Clinical and Experimental 2003; 21: 573-580. HYPOTHESIS Are adolescent idiopathic ABSTRACT vature occur more frequently and are and ankylosing Human spinal biomechanics are pro - c o n s i d e red to be "normal" deve l o p- foundly complex and not well under - mental va ri ations (8, 11). The spinal counter- stood, especially in terms of the dynam - d e fo rmities in scoliosis are thre e - opposing conditions? ic spine function. Translation of biome - dimensional however, and the complex A hypothesis on bio- chanics to disease is difficult, particu - p at t e rns ch a l l e n ge two - d i m e n s i o n a l mechanical contributions l a rly since cause must be sep a rat e d roe n t ge n o graphic cla s s i fi c a tion (12,13). predisposing to these from effect. Primary dynamics predis - Scoliosis (G. Skol i o s i s , a "croo ke d n e s s " ) spinal disorders posing to the onset of chronic spinal was fi rst described by Hippocrat e s d i s o rd e rs , e. g. , adolescent idiopat h i c (14). Clinically, scoliosis is a descrip- A.T. Masi1, J.L. Dorsch2, scoliosis (AIS) or ankylosing spondyli - tive term used to describe a structural tis (AS), must clearly be differentiated ( i . e. , fi xed) defo rmity of the spine, 3 J. Cholewicki from secondary alterations. characterized by lateral curvature and This commentary add resses pri m a ry rotation of involved vertebral bodies to 1Department of Medicine, 2Library of the biomechanics that may predispose to the convex side. However , co r onal plane Health Sciences, University of Illinois these idiopathic diseases. A nove l (lateral) curve flexibility occurs in AIS College of Medicine at Peoria (UICOMP), hypothesis is pro p o s e d, based upon (15). The curves may be significantly 3 Peoria, Illinois; Biomechanics Research inferences regarding their contrasting reduced by eliminating the effects of Laboratory, Department of Orthopaedics muscular dynamics. The hy p o t h e s i s grav i t y, by side-bending the spine & Rehabilitation, Yale University School of Medicine, New Haven, Connecticut, USA. p o s t u l ates opposing inherent mu s cl e a c t ive ly when supine, exe rting head- tonicity in AIS ve rsus A S. Conve rs e pelvis traction (14,15), or by employ- Alfonse T. Masi, MD, DR.P.H., Professor of Medicine; Josephine L. Dorsch, Health degrees of spinal stability may predis - ing a bending-brace (2,16), as well as Sciences Librarian; Jacek Cholewicki, pose to the respective curvature defor - ultimately reducing curves by surgical PhD, Associate Professor. mities of AIS and the enthesopat hy correction (17). A non-structural (pos- This study was supported in part by the lesions of AS. One condition is suspect - tural) scoliosis curve corrects on side- Department of Medicine, UICOMP, and ed to counter-oppose the other, within a bending or traction films (18). Marfan by a gift from the MTM Foundation. polymorphic spectrum of spinal stabili - syndrome is an example of secondary, Dr. Cholewicki is supported by a research ty. usually lumbar, scoliosis (1, 19). grant from the National Institute of The difficulty in applying complex bio- and Musculoskeletal and Skin The challenges of causation studies mechanical concepts of spine instabili- Disease (5R01 AR 46844). in AIS and AS ty to the etiology of AIS lies in the lack Please address correspondence and The onset risks and severity gradients of a demonstrable link between spine reprint requests to: Dr. Alfonse T. Masi, of polymorphic disorders, such as ado- buc kling and scoliotic deform i t y . Buck- MD, DR.P.H., Department of Medicine, lescent idiopathic scoliosis (AIS) and ling is the loss of struc t u r al stabi l i t y University of Illinois College of Medicine a n kylosing spondylitis (AS), re s u l t c a u sing a momentary defo rm at i o n , at Peoria (UICOMP), One Illini Drive, Box 1649, Peoria, Illinois 61656, USA. from complex interactions among mul- while AIS is a ch ro n i c a l ly evo l v i n g tifactorial determinants (1-7). Biome- de fo rm i t y . Nevert h e l e s s , scoliotic defor- Received on July 7, 2003; accepted on July 10, 2003. chanical va ri ations wh i ch initially mity could be the expression of passive cause deviations from normal physio- ac c o m m o d a tion to many repe a ted insta- © Copyright CLINICAL AND l ogical control may differ from sec- bility events stemming from insuffi- EXPERIMENTAL RHEUMATOLOGY 2003. o n d a ry pat h o l ogical processes wh i ch cient muscular