Basic Biomechanics of the Musculoskeletal System-3rd Edition

All these processes will accelerate the rale of in- ~i<: IlK'chanical prop<..Tt~· 01\" the tissue. Tht: nH)SI im terfacial and fatigue wear of the already disrupted cartilage microstructure. ponam I\"ailure-inilialillg rac((1l' appears I(J he I \"loost..'ning:\" of tile c()lla~cn nctwork tllal al!c,ws a Hypotheses on the Biomechanics normal PC c.\\pansiclIl and thus tissue :-,weJ[i of Cartilage Degeneration (:\\ilaroudas, 1976; McDL'vilt &: Muir, 1976). Asso ROLE OF BIOMECHANICAL FACTORS alL'd willl Ihis Chi.U1gc is a dL'Cn:i.ISL' in canibg.1.: stil Ill:SS and an incrl.:ase in canilage pi..'rI1lL'abil Articular cartilage has only a limited capacity for re- (Allman el aI., 19S-l; Armstrong &. Mow, 198 pair and regeneration, and if subjected lO an abnor- mal range of slress~s can quickly undergo total fail- Guilak L\"l aI., 1994. SL\"lton el aI., 1994). h,,'h ure (Fig. 3-26). It has been hypothesized that failure which aller canilagL' fUllction ill ~\\ diunhrodialjoi progression relates to the following: (1) the magni- during joilll mOlion, as showll in Figure 3-27 (!vlo tude of the imposed stresses; (2) the total numbe,· of sustained stress peaks; (3) 1I1C changes in the intrin- '\" Atcshian, 1997). sic molecular and microscopic structure of the col- ThL' magnitude of the stress sustained b,\\' lhe a lagen-PG Illalri.'\\; and (4) the changes in the intrin- ticular cartilage is dctennined b,\\' both the toti.lllo h .Cartilage Structure Mechanical....- Joint on the joint and how tlwt kli.\\d is distributed ()\\ the i.\\1·ticul~ir surface conl~lCt arca (Allmed 6.: Burk t Propenies Loading 19i'3; Annslrong L'I aI., 1979; Paul. 1976). :\\n.\\· h,:nsl..' stress COllcL'nlration in Ilk' l'ont~\\Ct i.lrea w Biochemical Composition + pla,\\' i.1 pl·imi.llY roIL, in tissu<..' (k'gL'Ilt.'ration, A lar Spatial and Temporal Ilumb<..'r or well-knowll condilions GillSi...' L'.\\cL'ss stress conccnlrations in anicular canilage alld t Slress-Slrain, Pressure and Fluid Fields sult in caniJage failure. Most of Illese stress L'once CaliagenlPG ECM II':Hiolls are C~ltISI,:d h.\\· joint :,urfacL' irH.'. ongruit.\\', 1 sulting in i.lll i.\\hnornwtly small conti.lCt are ChanreYleS ·41---- Cell Slimuli E.xi.lmplcs or conditions causing stich joint inco Synthetic Activities gruilil.:s include 0:\\ subscqllL'fl( to congeniwl a ~ L\"!i.lbular dysplasia, a slipped cnpilal femoral <.:pi Cartilage Function .,\"sis. and intra-articular fractures. Two fUrih eXi.\\mpk-s arL' knet: joint l1lcnisct.:uoll1~·, \\\\'hich eli Physical Activities inak's the load·dislributing function of the lll~n ellS ([vlow Cl aI., 1992), and ligi.llllCnl I\"llpllll\"<\"', whi Flow diagram of the events mediating the structure and function of articular cartilage, Physical activities result in allows cxccssi\\·<..' mo\\\"t:'1lll'1lI and the gen<..'r;:llion joint loads that are transmitted to the chondrocyte via the abnormal mechanical ~trLSSl:S ill Ihe afk'clI:d jo extracellular matrix (ECM). The chondrocyte varies its cellu- (Allman el aI., 1984; Guilak Cl ai, 1994; ivkDe\\\"ilt lar activities in response to the mechano-electrochemical stimuli generated by loading of its environment. The etiol- Mui,·. 1976; Sellon el al.. 1994). In all the ,11)O ogy of osteoarthritis is unclear but may be traced to intrin- cases, abnorllwl joint ~\\rtj(-ulation increases t sic changes to the chondrocyte or to an altered ECM (e.g\" slJ'i..'SS acting 011 tilL' joint slIrf~lce, which aPlk'ars resulting from injury or gradual wear) that leads to abnor- predispose Ihe caniiagL' to railllr<..'. mal chondrocyte stimuli and cell activities. iVIHcroscopiG\\II~', stress IOGlJiz<.ltion and cOllce tration at the joint surfaces li~I\\'L' i.\\ I\"url!ler dlt.'C High COntact pressures bctW('L'n Ihe anicular su faces decrease Ill<..' pr()babilit~· of fluid-fIlm lubric tion (Mow &. Aleshian, 1997). Subscqllcnl <.lelL orsurl'''lI.:e-lo-surracc contacl i.\\Slx.'rities will cau microscopic stress concentrations that arc rt.'SI)(> ble for further tissue damage (Atcshian et aI., 199 1998; !\\leshian '\" Wan!'. 1995) (Case Study 3-1). The high incidencL\" or speciiic joint dcgerlt'rati in indiddllals with certain occupmions. such football pl<.l~·L'rs' knccs and ballet danccrs' i.lnkl can bL' <,,'xplainL'd b\\ tilL' incn:i.lsL' in high i.lI1d i.lbn Illi.llioad rn:.·qllcnt:~· and magnitude sllslainc:d b~' t orjoinls Ihese: individuals. II has becn suggL'slt

•I Deformation (e.g., inlerleukin-I) (Ralcliffe el aI., 1986) a growth Factors (e.g .. transforming growth fact ,I bela I) also appear lO pia\\' an importanl role in O Another contributing factor to the etiology of QA Progression Ifluid Load ma~' be age-related changes to the chondroc (Case Study 3-2). exudal.on ~ :.i~.-~::ytl_~l+.f IMPLICATIONS ON CHONDROCYTE FUNCTION ..--.Normal PG Loss I I I ,--'-- ColJagen orThe ECM modulates the transmission joint lo Cartilage to the chondroc,yte, acting as a transducer that c Damage III verts mechanical loading to a plethora or envir mental cues that mediate chondrocyte function. II healthy articular cartilage. loads from norm ., _.1 _'--_ _--' joint function motion result in the generation 1 !Fixed Charge Density - - Swelling Pressure Knee Meniscectomy ! Frictional Drag - t Hydraulic Permeability F0rty-year-Old man who had a meniscecwmy 10 years ago in his right knee. Currently, he is sufiering pain as- Increased Matrix Deformarion sociated with movement, swelling, and lirnilaiions of knee Increased Fluid Flow motion (Fig. 3-1-1), Acts 10 diminish cartilage load-bearing properties. The history of knee meniscectomy not only implies an figure illustrating how osteoarthritic changes to the col- alteration in joint surface congruence but also the elimi· 'aqen·PG network can compromise the ability of articular nation of the load-distribution function of the meniscus. ca'til'lOe to maintain interstitial fluid pressurization, which The effect is an abnormal joint. characterized by an in- \"\"'~\"'''o< the tissue's load-bearing and joint lubrication ca· crease in the stress acting on the joint surface that results in cartilage failure. Most of these stress concentralions are Loss of PG and damage to the collagen fibers result caused byjoint surface incongruity, resulting in an abnor- mally sma!tconraet area. This small contact area will suf- an increased hydraulic permeability (decreased resis- fer hign.c9_ntact pressure. decreasing the probability of !'c!\"\"\"e to fluid flow) and supra-normal loads and strains on fluid-film lubrication, and thus the actual surface~lo~ solid matrix (and chondrocyte). surface contact will cause microscopic stress concentra- ;~ ~.;,f' tions that lead to damage. '<tehiie'L~3i~n' some cases, OA mtha~vt be cau sIeld1inbiy~lldiezcficpiecank- Case Study Figure 3-1-1, the mechani sms act to '~'ff6rc,~s~on the joints. Examples of these mechanisms ~jh~~l~(le the ~clive processes of joint nexion and _~:~,q~e, lengthening and the passive absol\"ption of ':;k,,,by the subehondral bone (Radin, 1976) and ciscus (Mow el al\" 1992), ~generativc changes to the structure and com- ~gion of articular cartilage could lead to abnor- kti:ssue swelling and funZtionally inferior biome~ ;;,iji8<11 properties. In this weakened state, the '~-,:J~ge ultrastruclure will then be gradually de- .-g.t~d by stresses of normal joinl articulalion (Fig. ~m)j7;OAmay also arise sec~ndarily from insult ~o :' ':- ~~i~tIinsic molecular and microscopic structure of /;f.~tfi~2so;qagen-PGmatrix. Manv conditions may pro- :\\-.Iil<?!~:~,l!ch a brea~down in .~latrix .integrity;· the~e -;111~e degeneratIon assoclatcd wllh rheumalOId --·.1isJ joint space hemorrhage associated with 'p.pilia. various collagen metabolism disorders. }~S§.tl.e degradation by proteolytic enzymes. The _,'l1C:c': of soluble mediators such as cytokincs

~ - - - - - - _.._-----~ ... t1I........ 10\\\\ j1l..'l'Illt.,<thilit.\\·, thl..· n(lnll~tI em il\"UIlIIll..·IH ell Osteoarthritis illl..· ChllJJdrlil:.\\·!I..· i df)lIlill~lil..'d h.\\· h.nlrli:-'I~ltic 1'1'1.......- Seventy.year-OJd woman, overweight, with OA of the :-'111\"1..' ill the illtL·r tili~d lluid. \\'~tl·i(jth phl..'lI(lllIL·II~ right hip joint with associated symptoms of pain, limi- tation of motion. joint deformity, and abnormal gait (Fig. origil1;llitl2:-' IrOll1 inIL'I\"slili~t111uid Ilo\\\\' l',\\ist ~IS \\\\l·11. 3-2-1). llJ)plil'~\\kd ill I..'nh;lIll..·ill~ Illitril...'llt dilfliSioll, illlL'!\" OA is characterized by erosive cartilage lesions, carti- or:-.{iti~d lIuid 11<1\\\\- (i.I.,:.. lage loss and destruction, subchondral bone sclerosis and unhoulld \\\\'~tlL'rJ ~i\\'L'~ cysts, and large osteophyte formation at the margins of tho joint (Mow & Ratcliff., t997). In this case. ri\"L' 10 l'1..'J111I~\\1' ....lillHlii Ill' ~lll 1..·ll..'cll'k,d 1l~lllll\"L', roentgenograms of the right hip of the patient show a decrease in the interarticular space and changes in bone «n~lnwl.\\' ... 1l\"l'~Hllillg p(ItL\"nti~d~ and (,.·UITL\"JllS {Fr~lllk surfaces as sclerolic and osteophyte formations. nle most Gr()t!l.insk\\-. 11.)~7: Gil L't ~J1. 190.). 1t)t)t'). III ,Iddi~ severe alterations are found at the point of maximum lioll, illk'rslili~d lluid 110\\\\' tlJr()lI~h tilL' \"mi.lll p0l\"es pressure against the opposing cartil(1ge surface, in this case at the superior aspect of the femoral head. ora....:-.(J(..·i~·lk·d with tilt.' ....olid Il1;'HI·j\\ (-?iO IlIll) Ilol\"lna Case Study Figure 3·2·1. \\:al'lila~l..', \\\\hkh olll'r 1..·(Ilbi<.IL-rahk rl..·si:-'l~lIKl· ti mcchano-e1ectrochemical stimuli (e.g,. hydrostatic Jluid 111)\\\\· (:\\lanlud;'I:--, I ':lit): ,\\kCtltchL'Il, 1<)6]: \\tluw pressure, SlI-ess and strain fields, streaming poten- ti~t1s) that promote normal caI·lilage maintenance 1...[ ~d .. ll..)~..j.). \\:~1I1 2:-'i\\'L\" l\"iSL' [0 ~\\ Jlll'l'h~\\llk;l1 phl'Jl()1I1 (by the chondroeytes) and normal tissue function (Fig, 3-26). However, when the integrity of the col- 1,.'lla tl..'l\"lllL'd Iluid-indlll'l'd 1\\1~\\Il\"i.\\ compadion (Lli I.\\. lagen-PC network (the transducer) of articular cm'- \\-10\\\\·, 1'J~OI. ThL' frktiollal illk'l\"~lcli(Jn hL\"l\\\\-t.·\\,.'1l in- tilage is compromised. such as from trauma or dis- ease. normal joinl articulation leads to abnonllal orkl\"slili,d Illiid and sldid ~\\rl' <l l\"L·....ull drag l\"L'\"is- Illcchano-clcctrochemical stimuli, with ensuing ab- normal ECM remodeling by the chondrocytes and t~lllL·L· to r(JI·I..·I..·d i1U\\\\ Ihrullgh Ihl..\" pllroll .. ·lkTlIll..·ahk debilitated tissue function. \",::ll\"lila~l' 1I1~\\1I\"i,\\ ~\\Ild ~l \\'iSCllll.\" sl'IL'~Il\" sll'l'ss L'.\\l·l·ll'd In the absence of joint loading, the normal envi- hy IhL' intl..'r... tiliailluid. Gi\\'(,.·ll tlll\" nominal !lo\\\\\" l'aks ronment of the chondrocyte is characterized by the pre-stress established by the balance between ten- 01 lhl.' ilHt.'l\":-.tilial i111id llh..·IUiulll..\"d I..·adil..'r ~1IH.1 Ih. sion in the collagen flbers and the Donnan osmotic pressure. During joint loading. by vit·tue or the lis- 10\\\\· pl·rrl1l..'~\\hilil\\· \"I lIll..' l';ll\"lil;qll' Irl'lll'i\\. cholldru- C.\\ II..' pl'l'ct.·ptilll1 of thi .... frictional illh-'ra(,.·,itlll f(Jl\"i..·l· is orlikL'h to Ik' dUlninalL'd \\1\\' thl..' dl\"~\\g rL'si:'oI~IIlCL' !lO\\\\ Ihl\"()lJ~h [III..' IlJ~\\lri\\ l\"allll'I' [ll~\\Jl h.\\ diJ'l·\\..\"[ \\,i:,c()\\.IS ~hl..'al· :'trL'S~ l,Jl I hI..' cL·II. This friL\"tjonal dr~lg forc(. 1..:<111 pr<'(\\UL''''' ....u!id 11\\;,\\[,.;\\ I..krOnll~t(i(1I1 011 1111..' urde (II' 15 10 .'(V-\" Frum tilL' disctls:-.ioll ahO\\'L', i..'l'lolldI'Ol·.\\-IL' (1...'1'01\" m~I[i()Jl L>~\\1l hI..' UlJJ~i<.lI,'I\"L·d 10 hI..' gO\\·lTI1L·d hy [hrL'e cuupkd loadjn~ Illl..'l'hallislll~: dirl..'ct I-:C.\\;, <.IL-for tl1~llioll: Ho\\\\··;ndllL·l·d L'(ll1lp~\\ctiotl: and fluid prl'S* sllri/'llilln. III OJ\\. I hI..' iIlI..T(,.·asl..·d lis~lll..· pt.·nlll·'lhil~ il.\\\" diminis!k· ... carlibgL\"~ !lormal flu;d pr...\"~~lIre Itl~I<.I·SllPP()I\"[ IllL'L·l1ani.\"lll. Thus, [i'lL'!\"...' i.\" a shirt or !O,ld support Ollto thl..' solid matrix. I..·i.lusing sllprallol\"nwl ,slrl..·S::>L·:' and s!l·ailb 10 hI..\" illlposl.'d 011 1111..' chondniL·.\\·!I..'S (Fig. 3-271. Th..:·si.' ahnor- mally high Stl'L'SS ~lnd .. tl'~lill (('\\-C Is , and utili..'! rn(\",,,,'k\\llo·l'iL'I.:II'Ol\"Jh'llli(,.·~\\ll·h~lll!:!I...'S [Iw[ ~\\rL\" nwni- k~l('d \\\\'itll 0;\\, C=ill triggl..·1' an irl1hal~IIKI..' of <.:IHIll <',,\"01..'.\\'1\\.' an;:lholic and I..·alaholic al'li\\'jtk\"s, further l,.'Ollll\"ibuling In ~l \\'icious c.n·1t.- Ill' progr...'s~i\\\"i.: Glr- !ilagl\" dl..\"gl..\"nl..·r~lli(lll. Itllk ..'. d, changes to tht.' bin L'hL'lnkal l:Olllpositioll ~llld s[l\"lIclUI\"l,: oj' cal'til~\\g Ctlll Iwu..· a profound inlp~lcl Oil tiSSlll..· and (,.'!lOIl d n)cy{t.' fUlll'1 ion. \\\\'i t h IntI! t iLl i:,dpli nary collaho* r~ltioll:' =md ~1Il appropri::lli..' thl·Ol\"I..'lil\"=-d rl'~IIllC* \\\\,(H-k, such as th ...' biphas:ic tl1 ....<I1·.\\·, iJlsight~ illW 'Ii'lL' factors that g()\\·1..'1'1l c!londnlC\\[<.' f\"llIKlion L'arlil<lgL' s[ruclllr...' <lnd l'UI'H,:lioll, ~\\IH.l lhc diology or 0:-\\ I..·an hI..' obtain..:d, , ., \"....'.~ .. ~.,t,--.

