mechanisms and effects of spinal high … 2002 - sm previous theories.pdf · review of the...

REVIEW OF THE LITERATURE

MECHANISMS AND EFFECTS OF SPINAL HIGH-VELOCITY,LOW-AMPLITUDE THRUST MANIPULATION: PREVIOUS

THEORIES

David W. Evans, BSc (Hons) Osta

ABSTRACT

Objectives: When the clinical efficacy of spinal manipulative treatment for spinal pain has been assessed,high-velocity low-amplitude thrust (HVLAT) manipulation and mobilization have been regarded as clinicalinterventions giving identical and equivalent biologic effects. The objective of this review is to criticallydiscuss previous theories and research of spinal HVLAT manipulation, highlighting reported neurophysiologiceffects that seem to be uniquely associated with cavitation of synovial fluid.

Data Source: The biomedical literature was searched for research and reviews on spinal manipulation.MEDLINE and EMBASE databases were used to help find relevant articles.

Study Selection: All articles relevant to the objectives were selected.

Data Extraction: All available data were used.

Data Synthesis: The main hypotheses for lesions that respond to HVLAT manipulation were criticallydiscussed: (1) release of entrapped synovial folds or plica, (2) relaxation of hypertonic muscle by suddenstretching, (3) disruption of articular or periarticular adhesions, and (4) unbuckling of motion segmentsthat have undergone disproportionate displacements.

Results: There appear to be 2 separate modes of action from zygapophyseal HVLAT manipulation. Intra-articular “mechanical” effects of zygapophyseal HVLAT manipulation seem to be absolutely separate from andirrelevant to the occurrence of reported “neurophysiologic” effects. Cavitation should not be an absoluterequirement for the mechanical effects to occur but may be a reliable indicator for successful joint gapping.

Conclusions: It is hoped that identification of these unique neurophysiologic effects will provideenough theoretical reason for HVLAT manipulation and mobilization to be assessed independently asindividual clinical interventions. (J Manipulative Physiol Ther 2002;25:251-62)

Key Indexing Terms: Chiropractic Manipulation; Synovial Fluid; Zygapophyseal Joint; Low Back Pain;Neurophysiology

INTRODUCTION

Spinal manipulation has been used for more than 2000years.1 There have been many attempts to explain thephysiology of the various effects of spinal manipu-

lation, particularly those of the high-velocity low-amplitude

thrust (HVLAT or HVT) type. As its name suggests, thistype of manipulation uses a high velocity “impulse” or“thrust” which is applied to a diarthrodial synovial jointover a very short amplitude. This type of manipulation isusually associated with an audible “crack,” which is oftenviewed as signifying a successful manipulation.2 The crack-ing sound is caused by an event termed “cavitation,” occur-ring within the synovial fluid (SF) of the joint (Fig 1).Cavitation is the term used to describe the formation andactivity of bubbles (or cavities) within fluid through localreduction in pressure.3,4

Although there is strong evidence for the clinical efficacyof spinal manipulative therapy for both acute and chronic

aResearch Associate, British School of Osteopathy, London,United Kingdom.

Submit requests for reprints to: David W. Evans BSc (Hons)Ost, 33 Granton Rd, Kings Heath, Birmingham B14 6HG, UK.

Paper submitted August 1, 2001.Copyright © 2002 by JMPT.0161-4754/2002/$35.00 � 0 76/1/123166doi:10.1067/mmt.2002.123166

251

low back pain,5,6 the physiological mechanisms behindthese clinical effects are not yet clear.7 This paucity of basicknowledge has led to the grouping of spinal HVLAT ma-nipulation and mobilization (a gentle, often oscillatory, pas-sive movement) together as 1 intervention when previouslyscrutinized for efficacy.5,6 The purpose of this review is tohighlight some of the unique effects that are seen withspinal HVLAT manipulation, particularly those that seemonly to occur in association with the cavitation event. Thismay help to provide enough theoretical reason to assessmobilization and manipulation as separate clinical entities.

DISCUSSION

Previous TheoriesIn a brief review, Shekelle8 states, “There are four main

hypotheses for lesions that respond to (HVLAT) manipula-tion: (1) release of entrapped synovial folds or plica, (2)relaxation of hypertonic muscle by sudden stretching, (3)disruption of articular or periarticular adhesions, and (4)unbuckling of motion segments that have undergone dis-proportionate displacements.” These “main hypotheses”will be discussed.

