Repair of Knee Ligaments in Dogs

Repair of Knee Ligaments in Dogs I. THE LATER.i L (1orL1 m Emt.u L LIGAMENT BY DON H. O DONOGHUE, M.D., CAPTAIN CHARLES A. ROCKWOOD, JR., Aledical Corps. United Stales.4ir Force, BASILIUS ZARICZNYJ, M.D., AND REX KENYON, M.D., OKLAHOMA CITY, OKLAHOMA Extensive clinical expen ienncc inn the treatment of imnjuries of the ligamemnts (If time knee inn unarm indicates that sum-gical repair of a completely torrn ligament. n ill, inn the majority of cases, resuilt inn nnone certain recovery with less disability than n ill non-surgical tm-eatnmmennt. We arc satisfied from our clinical experience that m-ecovery is more complete arid mmiore rapid after surgical treatment and that good resuilts an-c augmennted by, arid largely depemidemit on, early suirgery. In ounr experiemmce early suirgical repair has given consistently better resunits. However, we have i)eemi umnable amid umnnvillinng to carry ount a controlled study of paired cases tn-eat.ed with amid ivithout open sun-gical n-epair- inn the hunnamn being. Most of our patients have accepted ounr r-e(-omnnienndationl for- surgical repair amid have been able to tolerate it.. The patients we treated late connfinmncd oum- opiniiomn, since the results ol)tainned did riot equal those inn patients with fresh injuries. When this innvestigationn mn as initiated, the only article w e could find that seemed to I)ean specifically on the problcni of ligamnenntouis repair was that by Jack. Honvever, aftem- our experimiicnnts mn ere under way sinnilar m on-k was reported by Clayton annd Wcir. The pum-pose (If our exper-immmemntal project m as to answer the questions : (1) How do higaninemits m-epaim-? (2) What circumstances are most favorable fom tine pn-ocess of repair-? ani(1 (3) Ilow do these cir(-umninstani(-es affect the cornplet.eniess of tine n-epair? Tinis neport. concerns only tine lateral collateral ligament.. The niedial collat.er-al annd l)osteri(in liganmnenits (If tine knee differ froin tine lateral collateral ligammnemmt inn that they am-c riot discn-etc stn-imctures anmd are less accessible to surgical approach. Like (1laytorn ani(1 \Veir, we n em-e ulnnai)le to pn(ichtnce (-onimparable injuries (If the krnee ligainmcnnts suit.ai)le for- controlled stundy by tearing tine ligaminennts. For punrposes of conipar-isonn, uniifom-nnn innjurics were needed annd we counld only produlce these by actually cutting the ligaments. EXPERIMENTAL STUDY Sixty-four dogs were utilized inn this part of the project. They were divided into six groups. Each group received different tm-eatment, as indicated inn Table I. Inn Groups I, II, III, amid IV-with twelve dogs inn each grounp-tnvo dogs ivere sacrificed at onne, two, four, six, eight, amid ten weeks after operationn, respectively. lin Group V-severn dogs-onne was was sacrificed at six weeks arid two at eight, tern, and twelve weeks, respectively. Inn Group VI-nninne annimals-inne * Read at the Combined Meetiong of tine Orthopaedic Research Society annd Tine American Academy of Orthopaedic Surgeons, Miami Beach, Florida, January 8, 1961. t This project was jointly sponsored by the Nationmai Inistitimtes of Ilealtin Grant No. A-2789. the Orthopaodic Research and Education Foundation, anmd the University of Oklahoma Medical School. The contents of this article are tine personnal views of the Air Force author and are not to he construed as statememnts of oflicial Air Force policy. The aninial experiments in this project were conducted according to tine rules regarding animal care as established by the University of Oklahoma Medical Center :m,md the American Medical Association. VOL. 43-A. NO. 8, DECEMBER i961 1167

