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100 Journal of the Royal Society of Medicine Volume 79 February 1986 Intervertebral disc mechanics: a review J Nixon MA FRCS Nuffield Orthopaedic Centre, Headington, Oxford OX3 7LD Introduction Musculoskeletal problems account for up to 25% of general practitioner consultations1'2. Out of every 100 patients on the general practitioner's list, 4 will each year initiate a consultation for back pain3. Low back pain is responsible for over thirty million working days lost in Britain per annum4. Between 21%5 and 84%6 of such 'lumbago' occurs without a definite diagnosis, but it seems likely that degenerative disease of the spine underlies much of this absenteeism. Some occupations are affected more than others7. A study by the Royal College of Nursing8 reports the incidence of low back pain in nurses to be as great if not greater than amongst manual workers. Following skeletal maturation the spine begins to degenerate both biochemically and biomechanically, and this process continues throughout life at a rate which may be genetically predetermined9. Autoimmune mechanisms may also play a part in this process0'11. Degeneration occurs most rapidly at the L4/5 and L5/S1 levels. These are the levels subjected to the greatest mechanical stresses, so it is reasonable to assume that mechanical forces play a major role in disc degeneration. In this paper a number of mechanical influences on the disc, some physiological others pathological, will be considered (Table 1). Table 1. Intervertebral disc mechanics (1) Spinal column flexibility (2) Spinal column stability (3) Intervertebral joint motion (4) Loading mechanics (5) Protective mechanisms (6) Fatigue failure (7) Acute mechanical failure 0141-0768/86/ 020100-05/$02.00/0 C0 1986 The Royal Society of Medicine Spinal column flexibility The rigid elements of the spinal column consist of 24 presacral vertebrae which increase in size from above downwards. Mechanically each vertebra can be divided into four parts: (1) The body which transmits most of the applied load. (2) Posterior facet joints which control and restrict intervertebral joint motion and transmit a variable load. Normal facets carry between 3% and 25% of the applied load, whilst arthritic facet joints can carry as much as 40%12. (3) Pedicles and laminae which complete the spinal canal. (4) Transverse and spinous processes which provide mechanically advantageous sites for muscle and ligamentous attachments. Flexibility of the spinal column is provided by the disc which is composed of the central nucleus pulposus and surrounding annulus fibrosus. Each layer of the annulus has fibres directed at about 250 to 450 to the vertebral end-plate, and this angle diminishes with age13. The direction of the fibres alternates in each successive layer, providing flexibility whilst maintaining strength. If one layer of the annulus is relatively slack during movement, its adjacent layers will be taut. Spinal column stability The spinal column has both intrinsic and extrinsic stability. Intrinsic stability results from the opposing forces of (a) ligaments restraining vertebral motion, and (b) pressure within the nucleus pulposus tending to push them apart. This latter is known as the 'imbibition' pressure. Hydrophilic proteoglycans of the nucleus pulposus imbibe and retain water molecules to produce a turgid resilient nucleus. The vertebrae are pushed apart with a force of about 100 kPa'4, which essentially pre-stresses the ligaments. Extrinsic stability results largely from trunk musculature, and intra-abdominal pressure which is in turn maintained by abdominal wall musculature. With ageing the imbibition pressure falls. At birth the nucleus contains about 88-90% water15, but by 70 years of age it is only 65 700/o water"6. These values are similar for articular cartilage (approximately 75% by weight) where water content is highest next to the articular surface"7. In a sense, therefore, we do 'walk and move on water'. The gradual reduction with age in the water content of the nucleus occurs following proteoglycan breakdown, and associated ingrowth of collagenous tissue. Although collagen is largely responsible for the tensile strength of the disc, proteoglycan is the major component resisting compression and providing resilience18. The mucopolysaccharide-protein complexes of young discs are large molecules composed primarily of chondrotin sulphate A and C. These macromolecules are strongly hydrophilic and increase disc viscosity'9. During the early 20s they begin to break down into smaller molecules, possibly under the influence of changes in oxygen tension20 and blood supply. Mucopolysaccharide production is switched to chondroitin sulphate B and keratosulphate, smaller molecules which bind less water. The annulus fibrosus does not lose water with age21, but changes in the glycosaminoglycan ground substance 'lubrication' between adjacent lamellae may generate shear. stresses with movement22. The imbibition pressure of the nucleus is largely responsible for the variation in a person's height from morning to evening. Up to the age of 10 a child Journal of the