support. supervene in the fully expressed disor- The essential role of muscles in stabi- Key words: Adolescent idiopathic ders (1, 3). lizing the spine and controlling its scoliosis, , F u rther difficulties encountered in dynamic functions are unquestioned co-occurrence, counter-oppose, investigations of causation are the over- (20-28). Neve rt h e l e s s , s u ch norm a l biomechanics, muscle properties, l apping boundary limits between the i n t rinsic support ive mechanisms are muscle tone, spinal stability, spinal spectrum of clinical features in these conventionally interpreted within a sta- stiffness. diseases and the ranges of normal phe- tic confi g u ration and va ri o u s ly des- notypes. The Scoliosis Research Soci- cribed in biomechanical terms as stiff- ety has defined scoliosis as a lateral ness (i.e., resistance to deformation and curvature of the spine of greater than displacement), stability (i.e., the ability 10 degrees, as measured by the Cobb to re t u rn to the equilibrium stat e ) , method on a standing coronal plane forces (i.e., restraining versus displac- radiograph (3, 8, 9). Such degrees of ing movements), or other phenomena, curvature have been reported in about 1 alone or in combination (20). to 3 percent of otherwise healthy ado- In normal balanced posture, muscular lescents (8, 10). Lesser degrees of cur- support of the spine is often described

573 HYPOTHESIS Biomechanical contributions to spinal disorders / A.T. Masi et al. physiologically in terms of coordinated spinal stability induces increased stiff- Muscle tone (or tension) is essential for re fl ex activation (25, 2 9 - 3 1 ) , c o n c e n- ness and may predispose to excessive maintaining body posture (7, 30, 31, tri c , ec c e n t ri c , or isometric strength (32, tensional stres s e s , pa rt i c u l a r ly at att a c h- 41). Although it is influenced by the 3 3 ) , length dependent passive elastic ment sites, as may occur in AS (7). stretch reflex, little is known about the energy (22, 34), thixotropic properties Clinically, a spine may be considered full processes controlling this mysteri- (35-37) or tonicity (7, 29-31, 35, 38). stable when it is maintained in an opti- ous aspect of human physiology (29- Such complex mechanisms cannot be mal state of equilibrium by its restrain- 31, 35, 38). Overall tone results both expected to be accurately expressed by ing structures during varied functions from elastic muscular contractile prop- any single biomechanical or biological (28,42). Biomechanically, it is assessed erties, which do not require motor unit t e rm. Neve rt h e l e s s , the clinical term by its degrees of stiffness,mainly under action potentials (MUAPs), and from axial muscular tone (tonicity) is used m o m e n t a ry, minor pert u r b ations and e l e c t rogenic [i.e. , e l e c t ro myograp h i c for purposes of simplification and uni- static conditions (43). ( E M G ) - a c t ive] contra c t i o n s , wh i ch fication of the hypothesis that bridges Flexibility of the spine has been quanti- may be either voluntary or involuntary the contrasting biomechanics of A I S tatively analyzed in AIS (15). Ranges (i . e. , either refl e x responses or "spasms") versus AS, within the one dimension of of motion of the back (44) and subjec- (30, 31). Also, giant protein molecules spinal stability. Muscle tone (and ten- tive symptoms of tightness (4, 7, 45) (titin/connection and nebulin) con- sion) connotes stiffness or tightness of are routinely evaluated in AS. Rotation tribute viscoelastic properties to intrin- the muscle and its moving part (7, 30, of the thoracolumbar spine was the sic muscular tone (50). 31, 35, 38). clinical test of spinal mobility in AS Intrinsic muscle tone and joint mobility Without the essential supportive role of that best correlated with the duration of are complex and associated physiologi- muscles, the load which can be placed disease (44). However, biomechanical cal traits. Clinicians curre n t ly re c og- upon an isolated osteoligamentous tho- measures of stability, in terms of quan- nize individuals who have hypermobil- racolumbar spine befo re bu ckling is titating forces required to disturb spinal ity syndrome (HMS) (51), also referred 20N (about 4.5 lbs) of compre s s ive equilibrium, have not been performed to as joint or ligamentous laxity. Impor- force (i.e., less than the weight of the in either condition. tantly, muscular hypotonicity has been h e a d ) , wh