0.- 4 1168 D. H. O DONOGHITE, C. A. ROCK WOOD, JR., B. ZARICZNYJ, AND R. KENYOX TABLE I Lxm EBIMENTAL DATA (IX SIxTY-FouR 1)oGs ( ;roonp No. 1xpo rininental ( ategorv I)ogs Useml No. of I Transection of the lateral collateral liganuenit : no rm pair of liganinent ; 12 no immobilization; gross and microscopic stindy II Transection of the lateral collateral ligament : mo repair of iigannm nnt : I 2 leg inmnmobilized an l)laster cast: gross and microscolmic stu(lv III Transection of the lateral collateral ligamernt ; repair of ligarnnmnot : log I 2 inmnniobi1ized in l)laster cast ; gross amod mnicroscopic stmn(iy IV Transection of the lateral collateral ligament througim onne-ioalf of its 12 \vi(lth; leg innnnobilized un plaster cast; gross anmd nucroscopic stimdy V Transection of the lateral collateral ligament; no repair of liganmnemmt; 7 leg imnnobilized in plaster cast; tests of comparative stro ngth of the healing and normal liganmwnts at intervals after section VI Transection of time lateral collateral liganmnent; repair of liganmenit ; leg P immobilized in plaster cast ; tests of comparative streingth of the repaired and nnornnial ligarnnents at inmtervals after section animal was Sacrificed at four weeks amid two at six, eight, temi, amid twelve weeks, respectively. Xonne of the ligaments fn-om dogs sacrificed at four vceks amid only omne ligament from a dog sacrificed at six weeks were studied nnicmos(o)pieally l)ecause only the ligaments from the dogs surviving fom- mon-c than six w ceks after section showed appreciai)le evidence of solid union of the divided ligament. In all save Group I, the legs nver-e irnnn(ii)ilized in plaster casts which nn cme worn until the time of sacrifice. As the lateral collateral ligamcmit alone as severed, and the remainninmg st.i-uctures on the lateral side of the kmiee joint were left intact, instability n as riot marked even at the time of open-ation. At the time of sacrifice, the lateral collateral ligamcmnt was examined grossly and careful note was made of the amount of scari-inng amid inflammatiorn amid the...-.,,,,.,.,,;:, I Fic. 1 (ross specinnen of a fernnmnr anmd tibia with attachemi nominal laten al colhmten:ml lig:inno nmt shou inig:.4, the femur; B, time tibiofibular unmit : ammo! C, tine laten al collateral liganmenot. THE JOURNAL OF BONE AND JOINT SURGERY

Rn;p1nt OF KN11 TA(.\\lnX n S IN DOGS 11 () V()L. 43-A, NO. 8, n)em F:\nrmn:nm i mmn 1 nm;.2-a 1 a;. 2-B Fno;. 2-C Jig. 2-. :.l)l):tr:mt mis mnsmmi to to st t lie tenisi Ic st n onigt 11 0)! time lateral m ollaten al ligamnnenmt. \\(ights a mm :tmimlem1 to t he p:li I, \Vl)im lm is mmsl)enimle(l ln onmi time lmm)o)k mini t lie slimling sb-eve to nvimich t lie Ii I )IOiii )nnla r monni)lex is I bit ( (1. Fhe I mnnes :u e si nlnimlate(i I r Ilieces 0)1 \vm)m)(1. 1 ig. 2-13 : I )iagr:innn of sjxinnenm iinounited on t he apparatus to test t lme temmsile strenigt in omf t inc fihmnlar mullateral ligannent. I ho fernntmr is flxm1, ilolted to the upright. Time tii)iofibular m onmmplex is nmmm)v:i Imb, bolted t 0) t Ime slim hug sleo vo ( hit ). \\ eight. is susj )enldem! fronmn t lie imoo)k on t 1mm S1( (Ve. Noto I hat t lie long axes of the fennmur:ml anmmi tii)iohbular unmits are nnainitainied l)arallel as force is :Ll)1)liool. 