Release of entrapped synovial folds or plica. Intra-articular forma-tions have been identified throughout the vertebral column.9

Giles and Taylor10 demonstrated by light and transmissionelectron microscopy the presence of nerve fibers (0.6 to 1mm in diameter) coursing through synovial folds, remotefrom blood vessels, that were most likely nociceptive. Theyconcluded, “Should the synovial folds become pinched be-tween the articulating facet surfaces of the zygapophysealjoint, the small nerves demonstrated in this study may haveclinical importance as a source of low back pain.” Bogdukand Jull11 reviewed the likelihood of intra-articular entrap-ments within zygapophyseal joints as potential sources ofpain, leading to an “acute locked back.” They commented

that the theory of entrapment of tissue, causing pain as aresult of “pinching,” “demands that the joint be in, or nearto, a neutral position, for only in that position are thearticular surfaces sufficiently apposed to trap a meniscus (orsynovial fold). Consequently, this dictates that the lockedposition assumed by the patient is near to neutral, but theclinical features of an acute locked back are that the patientis locked in a flexion position, unable to extend.” Synovialtissue entrapment is therefore unlikely to be the cause of an“acute locked back” of this type but may be the cause ofother more transient “pinching” conditions.

Fibro-adipose meniscoids have also been identified asstructures capable of creating a painful situation.11,12 Bog-duk and Jull11 reviewed the possible role of fibro-adiposemeniscoids causing pain purely by creating a tractioningeffect on the zygapophyseal joint capsule, again after intra-articular pinching of tissue. They argued that it was unlikelythat the meniscoids would be sufficiently strong to distortthe zygapophyseal joint capsule. The basal segment of themeniscoid consists only of adipose tissue and synovium,and “traction exerted through such tissues would tend torupture them or cleave them from the joint capsule, ratherthan be transmitted in full force to the joint capsule.”

The theory of a meniscoid entrapment would also be anunlikely cause of an “acute locked back” because of theprerequisite of a neutral position, as discussed previously.Bogduk and Jull11 instead proposed that on flexion of thelumbar spine, the inferior articular process of a zygapophy-seal joint moves upward, taking a meniscoid with it. Onattempted extension, the inferior articular process returnstoward its neutral position, but instead of re-entering thejoint cavity, the meniscoid impacts against the edge of thearticular cartilage and buckles, forming a space-occupying“lesion” under the capsule: a meniscoid extrapment (Fig 2).A large number of type III and type IV nerve fibers (noci-

Fig 1. Cavitation. Schematic representation of surface geometry and shapes of growing cavities at a high separation speed (v � � vcas is likely with HVLAT manipulation) where doughnut (toroidal)-shaped cavities form around, rather than at the center, of the contactzone. A, During separation, the outer regions of the circular contact zone become pointed. This deformation occurs because at thisspeed, the central region of the contact zone separates, whereas the outer region remains almost unmoved, creating a circular rim. B,Surfaces snap back at the circular rim where the cavity initially forms. C, Coalescence of toroid into single dendritic cavity that growsto reach a maximum bubble size. D, The newly formed spherical bubble reaches its maximum size. E, Because of its instability, the singlebubble collapses to form a “cloud” of many smaller bubbles (demonstrable by radiography as a radiolucent region), which later shrinkas the gas and vapor dissolve (see later). Adapted from Chen YL, Kuhl T, Israelachvili J. Mechanism of cavitation damage in thin liquidfilms: collapse damage vs. inception damage. Wear 1992;153:31-51. Reproduced with permission from Elsevier Science.

252 Evans Journal of Manipulative and Physiological TherapeuticsHVLA Thrust Manipulation May 2002

ceptors) have been observed within capsules of zygapophy-seal joints.10,13,14 Pain occurs as distension of the jointcapsule provides a sufficient stimulus for these nociceptorsto depolarize. Muscle spasm would then occur to preventimpaction of the meniscoid. The patient would tend to bemore comfortable with the spine maintained in a flexedposition, because this will disengage the meniscoid. Exten-sion would therefore tend to be inhibited. This condition hasalso been termed a “joint lock” or “facet-lock,” the latter ofwhich indicates the involvement of the zygapophyseal joint.

The presence of fibro-adipose meniscoids in the cervicalzygapophyseal joints12,15 suggests that a similar phenome-non might occur, but in the neck the precipitating movementwould be excessive rotation. The clinical features of cervi-cal meniscoid extrapment would be those of an acute torti-collis in which attempted derotation would cause impactionand buckling of the extrapped meniscoid and painful cap-sular strain. Muscle spasm would then occur to preventimpaction of the meniscoid by keeping the neck in a rotatedposition. Under these circumstances the muscle spasmwould not be the primary cause of torticollis but a secondaryreaction to the extrapment of the meniscoid.12

An HVLAT manipulation, involving gapping of the zy-gapophyseal joint,16 reduces the impaction and opens thejoint, so encouraging the meniscoid to return to its normalanatomic position in the joint cavity. This ceases the dis-tension of the joint capsule, thus reducing pain11 (Fig 2).