i ch is its critical bu ck l i n g d e m o n s t rated in hy p e rmobile wo m e n load (39). Under balanced posture and Complex biomechanics of truncal (52). Studies of joint laxity or soft-tis- light loading conditions, it has not yet musculature sue extensibility have been reported in been determined if the critical column Muscle stiffness is related to muscle AIS (53-55) and in one adult case of s t ability is mainly provided by the fo rc e. Intrinsic mu s cle stiffness is a AS with hypermobility (56). No com- thixotropic properties of muscle stiff- m e chanical pro p e rty wh i ch stab i l i ze s p a rat ive data on hy p e rmobility we re n e s s , i . e. , unaccompanied by EMG the balanced spine in response to a found in AIS versus juvenile AS (JAS) amplitude changes (31, 35), or by low, variety of small perturbations, without patients. continuous muscle activation of syner- the need for active motor contro l Peripheral joint mobility was found to gist and antagonist groups (25). Mus- adjustment (34, 43). In the balanced va ry considerably in the populat i o n , cles act as “guy wires” and also con- upright posture under static conditions, depending upon age, gender, and the tribute compression, thereby stiffening as little as 2% of the maximum contrac- side of the body involved (57). Like the the column in all degrees of freedom tion effort on average is sufficient from peripheral joints, the normal range of and enhancing stability (37, 40). all trunk muscles to maintain a stable spinal mobility in lateral bending was The human spinal system has an exceed- spine (25). A reduction in either muscle found to be gre ater in females than ingly complex, evolutionary, multi-seg- tonus or inherent neuromotor activity males (58). Phy s i o l ogical ra n ges of mental arch i t e c t u re (41). Recently, will result in spinal instability and muscular tonicity, e s p e c i a l ly of the principles of “biotensegrity” have been bu ck l i n g. Larger spinal pert u r b at i o n s trunk, are most difficult to quantitate p roposed to explain spinal stru c t u re elicit mu s cle stre t ch re fl exes; such a c c u rat e ly in humans (38, 59). Such and functions, which posit that forces responses further stabilize or stiffen the limitations greatly complicate scientif- operate primarily via continuous net- spine and prevent its buckling failure ic investigations of muscular tonicity in works of tensional tissues (e.g., axial (46-48). However, such reflexive mus- AIS, AS, or other rheumatic disorders. muscles and ligaments) and secondari- cle activation and de-activation mu s t Like many other common physiologi- ly incorp o rate compressional loading still conform to a coordinated recruit- cal traits, such polymorphic character- into local islands, e.g., the bony el e - ment of mu s cle fo rces; otherwise, istics are suspected to manifest in natu r e ments of the (7, 41). structural instability could also occur in relatively normal or lognormal fre- Optimal or sufficient spinal structural (37). Thus, sufficient intrinsic muscle quency distributions (8, 10, 57, 58). stability of course is desirable for all tonus as well as the appropriate active normal tasks (42). Lesser stability per- c o n t ractile refl e x responses reg u l at e d Features implying contrasting mits hypermobility, but possibly at a by an intact motor control system are alterations of spinal stability in greater risk of buckling behavior (37), the necessary mechanisms to sat i s f y AIS versus AS as may occur in AI S . In contras t , great e r normal spinal stability (49). The most common form of idiopathic

574 Biomechanical contributions to spinal disorders / A.T. Masi et al. HYPOTHESIS

Table I. Clinical features of AIS: Host and biomechanical influences. after further mat u ration and mu s cl e strengthening (17). n AIS composes circa 85% of all idiopathic scoliosis (IS) in childhood. M u s c u l at u re, p a rt i c u l a rly tru n c a l , i s n A younger onset of idiopathic scoliosis heralds greater spinal deformity. significantly more developed (74, 75) n With younger age in childhood, both the severity of new onset IS and the degrees of and stronger (74, 76) in adolescent and hypermobility in the population increase, implying a relationship to muscle tonicity. adult males than females. In adoles- n The spurt of spinal growth during puberty increases the risk of developing AIS. cents with mild lateral curvatures, e.g., n Idiopathic scoliosis rarely develops following the stage of skeletal maturation. 