1 ig. 2-( : I Ii:igranrn siiovinmg time notation of the fmnnmor al armd tihiofibinlar units, vhicin o( m nnrs if t imese mlonnnonnt a ne smism)mnmm1cm1 a s simo)vnm. I m roe :ij )lied i ni t his va ( atls(m 1 t inc ligammienit to) It d ol f the borne. (legr-ee (If n-estonat ion of monitiniimitv. F1ie ligannnenits t hat vene studied nnni-ros-opi- (-all\ ven-e nesected fr-ominthe feror-al conl(lvle ttnn(1fr-omn tine Iiea(l of the fibula arid frxed inn I 0 per- cent fon-nialinn. Flne specinnicnis ene identified } nnummini)en- only to cnisimne mmniiliaseol stmndv by a I3oIam-(1-(ertifie(I patholo)gist (1. Ii.). \\imeni the strenngt.li of tine ligament was to be teste(l, the knee joint was (ussecte(l free (If all ligaments ex(ei)t tine lateral collateral ligament, whicin was left attat-ineti t o foir n-inncin segminennts m)1 t Inc distal l)ant (If t inc femnum n ani(l impper l)ant of the fihula arid I il)iin(i ig. I). Flne ternsile stremngtln of tine ligannienits was tested to failure by the apparatus shm)wnn inn Figure 2-.. 1]ne fermium vas fixe(l rigidly to the a)pamatils by t\v(i l)anitllel i)oilts, ivlnemeas tine til)im)fil)mmlar- unit \\as fixed by t\\mi simiiilan ilolts vhi-in ivere sectmm-etlto a sliding sjeee. as sinovni inn Figure 2-B. LmIads were ap)lied by pla(-inng nnnetal veigiits in to-pounnd inn(r cnnmo nnts inn tine 1)tnil at mij)pn olxinmiatcly thr-ee-seconnol intervals. F1iis devim-e ivas usemi to keep tine,jm)inlt surfaces l)arallel (luring test inig sini(-c,v1neni anngulat ion \vas allovcol to take place, the ligannncnit.tended to) peel off at its 055(OU5 Ill ta(lininenit to) tine fillmnla on! o-nnnnmn (Fig. 2-C). x. i onv.ni) OPr11A I mvr PrtOcF:DUmtF: line collateral arid crimciate ligannienits arid t iie nnnennisci inn the knee miirnt (If the (log tine essenitially tine sannne as in nnnani. i lne lat(-ral (-ollatemal ligamnienit att.a(-lies proximally to tine later-al fenniom-al eonmdyle, spans tine joint sligintly postemion to tine mnni(1-lirne (If the later-al aspect (If tine joint. ammo! attamhes dire-tly to the head (If tine

1170 D. H. O DONOGHUE, C. A. ROCKWOOD, JR., B. ZARICZNYJ, AND R. KENYON fibula. The ligament is covered superficially by a layer of loose areolar tissue which forms ann incomplete sheath. At operation this sheath was observed to be very vascular; it appears to supply the main blood supply to the ligament amid. therefore, should be protected. It was demonstrated by Jack that at the time of rumpture, the torrn ends of the ligannemnt retract and direct contact between the emnds is not restored because, when the torrn ends are separated momenntan-ily at the time of rupture, they are enveloped by the loose areolar sheath amid tinem-eby prevemntcd from re-establishing contact with each other. Inn our experiments the dogs w ere anesthetized w ith imntraveniouts nerni)irtal in a dosage sufficient to provide from one to onne amid a half hounrs of anesthesia. Using aseptic technniquic, w e made a three-inch incision through the skim arid fascia overlying the lateral collateral ligament which was readily palpable through the skin. When the ligament, coven-ed by its areolar sheath, was exposed, a small hemostat was inserted beneath it arid it was severed with a knife blade. The location and direction of the imicisiomi inn the ligament was the sanne in all animals. When the ligament was repaired every effort was made to minimize the surgical trauma. The delicate instruments used in plastic surgery were employed, including very small round needles. Three sutures of 000 black silk approximated the cut ends of the tendon very nicely, even though