the left side only. Themost severe osteophytes were found at L4/5, where13% of facets displayed grade 4, or large osteophytesencompassing the majority of the articular border. Theyoungest donor exhibiting a grade 4 osteophyte was a53-year-old male.

DISCUSSIONThe present study is the first gross/histological studyin a large sample (912 articular surfaces) of lumbarfacet joints from younger individuals (average age,59 years) who are not part of patient population, andin comparison to the integrity of the IVD as assessedby MRI. The opportunity to observe this number offacet joints gross morphologically is of particular

Figure 2. Representative examples of the five grades of grossmorphological appearance of the facet articular surfaces. (A)G0 ¼ normal; (B) G1 ¼ surface fibrillation; (C) G2 ¼ fissuring;(D) G3 ¼ erosion of 30% or less of the articular surface; (E)G4 ¼ erosion of more than 30% of the articular surface. Arrowspoint to the various lesions at each grade of degeneration.

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significance in that it is a joint difficult to evaluatewith current imaging methods. The data presentedhere demonstrate that facet degeneration and IVDdegeneration are observed concurrently. The incidenceof facet degeneration was surprisingly high even atyounger ages, at upper lumber levels, and with earlydisc degeneration. The observation of high levels offacet degeneration in comparison to other studies ismost likely due to the high sensitivity of gross andhistological evaluation as compared to other studiesusing planar radiography, computed tomography, orMRI evaluation.

Other studies have either utilized older cadavericspines,4,14 facet joints removed upon surgical interven-tion for pathology,10,15 or patients. For instance, usingMRI for disc degeneration and computed tomographyfor facet degeneration, Butler et al.16 claimed thatdiscs degenerate prior to facets. They found an over-whelmingly higher percentage of disc degenerationwithout facet degeneration than vice versa. Similarly,using MRI and CT, Fujiwara et al.11 found that nofacet joint degeneration was observed in the absence ofdisc degeneration and most facet degenerationappeared at IVD levels with advanced degeneration.However, even the study of younger patients is notwithout its limitations as it has previously been shownthat the specificity and sensitivity of arthrography fordegenerative disease of the lumbar facet joint is ratherlow.14 To further substantiate this, it has also been

shown that a full range of cartilage degeneration ofthe lumbar facet was observed grossly and histologi-cally even though plain radiographs and computedtomography showed normal or near-normal appear-ance of joint space.15

Challenging the view that facet degeneration fol-lows IVD degeneration is a study, by Eubanks et al.,6

of 647 skeletons in which facet osteophytosis wasused as a measure of facet degeneration and vertebralrim osteophytosis as a measure of IVD degeneration.Their results suggested that facet osteophytosisappears early in the degenerative process, precedingvertebral rim osteophytosis. However, they alsosuggested that once facets begin deteriorating withage, vertebral rim osteophytosis overtakes continuedfacet osteophytosis.

In the present study we found that most specimensfrom spines with grade 2 disc degeneration (dimin-ished signal intensity and AF is indistinguishable fromNP) were associated with facet grade 2 (cartilage fis-suring) or above. Of our sample of 57 spines fromdonors ranging in age from 15 through 85 (mean ¼ 59years), only the spines of a 15-year-old male (youngestdonor) and a 44-year-old male showed no signs of IVDdegeneration, as assessed through MRI, but bothshowed early fibrillation macro- and microscopicallyon the facet articular surfaces. It may be argued, how-ever, that early fibrillation is not necessarily pathologi-cal, may possibly be reversed, and does not inevitably

Figure 3. Representative examples of the most common histological lesions as seen in Safranin O/fast green sections. (A) An intactsuperficial zone but with loss of cells and some loss of matrix stain. Arrows point to regions where the articular cartilage has beenpartially (B) or completely (C,D) lost (�10).

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lead to more severe cartilage changes.17 However, thefact that none of the specimens displayed perfectlysmooth cartilage while other joints of the body areknown to be without degeneration at least in someindividuals even into old age9 leads to the notion thatthe facet joint is rather vulnerable to degenerationeven in the young. Also in consideration of the IVD/facet joint comparison of the present study is thecaveat that the MRI used to assess IVD integrity isless sensitive than the gross visual assessment of thefacet joints. It is surely likely that earliest IVDdegeneration was not detectable through MRI thusleading to slightly skewed results for the comparison,particularly at early stages.