10 degrees or less, the female to male n Femaleness is significantly associated with greater spinal deformity and progression. (F:M) sex ratio is equal. However, with n The primary curvature is mainly thoracic (80%), and less often lumbar (20%). either lateral curvatures of 30 degrees n The primary thoracic curvature is typically convex to the right side in both sexes, and is or greater or in those persons with pro- influenced by handedness. gre s s ive disease, gi rls pre d o m i n at e over boys in a ratio of fo u r- fold or scoliosis (IS) is AIS (Table I), which is cal spinal muscular weakness as a theo- greater (1,2,10,12), which is the direct detected between the age of 10 years retical cause of asymmetrical defl e c- opposite of AS (4). and the stage of skeletal maturity (17, tions resulting from instability (22). Despite their deformity, most patients 18). It is estimated to comprise almost Another biomechanical group (67) stat- with AIS live normal lives, and usually 90% of all childhood cases (1,9, 17, 18, ed that ro t ational and tra n s l at i o n a l function without limitations or pain (2, 60). In AIS, major curve(s) occur far i n s t ab i l i t y, alone or in combinat i o n , 62, 72), unlike patients with AS (7, 77). more commonly in the thoracic (circa always occur in scoliosis patients, but Those who reach skeletal maturity with 80%) than the lumbar (circ a 2 0 % ) made no reference to the causation of thoracic curves of less than 30 degrees s p i n e, and occasionally in both. Th e IS. are unlikely to worsen as adults (1, 2, thoracic curvatures in AIS are predomi- The overriding concept proposed in the 62), unlike the progressing course of nantly (80+ percent) convex to the right literature on the muscular biomechan- ra d i ographic spinal invo l vement in (1, 60-62), unlike the equal dominance ics of AIS is muscular asymmetri e s juvenile or adult AS (77). The younger of right and left curvatures seen in par- contributing to buckling, or a neuromo- the onset age, the more advanced and alytic scoliosis (60, 63). tor imbalance resulting in pri m a ry progressive is the course of IS (1, 62). With respect to our hy p o t h e s i s , s e c- deforming forces or otherwise causing Ava i l able data imply that yo u n ge r o n d a ry scoliosis often results fro m dysfunctional control (1, 3, 11, 68-72). onset ages result from a greater consti- numerous myopathic or neuromuscular A review of current concepts by the tutional defi c i e n cy of axial mu s c u l a r d e ficiencies that provide insuffi c i e n t Scoliosis Research Society Etiology support of the spine, as in many dis- support to the spine (1-3, 9, 18, 29, 60, Committee (3) stat e d, “ Th e re is no eases with a hereditary predisposition. 63, 64). Entities such as poliomyelitis, strong evidence implicating any partic- In addition, the relative protection of c e reb ral palsy, muscular dy s t ro p hy, ular biomechanical factor in the etiolo- males only begins to express in older spinal cord injuries, hypotonia, or dys- gy of idiopathic scoliosis”. JIS cases,and is fully evident in adoles- tonia often cause secondary spinal cur- In contrast to rare studies of predispos- cent onsets (2, 17, 18). vat u res (1-3, 9 , 1 8 , 2 9 , 6 0 , 6 3 , 6 4 ) . ing risk mechanisms, considerable re- The significant influence of yo u n ge r Occult intraspinal pathologies or neu- search has been done on biomechanical onset age upon severity is also noted in roanatomical abnormalities have been (3,72), clinical (2,3,17), electromyo- the period prior to, versus following, detected on magnetic resonance imag- graphic (29), and histochemical or the pubertal growth spurt of AIS pati e n t s ing (MRI) in 20-25% of juvenile "idio- pathological (1,3,68, 69,71) aspects of (73,74,78). The pubertal spinal growth pathic" scoliosis (JIS) patients (65, 66). mu s cle once scoliosis has pre s e n t e d spurt of adolescents, i.e., during a pop- The authors indicated that MRI should and progre s s e d. Unfo rt u n at e ly, s u ch ulation mean age of circa 12 in girls be routine in the evaluation of patients results probably do not reflect the pri- and 14 in boys (74), is an independent with scoliosis of "juvenile onset", i.e., mary alterations of axial musculature risk factor from gender for the develop- curvatures detected between ages 3 and that predisposed to the initiation of the ment of AIS (2, 7 0 , 73). Pe r h aps the 10 ye a rs. Such rep o rts suggest that d e fo rmity (1, 3). Rat h e r, t h ey are more rapid axial elongation of the spine muscular hypotonicity or other biome- believed to result from secondary mus- during that growth phase may result in chanical deficiencies of spinal support, cular responses to the altered biome- a relative instability of muscular sup- either inherent or due to myopathic dis- chanics of the spinal deformities (1,3, port (70) ? A smaller curve (i.e., 10-19 eases, may predispose to scoliosis. 