CURRENT CONCEPTS ON THE SAGITTAL BALANCE AND CLASSIFICATION OFSPONDYLOLYSIS AND SPONDYLOLISTHESIS

Discipline of Orthopaedics and Traumatology, Faculdade de Medicina de Jundiaí, Jundiaí, SP, Brazil

The term spondylolisthesis is defined as a translation of onevertebra over another in the anterior or posterior direction. Inthe adult, this occurs in the lumbar column as a result of adefect in bone architecture, trauma or degenerative process.1The term spondylolisthesis is derived from the Greekspondylos, meaning "vertebra", and olisthesis, meaning "toslide". The first observation of spondylolisthesis occurred in1772 by the Belgian obstetrician Herbiniaux2during a deliv-ery complicated by a narrowing in the channel because of aslippage of L5 vertebra over the sacrum.This term was first used in 1854 by Kilian in Lonstein et al.3Spondylolisthesis is defined as a translation of one vertebralbody over the adjacent caudal vertebra in an anterior or, inmore serious cases, anterior and caudal direction. Spondyloly-sis is a defect in the pars interarticularis, but without occurrenceof slippage.Spondylolisthesis has been a condition difficult to under-stand for orthopaedists, neurosurgeons and paediatricians,because of the great variety of existing anatomical and clinicalforms. There are few pathological conditions of the column inwhich there is so much therapeutic controversy.Considering that the spondylolisthesis is "a slippage of aportion of the column over other adjacent part", we mustremember that the column that slid also moved the entiretrunk, and this may bring clinical consequence.The aetiology of this disease is multifactorial and is notyet perfectly clear. The natural history is not well establishedfrom the point of view of the knowledge of its real causes,pathogenesis and development.4Spondylolisthesis and spondylolysis are usually well tol-erated by patients, but in some cases the severity of thesymptoms and a condition unresponsive to conventionalmedical treatment have caused the indication for surgicaltreatment.

Epidemiology and aetiology

The incidence of spondylolysis in the general population isabout 6%, with a male: female ratio of 2:1.6

The incidence of spondylolisthesis in children under 6years is 2.6%, while in adults it is 5.4%.6

The degenerative spondylolisthesis rarely affects individ-uals below the age of 40 years, and is four to five times morecommon in women than in men. In a study by Love et al.,7sub-jects who had facet orientation >45?in the sagittal plane were25 times more likely to develop degenerative spondylolisthe-sis.

There seems to exist a genetic and familial association withspondylolysis and spondylolisthesis, because 26% of patientswith isthmic spondylolisthesis had first-degree relatives withthe same disease.8

The incidence varies according to ethnicity: it is more com-mon in Caucasian than in black people. In a tribe of Eskimosin Alaska the incidence reaches about 50%.9

The exact aetiology of most cases remains obscure.

The dysplastic lesions of the pars interarticularis, fracture orof the elongament and of spina bifida conceal a broad distalspinal canal. Dysplasia in both facets (lower lumbar and uppersacral) is a common finding in spondylolisthesis, especially inthose with high grade.

The superior sacral facet together with the lower lumbarfacet forms a bone hook which prevents translation. Dysplasiacan occur in either or both facets. Thus, the hook effect is lost.6

The presence of spondylolysis/spondylolisthesis is rare innon-ambulatory patients, which attaches importance to theorthostatism role and of repeated microtraumas in the devel-opment of spondylolysis.Biomechanical studies have demonstrated an increase instress in the pars interarticularis with the column in exten-sion and increase of shear forces through the same area, withpersistence of lordosis.7Activities that increase lordosis and maintain the columnin extension, such as olympic gymnastics, diving, weightlift-ing, volleyball, football and pathologies such as kyphosis,increase the incidence of fracture of the pars and of spondy-lolysis and spondylolisthesis.

10Sagittal balance in spondylolisthesis

The spondylolistheses are divided into high (slippage >50%)and low (slippage 50%) grade.