these had separated appn-eciably immediately after sectionn. In all the animals the wounds were closed with 000 chromic catguit sutures inn the fascial layer and a running suture of 34-gauge stainless-steel nn ire inn the skin. Inn the experiments in w hich the limbs were immobilized, a small Steinimannn pimi was drilled transversely throungh the femur thn-ee inches pn-oximnal to the joint. line; a similar pin parallel to this was passed through the tibia three inches distal to the joint line. A plaster cast padded with sheet wadding was them applied to the leg, incorporating the pins inn the plaster. It was found to be practically impossible to obtain rigid fixatiomn of the dog s knee joint w itliout the use of these pins. A well molded cast w as applied with the knee in slight flcxion and exten(led as high as possible on the thigh arid distally to inn(-lulde pan-t of the foot.. We had previously found that when w e opem-ated on hotin hind legs, tine (logs were not active after operation arid they sickened annd refimsed to eat. On the corntrary, when only one leg n as operated on, the dogs nven-e ver-y active, walking on three legs as soomn as the anesthetic nn or-e off. After one on- two days the dogs were walking on all four legs. Each dog was given 250 niiilligrannns of a(-hn-omnny(-inn orally each day for severn days. Each dog was checked daily for evidence of infectiolmi and signs of the cast being chewed off. In one dog the operative woumnid becamne innfected but the wound healed well with antibiotic therapy. Onne-third of the casts had to be reinforced, but this did riot significantly vary the fixation. RESULTS Group I: Transection of the Lateral Collateral Ligament mit/moot Iniiinobiliza,tion or Repair (Twelve Dogs) These knees showed some loosemness of the ligament on gn-oss inspection at four weeks (two dogs) and in one of two dogs at six weeks after- opem-ationi. Edema, injection, amid local swelling at the site of the incision were rioted at onne arid two weeks after operation (four dogs). A lan-ge announit of irregulan scarrinng n as found inn the region of the severed ligamemnt in all twelve animals of this group, even at * In the dog there is a thin, superficial lateral collateral ligament which arises from tine lateral knnee-joint sesamoid, located just posterior to the lateral condyle of the fenniur, and attaches to the head of the fibimla and to the proxnmal part of the tibia just anterior and medial to the head of the fibula. n nme JO1 IONAL OF BONE ANI) JOINT S1 nt(;eioy

REPAIR OF KNEE LIGAMENTS IN DOGS 1171 Gross specimen of a dog s knee ten weeks after section of the lateral collateral ligament without suhsequemnt repair or imnnobilization. Note the irregular mass of scar, C, on the lateral side of the knee, extenoling between the tihiofihmnl:ir unmit, B, and the fenmrr,.1. No part of the ligament can he identified. v.;; ----::7-; p, * I.,.., - t kf).,.. - 4 *,,,. 0- _:, : : *,, t #{149} -#{149}#{149},..,.& % : 4 V 9 41.....,..,...., m,,,,p I.#{149} -4:.#{149} Ad.*, -. S #{149} 4, : r,... :, :.