71). Furt h e rm o re, AIS is a deve l o p- degrees) in a more mature adolescent In the literature, little or no attention mental disorder. A critical insufficiency has a ver y low (1.6%) prob a bility of pro- has been given to the possibility that that may have initially predisposed to gression, whereas a larger curve (i.e., inherent polymorphic spinal muscular instability at a critical period of muscu- 20-29 degrees) in a less mature adoles- insufficiency may be a primary predis- loskeletal immaturity and axial growth, cent has a high probability (68%) of posing factor to the onset of AIS. How- e.g., during the pubertal spurt in AIS (2, progressing (17, 78). Only infrequently ever, one group did mention symmetri- 70, 73, 74), may not necessarily persist does AIS begin after the stage of skele-

575 HYPOTHESIS Biomechanical contributions to spinal disorders / A.T. Masi et al. tal maturation (2,17), unlike the risk of condition caused by inherent relative d rome; HLA-B27 A n t i gen; Reiter's developing AS (4). insufficiency of the muscular support Disease; Spondylitis, Ankylosing; and As indicated, the thoracic curvature in of the spine, by virtue of its clinical and Arthritis, Rheumatoid (including juve- AIS is ch a ra c t e ri s t i c a l ly convexed to epidemiologic features (Table I). The nile). Hypermobility and hy p e rl a x i t y, the right (1, 2, 17, 61). Left thoracic contrasting features of AIS versus AS buckling, instability, tonicity, sacroili- patterns are less likely to occur in IS are summarized in Table II. If the con- i t i s , and spondy l o a rt h ro p at hy we re than in secondary scoliosis from under- cept is true, then AIS and AS would be searched as keywords. lying neuromotor disease (63, 79). In expected to rarely occur conjointly. O n ly five rep o rts we re found of the 254 girls with IS, the direction of the coexistence of either scoliosis (85, 86) convexity significantly correlated with Literature search to test a counter- or hy p e rmobility conditions (56, 8 7 , preferred handedness (61). Analogous- opposing occurrence of AIS and AS 88) with AS or SPA disord e rs as ly, adolescent athletes who engaged in A search of the English and non-Eng- opposed to a total of 17 arti c les retrieved stressful sports involving predominate- lish literat u re was conducted in the of these conditions having coex i s t e d ly one arm were reported to have had MEDLINE dat abase (1966-Feb ru a ry with juvenile rheumatoid art h ri t i s minor curvat u res convexed to the 2002). Search parameters were set to (JRA) or RA (Table III). A total of 20 respective side (80-82). Such associa- find the co-existence of scoliosis, a dditional rep o rts we re found of A S tions of curve laterality with handed- hypermobility conditions, and Marfan coexisting with RA, i.e., a concurrence ness suggest that biomechanical and syndrome (MFS) reported with either of the two inflammatory rheumatic dis- behavioral factors contribute to the pat- AS or other HLA-B27-related spondy- o rd e rs , although of diffe rent ge n e t i c tern of spinal deformity (61, 80-82). A loarthropathy (SPA). The two non-scol- predispositions (references not cited). pilot study utilized progressive resistive iosis disorders that were searched for in The relatively high frequency of the lat- torso rotation strengthening as a treat- c o existence with AS or SPA , i . e. , ter citations suggest that AS and RA are ment for AIS (83). Curve reduction was hy p e rmobility conditions and MFS, not counter- o c c u rring disord e rs. Nei- noted in 16 of 20 pat i e n t s , and no were selected for reasons analogous to ther was a formal attempt made to enu- increase in severity was found in any that of scoliosis. They too were sus- merate the frequent reports of scoliosis patient during a twice-weekly, 4-month pected to have negat ive associat i o n s co-existing with various hypermobility