The classifications used for spondylolisthesis are not use-ful for surgical treatment indications and, as noted in thelast decade, the sagittal balance is the key factor for surgicaltreatment.11

One explanation for the aetiology of developmentalspondylolisthesis, which takes into account the sagittal bal-ance, is that, in the presence of spondylolysis and bonedysplasia, the mechanical stress applied to the lumbosacraljunction is increased because of the altered sacro-pelvic mor-phology, which leads to an abnormal secondary spino-pelvicequilibrium. Because of bone remodelling by growth plates(Heuter-Volkman law), a secondary deformity of the body ofL5, sacrum and pelvis also alters the biomechanical forces inthe lumbosacral column, which contributes to the progres-sion of spondylolisthesis, in a process similar to what occursin Blount disease.

The pelvic incidence (PI) is a specific and constantparameter for each individual, measured in the lumbosacralradiograph on the profile incidence, and defined as theangle between the line connecting the midpoint of upperplateau of S1 and the centre of femoral rotation and the line

Fig. 1 - (A) Pelvic Incidence (PI) is defined as the angleformed by the intersection of a line drawn from the centreof the femoral head towards the midpoint of the sacralendplate (o-a) and a line perpendicular to the centre of thesacral endplate (a). The sacral endplate is defined by asegment (b-c) formed between the posterior horn of thesacrum and the anterior top of the S1 sacral promontory. (B)When the femoral heads are not perfectly overlapped, thecentre of each one of them is marked and a line drawnbetween two points (q-p) will connect the centre of the twoheads. The line (o-a) will be drawn from the centre of theline (q-p), i.e., point (o), to the centre of the sacral endplate.

perpendicular to the upper plateau of S1. PI increases slightlyand consistently in adulthood.12The value of PI is higher inspondylolisthesis, increasing linearly, according to the sever-ity of slippage12(Fig. 1).The pelvic tilt (PT) and the sacral slope (SS) measure thesacro-pelvic orientation in the sagittal plane, being evidencedin the lumbosacral lateral view. SS is defined as the anglebetween the upper horizontal plateau and S1, while PT is theangle between the line connecting the midpoint of the upperplateau of S1 and the centre of femoral rotation with a verticalline (Figs. 2A-B and 3B).PT has a value (+) when the line (o-a) is located posteriorto VRL value and (-) when the line (o-a) is anterior to VRL.We must understand that PI is a measure of a staticstructure. PT and SS, on the other hand, are dependent pos-itions, because they depend on the angular position of thesacrum/pelvis in relation to the femoral head, which changes

BFig. 2 - (A) Pelvic tilt (PT) is defined by the intersection of avertical reference line, which originates from the femoralhead centre (o) and the midpoint of the sacral endplate (a).(B) PT can be influenced by PI, since they share the line(o-a) and the terminal sacral plate is a common referenceline for both.

in the orthostatic and sitting positions. PT/SS ratio is alsoaffected by the bending and lumbosacral-pelvic extension.

PI is the sum of SS and PT (Fig. 3B); then, IP is a strongdeterminant of the spatial orientation of the pelvis in theosthostatism, i.e. the higher the PI, the greater will be the PTor SS, or both. The normal values of PI, SS and PT in childrenare 49.1?, 41.4?and 7.7?, respectively.13In adults the normalvalues are 51.8?, 39.7?and 12.1?.12

The values in spondylolisthesis12are shown in Table 1.In the study by Roussouly et al.,14patients with high PI andSS result in increased shear force incident on the lumbosacraljunction, which creates more stress on the pars interarticularisof L5. But in those patients with low PI and a minor SS, theremay be an impact among the posterior elements between L5and those of L4 and S1 during extension, thereby causing aneffect of "nutcracker" in pars interarticularis of the 5th lumbarvertebra.

BFig. 3 - (A) Sacral tilt (SS) is defined as the intersection ofthe horizontal reference line (HRL) and the sacral endplate(b-c). (B) The sacral slope (SS) is related to PI and PTbecause it shares a reference line (b-c) in common alongthe sacral endplate..

The sacral projection (distance from the sacrum to a plumbline from C7) is another biomechanical determinant. Typically,the plumb line (PL) passes through S1 (Fig. 4).