Royal-Society of Medicine Volume 79 February 1986 is 2% shorter at the end of the day than at the beginning. Young adults are on average 1.1 cm taller in the morning, whilst a 70-year old individual shows little change. A more bizarre example is an increase in height of over 5 cm of an astronaut on return to earth through imbibition pressure unopposed by gravity. As imbibition pressure falls with age, the nucleus pulposus becomes less turgid, more fibrotic, and less efficient at redistributing vertical compressive loads centrifugally to the inner layers of the annulus. A larger proportion of the load is therefore taken directly by the annulus itself. Bulging of the annulus occurs with loading" , and this may compress adjacent nerve roots or cauda equina23. Loss of disc height with advancing age results in relative lengthening of the ligaments, with consequent reduction of intrinsic spinal stability. This occurs at a time when the tone of trunk and abdominal musculature is reduced, compromising extrinsic stability also. which provides extrinsic stability and enables the spine to support tremendous loads. Vector diagram analysis at the lumbosacral junction of a person bending over to pick up a weight indicates that forces in the order of ten times the lifted load are generated. This implies that lifting a load of only 20 kg would be sufficient to fracture the vertebral end-plate30, since cadaver studies have shown endplate failure to occur under loads as small as 10 kN31 32. The normal disc is much stronger than the vertebral end-plate of the cadaver spine on vertical loading33. Mechanisms must exist, therefore, to protect the vertebral end-plate from tremendous loads transmitted by the disc. A number of protective mechanisms have been postulated. Theories of protective mechanisms Hydrostatic properties of the disc The hydrostatic model of the disc was first postulated by Schmorl34'35, and demonstrated in vivo by Nachemson36, both in normal and slightly degenerate discs. Pressure within the nucleus pulposus under loading conditions is redistributed both radially to the inner layers of the annulus fibrosus as well as vertically to the vertebral end-plates. This effectively converts compressive loading of the nucleus to tension within the annulus, helping, to unload adjacent vertebrae. Pressure is always present within the disc, even at rest37, so the annulus is effectively pre-stressed. Intervertebral joint motion The intervertebral joint (one disc and two facet joints) is a type of universal joint with six degrees of freedom24: three of translation (sideways, backwards-and-forwards, up-and-down) and three of rotation (side-to-side, bending forwards and backwards, and longitudinal rotation). In practice, however, the joint does not perform simple movements in isolation, but always couples one translational with one rotational movement. For example, as the spine axially rotates there is always lateral flexion and vice versa. Three-dimensional radiographic studies of spinal movement25 have shown that relatively little rotation occurs in the lumbar spine due to facet joint orientation. In the thoracic spine the centre of rotation lies within the nucleus, so the disc is subjected to rotational forces26, whereas in the lumbar spine this axis lies posterior to the disc, subjecting the disc to translational shear forces. Shear and rotational stresses are probably the most significant ones contributing to degeneration. Facet joint tropism, a rotational malalignment, displaces the axis of rotation of the intervertebral segment away from the midline, thus increasing the translational and rotational stresses imposed upon the opposite facet joint and contralateral side of the disc. This probably accelerates their degeneration, and it has been noted that the incidence of facet joint degeneration and annular rupture is increased on the side opposite the blocked facet joint27. Stress analysis of the intervertebral joint by Farfan et al.28 indicated that the greatest stresses are generated during rotation when only half of the oblique fibres of the annulus are under tension, and the others are relaxed. At this time, the nucleus pulposus is contained by only half of the annular fibres. Many patients with acute disc prolapse do report a twisting of the trunk in addition to forward bend as a precipitating factor. Pneumatic properties ofabdominal cavity Cross-sections through the trunk and CT scans demonstrate that the abdominal cavity lies laterally as well as anterior to the spinal column. It was first postulated by Bartelink38 that this cavity may, under loaded conditions, act as a semi-rigid cylinder capable of unloading to some extent the spinal column. To test this hypothesis, subjects swallowed tubes into the oesophagus and stomach and electromyographic measurements of various paraspinal muscles were taken39. The subject then lifted weights from 50 lb to 200 lb (22.7-90.9 kg), and as muscle activity increased, so did intra-abdominal pressure and to a lesser extent intrathoracic pressure. The same occurred on static loading of the spine when the subject pulled on a strain ring. On lifting 91 kg (200 lb), the