SumrlzalY REFERENCES !\\hllh:d, i\\\"\\1.. (\\: Burkt.:, D.L. (1983). In vilro mcnSliremen st:llil: pressure distribution in synovial joints-P,lrl 1: The function of anicular cartilage in clianhro- i:1I surface of the knee. J Biolllech Ell.!!,. 105, 216. v.e.,Akizuki. 5., \\lo\\\\'. joints is to increase the area of load distribution \"-,lulieI'. F.. (.'t a1. (1986). Tensih.: p ;'.(thereby reducing the stress) and provide a smooth, \"nies of knel.\" joint cartilage: 1. Influence of ionic: co (\\,vear-resistant bearing surface. tion. wcighl bearing. and fibrillalion on the tCllsill.\" mo i;~(2) Biomechanically, articular cartilage should IllS. J Orr/lOp U/.:.\\', 4. 379. !J~~viewed as a multiphasic material. In tcrrns or a Ahm~ln, R.D., Tt:nl'baum, J., Lilla, L. l'l \"I. (1984). Bio .of}biphasic material. articular cartilage is comprised Ch~1I1ic.:l1 <lnd bioc:ht:mical propenh:s of dog cartilage in ,i' porous-permeable collagen-PG solid matrix peri mentally induced oSlcoarthritis. All/I Rhl!/lI11 Dis. 43, (approximately 25% by wei weight) filled by the fl'e'~ly, movable interstitial fluid (approximately :\\ndri~u.:chi, T.P.. Natar~lj'tn, R.N., ~ Hurwitz. D.E. (19 i5r~',:bY wet weight). In addition to solid and Fluid :tIlel,~e', (~xists an additional ion phase when CO!1- Musculoskclc·t~d dyn,llllics, locomolion, anti dink'll ~l si~f~r'ing articular cartilage as a triphasic medium. l.:;llioll. In V.C. Mo\\\\' & \\V.e. H<'lyl'S (Eds.). Bw;;c I!wpw:dic BiViIlt.'dlllllics (2nd l.\"d.) (pp. 31-68). Phila phia: Lippincott-RHvcn. Armstrong, CG .. Balmllli, A.S., ~\\: Bardner. 0.1.. (1979) \\'itl'o measurement of articular c;lrlilage deformation lh~ intacl human hip joinl und\"r load. J B(m\" loi/a S /;:The ion phase is nccessa'\"y to describe the swcl- 61,1.744. >~cling and other electromechanical behaviors of the :\\rmslrong. CG., & Mow, V_e. (J980). Friclion, lubricil1ion :'~~/tissue. w,,'ar or syno\\'i,al join Is, III Owen, R.. Goodf...!low, J. (\\: lough, P. (Eds.). Sci~'IlIiric FOlll1dt/tions or OrtJ/(JI'l/~'tlic:s 'lH~:-'{~'lmporlanl biomcchanical properties of articular 7iwf/lllUO/Ogy (pp 213-232). London: William 1-ldncnn<'H ArmSIr<)IH!. e.G., & l\\.fo\\\\'. V.e. (1982). Varialions in dll.\" ;:',c~rlilage are the intrinsic material properties of the Irinsic-mcchank<.tl propt:r1ies of hum'lll anil:ulrtr ci.lni soli~1 matri:\\ and the frictional \"csistance to the flow Wilh agL', degencr;ltion. and w:lI..:'r COrllenl. } 8(111~' J 9f/':,~nterstitial fluid through the porous-permeable Sltff::, 64..1, 88. :spHcl,';',JTlatrix (n parameter inversely proportional to Ateshian, G.A. (1997'). Theoretical formulation for bound ,~h8i+issue permeability). Together, -these parameters rrktion in articular cartilage. J !3iOll/cc), ElIg, 119, Sl. ,;~;~,~efine the level of interstitial fluid pressurization, a :\\LL'shi~tn, G.A., K\\\\'~tk, S.D .. Soslowsk.\\', LJ., et al. (199- :\"'-};£6ajor detenninant of the load-bearing and lubrica- n..:'w sll:n:ophotogr:lInmctry lll..:'lhod for dctermining /iZ.J!ibn capacity of the tissue, which can be generated in situ conlact are;\\s in dianhrodinl joinls: A compar sludy. J Biol1/~'dlallics, 2i, III. )s:cartilage. Atc:shian. G.A., Lai, W.M., Zllli. \\V.B., (:t a!' (1995). An :lsy totic solution for the contact of twO biphasic c~nibgc '~,ti!i-~t;Damage to articular cartilage, from whatcver \\.'1':;. J Biol1lccJulIIics. 27, 1301 i. /~%g~use. can disrupt the normal interstitial fluid load- Ateshi:lll, G.A., & W'\\Ilg. H. (1995). ;\\ thl'oH:tical solution f;\"9~~ring capacity of the tissue and thus the normal til(.' friclionless rolling contact of cylindrical biphasic \"IH§n,fation process operating within the joint. ticular cartibge layers. J BiolIlCC/HlIlics, 28,1341. ~n~tTf()re, lubrication insufficiency may be a pd- Att:'shian, G.A., \\Vallg, H., & Lai. W,M. (1998). Thl..' roll.' o :m~~;y':(aclor in the etiology of OA. tcr::;titi,d fluid in pressurization ilnd surface porositie /i?~@;,- :.' the boundary friction of articular cartilage. 1 hi};ol ;\"G~hr~J'Nhen describing articular cartilage in the con- 120.241. ,:D'Jexl a()f rigorous theOl-etical framework such as the .-\\Ieshian. G.:\\., Warden. W.H., Kim. J.J .. d al. (1997). Fi (\"-,formation biplwsic malerial properties of bovine ,Ir J~.Jjlphasic. triphasic. or multiphasic theories. it is !;Ir cartilage from confined compr..:ssion experimellt ':ltnqssible 10 accurately predict Ihe biomechanical be- BiulI/t.'c/UlIlics. 3D, 1157. ,. ?:~}i~viors of anicular cartilage under loading and to Athan<lsioll, K.:\\ .• Ros('llwasser, i\\·I.P., Buckwallt.'r. J.:\\., e W~1,~!:;lJ~idate the underlying mechanisms that govern (1991). Inlerspecies comparison of in sill! Illcdmn ';r1M,01oad-bearing and lubrication function. Further- propl.\"rlies or diswl rcrnor,ll cartil:tgc. 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OCt 31 ( croscopy of normal and abnormal artlcuhll' curtilagc and or927-934 synovium. J BOl/c Joint SlIrg. 52/\\. 1395. Rcdlcr. L, Zimny. :'.'1.L., \\Ianscl!, J .. et al. (1975). Thc ultra- StoL:kWL'lI, R.S. (1979). Biolo.!!.y COJ\"/i!o!.!.c Cd/so Cambrid C:\\lllbridgl' Uni\\'crsit.\\' Prcss. structure and hiol11cchanical significancc of the tidemark of articular canilagc. Clill Or/hop Rei Res, / /2.357. Sun, D.N .. Gu. \\\\'.1'.. Guo. X.E .. L·t al. (199S1. ThL' infhll'llcL Rosenberg. L.. Choi. H.U .. Tang. 1..-H .. et a!. (1985), Isolation inhomogelleous fixed charge dL'l1sitv on canil,q!l' nlccha L'leetrochclllical belw\\'iors. '!i'mls On/lUp Res Soc. 23. 4 of dennatan sulf.ltc proteoglycans from mature bovine ar- tindar cartilage. J Bio! Cht'lJl, 260, 6304. Swann. I).A .. Radin, E.L .. & Hcndn:lL R.B. (1979). Thl·lu Roscnberg, L.. Hellmann, \\V., &. Kleinschmidt, A.K. (1975). c:ltion of :lrliclIbr cartilage b~' syn(wial I'luid gl,\\'co tL'ins. Arthriris Rhein. 12, 665. Electron microscopic studiL's or proteoglycan aggregatL'S from bo\\'ine articular cartilage. ./ Bio! Chew. 250, 1877. SW:\\l1Il. fL\\ .. Sih'L'r, F.H., Sla~'lL'r. H.S .. ct :d. {1%5L ThL' m Roth, V.. &: Mow. V.c. (1980). The intrinsic tensile bchavior of the nl<\\trix of bovine articular canilagc and its variation t'cubr structure ~lnd lubricating :lcti\\'it,\\' of lubricin f with age . ./ BOHi.' ./oilu SlIrg, 62A, 1102. bo\\\"inc and human s~'nO\\'ial fluids. BiucltoJl J. 225. 19 Roughlev. P.J.. &. Whitc, R.J. (1980). Age-related changes in S\\\\'cL'l. \\l.B.E .. Thonar. E../.-\\1.A., & \\1:lrsh . .I. (1979). A t';e structure of thc proteoglycan sub~lnits from hum7'1ll ar- rL'lated ch,lngcs in protcoglYC:1I1 structurL'. Arch Hioch ticular cartilage. J BioI Choll. 255, 2!i. Biopltys. / 98. 439~448. Roughley. P.l .. \\Vhite. R.l., & Santcr. V. (198 I). Comparison Thompson, R.C .. Ocgcma. TR .. Lcwis . .1.1\" L'l al. (1991 L of proteoglycans extracted from high- and low-weight tcoanhrotic changcs al'tcr anHe Iransarticular load. bearing human articular cartilage, with particular refer- animal model. J BOHL' lohll Slirfi. 73:\\. 990. encc to sialic acid content. J BioI Che/1/, 256, 12699. Thonar. E..I.-\\L·\\ .. Bjornsson, S., & KueHner. K.E. (19 Schinagl. R.M .. Gurskis. D., Chen, A.C., et a1. (!997). Depth- Age.related changcs in canil:lge proteoglycans. In Ku,-'ltner. R.S .. SclJle~'crbach. &. V. C. Hascall (Eds.). A dependent confined compression modulus of full- 1111/1' Clirrilllg.c Biochcl!/islJY (pp. 273,-287). Nl'\\\\' Y thickness bovine articular cartilage. J Ort/lOp Res. /5,499. Ra\\'en Prcss. Torzilli. P.A .. &: \\Iow. V.e. (19761. On the t'lInd:lI11elltal f Schinagl. R.M., Ting. M.K .. Pricc. J.H .. el a1. (1996). Video Iransport lllechanisms through normal and palhologic microscopy to quantitate the inhomogeneolls equilibrium tilage during function. 1. The formulation . ./ Biolllcch, 9 strain within articular cartilage during confined compres- 541-552. sion. illIll Biolllt'd Eng. 24. 500. Torzilli. P.A .. Rose. D.!:., & Dethl'mcrs, S.A. (I9821. Equ Schmidt, :\\-;1.B., Mow, V.C .. ChUll. L.E., et al. (1990). Effects of rium watn partition in articular cartilage. Biorhw/ogy, proteoglycan extraction on the tcnsile behavior of artiClI- 519. Jar canilage. ./ Or/hop Rcs, 8. 353. Schneiderman. R., Keret, D., &. Maroudas, A. (1986). Effects Urban . .l.P.G .. & \\-lc\\luliin . .I.F. (1985). Swclling prcssur thc intervertcbral disc: Influcnce of collagcn and pro of mechanical and osmotic pressure on thc rate of gly- glycan content. Biorhc%gy, 22. 145. cosaminoglycan synthesis in adult femoral head cartilage: Valhlllll. W.B .. StazmDc. E.J .. Bachrach. N.;vl . L'l a!. (19 An in vitro study. J Orthop Res. 4, 393. LO<ld-controlkd compression of articular cartilagL' Schubert, i\\'1.. &. Hamerman, D. (1968). A Primer 011 COIIlICC- tive Tisslle Biochelllistry. Philadelphia: Lea &: Fcbiger. duces a transicllt stimulation of aggn:can gene cxprcss Scott . .I.E.. & Orford, C.R. (1981). Dennatan sulphate-rich Arch Biocltc/!/ Biophys 353, 29. Venn, \\'I.F. (1978). Variation of chemical compOSition protcoglycan associates with rat tail-tendon collagen at age in hllman remora I head cartilagc. Ann RheulII Dis, the d band in the gap region. BiochelJl J, /97,113. 168. Selton, L.A., Gu, \\V.Y., Lai, \\V.M .. et a1. (1995), Predictions of \\Vada. T. & Akiwki. S. (1987). An ultrastructural stud solid matrix in articular cartilagc under uniaxial ten the swelling induced pre-stress in articular cartilage. In stress. J .Ifill On//tJfJ Assn. 61. A.P.S. Selvadurai (Ed.), .lleclulllics of Porous Atcdia (pp. \\Valker. P.S .. Dowson. D.. Longfeild. \\I.D .. et al. (19 299-311). Kluwer Academic Pubs. Dordrecht. the Nether- \"Boosted lubrication\" in syno\\'ial joints b~' rluid ent lllent and enrichment. :Inn !VIC/IIII Dis, 27, 511. lands.