It is noteworthy that the International Association for theStudy of Pain defines pain as “an unpleasant sensory andemotional experience associated with actual or potentialtissue damage, or described in terms of such damage.”17

This is significant because distension of a zygapophysealcapsule can cause pain without any actual tissue damage, acharacteristic of most episodes of nonspecific back pain.18

The onset of an acute locked back (or neck) is commonlyof little or no trauma,19 such as bending to pick up a

newspaper or turning over during sleep. Because theseconditions are unlikely to involve any significant tissuedamage, pain may be due only to potential damage. Non-traumatic onset such as that described previously shouldtherefore not be a contraindication for a high-velocity pro-cedure. On the contrary, in the absence of “red flags” forphysical risk factors,20,21 a nontraumatic onset should pro-vide a good indication for a favorable outcome from anHVLAT manipulation, even in a very painful and acutestate. This argument merits further investigation.

Zygapophyseal joint gapping induced during an HVLATmanipulation would further stretch the highly innervatedjoint capsule, leading to a “protective” reflex muscularcontraction, as shown in electromyograpic studies.22-30 Themost important characteristic of a manipulative procedurethat will provide joint gapping, before the induction ofprotective reflex muscular contraction, would be high ve-locity. Brennan et al31 found that the thrusting phase of anHVLAT manipulation required 91 � 20 ms to develop thepeak force. If this period is compared with the time delaybetween the onset of the thrusting force and the onset ofelectromyographic activity, which ranges from 50 to 200ms,24 we can see that a force of sufficient magnitude to gapthe joint can be applied in a shorter time than that requiredfor the initiation of a mechanoreceptor-mediated muscularreflex. Furthermore, once the muscle is activated (ie, there isan electromyographic signal), it will take approximatelyanother 40 to 100 ms until the onset of muscular force. Ittherefore seems unlikely that there are substantial muscularforces resisting the thrusting phase of HVLAT manipula-tion.24 Thus HVLAT manipulation would again appear tobe the treatment of choice for a meniscoid extrapment.

The cavitation event may not be a prerequisite for a“successful” HVLAT manipulation in the case of a menis-coid extrapment and may be an incidental side effect ofhigh-velocity zygapophyseal joint gapping (which would be

Fig 2. Meniscoid extrapment. A, On flexion, the inferior articular process of a zygapophyseal joint moves upward, taking a meniscoidwith it. B, On attempted extension, the inferior articular process returns toward its neutral position, but instead of re-entering the jointcavity, the meniscoid impacts against the edge of the articular cartilage and buckles, forming a space-occupying “lesion” under thecapsule. Pain occurs as a result of capsular tension, and extension is inhibited. C, Manipulation of the joint, involving flexion andgapping, reduces the impaction and opens the joint to encourage re-entry of the meniscoid into the joint space (D). From Bogduk N.Clinical anatomy of the lumbar spine and sacrum. 3rd ed. Edinburgh: Churchill Livingstone; 1997. p. 202. Reproduced with permissionfrom Churchill Livingstone, a division of Harcourt Publishers.

253Journal of Manipulative and Physiological Therapeutics EvansVolume 25, Number 4 HVLA Thrust Manipulation

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a prerequisite for success). Audible indication of successfuljoint gapping may, however, be regarded as desirable initself as a clinical measure of “success.” A clinician’s per-ception of the occurrence of cavitation during an HVLATmanipulation has been shown to be very accurate26 andwould therefore be a reliable measure of a “successful” jointgapping.

Gainsbury32 claims that these “acute locked joints” oftenoccur in joints with a history of “hypermobility.” However,there is no clinical evidence to validate this statement, andit is therefore only speculative. In theory, increased segmen-tal mobility, or more accurately, decreased active control ofintersegmental motion around the “neutral zone” (the mo-tion region of the joint where the passive osteo-ligamentousstability mechanisms exert little or no influence33,34) wouldbe a logical predisposing factor for zygapophyseal meniscalextrapment. Consequently, symptom-relieving HVLAT ma-nipulation will not provide a lasting solution to this seg-mental instability, and a segmental stabilization exerciseregimen should form the basis of rehabilitation35 in anattempt to avoid future recurrence.

Although meniscoid replacement may be the mechanismby which pain relief would be achieved from zygapophysealHVLAT manipulation in an “acute locked back,” it does notexplain reported nonmechanical effects that are associatedwith HVLAT manipulations (see following text).