-, ta,, #{149} s4:i.., t 4#{176}s : #{163} t2 t S : -... FIG. 4 Group I. Active fibroblastic proliferation and only nninimum amounts of collagenization are seen at eight weeks ( X 430). tern weeks after opem atiomi (Fig. 3). This mass of scam- involved the entire lateral side of the knee joint. It was impossil)le to identify any struncture that resembled a nnornnal ligament inn amy of the dogs inn this group. At eight amid ten weeks, the scam became more demise but othervise did not change inn appearance. Micm-oscopically, at one amid two weeks (four animals) the ligaments showed necrosis amid infiltration with inflannmatory cells iii the area of the severed crnds. Many of the cells were polymorphonuclear leukocytes; others, immature fibroblasts and undifferentiated cells. There was a minimum amount of fibroblastic pm-olifei-at.ion arid the fibroblasts were youmig with swollen nuclei. From founr weeks to tern weeks (eight animals) then-c was evidence of further fibm-oblastic proliferation but vcny little, if any, collagenizatiorn. The fibroblasts ns en-e vcmy imregumlar in size arid shape and showed rio evidence of l)cing oriented along lines of stress (Fig. 4). None of these scars showed any n-cal collagenizationi or true ligament formation. VOL. 43-A, NO). 8, DECEMBER 1961

1172 D. H. O DONOGHUE, C. A. ROCKWOOD, JR., B. ZARICZNYJ, AND B. KENYON FIG. 5 Group II. Disordered arrangement of the fibroblasts at six weeks. Only scattered areas show true collagenization (X 430). FIG. 6 Fir. 7 Fig. 6: Gross specimens of the left and right knees six weeks after sectiomm and repair o)f the right fibinlar collateral ligament. with subsequent irnrnoi)ilizatiomn in a plaster cast for six weeks. Connpare the healed sutured ligament in R with the normal in L. Note that the suttni ed ligament is retdily identifiable as a discrete structure with orderly dis1)ositiofl of the sear. Fig. 7 : Gross specimen of a knmee ten weeks after section of the Posterior half of the fibular collater:il ligamnncnt without subsequent rel)ai n or immoi)i lization. The ligament, C, extending i)et weemn the tibiofibmnlar unit, B, and the fennur, A, appears to be o ssenntially mmornial, vitin univ a umininiuni i)ulge at the site of partial section. ( roup II: Transection of the Latei al ( ollatei al Lif/U1/l( flt (1FU1 Jiiiiiiobilization bj Cast (tfl(/ ASteinmann Pins, without Svrgieal Repair Again looseness amid reduinidanicy of the ligannemnt \\ ene noted nnp to four weeks (six anninnals). Then-c was clennonistn-ahlv less scan-n-inmg than inn the animals in Group T, bitt. lien-c also) it n as impossible to) identify the fomnnatiomn of any nionmal liganiienit.. r#{231} nnonmmially sniiall collateral ligannienit was lost inn time nmiass of semon that cxtended tinr-ougliouit. the emntin-e area. ii\iicnoiscoi)ioal1y, one to) l onmn \\ eeks after oper ationn (loam aniirmnals) these ligannncmnts showed polynnion-phonmuicleam imnfiltiationn amnd niecn osis. At six veeks (twml animals) proliferation of large nnimnnnben-sof fibroblasts was observed (Fig. 5). At rhe JOURNAL OF BoNE AN1) JOINT SURGERY

REPAIR OF KNEE LIGAMENTS IN DOGS 1173 eight and tern weeks (foumr aniimnials) there n as a significant decncase inn the nuniber of fibnoblasts arnd an inner-case inn the aminoumnt of collagen. The process of healing in this gm-otmp as mon-c advanced tlmann inn Grouip I. Giomip III: Ti ansection of tine Lateral Collateral Lif](ll1l( flt, Surgical Repair, and IlIIlliObiliZ(ijiO1t Plaster ( as! ((11(1 Stei ninann \Vhem-eas inn Group I and Gi-oump II, looseness arid n-edumidamncy (If the later-al ligamnnemnts \vene nnoted imp to foimn- eeks, the t\\ oi ligannennts in this series which were exannninned at. (Inc week nvene tatmt. The great amnnoumnmt (If irregular scamrimng foumid inn tine umnn-epain-ed ligannnent.s was riot, 1)mesennt inn any of these ligannenits at four w ceks, amnd tine lat.em-al higannennt.s could he easily idermtiuied as annatonnnical structunes inn the t\\ () knees (If tine aniimnials sacrificed at. this timnie (Fig. 6). Inn fine rnnier-os(-opic seot,im )nis of tinese ligamiiennts, the stages of iniflaninnationi amnd fibi-oblast ie l)n(iliferatioml \ ere gmeat ly shontcnned, comnpamed vitin the liga- FIG. 8 Groinil I I. Flimn e is lit t b fibroidastim act ivitv inn t he lmo alinmg area at six wo eks. Alt homngh active monilagenmization is m enm, t inc fihen s :m! o not on im nmteol inmtm) lonigit mndimmal id:tnes. T ho nion nnal ligannent is at the right molgo mf time illmnstn atio)ni ; time smitiu o linim is inn time nnnidmllo ( )( 130). nncnnt.s inn tine pne\ ionns gm-oups., t t\v() i eeks, collageniizationn was a ver v pmolniiinlenlt feat umn-c ; at for nr Ir min I n-c weeks t mere was heavy co 1lagemn izat i ) rm, alt hoingin t he c(illagenn vas riot oriemnte(l lonigitudinnally, as inn nmm)n nnialtendon. The repaired area inn the tenndonns at six, eight, arid tent weeks after- r-ej)air- (twol anminnals at, each initem-val) consisted of very (lennse scar tissue (Fig. 8). (;111/) I I : Ti anseetion of t/i L(it( ial ( allatci-al Lu/aiil( ni t/1iou(//i One-I/al] of Its B iit/i, (1 1) (1 1 iii i1/dbiliz(i1ioil bj Jl(l. t(r ( (1St (1 ii (I 1( iil 111(1 ii 0 1??) 5 rfiie tauitniess (If tine liganinenit at. one \\ ( ( k (two anninials ) was commmpletely nioll-nnnal arid orn gross examniiniationi the hgannennt vas readily idennt.ificd (Fig. 7). In tine niio-n-oscopic sections at one veek tinene as fihn-ohlastic l)nolifcrat.ion w it.im only en sninall nnulmnli)en sof iniflaninnmnato)n vmells a(l,jamcnit to) the nion-nmnal-appeam-inig one-halt 0)! the higamnnenit..at blur- \\ ( ( ks,time l)n niinni( ni1feature \ts collagennizati(ini ( l ig. #{176}) ). _\t. six eeks, tine mlefeot. al)llcane(i t ( ) ha ye i leen I \ (IV ni icelv mepaine I (t \v I annininals mn.to am-hn I imnie in it en al ). IIo)\vever, ini ( nm nip II I, lonngit.udimial ai-i-anngennicnt (If tine collagen fibem s chnan am tem nstie of a nnor nnnal ligannncnnt was riot 1)1-csemnt. OL. 43-A. XCI. S. DECEMBER 1961

1174 D. H. O DONOGHUE, C. A. ROCKWOOD, JR., B. ZARICZNYJ, AND R. KENYOX TABLE II GROUP V (SEVEN DOGS): TENSILE STRENGTH OF LATERAL COLLATERAL Lm;AMENT AT STATED Ix- TERVALS AFI ER TRANSECTION AND IMMOBILIZATION IN PLASTER CAST WITHOUT SURGICAL REPAIR Time froni Operation to Sacrifice Dog No. Pounds of Weight at Rupture of Ligament Site of Rupture Control Experiment (Pounds) (POOL inds) (Per cent qf ( ont rot) Colnitrol Leg Experimental Leg 12 wks. 91 24 12 100 69 15 10 wks. l03 63 2:3 94 57 17 8 wks. 93 52 37 104 33 ii) 6 wks. 105 91 35 50 Pulled (1ff fenmnmrr witii ilonne flake 22 Pullemi off fennur with home flake 36 Pulled oft fenmurr witim llonmo flake 30 Pnnlleol oft fennnur with bonne flake 70 Pmnilo d off fenmunr with fragnmmmnmt of ilone 60 Pulled off Iiianla n it h i)onme flake 38 1ulled oil head of fil)mnia :tt :ittachnmmo nmt Pulled off fennur with bone flake Parted at line of transection Pulled off femur with bone flake Parted at line of transection Parto ol at line of t ranisect ion Parted at line of transection Parted at line of t ranmso ctiomm -(*..:N%.:....,,. s-,.usr III,,..., \ - -,. % 1%.:: FmG. 9 Group IV. At six weeks, the importanmt feature nnoted is the dense collagen tissue. Tlmis represemmts a higher degree of healing than is seen in Groirp III ( X 430). Group U: Transection of the Latcial Collateral Ligament, No Repair of Ligament, Iii, immobilization in Plaster Cast, a.n(1 Tests of Tensile Strength at Intervals after Transection With the