Walka. P.S .. Unswonh, :\\ .. Dowson, D.. I,:t a!. (1970). ~-lod(.' of Woo, S.L.Y.. LL'wsay G.A., Runco, 1.1., ct:ll. (199;). Struc ag!!rcgation of hyaluronic acid prntdn cOll1pk:x on tilL' aml function of (t:ndolls and ligalllt:nts. In V.C. ~·1o sll~facc of articular cartilage. ..\\/11I Wlt'lflll Dis. 29. 591. W.e. Hayes (Eds.), Basic Orthopaedic BiollleclUlllics ( \\V;JOg. C.B., &. Mow, V.C. (199S). Inhomogendty of aggreg,HL' n;odulus affects c~rtil:tgL' cornpn.:ssi\\·I..' strcss-n:la:Xi1tion cd., pp. 109-2.5 I). Phibddphia: Lippincolt-Raven. behavior. 1i'alls Or/hop Uc:s Soc, 13( I). 481. Zhu, \\V.B .. Iatridis, J.e.. Hlibczjk. V.. Cl al. (1996). DCle c..Weiss. Roscnbl.:rg. L., & J-1e1fL'1. A.J. (1968). Alluhraslrllc- n;ltioll of collagen-prot('oglycan interactions in vitr tural study of !lumlal young adllli hum;11l anicular cani· BioJl1cclwnics. 29, 7i3. lage. J BO//(: 10illl SlIrg, 50A, 663. \\Villiams, P.F., j1owdl. G.l.., &: Laberge, M. (1993). Sliding Zhu, \\-V.B., Lli, \\V.~-I., &: J'I·low. v.e. (1986). Intrinsic qu friction analysis of phosphatidylcholinl: as a boundary linl..'ar viscoebstic bL'havior of thc c.\\tracelllllut' m;:Hrl lubricant for anicul<\"lr cartilage. Prot Ills 1 l/ech EIl.!jI'S, cartilagL'. 7i'tIIIS OrthofJ Res Soc, 1/, 407. l07, 59. Zllu, \\V.B., Lai. W.i\\1., &. I\\\\OW, V.e. (1991). TIl(: dl.'nsity Woo. S.L.-Y., Mow, V.c., &: Lai, W.~,t. (1987). l3iorncchanical sll\"L'ngth of proteoglycan-proli..'oglycan interaction site propcnics of ;Irticubr cartilage. In /-IllIu/book of Bioengi- neering (pp. 4.1-.....·H. New York: McGrmv-Hill. C(IIlCenlrakd solutions. J Biolllt'C!liIllics, ],1, 1007. Zhll, W.B., ,\\In\\\\', V.C .. Koob. '1'.1 .. ct al. (1993). Viscoela shl..\"u· propi..'rtil..'s of articular cartilagL' and the <:ffcc!:. glycosidase treatments. 1 Ortlwp Res, I J. 771.

~ AIRTI'CULARCARTILA '.•···HI.,hlvSpeclalizedTlssu I ; ' 'I 1 \\~ CELlULAR COMPONENTS \" POROUS P -Qrg 0, :\":1 ~ j :1 II :,:,'1 \\! Animtropy,Visc ~., FLOW, CHART 3·1 Articular cartilage structure and biomechanicaJ pro '~\\j \"Thh How ChMl is d~si9ncd fOI das>room or group disCLl~~io\". Flow than i~ not mCi'lr'lt

AGE ,streSses sustlllned by cont::ict joint surfaces - u'e .\" '.' '\" \".\",.'.::~::~><,,:,>~' To provldoa smoothwear·reSistantbearing s'urfac~ecrease b1ction~' '~:,', EXTRACELLULAR COMPONENTS Extracellular M3trix-ECM- ,-'/,.,'-' .! ~;!~cTeEirR'S~~~IT~.~I!~%]!f~3i~;!'·1[f)'rH~A~S~E&!,,:i;~;;'> PERMEABLE SOUD PHASE i ganlt Component--: .A Biph;uic Str'uc(urc BIOMECHANICAL PROPERTIES cocl;micity. Swelling Bchavior-ColllprCHivc lo~d bearing c~pJcity- operties. ~ t \\0 be cxh<lustive.

~fLOW CHART 3'2\", Articular cart \"This flow chart is designed for c1assroorn o

Results in Disruption of collagen-PG solid matrix PG \"wash out\" Gross alteration of the normal load cartilage mechanisms tilage wear mechanisms. ~ or group discussion. Flow ch.Jr1 is not meant to be exhaustive.

.\" e:;; .\" 0 iii ~ § ,0 .\" 0 's -S <; 1;' :E ,J.' ! .';\".'i~'-

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Biomechanics of Tendons and ligaments Margareta Nordin, Tobias Lorenz, Marco Campello Introduction Composition and Structure of Tendons and Ligaments Collagen Elastin Ground Substance Vascularization Outer Structure and Insertion Into Bone Mechanical Behavior of Tendons and Ligaments Biomechanical Properties Physiological Loading of Tendons and Ligaments Viscoelastic Behavior (Rate Dependency) in Tendons and ligaments Ligament Failure and Tendon Injury Mechanisms Factors That Affect the Biomechanical Properties of Tendons and Ligaments Maturation and Aging Pregnancy and the Postpartum Period iVlobilization and Immobilization Diabetes lvIellltus Steroids Nonsteroidal Anti-Inflammatory Drugs Hemodialysis Grafts Summary References Flow Charts •

Introduction tutes a large portion of the organic matrix of b and ~artilage and has a unique mechanical supp The three principal structures that c10selv surround, ive function in other connective tissues such connect and stabilize the joints of the ~keletal svs- blood vessels, heart, ureters, kidneys, skin, and li t~Il1are tendons, ligaments, and joint capsules. ~\\l­ The great mechanical stability of collagen gives tendons and ligaments their characteristic stren tIlollgh these structures arc passive (i.e., thev do not and flexibility. acth'ely produce motion as do the l11usck:s), each Like other connective tissues, tendons and l ments consist of relatively few cells (fibroblasts) pl.iJ's an essential role in joint motion. an abundant extracellular matrix. In general, cellular material occupies approximatelv 2000 of The role of the ligaments and joint capsules, total tissue volume, while the extraccliular ma accounts for the remaining 80°/(;. Approxima \\vI11c.h connect bone with bone, is tgol1ai(uiaL~mjoeinntt the 70t;0 of the matrix consists of water, and appro I-IICchanical stability of the joints, to mo- mately 30% is solids. These solids are collag ground substance, and a small amount of c1a; tion, and to prevent excessive motion. Ligaments The collagen content is generallv over 75% and somewhat greater in tendons than in ligame anel joint capsules act as static restraints. Tile func- (Kassel', 1996); in extremitv tendons, the solid m rial may consist almost e~1tirely of collagen (up ticm of the tendons is to attach muscle to bone and 99% of the dry weight) (Table 4- I). to transmit tensile loads from muscle to bone, The structure and chemical composition or l ments and tendons are identical in humans and thereby.' producing joint motion, or to maintain the many animal species such as rats, rabbits, dogs, monkey's. Hence, extrapolations regarding~ th hpcly posture. The tendons and the muscles form structures in humans can be made from the res of studies on these animal species. the muscle-tendon unit, which acts as a dvnamic n> straint. The tendon also enables the mtls~le bell\\' to COLLAGEN p¢at an optimal distance from the joint on whi~h it The collagen molecule is synthesized hv the fl blast \\vithin the cell as a la;'ger precurso·r (proco acts without requiring an extended length of muscle gen), which is then secreted and cleaved extrace ~ larly' to. become collagen (Fitton-Jackson, 19 between origin and insertion. (Fig. 4-1). Tendons and ligaments, like bone, composed of the most common collagen molec Tendon and ligament injuries and derangements a~'e common. Proper management of these disor- (leI'S requires an understanding of the mechanical properties and function of tendons and ligaments ZtIld their capacity' for selF-repair. This chapter dis- cusses the following: Composition and structure of tendons and ligaments Biomechanical properties and behavior of normal tendon and ligament tissue Biomechanical properties and behavior of in- jured tendon and ligament tissue Several factors that affect the bioI11echanical function of tendons and licuo aments are a u\"\"i n u 't)fe'(<1:>- co' nancy, mobilization and immobilization, diabetes, nonsteroidal anti-intlammatory drug (NSAID) use, and the effects of hemodialvsis. Biomechanical con- Tendon siderations regarding graft~ are also given. 20% Composition and Structure I Cellular Material: 20% 80% of Tendons and Ligaments EX~~:~~I~'ari Fibroblast 80% 60-80% 60-80% 20-AO% Tendons and ligaments are dense connective tissues I Matnx 20-40% slightly hig knc)\\vn as parallel-flbered collagenous tissues. These 70-80% 9S-99% sl:arsely vascularized tissues are c0l11posed largelv I Solids: of- collagen, a fibrous protein constituting approxi- Collagen: 90% 1-5% mately one third of the total protein in the bodv Type 1 10% slightly (White, Handlel~ & Smith, 1964). Collagen consti- Type 3 20-30% Ground substance

En(l0!0f!On ProcoHagen f:1l1nd!e Fibroblasl Collagen molecules - - - - - - - - - - - - - _ . _ _ _-..._._---- - ...... ----._.--.~--- ._--._--------- Schematic representation of wllagen fibrils. fibers. and bun- f'xtrac('lIuiar lll<1!rl)( ill cl PiHt111e-! ilflangelll('llt {o form m;· dles in tendons and collagenous ligaments (not drawn to scale). Collagen molecules. triple helices of coiled polypep- crofibrils clnd then fibrils, The staggered array of the mole tide chains. are synthesized and secreted by the fibroblasts. (tIles, in which each overlaps the other, gives .1 banded ap- These molecules (depicted with \"heads\" and \"tails\" to repre- sent positive and negative polar charges) aggregate in the ,0pcarancE' the Coll<1gen iibri!s under the electron llIicro,:>wpe. Tilt:' hb!!l ... <)~J9rcgate further into hbers, ~\"... I1l<:h (omc together into dcn<,cly piicked bundles. type I collagen. This Il101eculc consists of three lihril k'\\'l'l. IL i...; till.' I,.'I'{):-;:,,-!illkl,d dl~II·~h.:[l'I' ur Llll'l' polypeptide chains (ex chains), each coiled in a left- 1~lgl'll lihrib ikll I~h'l'~ ,\"'II'l'll~lh [0 thl' li:--:-il.l('.'\" IIl handed helix wilh approximately 100 amino acids, C( lmpOSl' and <:t1I< I\\\\':-- I hl.':--l' I b:\"Ul'S I( I l\"tl1\"ll.·1 il III und which give it a total molecular weight or approxi. 1ll1.'(\"II<tllic~d :--lrl':\":--. \\\\'illlill 111(' lihril:-., !Ill.' mulecul mately 340,000 daltons (Rich & Crick, 1961) (Fig. <:tl\"t' ;Jppar('Il!I~' tTUss-lillked h.y \"hl'<:\\(.I·I(l-i~lil\" illte 4-2). Two or the peptide chains (called ,,·1 chains) <:ll:tiulb (Fi~_ -l~ I L hUI inlcrlihrilbr IT(I:-..... -linkill~ o are identical. and one differs slightly (the 0:-2 chain). The three a-chains are c0l11binccl in a right-handed rnOl\"L' complL'\\ n~llllr(' <:d~(l rn~l.'\" on·lll'. triple helix. which gives the collagen molecule a rod- like shape. The length or the molecule is approxi. III 111..'\\\\-1\\- fcwlllt:d ,,:(lll~l~l'l1. thl' CI'(l:-.:--·lillk:-- ~\\1\\':' r mately 280 nanOllleters (nIT}), and its diameter is ap- :lli\\\"\\,.,h- k\\\\' :lnd ~lrt' rl.~dlll.'ihl\\:: 1111.' l.'(llb~l.'l1 b :,>olll proximately 1.5 nm. ill rJt'lIlral sail :\"ohlliol\"l:' <:!llll ill ~Icid :\"(IIUliull:--, a Almost two thirds of the collagen molecule con- 1Ilt' i.:ro:--~-Ii111..:-; a I\"l' hI i rI., t'a~i I.,' dL'Il~llll rt'd hy hl.'at. sists of three amino acids: glycine (33%), proline t.:olla~t'n a~L':-', lilt' 1111<:11 rlullIhtT nl rl'lilldhk' tTOS (15%), and hydroxyproline (15°/(;) (Ramachandran, link:-. dl'LTl'a:-'L':-' lei ~l tllinilllurn ~b ~l 1~lr~l' lllllllhl'r 1963). Every third amino acid in each 0: chain is glycine, and this repetitive sequence is essential for :--(~lhk', nonrl,dul'ihk· lTCls:\"-lird,:,, ~lrl' fOI\"t'lll'd. \\bIUI the proper rormation of the triple helix. The small size 01' this amino acid allows the tight helical pack· l'<\"lI~l~t'n i~ nul sU[lIhk, ill Ilt'lllral :\"i.dl ~(lIt1ti(Jll:\" 01' ing of the collagen molecule. C'vlorco\\'cr. glycine en- ~ldd solulio1\\:\", and il :-illlyi\\'l'~:\\ hi~llL'l' dl'I1;,lllll'~l hances the stability of the molecule by forming hy- drogen bonds among the three chains of the tl'l1IjWl':lllll'l', (1\"-\"0[' ~\\ I\\~\\'il'\\\\' or lTo:\"s-link:\\1!l' ill ~'() superhelix. Hydroxyproline and proline form hydro- gen bonds, or hydrogen-bonded wal~r bridges. 12l'll, Sl.'l' Viidik, D~lllil'lsl'll, t~ Chlulld, 10~2,l within each chain, The intra- and inlcrchain bond- ing. or cross-linking. between specific groups on the or.:\\ lihril is !\"(Irllll,d h,\" till' a~~I·q.!.ali(l1l Sl'\\'t'l chains is essential (0 the stability of the molecule, l,'olla~l'1l lllolL'ctlk's ill ;1 qU<lltTn~lIY Slrtlc!url.'. Th Cross-links are also formed between collagen molecules and are essential to aggregation at the strllclllrl.', in \\\\·Ilh.:h t\"ach Illnkndt' O\\'t'!·bp:-. I otht'r, is I\\'spollsihk for 1I1l' J'L'lk'alillt! IXIII((:-; o :':'t'J\"Yl,d Oil thl' lihril\", lllH..kT till' t,k-l'II'OIl lllilTOS(O (Fi~, --l-2: ~l'l' :ds(l Fig, \"'''''). Till' qll,llt'l'll:II-,\" Slrll...:lu or l.T)lIa~cn rdalt'S 10 till.' or~~1I1i:t<:lli(l1l III l.·ollagl.: lllolt'ClIll's il110 :l :\"l~lbk. 10\\\\' l.'lll'r~i,:lic bi(llo!!ic unit ha:--t'd 011 :J rq:!.ul<:\\1· a:':\"(ll\"ial iOll (~r ~\\(,.l.iaCt'lll ';11 t'''.'lIks' h~ISil' <:llId ~lcidil' :llIlino ~ll·ids. B., :In:ll1gi ~\\d.iacl'lll col1at!.I.'l't 1I1pk'l:uks in a qLl~lnl'l'-st~lg1:-~t'r. o