Because of these morphological changes, the sagittal bal-ance can only be achieved by hyperlordosis. Greater verticaltilt of the sacrum will be required to maintain sagittal balance,when this is not possible only with hyperlordosis. This verti-calization of the sacrum is accompanied by contracture of thehamstrings, which circumvent caudally the ischial muscles,and the anterior pelvis cephalad.14

With these data, there are three possible biomechani-cal outcomes: first, the forces generated by an increase inlumbar lordosis have, as consequence, the development andprogression of spondylolisthesis; and second, the biomechan-ical changes generate changes in posture and gait that arecompensatory mechanisms to maintain sagittal balance; andfinally the biomechanical changes mould the adjacent verte-brae.

Evidence of the presence of abnormal sagittal spino-pelvicalignment in spondylolisthesis

Although the correlation between pelvic incidence (PI) andspondylolisthesis is evident, there are no published data inthe literature that may confirm the cause/effect relationshipbetween these two. However, as the pelvic incidence (PI) isC7C7

- 0 +
Negativo Neutro Positivo

ABFig. 4 - Sagittal Balance: PL = plumb line. The A line isdrawn from the superior-posterior border of S1perpendicular to the vertical edge of the radiograph. Itslength is measured in millimetres. The B line is drawn fromthe centre of C7 perpendicular to the vertical edge of theradiograph. Its length is measured in millimetres.

a morphological parameter that describes the shape of thepelvis, an increased PI is associated to an increase in lumbarlordosis, which predisposes to mechanical changes of the lum-bar column and of the lumbosacral junction and increases therisk of spondylolisthesis occurrence.15

Fig. 5 - The posture in shear and in "nutcracker", publishedby Roussouly et al.14for low-grade spondylolistheses..

However, not all patients with spondylolisthesis at L5-S1present with PI above the normal. Roussouly et al.14observed,in a study with 82 subjects with low-grade spondylolisthesis,the presence of two distinct subgroups with respect to formand sacro-pelvic balance, which can be affected by differentpathogenic mechanisms. According to these authors, patientswith high PI and sacral slope (SS) show an increase in the shearforces incident at the lumbosacral junction, which causes fur-ther tension on the pars articularis of L5: the shear type (Fig. 5).On the other hand, those patients with low PI and SS maypresent clamping of the posterior elements of L5 between L4and S1 during extension, which eventually causes an effect in"nutcracker" on the pars articularis of L5.For cases of high-grade spondylolisthesis, Hresko et al.16identified two subgroups of sacro-pelvic alignment: with bal-anced or unbalanced pelvic posture (Fig. 6). The "balanced"group includes patients who in the orthostatic position showhigh SS and low pelvic tilt (PT). Patients in the group "unbal-anced" include those who in the orthostatic position haveretroverted pelvis and verticalized sacrum, which correspondsto a low SS and high PT. It has been shown that patientswith high degree of vertebral slippage have a mean PI >60?.

Balanced pelvis Retroversed pelvis

Fig. 6 - Balanced and retroversed pelvic posture publishedby Hresko et al.16for high-grade spondylolistheses..

processesThis contrasts with those with low-grade spondylolisthesis,in whom PI values are low, normal or high.Furthermore, it was observed that the sagittal balance, i.e.the measurement of the plumb line from C7, was significantlyincreased (>3 cm) in those with retroverted posture (unbal-anced); this suggests that the positive sagittal imbalance maybe associated with this type of spino-pelvic alignment. Mac-Thiong et al.17showed in a comparative study between a groupof 131 patients with spondylolisthesis and a control group of120 patients, that the normal sagittal balance of the trunkwas maintained in patients with low-grade spondylolisthe-sis, while the sagittal balance was changed in patients withhigh-grade spondylolisthesis. Again, the spino-pelvic balancewas altered in the group of high-grade spondylolisthesis asso-ciated with sacral-pelvic imbalance.

Classification

The spondylolisthesis has been described by Wiltse et al.18classification (Table 2), based on etiological and topographicalcriteria, with five types. It is difficult to predict its progres-sion and response to treatment. The recognition that surgicaldecompression may lead to instability of the column madenecessary a sixth type: iatrogenic spondylolisthesis.

Another system used is the one proposed by Meyerdinget al.19in 1932 (Fig. 7), in which the degree of slippage is cal-culated by the ratio between the anterosuperior diameter ofthe sacrum and the distance of previous slippage of vertebraL5. Thus, it can be considered: grade I - 25% or less, grade II -between 25% and 50%, grade III - between 50% and 75%, andgrade IV - greater than 75%. The degree V, as spondyloptosis,does not belong to the original description.