Relaxation of hypertonic muscle by sudden stretching. Viscoelasticity isa property of soft tissues whereby the strain induced in thetissue is dependent on the rate of loading of the appliedstress.36 The connective tissue in and around the musclebelly, tendons, joint capsules, and ligaments all exhibitviscoelastic behavior under loading.37-39 This is thought tobe due to biochemical interaction between the collagenfibers and the ground substance.40 When ligament and ten-don specimens are subjected to increased strain rates (load-ing rates), the linear portion of the stress-strain curve be-comes steeper, indicating greater stiffness of the tissue athigher strain rates.41-43 This demonstrates that the faster therate of loading is, the more energy is “stored” within thetissue, allowing it to withstand larger forces when the forceis delivered more rapidly. This property is a valuable at-tribute in tendons44 but would also imply that rapid loadingwould not cause an efficient mechanical stretch of a “hy-pertonic” muscle and would be more likely to damagemusculotendinous structures in a similar way to “ballistic”type stretching.45 Efficient stretching should be of a verylow velocity, or at a constant force to cause “creep,” andshould be maintained for at least 12 to 18 seconds.39,46

The forces produced during HVLAT manipulation of azygapophyseal joint can be relatively large.47 However, ifapplied properly, these forces should not be significantlytransferred to the soft tissues and should be predominantlydissipated within the SF, which also has viscoelastic prop-erties,48-53 for cavitation to occur.54 Watson et al53 showedthat the “pulse area” parameter from an accelerometer mea-

suring cavitation (a measure of kinetic energy imparted tothe accelerometer) was highly correlated with the “drop inload” (resistance to distraction force) of a joint. Thus thesynovial fluid absorbs much of the kinetic energy requiredto cause cavitation.

Mechanoreceptors, proprioceptors, and even nociceptiveafferents of both joint capsules and musculotendinous struc-tures have long been viewed as the probable “gateway”through which the nervous system (and consequently motor“tone”) would be influenced by HVLAT manipula-tion.25,30,55-64 Avramov et al65 have shown that loading ofthe zygapophyseal joint excites 3 patterns of nerve dis-charges: short-duration bursts during change in loading,prolonged discharges at low load levels, and prolongeddischarges at high load levels, indicating that different unitsin the joint capsule have different levels of stress thresholds.It seems logical, however, that the receptor populations thatare activated on passive high load would be present in aprotective role and would tend to activate rather than relaxor inhibit protective muscular tissue. This is especially so,because it has been previously suggested that if forcesinvolved with a spinal HVLAT manipulation22,47,66,67 weretransferred to the surrounding joint capsule and soft tissues,nociceptive afferents would be activated.57,58 Lederman68

states, “It has long been believed that manual techniquessuch as high-velocity thrusts or adjustments can normalizeabnormal motor tone. The reduced motor tone is attributedto the stimulation of inhibitory afferents by manipulation.This is highly unlikely as sudden stretch produced by thisform of manipulation will excite rather than inhibit themotor neuron.”

The protective role of the musculature against potentiallyharmful force to joints, by way of reflex arcs, creates syn-ergism between the passive (capsuloligamentous) and active(muscular) joint restraints. These have been studied in var-ious animal and human joints.30,69-73 Wyke30 distracted thezygapophyseal joint between C3 and C4 in anesthetized catsand measured an increased electromyographic response as-sociated with such distractions in the neck and limb mus-culature. He concluded from this experiment that joint cap-sule mechanoreceptors will influence (most likely throughreflex pathways) the activation of the neck and limb mus-culature. These experiments indicated that an excitatorystimulus rather than an inhibitory (relaxatory) stimulus wasgiven to these muscles after stress placed through theirrelated joint capsules. Because of the rich innervation ofhuman zygapophyseal joint capsules,13,14,30,62,74 it would bereasonable to suggest that a similar synergistic relationshipbetween the capsular and ligamentous structures andparaspinal muscles occurs also in humans.

Observations made by Herzog et al22-24,26-29 confirm this.They observed that HVLAT manipulation caused (excita-tory) reflex responses in the back and limb musculature.They decided that the observed reflex responses could havea variety of origins (“the external force, the rate of force


application, the impulse, the cavitation, etc”) and thereforecompared the reflex responses of HVLAT manipulationtreatments that resulted in cavitation of the joint (as judgedby the treating chiropractor and confirmed by accelerometermeasurements) with corresponding treatments that did notresult in cavitation.26 They concluded, “the reflex responsesseemed to be the same in both cases, which suggests thatcavitation was not needed to elicit the observed reflexresponses.” They further attempted to evaluate the role ofcavitation in eliciting reflex responses by measuring reflexresponses associated with low-velocity “treatments” (ie,treatments in which the point and direction of force appli-cation were identical to the previous treatments; however,the peak forces were reached within approximately 2 to 3seconds rather than 100 to 150 ms). These slow treatmentsnever resulted in measurable reflex responses, regardless ofwhether cavitation was elicited.29 Thus they concluded,“Neither the cavitation event nor the magnitude of theapplied force caused the reflex activation of the back mus-culature.” High-velocity movement alone seemed to acti-vate the response, indicating that the reflex muscular con-tractions measured by electromyography were mediated bymechanoreceptor afferents in the joint capsules and mus-cles.