64 om arrangcn)cnt, which cquips the tendons to handl Fibril lhe high unidirectional (uni4lxial) lensile loads t which they are subjected during activity (Fig. 4-4A) 00, 00 The Iigamenls gencrally sLisrain tensile loads in on predominant direction but may also bear smalle or;: Overlap zone (cnsile loads in other directions; their fibers may no 010 be completely parallel but arc closely interiaccd with one another (Fig. 4-48). The specific orienta ;:r:r I I Hole zone tion of the fiber bundles varies to some cxten Micrafibrils among the ligaments and is dcpendcnl on the func ~~~=~'~'~'~~~~~~~~~~Packing of tion of the ligament (Arnie! et al .. 1984), 'molecules The metabolic tUI'nover of collagen may be stud II ied by tritium labeling of h)-!droxyprolinc or glycin and by autoradiographic methods, Studics in ani ..-\",/ ................. mals have shown that the half-life of collagen in ma lure animals is very long: the same collagen mole rColagen -~~/ / cules may exist throughout the animal's adult lire ' however, in young animals and in physically altered ... ........... (e.g., injured or immobilized) tissue, the turnover i i' molecule !r...'.'='='=====:2~I8,0~nm~======):J~ ! ........ .J .................. -. ,. \" , ....................... .......... i a.2~~~t1.5 nm acceleratcd. Rabbit studies have shown melaboli ~, 1 activity to be somewhat greater in ligaments than in tendons, probably because of different stress pat Schematic drawing of collagen microstructure. The colla- terns (Amie! et al .. 1984). gen molecule consists of three alpha chains in a triple helix (bonom). Several collagen molecules are aggregated into ELASTIN a staggered parallel array. This staggering, which creates hole zones and overlap zones, causes the cross-striation The mechanical properties of tendons and liga (banding pattern) visible in the collagen fibril under the ments are dependent not only on the architectur electron microscope. Adapled from Prockop, 0.1.. & Guzman, and properties of the collagen fibers but also on th ;\\! A. (1977). Col/agen dise,)ses and the biosynthesis of collagen \" Hasp Pract. Dec. 61-68. proportion of elastin that these su'uctures contain The protein elastin is scarcely present in tendon and extrcrnily ligaments, but in elastic ligamcnt such as the Iigamenlum Oavum, the proportion o positely charged amino acids are aligned. This sta- elastic fibers is substantial. Nachemson and Evan bl.c structure will require a great amount of energy (1968) found a 2 to I ratio of clastic to collage ,':~ri,d force to separate its molecules, thus contribut- fibers in the ligaments flava. These ligamcnls, which :.ipg to the strength of the structurc. In this way, or- connect the laminae of adjacent vertebrae, appea gU)lizcd collagen molecules (five) form units of mi- to have a specialized role, which is to protect th crofibrils, subfib\"ils, and fibrils (Fig. 4·3) (Simon, spinal nerve roots from mechanical impingement 1994). The fibrils aggregate f'urther to form collagen to pre·stress (preload) the motion segment (th fibers, which are visible under the light microscope. functional unit of the spine), and to provide som ;;./(~hese fibers, which range from I to 20 J.L111 in cliam- intrinsic stability to the spine. ''.;:,'',¢ter, do not branch and l11av be many centimeters \"j<lI1g. They reflect a 64-nm periodicity of the fibrils GROUND SUBSTANCE .:!: and have a characteristic undulated form. The fibers aggregate further into bundles. Fibroblasts are The ground substance in ligaments and tendons con aligned in rows between these bundles and arc elon- sists of proteoglycans (PGs) (ur> to approximatel gated along an axis in the direction of ligament or 20% of the solids) along with stnlctlll,JI glycoprotcins plasma proteins, and a variety of srnall n1olcculcs ;'i':.~.enclon function (Fig, 4-4). The PG units, macromolecules composed of variou ';/: The arrangement of the collagen j-ibers differs somewhat in the tendons and ligarncnls and is sulfated polysaccharidc chains (glycos<lminoglycans Suited to the function of each stru~ture. The fibers bonded to a corc protein, -bind to a long hyaluroni composing the tcndons have an orderl.y, parallel acid (HA) chain La form an cxtremely high molecula

Fibroblasts Crimp Fascicular membrane Schematic representation of the microarchitecture of a tendon. • • Nearly parallel weight PC aggregate like Lhm found in Lhc ground bundles of substance of anicular cartilage (set.:' Fig. 3-6). Parallel bundles of collagen fibers collagen fibers The PC aggregates bind most of the extracellular water of the ligament and tendon. making the ma- Tendon ~I~= trix a highl~' structured gel-like material rather than A Fibroblasts an amorphous solution. Furthermore. by acting as a ccment-likc substance betwcen the coHagen mi- ligament croflbrils. they ma),' help stabilize the collagenous skeleton of tendons and ligaments and contribute to B the o\\'crall strength of these composite structures. Only' a small number of these molecules exist in ten- Schematic diagram of the structural orientation of the dons. however, and their imporlance for its biorne- fibers of tendon (A) and ligament (8); insets show longitu- chanical properties has been questioned, dinal sections. In both structures the fibroblasts are elon- gated along an axis in the direction of function. Adapted VASCULARIZATION from Snell, R.5. (984), Cfinical and F~ln(tional Histology for Medical Stuejents. Boston: Liule. Brown Tendons and ligaments have a Iimitcd vasculariza- tion. which alTeets dircctl~' their healing process [lnd metabolic activit~;. Tendons receive their blood sup- ply dircctly from \\'cssels in the perim.vsiulll. the periosteal insertion. and the surrounding tissuc via vessels in the para tenon or mesotenon. Tendons sur- rounded b~) paratenon have been referred to as vas- cular tendons. and those sllrround~d by a tendon sheath as avascular tendons, In tendons surrounded by' a paratcnon, vessels enter rrom many points on the pcripher.v and anastomose with a longitudinal svstem or capilbries (Fig, 4-5),

The vascular pattern for tendons surrounded by tendon sheath is different. Here the meso tenons a reduced to vincula (Fig. 4-6). This avascuJar regio led a variety of researchers to propose a dual pat way for tendon nutrition: a vascular pathway, an for the avascular regions, a synovial (diffusio pathway. The concept of diffusional nutrition is primary clinical significance in that it implies th tendon healing and repair can occur in the absen of adhesions (i.e\" a blood supply). Conversely, lig ments in comparison with surrounding tissue a pear to be hypovascular. However, histological stu ies reveal that throughollt the ligament substan there is a uniform multivascularit)', which orig nates from the insertion sites of the ligament. D India ink-injected (Spalteholz technique) into the calcaneal spite the small size and limited blood flow of th tendon of a rabbit, illustrating the vasculature of a vascular s)'stem, it is of prima(y importance in t paratenon-covered tendon. Vessels enter from many points ··f maintenance of the ligament. Specifically, by pr \" on the periphery and anastomose with a longitudinal system viding nutrition for the cellular population. this va cular system maintains the continued process of capillaries. Reprinted wirh permission from Woo, S.L. Y, An, K.N., Amoczky, D.V.M., et at. (1994). And!Om}~ biology. and bio- matrix synthesis and repair. In its absence, damag mechanics of rhe iendon, ligament, and meniscus. In S.R. Simon fTom normal activities accumulates (fatigue) an (Ed) Orthopaedic Basic Science (p. 52). Rosemont, Ii: MOS. the ligament is at risk for rupture (Woo et aI., 1994 • Ligaments and tendons have been shown in bo human and animal studies to have a variety of sp cialized nervc endings and mcchanorcceptors, Th play an important role in proprioception and noc ception, which are directly related to the functio ality of joints. the tendon substance. ReprinlGd wirh permission from Woo, S.L. Y, An, K.N., Amoczk}~ D. VM., et al. (1994). Anatomy, biolog and biomechanics of (he rendon, ligament, and meniscus, In S.R Simon (Ed.). Orthopaedic Basic Science (p. 52). Rosemont. IL: MOS.

OUTER STRUCTURE AND INSERTION Electron micrograph of a patellar tendon insertion from INTO BONE dog, showing four zones (:<25,000). Zone 1, parallel coll Certain similarities arc found in the outer structure gen fibers; zone 2, unmineralized fibrocartilage; zone 3, of tendons and ligaments, but there are also impor- mineralized fibrocartilage; zone 4, cortical bone. The lig tant differences related to function. Both tendons and ligaments arc surrounded by' a loose areolar ment-bone junction (not pictured) has a similar appear- connective tissue. In ligaments, this tissue has no ance. Reprinted with permission from Cooper, R.R. & Misol, S specific name, but in tendons it is referred to as the (1970). Tendon and ligament insertion. A light and electron para tenon. More structured than the connective tis- microscopic study J Bone Joint Surg, 52A, I. sue surrounding the ligaments, the paratcnon forms a sheath that protects the tendon and enhances glid- • ing. In some tendons, such as the flexor tendons of the digits, the sheath runs the length of the tendons, strong enough to sustain the high tensile forces th and in others the sheath is found only! at the point result from muscle contraction during joint moti where the tendon bends in concert \\vith a joint. yet are sufficiently' flexible to angulate around bo surfaces and to deflect beneath retinacula to chan In locations where the tendons are subjected to the flnal direction of muscle pull. The ligaments particularly high friction forces (e.g., in the palm, in pliant and Oexible, allowing natural movements the digits, and at the level of the wrist joint), a pari- the bones to which they attach, but are strong a etal synovial layer is found just beneath the inextensible so as to ofTel' suitable resistance to paratenon; this synoviun1-like membrane, called the plied forces. epitenon, surrounds several flber bundles. The syn- ovial fluid produced by the synovial cells of the Analysis of the mechanical behavior of tendo epitenon facilitates gliding of the tendon. In loca- and ligaments provides important information tions where tendons are subjected to lower friction the understanding of injury mechanisms. Bo forces, they are surrounded by the panltenon only'. structures sustain chiefly tensile loads during n mal and excessive loading. When loading leads Each fiber bundle is bound together by the en- injury, the degree of damage is affected by' the r dotenon (Fig. 4-1), \\vhich continues at the musculo- of impact as well as the amount of load. tendinous junction into the perimysium. At the tendo-osseous junction, the collagen fibers of the endotenon continue into the bone as Sharpey's per- fOl·ating fibers and become continuous with the periosteum (Woo et aI., 1988). The structure of the insertions into bone is simi- lar in ligaments and tendons and consists of four zones; Figure 4-7 illustrates these zones in a tendon. At the end of the tendon (zone 1), the collagen fibers intermesh with fibrocartilage (zone 2). This fibro- cartilage gradually becon1es Inineralized fibrocarti- lage (zone 3) and then merges into cortical bone (zone 4). The change from more tendinous to more bony n1aterial produces a gradual alteration in the mechanical properties of the tissue (i.e., increased stiffness), which results in a decreased stress con- centration effect at the insertion of the tendon into the stiffer bone (Cooper & Misol, 1970). Merhanical Behavior of Tendons and Ligaments Tendons and ligaments arc viscoelastic structures \\vith unique mechanical properties. Tendons are

VIVI~,-.\"MI.\".\"'L PROPERTIES means of analyzing the biomechanical proper- of tendons and ligaments is to subject specimens tensile deformation lIsing a constant rate of elon- The tissue is elongated until it ruptures, and resulting force, or load (P), is plolted. The result- load-elongation Clll-ve has several regions that the behavior of the tissue (Fig. 4-8). The first region of the load-elongation cuniC is the \"toe\" region. The elongation reflected in region is believed to be the result of a change the wavy pattern of the relaxed collagen fibers. In region, the tissue stretches easily, without much and the collagen fibers become straight and their \\vavy appearance as the loading pro- a\",:sSl:s(Hirscb, 1974; Woo et a!., 1994) (Fig. 4-9, A B). Some data suggest, however, that this elonga- may' be caused mainly by' interfibrillar sliding 4 3 2 1I mmL- Elongation (%») _ I Load-elongation curve for rabbit tendon tested to failure Scanning electron micrographs of unloaded (relaxed) a I in tension. The numbers indicate the four characteristic re- loaded collagen fibers of human knee ligaments (x 10,000). A, The unloaded collagen fibers have a wavy I gions of the curve. (1) Primary or \"toe\" region, in which configuration. S, The collagen fibers have straightened under load. Reprinted with permission from Kennedy, J. C, the tissue elongated with a small increase in load as the Havjkins, R.I. Willis, R.B., et al. (7976). Tension stuclies of hu man knee ligaments, Yield point, ultimate failure, and disrup I wavy collagen fibers straightened out. (2) Secondary or of the erueiare and tibial collateral ligaments. J Bone Joint Su S8A.350. \"linear\" region, in which the fibers straightened out and the stiffness of the specimen increased rapidly. Deforma- tion of the tissue began and had a more or less linear rela- tionship with load. (3) End of secondary region. The load value at this point is designated as PI;,,' Progressive failure of the collagen fibers took place after PI'\" was reached, and and shear of the interfibrillar gel (ground substan small force reductions (dips) occurred in the curve. (4) Max- (for review, see Viidik, Danielson, & Oklund, 198 imum load (Pm.,,) reflecting the ultimate tensile strength of the tissue. Complete failure occurred rapidly, and the spec- As loading continues, the stiffness of the tis imen lost its ability to support loads. Adapted from Carls/edt, increases and progressively greater force is requi to produce equivalent amounts of elongation. T c.A. (7987). Mechanical and chemical factors in tendon healing: Effects of indomethacin ancl surgery in the rabbit. Acta Orthop elongation is often expressed as strain (e), whic Scand Suppl, 224. the deformation of the tissue calculated as a p centage of the original length of the specimen ~~---------