The scale of Meyerding only describes the degree of tan-gential slippage, though in high-grade dysplasias there iskyphosis, in addition to the tangential translation. The moreused grading system for high-grade slippages is that proposedby Newman and modified by DeWald et al.,20in which thedome and the anterior surface of the sacrum are divided intoten parts (Fig. 8). The measure is taken based on the positionof the posterior-inferior corner of the body of the fifth verte-bra in relation to the dome of the sacrum (first measure) andthe second measure is given by the position of the anterior-inferior corner of the body of the vertebra L5 in relation to theanterior surface of S1.

Marchetti et al. and Bartolozzi et al.21developed a classi-fication system that distinguishes spondylolisthesis acquired

- IIIIIIIVVFig. 7 - Meyerding classification.

versus developmental type and also divides the developmen-tal spondylolisthesis in dysplastic of low and high grade.

None of these classification systems were designed withthe goal of assisting in surgical planning of spondylolisthe-ses. Thus, the guidelines and outcome studies and clinicalfollow-up are mostly based on the degree of slippage.21,22Fur-thermore, these classifications20,21do not take into accountthe sacro-pelvic sagittal balance, although more recent stud-ies suggest the importance of this balance in the assessment,progression and treatment of spondylolisthesis.23,24This maybe the explanation for the large amount of published studieson surgical techniques.

,

,

ABCFig. 8 - Newman graduation system, modified by DeWald..

Recently, Mac-Thiong et al. and Labelle et al.25proposed anew classification system for spondylolisthesis, with the goalof assisting in the evaluation and treatment of lumbosacralspondylolisthesis. This classification clarifies the concepts ofdysplasia of low and high grade presented by Marchetti et al.and Bartolozzi et al.21and incorporates the latest knowledgeof the morphology and the sacral-pelvic sagittal balance. Eighttypes of spondylolisthesis are described as follows: (1) degreeof slippage (low and high grade), (2) degree of dysplasia (lowand high grade) and (3) sagittal sacro-pelvic balance. The clas-sification is organized into groups and subgroups in ascendingdegrees of seriousness, in order to develop a progressive algo-rithm of surgical complexity proportional to the increase inthe severity of spondylolisthesis.

Classification proposed by the study group of spinaldeformities (Spinal Deformity Study Group [SDSG])

The SDSG submitted a classification for spondylolisthesisbetween L5 and S1 that has been simplified and refined. Thisclassification is based on three characteristics that can be eval-uated in lateral view (sagittal) radiograph of the column andpelvis: (1) degree of slippage (low or high), (2) pelvic incidence(low, normal or high) and (3) spino-pelvic balance (balanced orunbalanced). Thus, six subtypes can be identified (Table 3).23-25To apply the classification, in the first place the degree of slip-page is measured on a lateral radiograph of the column. So itcan be determined whether the slippage is low-grade (0, 1 and2: <50% slippage) or high grade (3, 4 or spondyloptosis: >50%slippage). Then, the sagittal balance is measured to determinethe sacro-pelvic and spino-pelvic alignment. The measures ofPI, SS, PT and of the plumb line of C7 are used. For low-gradespondylolistheses, three types of sacro-pelvic balance can befound: type 1, "nutcracker", a subgroup with low PI (<45?); Type2, a subgroup with normal PI (between 45?and 60?); and type3, a shear type, a subgroup with high PI (>60?). For those caseswith high-grade spondylolisthesis, three types are also found.Each case must first be classified as if presenting a balancedor unbalanced sacro-pelvic, using values of PI and SS.16Thespino-pelvic balance is determined with the use of the plumbline of C7. If this line falls on or behind the femoral head, thecolumn will be balanced; if it falls in front of the femoral head,the column will be unbalanced.