There is recent evidence that both lumbar spine mobili-zation and manipulation result in significant transient atten-uation of alpha motor neuronal activity, as measured by theamplitude of the extremely sensitive gastrocnemius Hoff-mann reflex (H-reflex or H-wave), with a return to baselinevalues exhibited 30 seconds after intervention.75 Cavitationwas also an unimportant component of this temporary ef-fect. However, it is quite likely that this transient H-waveattenuation is simply a latent artefact of the mechanorecep-tor-mediated excitatory muscular reflex response and there-fore has equivocal clinical relevance.

Herzog et al27 came to the logical conclusion that “anaudible release does not (by itself) evoke muscle activationor a joint proprioceptive reflex response as has been spec-ulated in the literature.” This conclusion can be taken in 2directions. If the excitatory muscular reflex response (andconsequential H-wave attenuation) was taken as an impor-tant requisite for the beneficial effects of an HVLAT ma-nipulation, then the cavitation event would be unimportant.However, it could also be argued that these muscular reflexresponses are incidental to any potentially beneficial effectsachieved from an HVLAT manipulation, and the cavitationevent alone produces responses not observable by electro-myography (see following text).

A rapid “sudden stretch” seems unlikely to produce aclinically beneficial and lasting neurophysiologic relaxationof hypertonic muscles. Therefore, if an HVLAT manipula-tion has a lasting modifying effect on the tone or “irritabil-ity” of muscles associated with the joint, the nervous systemis being influenced in some other way. If cavitation was anunimportant element of a spinal HVLAT manipulation and

it was only mechanoreceptor stimulation that created thebeneficial effects, it should follow that continual repetitiveHVLAT manipulations immediately after the initial cavita-tion-producing thrust (ie, within the 15- to 20-minute “re-fractory period” during which further cavitation is not pos-sible) would create cumulative beneficial effects. From clin-ical experience, this is clearly not the case but requiresfurther investigation.

The term “relaxation of hypertonic muscle”8 implies thatthere is a reduction of alpha-motorneurone excitability oractivity to innervated muscle. Facilitation of some motorreflexes, however, is independent of changes in the excit-ability of afferent terminals in the dorsal horn and of mo-torneurones. A more likely explanation for the behavior ofthis “hypertonic muscle” is that its innervation is mediatedby sensitized spinal interneurones.76 Muscles innervated bya sensitized interneurone population, eliciting properties ofsecondary hyperalgesia (sometimes described in terms of“myofascial trigger points”77,78) have been associated withvery small loci of spontaneous electromyographic activi-ty.79,80 These hyperalgesic regions seem also to be associ-ated with a palpable “taut band,” which gives increasedmuscle “tone.”81

After zygapophyseal HVLAT manipulation, reductionsin paraspinal spontaneous electromyographic activity82,83

and reduced hyperalgesia of paraspinal myofascial triggerpoints84 have been demonstrated. This finding seems toindicate that any observable “motor” effects that HVLATmanipulation has may be mediated by alterations in centralsensitization of the dorsal horn.

Regarding alterations in central sensitization, it has alsobeen demonstrated that zygapophyseal HVLAT manipula-tion caused not only a reduction of paraspinal hyperalgesiain subjects with symptoms84-86 but also an increase inparaspinal pain thresholds to a noxious stimulus in subjectswith no symptoms.87

Thus it seems more appropriate to describe one of theneurophysiologic effects of zygapophyseal HVLAT manip-ulation as creating “hypoalgesia” (of the dorsal horn asso-ciated with) the spinal segment manipulated,88 rather than“relaxation of hypertonic muscle,” whatever the mechanismby which this is achieved.

In a series of studies, Brennan et al31,89-92 investigated theeffect of spinal HVLAT manipulation causing cavitation(“sufficient to produce an auditory release or palpable jointmovement”) on cells of the immune system. They foundthat a single manipulation to either the thoracic or lumbarspine resulted in a short-term priming of polymorphonu-clear neutrophils to respond to an in vitro particulate chal-lenge with an enhanced respiratory burst (RB) as measuredby chemiluminescence in subjects with and without symp-toms. The enhanced RB was accompanied by a two-fold risein plasma levels of the neuropeptide substance P (SP).

SP is an 11-amino acid polypeptide and is one of a groupof neuropeptides known as tachykinins. These are peptides


that are produced in the dorsal root ganglion (DRG) andreleased by the slow-conducting, unmyelinated C-poly-modal nociceptors in a process known as an “axon reflex.”They are released into peripheral tissues from the peripheralterminals of the C-fibers, modulating the inflammatory pro-cess by “neurogenic inflammation.”93-96 They are also re-leased from the central terminals of the nociceptors into thedorsal horn of the spinal cord, where they modulate painprocessing and spinal cord reflex activity.97-99

This neurophysiologic effect of spinal HVLAT manipu-lation seems to be force threshold-dependent.31,100 Thethreshold was found to lie somewhere between 450N and500N for the thoracic spine and 400N for the lumbarspine.101 When compared with data from biomechanicalstudies of spinal manipulation,47 these forces would besufficient to cause cavitation. The “SP” studies used “shammanipulation” as a control, consisting of a “low-velocitylight-force thrust to the selected segment,” rather like amobilization. This illustrates that zygapophyseal HVLATmanipulations that cause cavitation produce physiologicaleffects, not demonstrable by electromyography, that aretotally different from effects created by zygapophyseal ma-nipulations that do not cause cavitation.