strains arc increased (strain values of between 1.5 elastic deformation that they endure under tensi and 4% [Viidik, 1973]), a linear region will follow strain and the storage and loss of energy. Durin the toe region. This sudden increase in slope repre- loading and unloading of a ligament between tw sents the second region in the diagram and con\"c- limits of elongation, the elastic fibers allow the m sponds to the response of Ihe tissue to further elon- tcrial to return to its original shape and size aft gation (Diamant et al.. 1972). being deformed. Meanwhile, part of the enel- spent is stOt\"cd; what is left will represent lhe energ Following the linear region. at large strains the loss during Ihe cycle and is called hysteresis. Th stress-strain ClIlve can end abruptly or curve down- area enclosed by the loop represents the energy lo ward as a result of irreversible changes (failure) (Fig. 4-1 I). (Woo et aI., 1994). Where the curve levels off toward the strain axis, the load value is designated as Plin, PHYSIOLOGICAL LOADING OF TENDONS The point at which this value is reached is the yield AND LIGAMENTS point [or the tissue. The energy uptake to PHn is rep- The ultimate tensile strength (P,,,:..,,) of ligamen resented by the area under the ClIl·ve lip [0 the end and tendons is of limited interest from a function of the linear region. standpoint because under normal physiologic conditions in vivo these structures are subjected \\Vhen the linear region is surpassed, major fail- a stress magnitude that is only approxirnately on ure of fiber bundles occurs in an unpredictable third of this value. The upper limit for physiologic l11anne1'. \\Vith the attainment of maximum load that strain in tendons and ligaments (when running an reflects the uhimatc tensile strength of the speci- jumping, for example) is from 2 to 5% (Fung, 1981 men, complete Failure occurs rapidly, and the load- supporting ability of the tendon or ligament is sub- o -70 stantially reduced. Elongation (~o) The modulus of elasticity for tendons and liga~ ments has been determined in several investigations Load·elongation curve for a human ligamentum flavum (Fung, 1967, 1972; Viidik, 1968). This parameter is (60 to 70% elastic fibers) tested in tension to failure. At based all a linear relationship between load and de- 70% elongation the ligament exhibited a great increase formation (elongation), or stress and strain; that is, stiffness with additional loading and failed abruptly with the stress (force per unit area) is proportional to the out further deformation. Adapted from Nachemson, A.L., & strain: Evans, J.H. (1968). Some mechanical properties of tile third hu man lumbar imerlaminar ligamenr (ligamentum flavum). ) B;o- E = rIlE mech, 1, 21/-220. where E = modulus of elasticity • (T = stress E = strain In the toe portion of the load-elongation curve (or stress~slrain curve), the modulus of elasticity is not constant but increases gradually. The modulus sta- bilizes in the fairly linear secondary region of the curve. The load-elongation CUPie depicted in Figure 4-8 generally applies to tendons and extremity liga- ments. The curve for the ligamentum flavulll, with its high proportion of elastic fibers, is entirely dif- ferent (Fig. 4-10). In tensile testing or a human ligamentum flavlIIll, elongation of the specimen reached 50% before the stiffness increased appre- ciably. Beyond this point. the stiffness increased greatly with additional loading and the ligament failed abruptlv (!'eached P\"\",,), with little further de- formation (Nachemson & Evans, 1968). The proportion of elastic proteins in ligaments and capsules is extremely important for lhe small ~1.'· ,--? .

1 cycle ~Peakload store more energy, require marc force to I1.lptu ~ and undergo greater elongation (Kenncd.\", Hawki Willis, & Danylchuk, 1976). Elongation Dw-ing cyclic testing of ligaments and tendo Typical loading (top) and unloading curves (bottom) from where loads are applied and released al specific tensile testing of knee ligaments. The two nonlinear curves tenmls, the stress-strain curve is displaced to form a hysteresis loop. The area between the curves, called riglll along the deformation (strain) axis with ea the area of hysteresis, represents the energy losses within loading cycle, revealing the presence of a nonel the tissue. tic (plastic) cOlllponcnt; thc amount 01\" perm nent (nonrecoverable) deformation is progressiv '0 ,Few studies or loading of tendons or Ii!!aments in greater with every loading cycle. As cyclic load progresses, the specimcn also shows an increase \\:ivo have been perrorm~d. Kear and Smith (1975), clastic stiffness as a result of plastic dcfonnati (molecular displacement). IVlicrofailure can oc using the strain gauge method, measured the rnaxi- within the physiological range if frequcnt loading nUll strain in the latcral digital extensor tendons of imposed on an already damaged struclUrc wh sheep. The strain reached 2_6t}~ while the shl:cp lhe stiffness has decreased. were trolling rapidly and decreased when the trol- ting speed decreased. This maximal strain occurred Two standard tests that reveal the viscoelastic for only 0.1 second during each stride. The maximal or ligaments and tendons are the stress-relaxat load imposed on the entire tendon was approxi- test and the creep test (Fig, 4~12). During a stre mately 45 newtons (N). These results suggest that relaxation test, loading is hailed safely below during normal activity, a tendon in vivo is subjected linear region of the stress-strain curve and the str LO less than one fourth of its ultimate stress. is kept constant over an extended period. The str decreases rapidly at first and then more sl()\\v VISCOELASTIC BEHAVIOR (RATE \\Vhen the stress-relaxation test is repeated cy DEPENDENCY) IN TENDONS AND LIGAMENTS cally, the decrease in stress gradually becomes l pronou need. Ligaments and tendons exhibit viscoelastic, or rate- dependent (time-dependent), behavior under load- During a creep lcst,loading is halted saFely bel ing; their mechanical propelties change with differ- the linear region of the stress-strain curve and ent rates of 1041ding. v\"hen ligament and tendon stress is kept constanl over an extended period. T specimens are subjected to increased strain rates strain increases relatively quickly at first and th (loading rates), the linear portion of the stress-strain more and more slowl.':. \\Vhen this tcst is perform curve becomes steeper, indicating greater stiffness cyclically. the increase in strain gradually becom of the tissue at higher strain rates. v\\lith higher less pronounced, strain rates, ligaments and tendons in isolation The clinical application or a constant low load the soft tissues over a prolonged period, which ta advantage of the creep response. is a llseful tre ment for several types of deformities. One exam is the manipulation of a child's clubfoot by subje ing it to constant loads by means of a plaster ca Another example is the treatment of idiopathic s liosis with a brace, whereby constant loads are plied to the spinal area to elongate the soft tiss surrounding the abnormally curved spine, More complex viscoelastic beh41vior is observed the entire bone-ligament-bone complex_ Antel cnlciate ligaments (ACLs) in knee specimens tak from 30 primates were tested in tension to failure a slow and a fast loading rale (Noyes el aI., 1976). , the slow loading rate (60 seconds), much slower th that of an injury mechanism in vivo, the bony ins tion of the ligament was 'the weakest component the bone-ligament-bone complex.. and a tibial sp c',,\"

Load relaxation bone-ligament-bone complex \\vas nearly' the sam These results suggest that as the loading rate is i \"'\" (length held constant) creased, bone shows a greater increase in streng than does ligament. o --' Ligal1zel1t Failure and Tendon Injury Mechanisms A Time Injury mechanisms arc similar for ligaments an oc Creep phenomenon tendons, therefore the following description of lig (load held constant) ment injury and failure is gencrall~1 applicable .~ tendons. \\Vhen a ligament in vivo is subjected E loading that exceeds the physiological range. micr \"<oii failure takes place even before the yield point (P\" is reached. \\\"'hen Ph\" is exceeded, the ligament b gins to undergo gross failure and simultaneolls the joint begins to displace abnormally. This d placement can also result in damage to the su Time B The viscoelasticity (rate dependency, or time dependency) Microfaiture of ligaments and tendons can be demonstrated by two o 2 34 56 standard tests: the load-relaxation test and the creep test. Elongation (mm) A, Load relaxation is demonstrated when the loading of a specimen is halted safely below the linear region of the Progressive failure of the anterior cruciate ligament from load-deformation curve and the specimen is maintained at cadaver knee tested in tension to failure at a physiologic strain rate. The joint was displaced 7 mm before the liga a constant length over an extended period (i.e., the ment failed completely. The force-elongation curve gene ated during this experiment is correlated with various de amount of elongation is constant). The load decreases grees of joint displacement recorded photographically; rapidly at first (Le., during the first 6 to 8 hours of loading) photos correspond to similarly numbered points on the and then gradually more slOWly, but the phenomenon may curve. Reprinted wirh permission from Noyes, F.R., and Graae continue at a low rate for months. B, The creep response E.S. (976). The strengrh of the anterior cruciare ligament in h takes place when loading of a specimen is halted safely be· mans and Rhesus monkeys. Age-relared and species~relared low the linear region of the load·deformation curve and changes. J Bone Joint Surg, 58A. 1074-1082. the amount of load remains constant over an extended pe- riod. The deformation increases relatively quickly at first (within the first 6 to 8 hours of loading) but then progres~ sively more slowly. continuing at a low rate for months. avulsion was produced. At the fast loading rate (0.6 seconds), which simulated an injury mechanism in vivo, the ligament was the weakest component in t\\Vo thirds of the specimens tested. At the slower rate, the load to failure decreased by 20%, and 30% less en- ergy was stored to failure, but the stillness of the

350 Complete spectivcly to (I) the load placed on the ACL duri (3) failure tests of knee joint stability performed clinical ~ (2) the load placed on this ligament during phys 23456 7 8 logical activity, and (3) that imposed on the lig \"-0 200 Joint Displacement (mm) ment during injury from the beginning of micr failure to complete rupture. Microfailurc begi 0 even before the physiological loading range is e ceeded and can occur throughout the physiologic -' range in any given ligament. In fact, under expe mental testing, the ultimate tensile loaels-or t o load at failure for human ACL-is between 340 a 390 N (Case Study 4-1), o --- The curve produced during tensile testing of a human an- ACL Failure: Failure of the ACL terior cruciate ligament in vitro (20) (see Fig. 4-13) has Associated With High Strain and Stress been converted to a load-displacement curve and divided into three regions correlating with clinical findings: (1) the A25-year·old male occasional soccer player injured load imposed on the anterior crudale ligament during the . his ACl as a result of an abnormal torque in rotation of the knee. The player locked his foot on the ground ~,. and pivoted on his lower limb to produce a high rota· , tional torque on the knee, which increased tensile loads anterior drawer test; (2) that placed on the ligament dur- ing physiological activity; and (3) that imposed on the liga w on the ACL, men! from partial injury to complete rupture. It should be noted that the divisions shown here represent a general- The first region of the load-displacement curve shows ization. Microfailure is shown to begin toward the end of the physiological loading region, but it may take place a normal physiological loading response. In the microfail- well before this point in any given ligament. ure region, the increase in strain deformation leads to rounding structures, such as the joint capsule, the high internal stress and finally a complete rupture. Experi- adjacent ligaments, and the blood vessels that sup- ply [h~sc structures. mental testing in vitro in human ACl yielded a point of Noyes (1977) demonstrated the progressive fail- failure between 340 and 390 N. ure of the ACL and displacement of lhe tibiofemoral The knee with the ACl injury will increase intra-articu- joint by applying a clinical test, the antel-iOl- drawer '.\" tc;-st, to a cadaver knee up to the point of ACL failure lar joint motion, producing abnormally high stresses on 'AFig, 4-13), At maximum load, the joint had dis- other joint structures such as cartilage, which can lead to placed several millimeters. The ligament \\vas still in osteoarthritis. A deficiency in joint stability that results '~o,ntinuit.y even though it had undergone extensive from ACl impairments will increase the likelihood of ex· ~jacro- and microfailure and extensive elongation, periencing the \"giving way\" sensation or functional insta- bility, thus affecting activities of daily living such as gait, 'In Figure 4-13, the force-elongation curve generated jogging, and squatting (Case Study fig 4-1- 1). during the experiment, indicaling where Illicrofail- o 234 56 7 8 .,:. ure of the ligament began, is compared with val\"ious stages of joint displacement t-ecordcd photographi- Joint Displacement (mm) cally, Case Study Figure 4-1-1. Correlation of the results of this test in vitro with clinical findincrs sheds Jjcrht on the microevents that ~~ take place in the ACL during normal daily activitv and during injuries of variou~ degrees or s~verity. I~ Figure 4-14, the curve for the experimental study On cadaver knees that was presented in Figure 4-J3 been converted into a load-displacement curve divided into three regions, corresponding re-

Ligament injuries arc categorized clinically in thus the greater the tensile loads transmitlcc! three ways according to degree of severity. Injuries through the tendon. Similarly, rhe larger the cross- in the first category produce negligible clinical sectional area of the tendon, the greater the loads it symptoms. Some pain is felt, but no joint instability can bear. Although the maximal stress to failure for can be detected clinically, CYCI1 though microfaillire a muscle has been difficult LO compute accurately, of the collagen fibers may have occurred. such measurements ha\\'c shown that the tensile Injuries in the second category produce severe orstrength a healthy tendon 111<1)-.' be mon: than pain and some joint instability can be detected clin- t\\Vice that or its Illuscle (Elliot, 1967), This finding ically. Progressive failure of the collagen fibers has taken place. resulting in parlial ligament nlplure. is supponed clinically by the fact that muscle fUp- The strength and stiffness of the ligament may have lures are more common than are ruptures through decreased by 50% or more, mainly because the amount of undamaged tissue has been reduced. The a tendon. joint instability produced by the partial rupture or a ligament is oflen masked by muscle activity, and Large muscles usually' have tendons with larg~ thus the clinical test for joint stability is usually cross-sectional areas. Examples arc the quadriceps performed with the patient under anesthesia. - - - --------<0 Injuries in the third categOlY produce severe pain during the course of trauma with less pain after -rend on Injuries: Achilles Tendon Injuries in injury Clinically, the joint is founelto be completely Runners. Which Result From a High Strain unstable. Most collagen fibers have ruptured, but a Rate few Illay still be intact, giving the ligament the ap- pearance of continuity even though it is unable to .·.. middle-aged male marathoner engaged in a strenuous SUppOrl any loads. A running activity expenenced pain and a popping sensa~ Loading of a joint that is unstable as a result of tion in his posterior calf. An overuse injury is diagnosed. ligament or joint capsule rupture produces abnor- mally high stresses on the articular cartilage. This The first region of the load-deformation curve ShQ\\.V5 a abnormal loading of the articular cartilage in the knee has been correlated with carl~,' osteoarthritis in normal physiological toe-loading response. In the linear humans and in animals. region, high load is producing a higher deformation Although injury mechanisms are generally com- parable in ligaments and tendons, two additional within the tendon structure. When the Achilles tendon is factors become important in tendons because of their attachment to muscles: the amount of force subjected to higher strain rates during frequent loading produced by contraction of the muscle to which the tendon is attached and the cross-sectional area of ;_ ~ycles and insufficient time is allowed for the healing the tendon in relation to lhat of its muscle. A tendon process, the result is an overuse injury. Histological studies is subjected to increasing stress as its muscle con- tracls (see Fig, 6-10), When the Illuscle is maximally ot',these injuries reveal a pathological pattern described as contracted, the tensile stress on the tendon reaches ~'angiofibrotjc hyperplasia,\" which suggests a degenera- high levels. This slress can be increased fl.lrlher if rapid eccentric contraction of the muscle takes \" tive process. This failure in tendon remodeling frequently place; for example, rapid dorsiflexion of the ankle, which does not allow for reflex relaxation of the gas- ,. occurs before the abrupt ruplure of the tendon. Relative trocnemius and soleus muscles, increases the ten- sion on lhe Achilles tendon, The load imposed on aydscu!arity, inflammatory disease, and other local factors the tendon under these circumstances may exceed the yield point. causing Achilles tendon rupture also contribute to midsubstance ruptures (Case Study 4·2-1), (Case Study 4-21- 250,00 Toe Linear OVERUSE ~ RUPTURE The strength of a muscle depends on ilS physio- 200,00 region region yield and logical cross-sectional area. The larger the cross- sectional area of the muscle, the higher the magni;:' failure region lude of the foree produced by the contraction and ~ 150,00 .3u 100.00 50,00 1,00 2,00 3,00 4,00 5,00 6,00 7,00 Def9rmation (mm) Case Study Figure 4·2·1.