The three types of high-grade spondylolisthesis are: type4 (balanced pelvis), type 5 (pelvis retroverted with balanced

column) and type 6 (retroverted pelvis with unbalanced col-umn). Fig. 9 shows six clinical examples of these positions.Progression factorsAccording to Boxal et al.,26the best parameter to predict pro-gression is a great slippage angle (>55?); this angle is formedby the intersection of a line drawn parallel to the inferior faceof L5 and a perpendicular to the posterior face of the body ofS1. The authors also report that a progression may occur, evenafter a solid posterior arthrodesis.Patients with low PI and low SS ("nutcracker" mechanism)have a low risk of progression. Dysplasia and slippage of highgrade (>50%) were also reported as a factor for progression ofspondylolisthesis.27Other factors in favour of progression to isthmic spondy-lolistheses are female gender, slippage >50% and childrenbefore the growth spurt.24It was observed that patients with spondylolisthesis causedby dysplasia have a higher chance of progression versus thosewith spondylolitic spondylolisthesis.28Clinical manifestationsThe symptoms can be divided into symptoms in children andadults.

In children, the spondylolisthesis is usually asymptomatic.Exaggerated lumbar lordosis may be the first warning sign anda shortening of hamstrings occurs. With the verticalizationof the sacrum, the buttocks become heart-shaped, because ofthe bony prominence. With the progression, the patient devel-ops a typical posture, because of the hamstring shortening,verticalization of the sacrum and increased lordosis, knownas Phalen-Dickson signal (bending of the knees and hips). Insymptomatic cases, the mechanical low back pain is the mostcommon complaint.3The severity of pain may or may not berelated to the degree of slippage. Radiculopathy is less com-mon, but is observed with the progressive translation, wheninstability is present. Radiculopathy of L5 occurs more oftenthan radiculopathy of S1. S1 root compression occurs in highdegrees of slippage because of the root stretching stress abovethe edge of the sacrum. The pain increases with the extensionof the column and improves with rest.29

In adults the lumbar pain with or without irradiation tothe lower limbs is common; this is typically a mechanicalpain that worsens with extension. The pain must be differ-entiated from discogenic pain, which worsens with flexionand in the sitting position. Neurogenic claudication is also acommon symptom, defined as a pain in the lower extremi-ties, numbness or weakness associated with ambulation orwith the seated position.30Pain is the predominant symptom,present in 94% of patients, followed by paresthesia (63%) andweakness (43%).31Neurogenic claudication must be differen-tiated from vascular claudication, as shown in Tables 3 and 4.

DiagnosisThe diagnosis is established on radiographs of the lumbar col-umn in frontal and profile incidences with the patient in theorthostatic position. Other views used are located profile andright and left oblique incidences.

In radiographs in oblique incidence, the "Scottish dog" canbe seen, where the "collar" represents lysis in the pars.26

Computed tomography has little value in the diagnosis;this technique can demonstrate sclerosis and the defect inthe pars.MRI is the exam of choice to view the disc at the levelof the deformity. This imaging technique is used in casesof radiculopathy and to visualize bone oedema and defectsin the pars articularis. More advanced image examinations,such as computed tomography by single photon emission(SPECT),32are more sensitive and provide more details. Ander-son et al.33reported that 20% of patients with negative resultson a standard bone scan with suspected acute spondylolysisshowed a lesion of the pars when assessed with SPECT.

Treatment of spondylolisthesis

The spondylolisthesis can be of low grade (slippage <50%)or of high grade (slippage >50%) and both types can betreated conservatively. However, the high-degree spondylolis-theses respond more poorly to conservative treatment whencompared with those conditions of low degree.31The conser-vative treatment is best suited for displacements smaller than30-50% in the growing child and for some displacements largerthan 50% in young adults. For symptomatic patients, excel-lent clinical response has been obtained with restriction ofphysical activity and the use of ortheses (TLSO) in order toavoid repetitive movements of hyperextension of the lumbarcolumn.13

For patients with chronic low back pain, Panjabi et al.34demonstrated that the strengthening of specific musclegroups improves the patient's response to pain; so, theseauthors started to recommend the strengthening of the trans-verse abdominal, internal oblique and multifidus muscles.Besides the strengthening of these specific muscle groups, thestrengthening of the hip flexors and the stretching of ham-strings also improve the patient response to low back pain.13