exercise regimen. Such data are prelim- with the HLA-B27-re l ated disord e rs . syndromes or MFS (1, 19,54,55). Such inary and uncontrolled, but may in fe r Rheumatoid arthritis (RA) was includ- f requent rep o rts endorse the concep t in s u f fic i e n c y of torso rot a tional stren g t h ed in the search as a control inflamma- t h at insufficient spinal support (i.e. , as a predisposing factor in AIS. tory rheumatic disease for AS and SPA, either ligamentous or muscular) predis- The etiologies of AIS (1-3, 84) and AS in order to compare its frequency of poses to scoliosis (1, 19). (4-7) remain unproven, although their coexistence with scoliosis and the other Two case reports were retrieved of AS clinical ep i d e m i o l ogy and disease specified hypermobility disorders. patients with the mention of coexistent courses are well described. Such theo- The medical subject headings searched scoliosis (85,86). In contrast,three sur- ries cannot be rev i ewed cri t i c a l ly in were: Scoliosis (including the idiopath- vey publications (89-91) and two case this commentary. Although, the genetic ic and secondary forms); Marfan Syn- reports (92, 93) were found on coexist- (1, 3, 5, 6, 84) and host (2, 4, 6, 7, 17) contributions to these diseases clearly Table II. Co n t r asting fe at u res of adolescent idiopathic scoliosis and ankylosing spondyl i t i s . differ, they both centrally involve the n About 90% of all idiopathic scoliosis has an adolescent onset versus 10% of AS. spinal system. A c c o rd i n g ly, b i o m e- n In more advanced cases of AIS, the female to male (F:M) sex ratio is 4 to 1 or greater, which is chanical alterations were suspected to the direct opposite of AS. be pri m a ry predisposing fa c t o rs fo r n In milder or moderate cases of AIS, the deformity does not typically advance radiographically these spinal disorders. during adulthood, compared with continued radiographic progression in juvenile and adult AS. A novel hypothesis was re c e n t ly n is not a typical feature of uncomplicated AIS, unlike AS. reported that inherent axial muscular n Tarsal or hip joint arthropathy is not increased in AIS, in contrast to juvenile AS. hypertonicity contributes to AS, based n Spinal involvement typically begins in the more mobile and unstable thoracolumbar spine in AIS upon its characteristic and differentiat- versus the more stable and compression-bearing lumbosacral spine in AS. ing features from other rheumatic dis- n Strengthening exercises improve symptoms and maintain or reduce curve deformity in AIS, orders (see Table I in ref. 7). Such a pri- whereas stretching exercises are symptomatically beneficial in AS. mary diathesis was proposed to exert n Rotational hypermobility is characteristic of AIS, but decreased rotational ability significantly i n c reased tensional strains on the correlates with the duration of AS. attachments of ligaments, tendons, or n Increased muscular tension is noted on the convex versus concave side of AIS curvatures, but joint capsules on bone within the axial neo-osteogenesis does not occur, unlike the syndesmophyte formation typical in AS. skeleton and at peripheral joints (i.e., n Unlike AIS, tissue injury is typical in AS, presumably contributed to by compressional forces e n t h e s o p at hy). Adolescent idiopat h i c or tensional stresses (or other biomechanical variables) which exceed tissue tolerance. n scoliosis, was then perceived to be a Handedness is significantly correlated with the thoracic convexity in AIS, suggesting spinal instability, but is independent of patterns of pathology in juvenile AS. possible example of an acquired spinal

576 Biomechanical contributions to spinal disorders / A.T. Masi et al. HYPOTHESIS

Table III. Numbers of reports of specified coexisting disorders found in a literature search, (89-93) suggested that the scoliosis from 1966 to 2002.* was mainly secondary, rather than a HLA-B27-related disorders* primary idiopathic diathesis. Axial hypotonicity or Ankylosing Other spondylo- The search turned up two reports of hi s - hypermobility syndromes* spondylitis† arthropathy†† JRA/RA† t o c o m p atibility determinants in idio- pathic scoliosis that were compared to Scoliosis 2 0 5 n o rmal control populations (94, 9 5 ) . # Hypermobility syndrome 1 1 8 Both indicated relative frequencies of ¤ # Marfan syndrome 1 0 4 HLA-B27 in scoliosis patients similar Total 4 1 17 to the respective control populations.