muscle with its patellar lendon and the triceps Slifac did nOl differ signillcanLi~1(Kaspcrczyk et aI., 1991). muscle with its Achilles tendon. Some small mus- This may be due 10 the fact lhal only lhe ACL was cles have tendons with large cross-sectional areas; taken from donors in \\I,,1hom no vascular or car- such as the plantaris. which is a liny muscle with a diopulmonary disease and no ostcoanhritis of the large tendon. knee was found on autopsy. Factors That Affect the PREGNANCY AND THE POSTPARTUM PERIOD Biomechal1ical Properties of Tendons and Ligaments A common clinical observation is thc incrcasecllax- ity of the tendons and ligaments in the pubic arca Numerous factors alTecl I he biomcchanical proper- during later stages of pregnancy and the postpar- ties of tendons and ligaments. The most common tum period. This obsen\"~llion has been confirmed in are aging. pregnancy, mobilization and immobiliza- animal studies, Rundgren (1974) found lhmlhe ten- lion. diabeles. steroids. NSAID use. and hemodialy- sile strength of the lendons and the pubic symphysis sis. The biomcchanical properties of grafts are also in rats decreased at the end of pregnancy and dur- d,iscllssed because reconstruction, particularly of the ing the postpartum period. Stiffness of these stnlc- anterior and posterior knee ligaments, is common. tures decreased in the early postpartum pCI'iod but was later restored. MOBILIZATION AND IMMOBILIZATION MATURATION AND AGING Living tissues are dynamic and change their me- The physical properlies of collagen and of lhe lis- chanical properties in response to stress, which sues it composes are closely associaled with the leads to functional adaptation and optimal opera- , number and quality of the crossMlinks within and be- lion of the tissue. / tween the collagen molecules. During maturation Like bonc, ligament and tcndon appear to re- (up to 20 years of age), the number and quality of model in response to the mechanical demands cross-links increases. resulting in increased tensile placed on them; they become stronger and stiffer strength of the tendon and ligament (Viidik, when subjected to increased stress and weaker and Danielsen, & Oxluncl, 1982). An increase in collagen less stiff when the stress is reduced (Noyes el aL. fibril diameter is also observed (Parry et aL. 1978) I 977a), wilh high variabilily in size (range 20-180 nm) Physical training has been found to increase the (Strocchi. el aL. 1996) noted in lhe ~'oung «20 tensile strength of tendons and of the Iigament Mbone years), The diameler in adults (20-60 veal's) and in interface (Woo et aL. 1981), Tipton and coworkers lhe elderly (>60 years) decreases remarkably (120 (1970) compared the slrenglh and sliffness of me- and 110 nm) but \\vith a marc even distribution. dial collateral ligaments from dogs that were e~cr­ Slrocchi et al. (1996) investigated age-related ciscd strenuously for 6 weeks with the values for lig- changes in human ACL collagen fibrils and reports aments from a control group of animals. The an increase of libril concenlration from 68librils/mu' ligamcnts of the exercised dogs were stronger and in the young to 140 fibrils/mu' in the elderly. How- stiffer than lhose of lhe control dogs. and the colla- evel; Amiel (1991) reports Ihal lhe waleI' content gen fiber bundles had largel- dianlelers. and the collagen concentration decreases signifi- (mmobilization has been found to decrease the cantly in the medial cruciate ligament of 2M, 12-, and tensile strength of ligaments (Newton et al., 1995; 39-month-old rabbits, Walsh et aL. 1993), Noyes (1977a) demonstrated a After maturation, as aging progresses, collagen reduction in the mechanical properties of the reaches a plateau with respect to its mechanical bone-ligament-bone complex in knees of primates properties, afler which the tensile strength and stiff- immobilized in body casts for 8 weeks. When i': ness of the tissue begin to decrease. This may be the lested in tension to failure, the ACLs from these result of an increase in small collagen fibrils. Con- animals showed a 391'10 decrease in maximum .load versely, when the ACL of younger donors (average to failure and a 32% decrease in energy stored to age 30 years) was compared wilh the ACL of older failul-e compared with ligaments fl'om a control donors (average age 64.7 years), the material prop- group of animals (Fig. 4-15A), The immobilized erties (strain. elastic modules, and maximum stress) ligaments also displayed more elongation and were oF\"'-';- ,

significanlly less stitT than the control spcc..:imens ments (Fig. 4-1 SA). Woo et \"I. (1987) found that the (Fig, 4-158), stress-strain characteristics after rcmobilization re- turn to normal but that the energy-absorbing capa- Amid and coworkers (1982) showed a similar de- bilities or the bone-ligament complex improved but crease in the strength ancl stiffness or lateral collat- did not return to normal. eral ligaments in rabbits immobilized for 9 weeks. As the cross-sectional area of the specimens did 110t DIABETES MELLITUS change Significantly, the degeneration of mechani- cal properties was altributed to changes in the liga- The term diabetes rcfcrs to disorders characterized ment substance itself. The tissue metabolism was by excessive urine excretion. Diabetes mellitus is a noted to increase, leading to proportionally more metabolic disorder in which the ability to oxidize immature collagen with a decrease in the amount carbohydrates is more or less completely lost. This and quality of the cross-links between collagen mol- is usually caused by pancreas insufficiency and a ecules. Newton et al. (1995) reported that the cross- disturbance of the normal insulin mechanism, rc- sectional area of ligaments in immobilized n1bbit sulting in hyperglycemia, glycosuria, and polyuria. knees waS 740/0 of the control valuc. Diabetes mellitus is known to cause musculoskele- tal disorders. Diabetics compared with nondiabetics In Noves' (I977a) experiment, assessment of the show higher rates of tendon contracture (29 \\IS. 9%), effects of a reconditioning program initiated di- tenosynovitis (59 vs. 7%), joint stillness (40 vs. 9%), rectly aftcr the 8-\\\\'cek immobilization pel\"iod and capsulitis (16 \\'s. 1%). Diabetes also causes os- demonstraLcd that considerable time was needed teoporosis (Calvallo et aI., 1991; Lancaster et aI., 1'01' the immobilized ligaments to regain their for- 1994). mer strength and stiffncss. After 5 months, the re- conditioned ligaments still showed considerably Duquette (1996) examined the effects of diabetes less stiffness and 20% less strength than did liga- on the properties of the collateral knee ligament in ments from control animals. At 12 months, the re- rats. The tissue elastic properties did not differ be- conditioned ligaments had strength and stiffness tween the diabetic and the control group. The vis- values comparable to those of control group liga- 100 -- ,.- \" \" \"\"\" .------- Immobilized 60 o A' --~8 weeks) -0,\"2 I ~~ 60 \\ l'l E \\ c~ \"~·Ex 40 \\ Q\".'.E\" Maximum load Energy slored Elongation (mm) 10 failure 10 failure 20 B A A, Maximal load to failure and energy stored to failure for program for 12 months. 8. Compared with controls. liga- primate anterior cruciate ligaments tested in tension to faH- ments immobilized for 8 weeks were significantly less stiff (as indicated by the slope of the curve) and underwent greater ure. Values are shown as a percentage of control values for elongation. Adapred from Noyes. FR. 0977(1). Functional proper~ I ties of knee ligaments and alterations induced by immobilization. three groups of experimental animals: (1) those immobilized (lin Onhop, 123,2/0-242. in body casts for 8 weeks; (2) those immobilized for 8 weeks and given a reconditioning program for 5 months; and (3) those immobilized for 8 weeks and given a reconditioning

COllS component of the tissue response, however, (1997) reports that physiological levels of estrogen \\vas increased in the hy'perglycemic group. Insulin reduce the collagen production by 40(;1(; and at phar therapy seems to lessen such alterations. Lancaster, macological levels of estrogen, collagen production ct al. (1994) examined the changes in the mechani~ is decreased by' more than 50%, Estrogen fluctua cal properties of the patellar tendon in diabetic dogs. tions may alter ligament metabolism and ma The results showed the stiffness of the canine patel- change the composition of ligament, rendering i lar tendon-tibia complex in a phy'sioiogical range of more susceptible to injury. loading was 13% greater than in the control group. There was no difference in the strength of the tendon NONSTEROIDAL ANTI-INFLAMMATORY DRUGS between the groups, but the mode of failure was dif~ ferent. In the control group, failure was caused by NSAIDs (which include aspirin, acetaminophen, and substance and avulsion failure, whereas failure of indomethacin) are frequently used in the treatmen the tendon in the diabetic group was caused by ten- of various painful conditions of the musculoskeleta sile fractures of the patella (Lancaster et al\" 1994). system. NSAIDs are also widely used in the treat ment of soft tissue injuries such as inflammatOl)' dis STEROIDS orders and partial ruptures of tendons and liga ments. Vogel (1977) found that treatment wit Corticosteroids, when applied immediately after in- indomethacin resulted in increased tensile strengt jury, may' cause significant impairment of the bio~ in rat tail tendons. An increase in the proportion o mechanical and histological properties in liga~ insoluble collagen and in the total collagen conten ments. Corticosteroids also are known to inhibit also was observed. Ohkawa (1982) found increase collagen synthesis in vitro (\\'Valsh et aL, 1995). \\Vig- tensile strength in the periodontium of rats after in gins et a!. (1994) described these results in rabbits domethacin treatment. Carlstedt and associate and implied that an acute injured ligament treated (1986a, 1986b) found that indomethacin treatmen with corticosteroid injections may not \\vithstand increased the tensile strength in developing an the mechanical loads of an earl)!, vigorous rehabili- healing plantaris longus tendons in the rabbit an tation. Noyes et a!. (1977b) reported decreased liga- noted that the mechanism for this increase wa ment stiffness, failure load, and energy absorption probably an increased cross-linkage of collagen mol in monkey ligaments after injection of long-acting ecules. These animal studies suggest that short~tern corticosteroids. These findings were tin1e- and administration of NSAlDs would not be deleteriou dosage-dependent. After application of a dosage for tendon healing but instead \\vould increase th that was approximately 10 times an equivalent hu- rate of biomechanical restoration of the tissue. man dose. only! minimal changes were found after 6 \\veeks, but after IS weeks the maximum failure load HEMODIALYSIS (20%), energy absorption prior to failure (11%), and Tendinous failure resulting from chronic renal failur stiffness (11 %) decreased significantly. After does occur, \\vith tendon rupture reaching 36% amon application of a dosage equivalent to the human individuals receiving hemodialysis. Hyperlaxity o dose, the maximum failure load (9%) and the en- tendons and ligaments \\vas found in 74%, patella tendon elongation in 49%, and articular hypermobil absorption (8%) decreased significantly. ity in 51 % of individuals receiving long-term he Campbell ct al. (1996), however, showed that a modialysis (Rillo et a!., 1991). Dialysis-related amy single injection of long-acting corticosteroid does loidosis may cause the deposition of amyloid in th not cause histological differences in rats with acute synovium of tendons. The major constituent of th injured ligaments as compared \\vith rats with acute amyloid fibrils is the beta 2-microglobulin (Morita e ligament injury and no injection of corticosteroids. a!., 1995; Honda et a!., 1990; Bardin et a!., 1985). lv1cchanical testing showed no significant difference in ultimate load or ultimate stress in the two GRAFTS groups. Oxlund et a!. (1980) reports that local injec- tions of corticosteroids every 3 days for 24 days in- Reconstruction of torn ligaments, especially or th crease the tensile strength and maxin1um load stiff~ anterior and posterior cruciate ligament, is now ness of muscle tendons but decrease the strength of frequent procedure. The need for reconstruction the bone attachments of ligaments. related to age, activity level, and associated injurie Laborator).' investigations established the pres- ence of estrogen receptors in hun1an ACLs. Liu et al.