It has been proven that this neuropeptide release canoccur only if cavitation is produced; however, it has alsobeen proven to be a unique occurrence with manipulation ofa zygapophyseal joint. These effects do not occur if HVLATmanipulation is applied to a peripheral joint such as theankle joint.102 This result indicates that this response to aspinal HVLAT manipulation, although obviously mediatedby the nervous system, cannot be explained by simplemechanoreceptor-mediated reflex arcs. An equivalent forceor pressure exerted directly to other parts of the musculo-skeletal system such as the glutei91,102 or even directly to invitro neutrophils in an attempt to manifest a cellular stressresponse103 also fails to create a significant increase inplasma levels of SP. It would seem, therefore, that thiseffect of zygapophyseal HVLAT manipulation might de-pend on the unique anatomic location of these joints.

The zygapophyseal joints of the spine are in very closeproximity to the DRG at each intervertebral segment.Badalemente et al104 demonstrated that production of SPcould be induced by mechanical stimulation of the DRG.From the aforementioned experiments conducted by Bren-nan et al,31,89-92,102 it is likely that a form of stimulation ofthe DRG caused the production of SP. However, in view ofbiomechanical studies of HVLAT manipulation,22,25,105-107

this stimulation could not realistically be mechanical.Brennan et al did not provide a full explanation of the

exact cause of the SP release but instead drew the reservedconclusion that “regardless of the mechanism whereby spi-nal manipulation primes phagocytic cells for an enhancedRB, it is a consistent response of cells from asymptomaticsubjects receiving manipulation that is not observed fromasymptomatic subjects receiving either sham manipulation

or soft tissue mobilization. Therefore, it is likely that RBactivity can be used as a physiological indicator that a truemanipulative procedure of the thoracic spine (and the lum-bar spine92) has been carried out. As clinical research in-volving the therapeutic effects of manipulation becomesmore common, the need for a tool to verify that an appro-priate sham procedure has been administered becomes cru-cial to understanding treatment efficacy. The monitoring ofbiological effects such as those described in this study mayprovide that tool.”31 The efficacy of this temporarily en-hanced RB as a “reliable quality control for monitoring thedelivery of both a manipulation procedure and a controlmobilization procedure in patients enrolled in a randomizedcontrol trial of spinal manipulative therapy” has since beenshown.91

Disruption of articular or periarticular adhesions. The normal range ofmovement of any synovial joint has been termed the “phys-iological zone.”108 Before the application of the “thrust”phase of an HVLAT manipulation, a “pre-load” force isapplied.47,109 This involves taking the viscoelastic SF to awell-defined elastic recoil (which is particularly strong withsmall displacements),49 characterized by increased stiff-ness.53 Sandoz108 described this as the “physiological bar-rier.” The additional impulse, which creates the (high-ve-locity) movement between the articular surfaces of the joint,is ultimately delivered to the SF.54 It is known that whensubjected to very high shear rates, liquids begin to behavemechanically like solids; for example, fracturing like abrittle solid.110,111 Cavitation occurs when the articular sur-faces are separated through the elastic recoil of the SF abovea critical velocity (vc), causing the SF to “fracture” or“crack” open like a solid. A proportion of the “cracking”noise during cavitation of SF may therefore be consideredas synonymous with the “nucleation” or “inception” of thecavity112,113 (Fig 1).

It is interesting that the speed of force application duringspinal HVLAT manipulation appears clinically relevant. Ithas been shown that less total force is required to producecavitation when a fast rate of force application is usedcompared with a slow rate.66 Thus, if the rate of forceapplication is fast (v � � vc as in Fig 1), the total forceapplied to the manipulated joint will be less, and conse-quently, potentially safer (as long as the force is appliedover a very short amplitude, ie, within the “physiologicalzone”).

A second “crack” cannot be produced until approxi-mately 20 minutes after cavitation, because during thisperiod gas remains in solution in the form of small bubblesthat act as nuclei.114,115 This period is known as the “re-fractory period.”3,108 Any further tension simply reduces thepressure of the gas bubbles, leaving the liquid relativelyundisturbed and under no influence of the tension.3 Thus,during the refractory period, the SF offers little resistance toforce, and a temporary increased range of motion is given tothe joint. If a second attempt at “cracking” the joint is made


during the refractory period, the joint will immediately bepushed toward the limit of anatomic integrity (the anatomicbarrier of resistance), because the (fluid cohesion) elasticbarrier of resistance has been temporarily eliminated by theinitial crack.116 Any further resistance to movement offeredby this joint is from anatomic tissues.