As expected, and from what is known from previousstudies18 as well as from loading characteristics,degeneration was generally worse at lower spinelevels, particularly with aging. Facet degeneration

showed characteristics seen in other synovial joints;however, facet degeneration appeared to begin at thearticular borders and later occupy most of the articu-lar surface, sparing little surface. Furthermore, incomparison to the level of degeneration seen in the hipand knee joints as previously reported,9 in our studysample degeneration occurred in the facet joint at anearlier age and more severely. This may be due to thefact the facet joint is small and thus has most, if notall, of its articulating surfaces in contact with oneanother (congruent) throughout spine motion. This isunlike the situation with joints such as the hip andknee, in particular, in which the regions of weight-bearing change through the gait cycle; some areaseven being of low-load and/or with reduced contact.19–24

Although we did not record degeneration scores onsuperior and inferior facets separately, we did noticethat the superior facet often showed earlier and moresevere damage as compared to the inferior facet. Thisis in agreement with Tischer et al.4 who also foundthat damage on the superior facet occurred most fre-quently at the superior pole while the inferior facetshowed most damage at the superior and inferiorpoles. They reasoned that during spinal flexion theinferior facet causes maximum pressure on thesuperior pole of the superior facet. During spinalextension, however, there is contact between theinferior pole of the inferior face and the arch of thesuperior facet.25,26 Furthermore, gaping of the facetjoint during the final phases of movement can resultin high pressure on the lower edge of the inferior facetduring extension and on the upper edge of the superiorfacet during flexion.18

The L4/5 level displayed greater degeneration thandid the higher lumbar levels which agrees with whathas previously been reported4 and is in keeping withthe greater load at this spinal level. There were nostatistical differences in the degeneration scoresbetween the right and left sides at any level. Therewas a strong correlation between facet joint degener-ation, as assessed through gross and histologicalexamination, and IVD degeneration, as assessedthrough the MRI grade (p ¼ 0.0001 for each) thussuggesting a probable progressive association betweenthem. Certainly, because of the close associationbetween these joints within the confines of the spine,it is apparent that any biomechanical change in a jointwill negatively affect the alignment of that segment aswell as other segments of the spine.

Along these lines of thought, Master et al.27

showed, on a large sample of skeletal remains, thatalthough lumbar disc and facet arthrosis were signifi-cantly greater than cervical arthrosis, lumbar arthro-sis preceded cervical arthrosis, and was highlyassociated with cervical arthrosis with advancing age.In a separate study, Eubanks et al.28 showed thatinterfacet distance appears to have a bearing on facetarthrosis. In a sample of 400 cadaveric lumbar spines,insufficient increase in interfacet distance from L4 to

Figure 4. Graphs showing the positive correlation of the grossmorphological grade (A) and the histological grade (B) with theintervertebral disc grade as assessed through MRI (p < 0.0001for both).

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S1 levels correlated with a greater arthrosis. The sup-position is that increasing the interfacet distance downthe lumbar spine results in a more pyramidal confi-guration of the most caudal lumbar facets which moreefficiently dissipates the forces at this level.

The data of the present study show that it is mostoften the case that all spine levels displayed similar(i.e., within one grade of degeneration difference)levels of facet degeneration within donors. It was farless common (<10%) that one level displayed a facetwith severe degeneration while another displayedlittle degeneration within the same donor. However, indonors with at least one IVD with severe degeneration(Thompson grades 4 or 5) 52% of these donors had atleast one other IVD displaying little degeneration.Thus it appears that there are greater differences inseverity of degeneration between the IVDs of an indi-vidual than between the facet joints. The reason forthis is unclear to us. If the possible lack of sensitivityof the MRIs to allow detection of degenerative changesis a consideration, then one would expect this problemto exist for all degrees of degeneration, unless MRI isselectively less sensitive for early signs.

Although we found that 52% of our sample dis-played osteophytes, which is higher than mostprevious studies,4,15 it is possible that we were lessdiscerning in our identification by perhaps identifyinglipping as low-grade osteophytosis—this level of dis-tinction is quite subjective. As expected, the mostextensive osteophytes were associated with the mostsevere cartilage degeneration, primarily forming onthe lateral margin of the superior facet, the location ofthe attachment of the dorsal capsule. This agrees withTischer et al.,4 in a study of older individuals.

The importance of a cadaveric study such as thepresent lies in the fact that MRI underestimates theseverity of OA11 and patient studies, particularlyinvolving back surgery utilize an abnormal sample.Here, we were able to show prevalence of jointdegeneration in a fairly young sample from the gen-eral donor population.

Taken together these results demonstrate that facetjoint degeneration is common, occurs early, progresseswith IVD degeneration and should not be overlookedwhen assessing OA of the spine and causes of lowerback pain.

ACKNOWLEDGMENTSWe wish to thank the families of the donors to the Gift ofHope Organ and Tissue Donor Network. We also acknowl-edge NIH grants P01AR48152 and AR044058.

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