Grafts derived from different individuals of the substantial proportion of elastin. which lends these same species ar~ called allografts; grafts derived structures their great elasticity. from the same individual are called aUlograhs. Allo- grafr tissue preservation is done through freezc- 2 The arrangement of the collagen fibers is drying and low·dose irrndiation to reduce rales of nearly parallel in tendons. equipping them to with- rejection ancl infection and to limit effects on the stand high unidirectional loads_ The less parallel structural properties. Bone-patellar. tendon-bone, arrangement of the collagen fibers in ligaments al~ and Achilles tendon are llsually L1sed as allograft tis- lows these structures to sustain predominant tensile sue, whereas the central tissue of the patellar ten- stresses in one direction and smaller stresses in don is commonly llsed as autograft tisslie. other directions. Shino ct al. (1995) L1sed fresh-frozen allogenic ,;:~~)': At the insertion of ligament and tendon into Achilles, tibialis anterior or posterior. and peroneus stiffer bone. the gradual change from a morc fibrous longus or brevis tendons for ACL reconstruction in [0 a morc bony rnaterial results in a dccreased stress humans. Specimens were procured during second- concentration effect. look anhroscop~'. Several years after reconstruction. the allografts had collagen fibril profiles that did not ~ ~ Tendons and ligaments undergo deformation resemble normal tendon grafts or normal ACL. before failure. ,,\"\"hen the ultimate tensile strength of these structures is surpassed. complete failure DC· Strocchi et al. (1992) L1sed patellar tendons that had curs rapidl~!. and their load~bearing ability is sub~ been autograftcd to reconstn1C[ [onl ACLs. Follow-up stantially decreased. biopsies were performed 6, 12. and 24 months after surgel}'. During this time, the aUlOgraft underwent 5. Studies suggest that during nonllal activity. a considerable changes. and after 24 months the auto- tendon in vivo is subjected [0 less than one fourth of graft had the appearance of normal ligament tissue. its ultimate stress. Strocchi suggested that the patellar tendon autograft '/'~:(: Injul\"\\! mechanisms in a tendon are influenced is a valid functional ACL substitution for patients who desire to perform normal mechanical activity. by\"{he ~lm~unt of force produced by the contraction Corselli el al. (1996) reports thal replacement tis- or the muscle to which the tendon is attached and sue undergoes extensive biological remodeling and incorporation. However. even a fully incorporated the cross-sectional area or the tendon in relation to graft will never duplicate the native ACL but works instead as a check reign that increases the knee that of ilS muscle. function_ Tohayama et al. (1996) stated that the graft elongation at the time of implantation influ- 7 i The biomechanical behavior of ligaments and ences the long-term outcome of ACL rcconstruc· tendons is viscoelastic. or rate·dependent. so thal tions. at least in the canine model. They compared these structures display an increase in strength and those cases where the graft elongation behavior was stiffness with an increased loading rate. within the 95% confidence limit of normal ACL (group 1) with those cases where the graft elonga- S An additional effect of rate dependency is the tion behavior was more than lhe 95(1'0 confidence limit of the normal ACL (group 2). Group 2 had sig- slow deformation, or creep. that occurs when ten- nificantly less inner stiffness of the graft than did dons and ligamcnts are subjected to a constant low group 1. Group 2 showed a significantly increased load over an extended period; stress relaxation takes anteroposterior laxity. but there was no difference place when these structures sustain a constant elon- in ultimate failure load and absorbed energy. gation over time. Summary /{g,/i),:,:,',: A:n;;. inba results in a decline in the mechanical properties of tendons and ligaments, th~1t is, their f~1-~Tendonsand extremity ligaments are composed strength, stiffness, and abilily to withsland defor- largely of collagen, whose mechanical stability gives mation. lhese structures their characteristic strength and flexibility. The ligaments flava of the spine have a 10 Pregnancy, immobilization. diabetes. steroids. NSAlD Lise, and hemodialysis affect the biomechan- ical properties of ligaments and tendons. 11 Allografts and autografts are useful in ligament reconstruction but material propenies do not re- 'turn completel~\" to normal levels. 12) Ligaments and tendons remodel in response to the mechanical demands placed on them_

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Tensile properties during tendon healinl!. between fibril size ;\\Ild llll'chanicO'1 propcrlil's. Proc R So ..lCla Or/hop Scellld. SIIPl'l 153. - Lrmd. 203. 305-321.

Prockop. D.J .. Ii: Guz.man, N...\\. (1977). Collagl.:1l dist.'asi,.'s ;\\ltd Viidik, A., D'lllidscn, C.e.. Oxlund, H. (1982). Fourlh tnlem,l- the bios,\\'lllhcsis of collagen. /-Iosp Prw.:t, Dec, 61-68. tional Congress of Biorhl'oJogy Symposiulll on Mcc.:hHnical Rarnachalldr<\\ll. G.N. (1963). Molecular strllC!lln: of collagen. lilt Rev COllllcet TisslU' Uc.~·, /, 127. Propcnics of Living Tisslles: On fundamental and plll:llOnl- cnological models, SlrllC(llrc and mcch:lJlical properties of Rich, A., Crick, F.H.C. (1961), The molecuhll' structure of col· collagen, elastic and glycosaminoglyc'1I1 complexes. Bio- lagen. J .Hol Bioi, 3. 483. rll/:o!o,~y. 19,437. Vogel. 1·1.e. (I 97i). ~'kcll<:lnh.:al and chl'mic:d properties of nil'· Rillo. D.L. Babini. S.M., B<lsn;lk. A., Wrlincr. E., BaHwclwl1. iOlls conneclive lissue org.tns in rats as iniluenced by non- E.. Cocco. J.:\\. (1991). Tendinous .md Iig:Ulll'lltoliS hyper- sleroidaJ anlirheum:ltic drugs. COI11/l!ct Tisslle! Res. 5, 91. laxity in patients reechoing long-Icrm hemodialysis. J Walsh, W.R., Wiggins. r-,·1.E .. Fadak P.O., Ehrlich, !\\·I.G. Rht'lIl1ullof. /8(8), 1227-1231. (1995). Errc:cts of dd;tyed steroid injection on ligamenl Runc.lgrcn, A. (1974). Physical properties of conncctin: Lissuc healing using a rabbit medial colialen,1 ligament model. BilJllwt..:,-;a!s. 16( I 1), 905-910. as influenced by single and n::pc<I!L.'d pr~gn;\\ncics ill thl.' r;IL .·kltl Pilysiol Scam!, Sl/ppl.. 417. c..Walsh,S .. Fr'lIlk. Shrive. N., Han, D. (1993). Knee immo- Shino, K., Oakt-s, B.W.• I-Ioribe. S.. Nnkaw, K.. Nakamurn. N. biliz;Hion inhibits biolllcchanic<llmatllnHioll of the r:\\bbit (1995). Collagen fibril popuhltions in human ;:Ulterior cru· medinl collateral lig:ll11l:111. Clill Orrhop. 297, 253-261. ciate lig;unent allografts. Electron micfoscopic analysis. \\Vhite, A., H;:lndler, P., & Smith, E.L. (1964). Prillciples o{Bio. A/1/ } Sport.~· Mal, 23(2), 203-208. Simon, S.R. (1994). Orthopedic Basic SciclI\"'~. Rosemont, IL: cI/!:/IIistry. Ncw York: McGraw-Hill. MDS, \\Viggir\\,o;, [VI. E., Fadale, P.O., B<lITach, H., Ehrilich, ,,\"I.G., Snell. R.S. (198-1). Clillicld al/{! FI/Ilctiomd Histology {or ,\\It,d· Walsh. W.R. (1994). Healing ch<lr;tClcrislics of a type I col· icaf SIUt/CIIIS. Boslon: Lillk\" Brown. Iag('1l01lS SlnlClUre treJh:d wilh corticosteroids. .-\\1/1 j Stfocchi, R., Dl' P<lsquale. v., Facchini. ,\\ .. Rnsp,ulli, M .. SPOI\"/S ,\\kd, 22(2), 279-188. Woo, S.L.Y.....\\n, K.N., Arnoczky, D.\\I.\\1.. Fithian, D., & ~ly('rs Zaffagnini, 5 .. ~'larcacci, ~1. t 1996). Agc:·rcbted changes in B. (1994). Anatomy, biology, and biomechanics of the len- human anterior cruciatt: ligament (ACL) collagen fibrils. don, ligaml'nl, ;Iud m..:niscus. In S.R. Simon (Ed.). Or· Ira! ..lWI/ E\",bryui. /01(-1).213-120. rJ/Of/at'die Basic SCit'IICt' (p. 51). Ros\\,'monl. Il: .-\\AOS. Slrocchi, R.. DePasqu:lIL', V.. Guizzardi, S., ~I:lrcacci, M.. Woo, S.L.Y., Gomez, \\-1.,.\\.. Siles, T.J., Cl :11. (1987). Thc bin· Ruggeri. A. (1992). Ultr.\\slructural modificalions of patd- mechanical .llld morphological clwngcs in the Illcdi:d (01- lar tendon fibres lIscd as 'Ulterior cruci.\\te ligament (ACI..) latcr,tl ligamelll of the rabbit after imlT1obilization (lnd rc- repbcclllcnL/uJ! } Allat EII/bryo!, 97(4). 221-228. Tipton, C. =\\<1. , James, S.L., Mcrgner, W., Cl al. (1970). Influ· [T\\obiliz;llion. ) !3lme )0;1// SlIrg, 69..1(8),1200-1211. encc of e-xcn::ise on slrl.:ngth of medial (ollatcralliganH:nls \\Von, S.L.Y., Gomez, M.A., Amid, D., Ritl('r, ~·l.A., Gdbt.'rman, of dogs. Alii) Physio!, 2/8. 894. Tohayama. 1-1 .• Beynnon. B. D.. Johnson, R.J., Renstrom, P.A .. R.I,!.. Akcson, W.H. (1981). The effects of e.\\crcise on the Arms S.W. (1996). The effect of <lnlerior cruciate Jig.lInent biomcchanical and biochemical propcnies of swine digiwl graft c1ong'llion at the lime of implantation on the biollle- flc:.\\or leudons. } B;ol1l~!c.:h Ellg, 103, 51. chanical behavior of the graft and knee. ,.\\/1/ j Sports .\\lcd, Woo. S.L.Y. (1988). Lig;\\mellt, tendon. :HH.l join! capsule in- sertions tu bone. In S.L.Y. Woo, & J. Buckwalter(Eds.), Ill- 24(5),608-614, jllly (II/(/ Repair of th~ ,HlISCU!oskduli So{t Ti...... uc:s (pp. Viidik, A. (1968). EJ<lslicil)' <IIul lensile strenglh of Ihe antl.'· 133-166). Park Ridge. II. :\\meric.w Academy of Or· rior cruci<llc ligament in rabbils :lS influcnced by Iraining. Ihop<:ledi(..· Surgeons. Acta Ph\\'sio! Scallll, 7~, 372. orViidik, A. '(1973). Functional propertics collagenous tis- sues. IlIr Rei' COllllcct Tissue Res, 6. 127.

,,\\', \" ST~UC,;,UR~ ',,'- Nutrition. mct.'lbolism CEL(:FIBROBJ-ST't;\\, ! .~, ~'\\.\\, \\},o' Synthesize Ex(r!:lcclJuI3r Mmix 81 l -\\ \"\" EXTRACEllltLAR .\" -{ -Collagen type J: suPPOrt tensile loads The mcc~anjc is depende -Ground $ubsL.,ncc rate at whic Gel.like matcrialfSt.abilizc arc ap collagenous skclC!ton 'El:min pS;.;~\"NEUAAl Nm:ORK' '~\\, , :.~\\:' ,- M~chjlnoreccp[ors ·Proprioception ·Sensorimotor Mechanism '- ',;:'-c:, FLOW CHA~T 4-1 Common structure and mechanical properties of t *This flow chart is designed for classroom Of group di~cussion. Flow chart is not mean

;;' ,~ cal response STRONG AND FlEXIBlES, ent on the ch thl! loads Resistance of pplied high tensile forces with limited elongation ,,;,,' ; tendons and ligaments. * ~: nt to be exhaustive. f R R \" .. ..• ••\"\"......\"\"\"\"...~.~.\"\" ,~,.\"\"\"\".~~ \"\"\",,,,,,,,,,,,,,,,,,'\",,\"_~,_,,~,,,,.,,-\"\",\",,,,,,,,,,,~,_,,,,,!.'<=J

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I' 'r.\" l,: The Cell andfo 1? tI' '{ ;, i{ ~: :{I ~'\"I j -Thermal injuries 'Inherit injuries 'Corticosleroids 'Endocrinologic and metabolic discases: diabetes -Rheumatoid arthritis ),I! -Congenital diseases 'Inf~ctions \\)i , :l\")1; ,if FLOW CHART 4·3 Tendon injuries. Clinical examples. * \"This flow chart is designed fOf cla5sroom Of group discussion. Flow chart is not mean '/01

or eXlracel1ubr matrix components Mechanical Caused InjurJes Injuries in association with local strain type and/or level of stress t +-Stre5s Str:lin J l ) lMicrotr.lumJS that ... _._- J exceed the reparative procc5S t Stress Tendon 'Gun injurie5 'Paratcnonilis ·L1cer3.tions 'Bone fr.lCIUre5 ·Tcndinosis 'Colli5iol1s -Tendinitis ' Tendon's Jtuchment ~ 'ApophY5it is -EnthcsopJtics RUPTURE TOlal/PJrti;a1 nt to be exhaustive. . .\". ._. -'--~---'-'-=-- '\"

Structure FLOW CHART 4·4 Ligaments structure and mechanical properties.* (P ~This flow chart is designed for classroom or group discussion. Flow chart is not mean

Function ViSCOElASTIC. MECHANICAC PROPERTY PG, Proteoglycan) nt to be exhaustive.

.:; The Cell and *1 Injurics in a~sociation with diseases ),~ 'Iatrogenic Injuries: Corticosteroids i: ·Endocrinologic ;lOd ~i! metJbolic diseases: ;J Diabetes Mellitus I 'FLOW CHART 4·5 Ligament failure. Clinical examples.'\" '\"I'.t.,. -This flow chart is designed for classroom or group discussion. Flow chart is not mea I '1 I

d/or cxtracellular matrix componcnts Injuries in association with local strain type and/or Icvel of stress Dccre.lsc in mechanical t Sinin r.ltC t Amount of load per properties Microtraumas that unit area +- -+Stress Strain exceed the reparative t Stress process 'Bone fnlCtureS 'Collisions -Gun injuries -l~cerations RUPTURE Tot~I/PJrtial ant to be exhaustive.