limb rigidly immobilized in plaster, these dogs were able to walk very well after operation. Sacrifice was carried out at designated times, and the strength of the lateral collateral ligament of the experimental leg was compared ivith that of tine normal opposite leg, which served as a control (Table II). In both of the dogs sacrificed at ten w eeks and inn one of the two sacrificed at twelve weeks, the unrepaired ligament parted at the site of transection, in contrast to the control ligaments, which parted at the osseous jurnnctioni (Fig. 10). THE JOURNAL OF BONE AND JOINT SURGERY

REPAIR OF KNEE LIGAMENTS IN DOGS 1175 TABLE III GROUP VI (NINE I)OGS) i FNsmmE STRENGTH OF LATERAL COLLATERAL LnGAMENTS AT STATEn INTERVALS AFTER TRANSECTION, SURGICAL REPAnR, AN ni InIMOBILnzATI0N IN 1LASTER CAST Tinne fronim Operation to Sacrifice Dog No. Pomnnds of \\ eight at Rmnptmnre of Ligament. Control (Pounds) Experinmnenit (Pounds) (Per cent of Control) Control Leg Site of Rmnptinro Experinmental Leg 12 ks. 95 31 27 96 57 17 10 vks. (,)7 8#{176}.) 33 98 90 43 8 wks. 101 66 42 102 86 :32 6 w ks. 92 112 57 106 93 47 4 wks. 107 57 23 87 Pulled off fibula witin flake of bone 30 P1111(51 off attachnnnent at head of fibmnla 37 1ulled oft feniur with borne flake 50 Pulled off fennnur with bone flake 64 Ponlled off attaclmnmnenmt at Imead of fibnnla 37 Ponlied off fenninr with boric flake Si Pulled off fcmnnur with bomme flake 51 Pnnlled off fennnnr nvitlm borne flake 40 Pulled off head of fibula at attacimnionit Pulled off fibula with bomme flake Pulled off fennmnr vit1m i)one flake Pulled off head of fibula at attacinminent Partiall pulled off femoral attachnnenmt then split down ligamnnent to tear partially through suture line I\nlled off fennur with bone flake Pulled off head of fibula at. att achrnnennt Pulled off fennur with bone flake Pulled off hea(l of fibula at attachmenmt Parted inn rmniddlo at smntirre line Inn this group of animals the sever-ed liganinenit parted at much less weight than did the c(inntrol liganncnnt. Also, the experinntenital ligament n as stronger at. eight weeks than it was at tern or twelve weeks (Table II). We have riot attached particular significance to this apparent loss of strength inn view of the small nninmher of amninnals studied. However, it does seem significant that all except one of the ligaments in this gn-oup parted at the suture line, rather than at the osseous jimnictioni. WC presume that inn the dog inn w hich m-upture occurred at the osseous jumictioni, the ligament ends actually were well approximated, even without surgical repain. This certainly happens in man, which accounts for the excellent results that an-c observed inn some patients n ho have not had surgical repair. Inn these cases we presume that the m-upt.ur-ed ends (If the higannennt spontaneously becanne closely approximated. We believe that it is the approxinnatiomn of the temndonn ennds arid riot the stability afforded by tine sutume that is the importaint factor. Group VI: Transection of the Lateral ( ollateial Ligament, Repair of Ligament, Immmnmobilization in Plaster Cast, and Tests of Tensile Strength at Intervals after Repair As inn Group V, these dogs w alked on tine innmnnobilized cxperimenntal hinib until the tinne of sacn-ifice. Tensile stn-enigth of the collateral ligamemit of the miornial leg was compared with that of the same ligament inn the experimental leg (Table VOL. 43-A. NO. 8, DECEMBER 1961