increased intra-abdominal pressure reduced the calculated forces at the lumbosacral junction from 939 kg (2071 lb) to 673 kg (1483 lb), a drop of 30%/0. Eie40 tested Nordic ski-jumpers who swallowed intra-abdominal tubes linked to tape recorders with a retarder in the pocket to measure the gravitational force on landing. He found the landing force to be 10 G, which would theoretically have generated 420 kg of compression at the lumbosacral junction, but this was reduced to 310 kg by intra-abdominal pressure elevation since the jumper held his breath at the moment of impact. Loading mechanics The ligamentous cadaver spine devoid of muscle control can support a compressive weight of only 20 N (4 lb or approximately 2 kg) before collapse of the column occurs29. It is the trunk musculature Dorsolumbarfascia Selective layers of the anterior abdominal wall arise posteriorly from the dorsolumbar and iliolumbar fascia and maintain its shape and length during lifting. Gluteus maximus and the ham-strings also generate forces in this fascia during lifting. The 101 102 Journal of the Royal Society of Medicine Volume 79 February 1986 posterior layer of fascia converges upon the tips of the spinous processes posterior to the erector spinalis muscle"1. Its action through a long lever arm is therefore to extend the spine and possibly to reduce the force required in the erector spinae muscles during lifting. Blood diversion During lifting, blood is diverted from the inferior vena cava via Batson's plexus to the epidural veins. From here it flows freely into the spongiosa of the vertebral bodies to increase the intraosseous venous pressure. This may strengthen the vertebral body against compressive loads, but the hypothesis awaits experimental confirmation. Weight-lifters attempting to break their record wear a broad belt pulled tightly around the waist which increases abdominal'pressure. It seems likely, however, that the 'turgor hypothesis' would be more effective in conditions of acute compression, such as ski-jumpers landing or aircraft pilots ejecting whilst performing a Valsalva manoeuvre42. Measurement of intradiscalpressure Intradiscal pressures have been measured in normal subjects (medical students) by inserting a needle attached to a pressure transducer posterolaterally36. The pressure was increased during sitting, and especially when slumped forwards. This may help to explain a patient's increased back pain and sciatica in these positions. Lifting a- heavy object with the knees bent and trunk straight generates a lower pressure than lifting whilst bending at the waist42. The distance between the centre of gravity of the lifted load and the body is of most significance in reducing intradiscal pressure. Intraabdominal pressure is conversely much higher when lifting properly. This type of pressure measurement has been employed to aid the design of car seats in Sweden. Some physiotherapy exercises recommended for patients with low back pain were found to generate enormous intradiscal pressures,' particularly sit-up exercises. Isometric exercises produced least elevation of intradiscal pressure'3. Pressures were measured in 2 patients following spinal fusion and were found to be reduced during lifting. Fatigue failure On histological examination of cadaver discs of people who had not had significant back pain, Farfan25 and Hirsch44" demonstrated distortion of the lamellae of the annulus fibrosus particularly posteriorly, and in 10-15% radial fissures were seen posterolaterally. Recently nerve endings have been visualized in the annulus fibrosus, and it may be that fissures or the products of degeneration associated with them are a source of pain45. Fissures appear to be more a fatigue phenomenon -than the result of acute trauma'6. Although theoretical stress analysis would suggest that the proximity and orientation of the facet joints does to some extent protect the posterior annulus during axial rotation, such protection is not afforded during spinal flexion when the annulus is highly stressed posteriorly. To assess the fatigue effect of flexion on the loaded spine simulating heavy manual labour such as digging, a cadaver spine was cyclically loaded in a jig within the physiological range of flexion. A compressive force of between 1500 and 6000 Newtons, depending upon age and sex, was applied 40 times per minute to simulate the fastest a British workman could possibly work, and this was continued for a maximum of four hours giving 9600 loading cycles'6. Some vertebral bodies failed through fatigue fracture within 4 hours of 'testing. Following this, dissection of the discs revealed that in over 50% the lamellae were closely packed anteriorly, widely spaced laterally, and tightly curved posterolaterally. Posterolateral radiate fissures were found in 70% of all discs, and in 100% of L4-5 and L5-S1 discs from 30-50-year-olds. These occurred most noticeably where the annulus was most stretched by an inbuilt eccentric setting of the flexion apparatus. The degree of distortion of the lamellae is determined by the centrifugal force of the nucleus against the inner layers of the annulus, posterior