Biomechanics of Peripheral Nerves and Spinal Nerve Roots Bjorn Rydevik, Goran Lundborg, Kje/l O/marker. Robert R Myers Introduction Anatomy and Physiology of Peripheral Nerves The Nerve Fibers: Structure and Function Intraneural Connective Tissue oi Peripheral Nerves The Microvascular System of Peripheral Nerves Anatomy and Physiology of Spinal Nerve Roots Microscopic Anatomy of Spinal Nerve Roots Membranous Coverings of Spinal Nerve ROOlS The Microvascular System of Spinal Nerve Roots Biomechanical Behavior of Peripheral Nerves Stretching (Tensile) Injuries of Peripheral Nerves Compression Injuries of Peripheral Nerves Critical Pressure levels Mode of Pressure Application Mechanical Aspects of Nerve Compression Duration of Pressure Versus Pressure level Biomechanical Behavior of Spinal Nerve Roots Experimental Compression of Spinal Nerve Roots Onset Rate of Compression Multiple levels 01 Spinal Nerve Root Compression Chronic Nerve Root Compression in Experimental Models Summary References Flow Charts • _ -._~.. ..._-~

Introduction pression. In this chapter, the basic microanatomy the peripheral nentes and the spinal nCIYC roots The nervouS s)'stcm scn'cs as the bod.:,/s control cen- revicwed \\vith special reference to thesc buil ter and communications nct\\vork. As slIch, it has mechanisms of protection. The mechanical behav three broad roles: it senses changes in the bod)! and of peripheral nen'es that are subjected to tension in the external environment, it interprets these compression is also described in some detail. changes, and it responds to this interpretation b)· initiating action in the form of muscle contraction Anatomy and Physiology of or gland secretion. Peripheral Nerves For descriptive purposes, the nen'OllS s)'stem can be divided into two parts: the central nervous sys- The peripheral nervcs are complcx composite str tem, consisting of the brain and spinal cord, and the tures consisting of nen'e fibers, connective tiss peripheral nervous system, composed of the various and blood vessels. Because the three tissue cleme that make up these nen'es react to trauma in dif processes that extend from the brain and ent ways and may each pia)' distinct roles in spinal corel. These peripheral nerve processes pro- functional deterioration of the nerve after inju each element is described separatel)'. input to the central nervous system from sen- receptors in skin, joints, muscles, tendons, vis- THE NERVE FIBERS: STRUCTURE AND cera, and sense organs and provide output from it to FUNCTION effectors (muscles and glands). The peripheral ner- vous system includes 12 pairs of cranial nen'es and The term nerve fiber refers to the elongated pn)c branches and 31 pairs of spinal nerves and (axon) extending from the nerve cell bod)' along w their branches (Fig. 5- lil). These branches arc its myelin sheath and Schwann cells (Figs. 5~2 called peripheral nerveS. 5-3). The nerve fibers of sensory neurons cond Each spinal nerve is connected to the spinal cord impulses frolll the skin, skeletal I11uscles, and jo to the central nervous svstem. The nerve fibers of a posterior (dorsal) root and an anterior motor neurons conve)' impulses from the cen root, which unite to form the spinal nerve nen'ous system to the skeletal muscles, causing m intervertebral foramen (Fig. 5-1, B-D). The cle contraction. (A detailed description of the noste,ric)r roots contain fibers of sensory' neurons chanics of muscle contraction is given in Chapter conducting sensory information from recep- in the skin, muscles, tendons, and joints to the The nen'e fibers not only transmit impulses celHr.al nervous system) and the anterior roots con~ also sen'e as an anatomical connection between mainly fibers of motor neurons (those that con- nerve cell body' and its end organs. This connect impulses from the central nen'ous system to is maintained by axonal transport systems, thro targets such as muscle fibers). which various substances synthesized within Sh,ortlv after the spinal nerves leave their inter- cell body (e.g., proteins) are transported from cell body to the periphel)' and in the opposite di foramina, they divide into two main tion. The axonal transport takes place at speeds t the dorsal rami, which innervate the mus- Vat)' from approxilnatcly 1 to approximatel)\" and skin of the head, neck, and back. and the mm per day. generally.' larger and more important ventral rami, innervate the ventral and lateral parts of Most aXO!lS of the peripheral nervous system structures as well as the upper and lower ex~ surrounded by multilayered, segmented coveri ,,.,'m;t;,>< Except in the thoracic region, the ventral known as myelin sheaths (Fig. 5-3). Fibers with do not run directly to the structures that they' covering are said to be myelinated, whereas th innervate but first form interlacing networks, or without it (mainly small sensol)' fibers conduct with adjacent nen·'es (Fig. 5-1A). impulses for pain from the skin) are unmyelina This chapter focuses on both the peripheral nerves The myelin sheath of the axons of the periph spinal nerve roots, which cOlltain not only nerve nerves is produced b).' flattened cells called Schw fibers but also connective tissue elements and vascu- cells arranged along the axon (Fig. 5-3). A sheat lar structures that encompass the nerve fibers. The formed as the Schwann cell encircles the axon possess some special anatomical properties that may sen/e to protect the nente from mechanical damage, for instance, stretching (tension) and com-

Vertebral Ventral Intervertebral body foramen Cl-::>\"_--., C2 C3 C4 Cervical nerves Vertebral B arch Dorsal Ventral Thoracic nerves Lumbar Cauda Spinal nerve plexus equina A ~~ ~~ MOlor _ -->\"\",,--,-,'00' I---~' ~Dorsal root -~- ganglion Sensory Coccygeal rOOI nerve o A, Schematic drawing of the spinal cord and the spinal is depicted. Adapted from rorrord, GJ & Anllgnostako5. N.fl. nerves (posterior view). The spinal nerves emerge from the (J 984). Principles oj Anatomy and PhySiology (.1lh ed.J. New York: spinal canal through the intervertebral foramina. There are 8 Harper & Row. B, Cross-section of the cervi<al spine showing pairs of cervi<al nerves, 12 pairs of thoracic nerves,S pairs of the spinal cord in the spinal canal and the nerve roots exiting lumbar nerves, 5 pairs of sacral nerves, and 1 pair of coc- through the intervertebral foramina. C, Cross-section of the cygeal nerves. Except in the region of the 2nd to the 11 th lumbar spine shOWing the nerve roots of the cauda equina in thoraci< vertebrae (T2-T11), the nerves form complex net- the spinal canal. 0, Each exiting nerve root complex in the in- works called plexuses after exiting the intervertebral forClm- tervertebral foramen consists of a motor root, a sensory root, ina. Only the main branch of each nerve, the ventral ramus, and a dorsal root ganglion. • \\vinds around it many times, pushing its cytoplasm unmyelinated nerve fibers in a slow, continuous way, and nucleus to the outside layer. Unmyelinated gaps whereas in the myelinaled nerve fibers the impulses called nodes of Ranvier lie between the segments of \"jump\" al a higher speed from one node of Ranvicr the myelin sheath at approximately I to 2 I11Ill apart. to the next in a process called saltatOl)\" conduction. The conduction velocity of a myelinated nerve is di- The myelin sheath increases the speed of the con- rectly proportional to the diameter of the fiber, duction of nerve impulses, and insulates and main- which lIsually ranges [Tom 2 La 20 J-l111. MOlar f-ibers tains the aXOIl. Impulses arc propagated along the -. f:

innervate skeletal muscle have large diameters, tive tissue la)rers is essential becausc nerve flbcrs do sensor~y' fibers that relay impulses associated extremely susceptible to stretching and comp sion. touch, pressure, heat, cold, and kinesthetic such as skeletal muscle tension and joint po- The outcnTlOst layer, the epineurium, is loc Sensory fibers that conduct impulses for dull, between the fascicles and superficially in the ne diffuse pain (as opposed to sharp, immediate pain) This rather loose connective tissue layer serves the smallest diameters. Nerve fibers are packed cushion during movements of the nel\\'e, protec closely in fascicles, \\vhieh are further arranged into the fascicles from external trauma and maintain bUIl1(II·es that make lip the nen'c itself. The fascicles the oxygen supply sy'stem via the epineural bl arc the functional subunits of the nCI-ve. vessels. The amount of epineural connective ti varies among nerves and at different levels wi INTRANEURAL CONNECTIVE TISSUE OF the same nerve. \\!Vhere the nerves lie close to b PERIPHERAL NERVES or pass joints, the epineurium is often more ab c1ant than e1scwhere, as the need for protection Successive layers of connective tissue surround the be greater in these locations. The spinal nerve r nerve fibers-called the endoneurium, perineuriUl11, are devoid of both epineuriurn and perincuri ,'mel epineurium-and protect the fibers' continuity and the ncrvc fibcrs in the nel\\'e root may therc (Fig. SA). The protective function of these connec- bc morc susceptible to trauma (Rydevik et aI., 19 Sensory nerve root The perineurium is a lamellar sheath that compasses each fascicle. This sheath has great Sensory cell Motor cell body chanical strength as well as a specific biochem body in dorsal in anterior horn barrier. Its strength is demonstrated by the fact rool ganglion of spinal cord the fascicles can be inflated by fluid to a pressur approximately! 1000 mm of mercury (I-Ig) beFore ! Dorsal perineuI'ium ruptuI·es. Spinal nerve \\ The barrier function or the perineurium che cally isolates the l1el\\'e fibers From their surrou \\\\ ings, thus preserving an ionic environment of th terior of the fascicles, a special milieu interieur. Dorsal ./ endoneurium, the connective tissuc inside the f ramus / cles, is composed principally of fibroblasts and lagen. Peripheral nerve ... '- Ventral Motor nerve rool The interstitial tissue pressure in the fasci the endoneurial fluid pressure, is normally slig I nerve elevated (+ 1.5 ± 0.7 mm Hg [Myers & Pow 1981]) comparecl \\\\'ith the pressure in surround ~1 '----fi-ber ------ tissues sLIch as subcutaneous tissue (-4.7 ± 0.8 Schematic representation of the arrangement of a typical Hg) and muscle tissue (~2 ± 2 mm Hg). The elev spinal nerve as it emerges from its dorsal and ventral nerve endoneurial fluid pressure is illustrated by the roots. The peripheral nerve begins after the dorsal ramus nomenon whereby' incision of the perineurium branches off. (For the sake of simplicity, the nerve is not sults in herniation of nerve fibers. The endoneu shown entering a plexus.) Spinal nerves and most periph- fluid pressure may increase further as a resu eral nerves are mixed nerves: they contain both sensory trauma to the nerve, with subsequent edema. S (afferent) and motor (efferent) nerve fibers. The cell body a pressure increase ma.y affect the microcircula and its nerve fibers make up the neuron. The cell bodies of and the function of the nerve. the motor neurons are located in the anterior horn of the spinal cord, and those of the sensory neurons are found in THE MICROVASCULAR SYSTEM OF the dorsal root ganglia. Here, a motor nerve fiber is shown PERIPHERAL NERVES innervating muscle and a sensory nerve fiber is depicted innervating skin. Adapted from Rydevik, B., Brown, MD., & The peripheral nerve is a well-vascularized struc Lundborg, G. (/98·4). Pathoanatomy and pathophysiology of containing vascular networks in the epineurium nerve root compression. Spine, 9, 7. perineurium, and the endoneurium. Because inlpulse propagation and axonal transport dep ? .... ..,':;.-

Node of Ranvier Schwann cell \\Myelin sheath \\ Axon Node of Ranvier Schematic drawings of the structural features of a myelinated nerve fiber. Ad(1fJted from Sunderland 5. 0978j. Nerves and Nerve Injuries (2nd ed.). Edinburgh: Churchill Livings/one. • on a local oxygen supply, it is natural that the Epineurium microvascular system has a large reserve capacity. Perineurium The blood supply to the peripheral nerve as a Endoneurium whole is provided by large vessels that approach the nCl\\'C segmentally along its course. \\,Vhen these lo- Schematic drawing of a segment of a peripheral nerve. cal nutrient vessels reach the nerve, they divide into The individual nerve fibers are located within the en· ascending and descending branches. These vessels doneurium. They are closely packed in fascicles, each of run longitudinally and frequently anastomose with which is surrounded by a strong sheath, the perineurium. the vessels in the perineurium and endoncuriul11. A bundle of fascicles is embedded in a loose connective tis- Within the epineurium, large arterioles and venules. sue, the epineurium. Blood vessels are present in all layer 50 to 100 fl-l11 in dial11etel~ constitute a longitudinal vascular system (Fig. SA). of the nerve. A, arterioles (shaded); V. venules (unshaded). \\Vithin each fascicle lies a longitudinally oriented The arrows indicated the direction of blood flow. Adapted capillary plexus with loop formations at various lev- from Dahlin, L.B., Rydevik, B., & Lundborg, G. (1986). The cis. The capillary system is Fed by arterioles 25 to parhophysiology of nerve entrapments and nerve compression 150 fLrn in diameter that penetrate the perineurial injuries. In A.R. Hargens (Ed.). Effects of lv1echanical Stress on membrane. These vessels run an oblique course Tissue Viability. New York: Springer-Verlag. through the perineurium, and it is believed that be- cause of this structural peculiarity, they arc easily • closed like valves in the event that tissuc prcssurc inside the fascicles increases (Lundborg, 1975; Myers et aI., 1986). This phenomenon may explain why even a limited increase in endoncurial fluid pressure is associated with a reduction in intrafas- cicular blood flow. The built-in safety system of longitudinal anasto- moses provides a wide margin of safety if the re- gional segmental vessels arc transectcd. In an ex-

peri mental animal in vivo model, it is extremely dif- \"swdling\" of the most caudal part of the respective ficuh to induce complete ischemia to a nerve by 10- dorsal neryc root, called the dorsal rOOl ganglion. The dorsal root ganglia arc locatcd in or close to the surgical procedures. For example, if the whole intervertebral Foramen. Unlike the nCn!c roots, the sciatic··til.\"'1i nerve complex of a rabbit (15 em long) is surgically Sepal\"aled from its surrounding struc- dorsal root ganglia arc not enclosed by cercw tures and the region\"11 nutrient vessels arc ClIt. there brospinal fluid and the meninges. Instead. they are is no detectable reduction in the intrafascicular enclosed by both a multilayc:rcd connective tissue blood flow as studied by intravital microscopic tcch· sheath, similar lo the perineurium of the peripheral Y\"iGucs. Even if such a mobilized nerve is ellt distally or proximall~'. the intraneural longiwdinal vascular 2 4 systems cnn maintain the microcirculation at least 7 l~ 8 ern rTom the clil end. If a non mobilized nerve is 3 .. 2 0\"'.,'\" cut, there is still perfect microcirculation even at the 3 vcr\")' tip of the nerve; this phenomenon demon- strates the sufficiency of the intraneural vascular collalcrals. Howevcr~ othcr sllldies in rats indicate .that stripping the epineural circulation rronl nerve bundles causes demyelination of subpel'ineural nerve fibers. Anatomy and Physiology of Spinal Nerve Roots ~ In the earl~' embryological developmental stages, 7 t the spinal cord has the same length as the spinal column. However, in the full~: grown individual, the 8 I spinal cord ends as the COIlUS mcdullaris, approxi- 5 mately at the level of the fit'st lumbar vertebra. A I nerve root that leaves the spinal canal through an 6 intervertebral foramen in lhe lumbar or sacral spine f therefore has to pass from the point where it leaves The intraspinal nervous structures as seen from behind. the spinal corel. which is in the lower thoracic spine. The vertebral arches are removed by cutting the pedicles ! lO the point of exit li'om the spine (Fig. 5-5). Be- (1). A ventral (2) and a dorsal (3) nerve root leave the cause the spinal cord is not present be.low the first spinal cord as small rootlets (4). Before leaving the spinal lumbar vertebra, dte nervous content of the spinal canal, the dorsal root forms a swelling called the dorsal canal is only comprised of the lumbosacral nerve root ganglion (5), which contains the sensory cell bodies. roots. This \"bundle\" of nerve roots within the IUI11- before forming the spinal nerve (6) together with the bar and sacral pan of the spinal canal has been sug- ventral nerve root. The nerve roots are covered by a cen· gested to resemble the tail of a horse and is therefore tral dural sac (7) or with extensions of this sac called often called the cauda equina, that is, lail of horse. nerve root sleeves (B). ReprodtlCec/ with permission ;,om Two different lypes of nerve roots are (\"ound O/marker. K. (J 99/ J. Spinal nerve rOOI compression. ACt/Ie within the lumbosacral spine, ventral/motor roots and dorsal/sensory roots. The cell bodies of (he mo- compression of the cauda equina sludied in pigs. Acta Orthop tor axons are located in the anterior horns of the Scand. 62. Suppf 242. gray malleI' in the spinal cord, and because these nerve roots leave the spinal cord from the ventral as- • pect, they are also called ventral roots. The other type of nelVC root is the SenSOl)', or dorsal root: As the name suggests, these nerve roots mainly COll1 w prise sensory (Le., afferent) axons and reach lhe spinal cord at the dorsal region of the spinal cord. The cell bodies of the sensory axons are located in a