*The search focused primarily on the coexistence of scoliosis, hypermobility syndrome, or Marfan syndrome with ankylosing spondylitis (AS) or other (SPA). Juvenile or adult RA were included as Biomechanical concepts in support control conditions to the HLA-B27-related disorders. of the hypothesis (Table IV) †The coexistence of AS with JRA or RA was reported in 20 articles (references not cited). ††Includes Reiter's syndrome, , and other HLA-B27-related SPA. As early as 1907, Feiss (96) considered ¤The suggestion of Marfan syndrome was provided by Dr. Dennis McGonagle. mechanical factors as the cause of scol- # References not cited (the search was focused primarily upon scoliosis). iosis. He used a physical model of the thoracolumbar spine and leather straps ing JRA or RA with scoliosis. The first a repo r t of two cases of seron egat ive to simu l ate mu s cle fo rces. Later in article on AS was a case report of a 27- SPA and coexisting hypermobility syn- 1 9 3 2 ,C a rey (97) developed a more elab- ye a r-old male patient with a cl i n i c a l drome, this author also raised the issue: o rate physical model to demonstrat e diagnosis of HLA-B27-negative anky- "Do pathological opposites cancel each that all combinations of lateral curva- losing spondylitis who had radiograph- other out ?" (56). ture and axial rotation deformities can ic documentation of syndesmophy t e s Scoliosis was reported to coexist with result from imbalances of both the and vari e gated sacroiliitis (85). He was either JRA or juvenile chronic arthritis superficial and the deep intrinsic mus- m e ntioned to have right-sided leg (JCA) more commonly than with adult cles of the spine. He concluded that length shortening of about 1 cm, a RA (89-93). Scoliosis was believed to scoliosis is not a specific disease entity, slanted pelvis, and a gentle left convex occur more commonly in JCA or JRA but rather a “spinal sign of imbalance T12, L1, and L2 scoliosis (85). It is than in the population at large (89-93). of muscle, bone growth, and the motor likely that the lumbar scoliosis was a In a study of 124 JRA pat i e n t s , 1 1 system of the spine”. Both models rep- s e c o n d a ry compensation mech a n i s m (8.9%) we re found to have scoliosis resent progressive thought and recog- (1,9,17,60) and not due to AIS.The with a curve of over 20 degrees (89). In nized the totality of bone-muscle inter- second art i cle on AS was the case another study of 320 JRA patients (90), actions. Interestingly, much later when report of an 18-year-old woman who scoliosis of the thoracic or lumbar a n a lytical methods became more had destructive, multilevel diskoverte- spine was detected in 17 (5.3%) pati e n t s , sophisticated, many investigators aban- bral lesions mimicking infectious dis- a freq u e n c y whi c h was believed to be doned the muscles in their biomechani- ease, bilateral sacroiliitis on computed considerably higher than in the normal cal studies of scoliosis. tomography, and the presence of HLA- population. AIS was not studied specif- Many modeling studies that investigat- B27 antigen (86). During followup, she ically, and the reports on JCA or JRA ed spine bu ckling confi g u rations in d eveloped a slight thoracic scoliosis (86), probably secondary to the preced- ing ext e n s i ve diskovert eb r al lesions and Table IV. A summary of the relevance of muscles to spinal mechanics. not attributable to AIS (1,9,17,60). n A single case report was retrieved on Buckling is the loss of structural stability causing a momentary deformation, which may not necessarily cause an acute injury. AS and coexistent Marfan syndro m e n Inherent muscle “stiffness” or “tone” is the main stabilizer of balanced spinal postures and (88). The 46-year-old male patient had is the most metabolically efficient. a late onset of spinal symptoms at age n Trunk muscles, under the control of the central nervous system,are the most important structures 42 years and radiographic findings con- providing stability to the spine. sistent with his diagnosis of HLA-B27- n Appropriate muscle recruitment patterns are necessary to stabilize the spine and prevent injury in postive AS, in addition to typical phys- response to sudden loadings. Such responses are reflexive in nature and under the control of the ical traits of MFS (88). The authors central nervous system. noted the co-existence of peri p h e ra l n Impaired motor control permits spine instability. joint hypermobility due to the ligamen- n All truncal muscles contribute to spinal stability and their relative importance is highly tous hyperlaxity of MFS, but the reduc- context-dependent, i.e., postures, loads, and load directions. tion of both axial skeletal mobility and n Buckled configurations of the spine are complex three-dimensional shapes, which are also chest expansion re l ated to AS (88). highly context-dependent, and may not be predicted by the primary deficiency. n They commented upon the interesting A great degree of spinal muscular insufficiency exists in primary and secondary neuromuscular disorders. association of these two pathologies. In