Mierau et al117 compared manipulation (“high velocity-low amplitude force, often accompanied by an audiblecracking sound coming from the target joint”) and mobili-zation (“a gentle, often oscillatory, passive movement”) ofthe third metacarpophalangeal (MCP) joint. They found thatthe manipulated group demonstrated a significant temporaryincrease in passive MCP joint flexion over the mobilizedgroup and concluded, “manipulation and mobilization aredistinct therapies with different effects on joint function andshould not be considered equivalent as they have been in thepast.” It is likely that this “different effect” is solely due tothe cavitation of the SF of the joint and not due to anymechanoreceptor-mediated muscular reflex response. Thisis because the collateral ligaments of the MCP joints playprimary roles in joint stability,118 and, hence, stability sup-plied by muscles would not be very significant. Any in-crease in range of motion would therefore be relativelyindependent of muscular influence.

Short-term increases in cervical range of motion imme-diately after HVLAT manipulation have previously beenshown.119-122 Lewit123 examined the cervical spine of 10patients before operation (most for abdominal surgery) andre-examined during anesthesia with myo-relaxants and in-tubation with artificial respiration. In all cases movementrestriction remained unchanged and was even more easilyrecognizable under narcosis, because the patient was com-pletely relaxed. He concluded, “the importance of this ex-periment is not only that it proves that movement restrictionis (also) an articular phenomenon, but it also proves we aredealing with a mechanical obstacle in the joint.”

This “obstacle” may be due to meniscoids as mentionedpreviously, but this situation is more likely to present as apainful “acute locked” joint rather than just an asymptom-atic “restriction.” The latter condition may simply be due toatmospheric pressure combined with the cohesive propertyof SF, creating strong elastic recoil.2,3,49,50,54,115 This find-ing suggests that the temporary increase in mobility ofzygapophyseal joints after HVLAT manipulation found byNilsson et al122 may also be relatively independent of anyneurophysiologic “reflex” effects on the motor system.

Manipulation of an intra-articular “adhesion” that ismaintained only by atmospheric pressure and the cohesivebehavior of the SF54 has the potential only to temporarilyincrease range of motion. SF adhesion between articularsurfaces (reducing mobility) cannot alone create a noxiousstimulus. Burton et al124 have shown that symptomaticimprovement in patients with low-back pain treated withmanipulation does not rely on alterations in mobility and ispoorly correlated with increased sagittal mobility. Conse-

quently, removal of this adhesion by breaking the “seal”created by the SF cannot explain pain-related or nonme-chanical effects of zygapophyseal HVLAT manipulation.

It is also possible that after injuries to a zygapophysealjoint such as a capsular tear or a subchondral fracture,intra-articular hemorrhage could act as a precipitating factorfor intra-articular fibrosis.12 It is known from studies ofanimal and human knee joints that immobilization of thejoint results in proliferation of intra-articular fat pads.125,126

Such adhesions could account for the stiffness of cervicaljoints evident on manual examination of inter-segmentalmotion as reported in the literature.123,127 These “adhe-sions,” however, are likely to be of a collagenous na-ture125,128 and would thus have viscoelastic properties.40 Ifincreased mobility of these tissues was required, they shouldbe “stretched” at a slower rate than is involved in anHVLAT manipulation.46,129

Unbuckling of motion segments that have undergone disproportionatedisplacements. This vague heading is assumed to be in relationeither to realignment of joint “subluxations” or to previousspeculations of the “replacement” of fragments from thenucleus pulposus of the intervertebral disks after HVLATmanipulation.

The concept that HVLAT manipulation “realigns” or“replaces” “misaligned” or “subluxed” joints is one of theoldest theories of spinal manipulation.130 This theory wasthe likely reason that “bonesetters” gained their name.20

One of the reasons for the conception of this theory is dueto the audible joint “crack” caused by cavitation, whichoften conveniently coincides with immediate symptomaticrelief. Before cavitation was widely accepted as the sourceof the crack, manipulating practitioners felt that they were“putting the bone back in place” (many patients still holdthis concept after HVLAT manipulative treatment, and pa-tient education to dispel these inaccurate beliefs is verynecessary).

Recent biomechanical studies examining the motions ofvertebrae after HVLAT manipulations show this “position-al” theory to be false and merely demonstrate transientrelative movements of the manipulated vertebrae associatedwith cavitation.25,105-107,131 Radiographs, computed tomog-raphy, and magnetic resonance imaging scans have beenshown to be an unreliable method for diagnosing backpain.132-136 Therefore, with regard to sources of spinal painthat respond to HVLAT manipulation, “subluxations” or“misaligned vertebrae” appear to be an epiphenomenon.