According to DeWald,20the goal in the surgical treatment ofspondylolisthesis is the fusion of the smallest possible num-ber of mobile segments of the column, which restores thesagittal vertical axis, with the sacrum and lumbar column inas normal as possible a position, and the fusion of the non-competent disc spaces. This type of treatment is indicatedin asymptomatic children with greater than 50% slippage,for asymptomatic patients with skeletal maturity and greaterthan 75% slippage, for symptomatic patients who do notrespond to conservative treatment, progression of deformityand neurological deficit.30

In symptomatic adult patients with low-grade degenera-tive spondylolisthesis, posterolateral arthrodesis (PLA) in situhas better clinical outcomes when compared to supervisedexercise programmes.35,36However, PLA has been unable tomaintain intraoperative correction of the slippage angle, dueto the progressive degeneration of the anterior disc space.35Suk et al.37and La Rosa et al.38conducted a comparative studybetween PLA and 360?arthrodesis (PLA + PLIF) and found thatmany postoperative radiological parameters, such as fusionrate, reduction of the slippage angle and maintenance of thecorrection of the deformity, were superior in patients witharthrodesis 360?. However, clinically in none of these studiesPLA or PLIF was statistically superior.39A decompression is indicated in cases of radiculopathy.Usually the L5 root is involved at the foraminal level and com-pressed by the proximal portion of the pars as the slippage isenhanced by fibrocartilaginous tissue in the defective pars. Incases of radiculopathy or other neurological deficits, such ascauda equina, decompression is indicated. The Gill procedureis the basis for decompression by removing the loose blade.39

The decompression of the nerve root can be done only in adultpatients with radiculopathy and low grade spondylolisthesisthrough the procedure of Gill et al.40However, this procedureis contraindicated in paediatric patients, in whom it shouldalways be accompanied by an arthrodesis.

The reduction of high grade spondylolisthesis has beenindicated, since this procedure is able to improve the aestheticappearance, correct the lumbar angles, improve the pelvicindex and the sagittal balance and even recover the kypho-sis that occurs in the lower lumbar region.40In most cases,this reduction is not made in adult patients with spondylolis-thesis. This is due not only to the degree of slippage, but also tothe anatomic position of the roots, which are more cephalad;and to the presence of a bend formed in the dural sac, which is relatively more elongated. Because of these anatomical find-ings, the reduction manoeuvre can apply tension to the roots,with the risk of neurological injury.41

Final considerationsThe isthmic spondylolisthesis is an acquired disease thatbecomes symptomatic in young adults, because of the pre-mature degenerative process of the intervertebral disc andfacet joints, as well as the mechanical imbalances that lead tochanges in the sagittal balance of the column. The progressionof slippage is more rare in adults than in children.

The radiographic examination of these patients shouldinclude the panoramic radiograph of the column and the visu-alization of the femoral heads, to allow an angular evaluationof the lumbosacral junction and of the sagittal balance.

Conservative treatment with physical rehabilitation andanalgesics has generally shown good results.

The surgical treatment with nerve root decompression andarthrodesis is indicated in cases where the conservative treat-ment has failed or there is a progressive neurological deficit.The result of surgical treatment has been good in terms ofrelieving the chronic low back and radicular pain.

The classification system proposed by SDSG is practicaland easy to apply and should be used and more studied inour country. The purpose of this classification emphasizesthat patients with spondylolisthesis L5/S1 form a heteroge-neous group with several postural adjustments and that thisshould be considered by physicians when indicating any typeof treatment. While we cannot employ an algorithm thatestablishes a specific treatment for each subtype, it is sug-gested that in patients with type 4 of spino-pelvic alignment,forced attempts at reduction may not be necessary. Obtainingthe sagittal alignment with arthrodesis and surgical instru-mentation is enough. For those patients with type 5, we shouldpreferably try to reduce and realign, but in very difficult cases,instrumentation and arthrodesis after postural reduction maybe sufficient for obtaining the proper sagittal alignment, sincethat the alignment of the column is maintained. The reduc-tion and alignment are mandatory in type 6 patients, in whomthe sagittal alignment is seriously impaired.

The circumferential fusion (360?) with surgical instrumen-tation has shown a lower rate of non-union, but this cannot becorrelated with results superior to those of the posterolateralarthrodesis.Conflicts of interestThe author declares no conflicts of interest.

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