displacement of the nucleus during flexion, and vulnerability of the annulus posterolaterally to 'creep' or stretching. It may be that when radial fissures become confluent, a pathway is provided by which nuclear material can escape, usually posterolaterally. Clearly, in vivo the long-term effects of fatigue are modified by the cellular repair mechanisms. Chondrocytes of a mature disc can manufacture collagen and large proteoglycan molecules. The turnover of proteoglycans is 500 days in dogs, and collagen production is probably even slower47, such that the repair processes will have only minimal effect over days or weeks, but may be substantial over a period of months or years. Acute mechanical failure The mechanism underlying acute extrusion of the nucleus pulposus must be clarified. As stated, pure compression of the intervertebral joint leads invariably to vertebral body failure, even with a fatigue pattern of loading31. Flexion just beyond the physiological limit results in damage to the ligaments of the neural arch but not the disc48. Torsion damages the articular facets and, if carried beyond the physiological range, produces circumferential tears of the annulus fibrosus49. However, when the intervertebral joint is flexed a few degrees beyond the normal range and then compressed with about 8000 Newtons, comparable to the compressive forces generated within the discs of a healthy young man straining to lift a heavy weight, acute disc prolapse has been produced in cadaver spines in 26 out of 61 joints'9. Adams and Hutton'9 found that the intervertebral joint could fail in one offour ways: (1) Nuclear extrusion, with nuclear material appearing on a posterolateral edge of the vertebral body or within the canal. (2) Annular protrusion, with an annular ring disruption occurring at a point of bulging and the nucleus displaced posterolaterally behind the bulge. (3) Compression fracture - anterior crushing of the vertebral body and occasional end-plate fracture, with nuclear material sometimes entering the vertebral body. (4) Hyperflexion fracture - even before compressive loads were applied, the posterior rim of the vertebral body could become detached and the anterior rim of Journal ofthe Royal Society of Medicine Volume 79 February 1986 the body fracture. Sufficient flexion had to occur to render the annulus vulnerable and this is achieved by overstretching the interspinous ligaments. It was reported many years ago that the spinous and interspinous ligaments were frequently found to be ruptured in patients undergoing disc surgery the so-called 'sprung back' described by Philip Newman50. Across the age range, 26 out- of 61 discs tested failed by nuclear extrusion, but on looking at the IA-6 and Lb-Si-discs of cadaver specimens from 30-50-year-old patients, the rate of prolapse rose to 14 out of the 17 discs tested. It is possible that there is a greater degree of pre-existing degeneration at these two levels resulting from their increased range of flexion. Alternatively, these levels may be more susceptible to prolapse because of morphological or biochemical variations. References 1 Orthopaedic services: Waiting time for outpatient appointments and inpatient treatment (Duthie Report). Dd 718943 C 8 4/81. London: HMSO, 1981 2 Morbidity statistics from general practice (1971-2). HMSO Publication No. 36. London: HMSO, 1979 3 Office of Population Censuses and Surveys. Studies on medical and population subjects No. 26. London: HMSO, 1974 4 Department of Health and Social Security: Sickness and/or Invalidity Benefit. 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Spine 1982;7:374-89 25 Pearcy MJ, Tibrewal SB. Axial rotation and lateral bending in the normal lumbar spine measured by three-dimensional radiography. Spine 1984;6:582-7 26 Gregersen GG, Lucas DB. An in vivo study of axial rotation of the human thoracolumbar spine. J. Bone Joint Surg (Am) 1967;49A:247-62 27 Farfan HF, Sullivan JDK. The relationship of facet orientation to intervertebral disc failure. Can J Surg 1967;10:179-85 28 Farfan HF, Huberdeau RM, Dubow HI. Lumbar intervertebral disc degeneration: the influence of geometrical features on the pattern of disc degeneration: a post mortem study. J Bone Joint Surg (Am) 1972;54A: 492-510 29 Lucas DB, Bresley B. Stability of the ligamentous spine (Biomechanics lab report 40). San Francisco: University of California, 1961 30 Armstrong JR. Lumbar disc lesions, 3rd ed. Edinburgh: Livingstone, 1965 31 Perey 0. Fracture of the vertebral end plates in the lumbar spine: an experimental biomechanical investigation. 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The effect of fatigue on the lumbar intervertebral discs. J Bone Joint Surg (Br) 1983;66B:199-203 47 Urban JP, Holm S, Maroudlas A. Diffusion of small solutes into the intervertebral disc: an in vivo study. Biorheology 1978;15:203-21 48 Adams MA, Hutton WC, Scott JRR. The resistance to flexion of the lumbar intervertebral joint. Spine 1980; 3:245-53 49 Adams MA, Hutton WC. Prolapsed intervertebral disc. A hyperflexion injury. Spine 1982;7:184-91 50 Newman PH. Sprung back. J Bone Joint Surg (Br) 1952;34B:30-7 (Accepted 6 August 1985)