The theory of the “replacement” of fragments of thenucleus pulposus of the intervertebral disks after HVLATmanipulations, as advocated by Cyriax137 and those whofollow his approach,138 is another unlikely theory to explainboth the cracking sound and symptom-relieving effects ofspinal HVLAT manipulations. If this were the case, it wouldnot be possible to produce a joint “crack” from many othersynovial joints in the body including MCP, sacroiliac, oc-cipito-atlantal, and atlanto-axial joints, where there are no


intervertebral disks (or any similar structures) present. Fromthis theory, it also should not be possible to produce a“crack” from all spinal segments, because a displaced frag-ment of nucleus pulposus (that needs “replacing”) wouldnot occur in all spinal segments of every person.

An acute cervical or lumbar disk herniation has generallybeen regarded as a contraindication to HVLAT manipula-tion of the herniated segment,139,140 especially in the pres-ence of severe or progressive neurologic deficit. However, along-term beneficial effect of manipulation on symptomaticlumber disk herniation has been demonstrated, showingimprovements in leg pain, back pain, and self-reporteddisability.141 It is unlikely that these improvements weredue to structural changes to the disk because, although therehave been case reports of apparent reductions of smalllumbar disk protrusions after manipulation,142 computedtomography imaging and myelography have failed to dem-onstrate persistent reduction of disk protrusion after manip-ulation.143-145

The nucleus pulposus is rich in hydrophilic (water-bind-ing) glycosaminoglycans (in the young adult). During load-ing of the spine, it acts hydrostatically,146 allowing a uni-form distribution of pressure throughout the disk. Thereforethe disk acts as a cushion, storing energy and distributingloads.147 The nucleus pulposus also has viscoelastic (rate-dependent) properties, causing greater stiffness (resistanceto deformity) of the tissue at higher strain rates. Recentbiomechanical evidence148 suggests that variable transientchanges in intradiscal pressure do arise during spinal ma-nipulation, but the clinical significance of this is unknown.Excessive displacements of the fluid nucleus, from the areaof greatest to the area of least load, may also result from theadoption of prolonged static positions.148 Thus it would belogical that if a nuclear fragment was to be gradually “en-couraged” to safely return toward the center of the interver-tebral disk, then a more static or very low velocity maneuvershould be sought. Bogduk and Jull11 reviewed the possibil-ity of the replacement of an “intra-discal nuclear displace-ment” by manipulative therapy. They described a series ofcombined movements of the “affected motion segment,”emphasizing the word “progressively,” thereby discountinga high-velocity procedure.

The existence of gas bubbles in synovial joints (aftercavitation) has been demonstrated by radiography as a dark,intra-articular radiolucent region since early in the twentiethcentury.3,114,149-152 Magnetic resonance imaging scans haveshown that lumbar HVLAT manipulation gaps zygapophy-seal joints and increases dimensions of the intervertebralforamen.16,153 These studies provide clear evidence that theanatomic source of the cracking sound associated withspinal HVLAT manipulations is the zygapophyseal jointsand not the intervertebral disks, and that the audible “crack”is associated with cavitation of the SF.

Summary of Previous TheoriesFrom this information, there seem to be unique neuro-

physiological effects associated with cavitation from a zy-gapophyseal HVLAT manipulation in subjects with andwithout symptoms.31,82-87,89-92,102

Some reasonable theoretical “mechanical” explanationshave been offered for beneficial mechanisms of zygapophy-seal HVLAT manipulation for acute low back pain.11 How-ever, because of the non-nociceptive behavior of chroniclow back pain (involving “central” pain mechanisms), clin-ical improvements in this condition from manipulation can-not be explained by “mechanical” theories alone or by anypublished hypothesis.7,25 There are also non–symptom-related neurophysiologic effects that also cannot be suffi-ciently explained by any published theory.31,82-87,89-92,102

CONCLUSION

There seem to be 2 totally separate modes of action fromzygapophyseal HVLAT manipulation. The intra-articular“mechanical” effects of zygapophyseal HVLAT manipula-tion seem to be absolutely separate from, and irrelevant to,the occurrence of observed “neurophysiologic” effects.Cavitation should not be an absolute requirement for themechanical effects to occur but may be a reliable indicatorfor successful joint gapping.

When clinical efficacy has been previously assessed, spi-nal mobilization and HVLAT manipulation have beengrouped together as equivalent interventions.5,6 This hasalways implied that these 2 interventions have identicalbiologic effects. There may now be enough theoreticalreasons to assess mobilization and manipulation as separateclinical entities.

ACKNOWLEDGMENTS

Thanks for useful comments are due to Prof. John Blake,University of Birmingham (cavitation), and Mick Thacker,Kings College, London (neurophysiology). Thanks are alsodue to Will Podmore, British School of Osteopathy, Lon-don, for proofreading the manuscript.

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