577 HYPOTHESIS Biomechanical contributions to spinal disorders / A.T. Masi et al. comparison to the deformities of scol- deformities are likely influenced by the from effect relations. iosis had not considered muscles that co m p l e x struc t u r e and loading sche m e s . The stiffness of axial rotation of the s t ab i l i ze the spine (98-100). Biome- Nevertheless, axial muscles and their lower human spine was measured using chanical modeling of the three-dimen- motor control should again become the a “ B a l a n s ” ch a i r, and by rhy t h m i c sional ge o m e t ric defo rm ation of the most re l evant focal points of future torques generated automatically at the spine in AIS without muscles is incor- i nve s t i gations into the initiating ri s k resonant fre q u e n cy (59). Pa ra m e t e rs rect with respect to the complex theo- factors for acquiring AIS. relevant to back function (i.e. stiffness, ries of stru c t u ral bu ckling (70, 1 0 1 ) . i n e rt i a , and damping fa c t o rs) we re The relatively simple Euler theory for Future research challenges eva l u ated non-inva s ive ly. Such mea- beams and columns was often inappro- The proposed hypothesis may not surements are relevant to objective and priately applied to the structurally more prove to be valid. Nor may the concept symptomatic low back tightness in AS. c o m p l ex spine (102-104). Th e re fo re, of axial muscular tonicity meaningfully Analogous techniques directed toward the bu ckled shapes derived in these cl a rify complex inter- re l at i o n s h i p s the thoracolumbar spine would be rele- studies are irrelevant, whether or not between the multiple factors that play a vant in AIS. Other non-invasive meth- they corresponded with the clinically role in AIS and AS. Nevertheless, the ods of estimating trunk stiff n e s s observed curves. b i o m e chanics concepts invo l ved are i nvo l ve quick fo rce release pert u r b a- The entire spinal system (bones, liga- n ovel and dire c t ly re l ate to curre n t tions to the trunk (47) and direct mea- ments, and muscles) would have a very research on spinal stability and its clin- surements on a low friction platform complex first mode of buckling (i.e., ical ramifications. Some examples may (37). The former method includes the the shape of buckling which occurs at be offered of controlled clinical, epi- muscle reflex response, while the latter the lowest critical load). Such buckling d e m i o l ogi c a l , ge n e t i c, ra d i ograp h i c, focuses on passive trunk stiffness. (23) is largely determined by all of the and biomechanical studies of AIS and Profoundly complex mechanisms con- trunk muscle forces, external loading AS to explore the hypothesis. trol biomechanical vis-à-vis inflamma- schemes, and spine postures. In addi- One radiographic survey of the lumbar tory processes in AS and SPA disorders tion, the spine has normal kyphotic and spine in Gre e n l a n d e rs ve rsus Danes (112). Critical studies need to deter- lordotic curvatures (and their support- found sacroiliitis in 18 versus 3 per- mine wh i ch processes may pre d o m i- ing liga m e n t s - mu s cl e s ) , a rt i c u l at i o n s c e n t , re s p e c t ive ly, wh e reas scoliosis nate in the pre-clinical, early, and later within facet joints, and disk mechanics. was less frequent in Greenlanders than clinical phases of these diseases (45). That complex structure contributes to in Danes (109). Controlled age - a n d Unlike AS or SPA, however, AIS is not three-dimensional coupled rotations in sex-adjusted clinical, geoepidemiologi- characterized by inflammatory activa- the spine, which can be further modi- cal, and radiological studies are obvi- tion. Whether or not HLA-B27 (113) fied by muscle forces (105, 106). The ously needed to determine if AIS and predisposes AS patients to the biome- contribution of each muscle to spine AS are counter-opposing disord e rs . chanical activation of infl a m m at i o n s t ability is highly context dep e n d e n t Hereditary factors are widely accepted (112) will also require critical investi- (107). Accordingly, buckled shapes can to play a role in both conditions (1,3,5, gations. differ under varied circumstances and 6, 84). Critical collaborative compar- will depend upon the directions of isons of genomes from AIS versus AS Acknowledgments The authors thank Noura Dajani and Tom external loads, their magnitude, and the p atients (and families) may reve a l Shahwan for their diligent assistance in re- initial spine posture. These complexi- diversities which could clarify the basis view of the literature; and Melissa Ginczyc- ties do not include the effects of the of the proposed polymorphism or more ki, Susan Jenkins, and Evan Lagouros for thoracic cage, which provide an addi- specific mechanisms in each condition. their outstanding contributions in the prepa- tional stabilization to the thoracic spine In one study (110), no consistent differ- ration of the manuscript. (20, 108). ence was found in the maximum volun- References D e fi c i e n cy in motor control of the tary trunk strength in attempted flex- 1. 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