1176 D. H. O DONOGHE, C. A. ROCKWOOD, JR., B. ZARICZNYJ, AND R. KENYON Fnc. 10 13estilt (If test of temnsil( st nenigt h of a so ( t ionmo d :tmioi iinistntum eol fil )lilan ( Ollaten :nl lig:onmnonit teni \( ek after section with subsequent innmnnioi iilizat toni inn a 1il:tst (n cast Ion six weeks. to t hat time temisi b test has o-aused rupture at t he site of originmal section, (.(. The gn osl oregonian soar is appan enit The hole inn the femur,.1, was made for one of the bolts oni tine testinig appan atois. Till tii)iofilmulan unit is marked B. FIG. 11 Result of test of tensile strength of a sectionmed and ro pain ( (b fibular coliato ral ligannnennt six weeks after section with subsequent innflnobilizatioimi in a Ilinoster cast for six veo ks. Noto timat the iiganmicnmt, C, is intact and that. it has avulsed a small iiece of i)onme (metal Pointer ) fn oni t he femonr,.1. Tine attachnnnent of the liganment to time tibiofilnilar unmit, h is initact. III). At four w eeks (one animal) the repaim-ed ligamincnit parted at tine sutun-c line. Thereaftem-, all the ligamemits (eight amninnals) pan-ted at the osseous attaclnmcmnt in a fashion sinnilar to that observed inn tine conntm-ol limbs (Fig. 1 1 ). Inn onne dog ( No. 98) there was also partial m-uptum-e at. the suture line. As inn Group V, the oven-- all tensile strength of the ligannenit arid its osseous attachnnemnt was substantially less in the immobilized limb than iii the control linnb, pi-esinnnnably because of disuse atrophy of the bone. We think that the sigmiificamit findiiig.imi this group of dogs was that with oinly one partial exception, the repaired area inn the ligament was stromiger than its THE JOURNAL OF BONE AND JOINT SURGERY

REPAIR OF KNEE LIGAMENTS IN DOGS I 177 at.t.achnnnent to bone. Inn Dog 96, the repaired ligament at twelve weeks parted at its (I55e(IUS jimnnctionn w ith a load of only seventeen pounds, or 30 per cemit of the I(Itt(l, at failure of the contm-ol ligamemnt. This obviously was not a test of the si remngtii of the n-epaim- l)ut of the bone attachment of the ligament in a leg which had bcenn ininminobilized inn plaster for over tnvelve weeks, with resultant atrophy of the borne. Inn comntrast to this, the experimeintal ligament in the other dog immobilized for- tw elve iveeks gave w ay at the osseous attachment to the fibula at a load e(lluvalenit to 87 pen- cemnt of the load that caused n-upture at the same point in the c(init.nol ligannnennt. Inn the tw o animals immobilized for tern weeks, the experimental liganinenit. inn Dog 98 nn as the one exceptionn. This ligannent split longitudinally; (Inme-inalf pinhlinmg off the boric, the other- iialf rtmpturimng through the repair. This was believed to inl(iicate a iveak area inn the repair, possibly the result of poor surgical appmoxinnationi. With this omne exception, from six weeks on, the repaired am-ca nn as comisistenntly stm-omiger than the attachment of the ligament to the bone (eight animals). We did mnot. attempt to devise an apparatus to grasp the two ends of tine ligannnenit arid test. its strength directly. Since the ligament was hardly large enough to ernsume unnifom-min gm-ippinig i)y the appam-atus, it was our belief that pulling (Iii the 1)onme itself woinid I)e more satisfactory. 1#{176} mnn-t.her (xl)(ninmi(9it5 an-c mnuder w ay inn nvhich the anninnals nn ill be allow ed to) mann arid mnse tinein- legs fon a w hulc after removal of the plaster cast in order to eliminate the factor- (If disuse atn-ophy and possibly to allonv a nnore accurate test (If the conipar-ative strength of the m-epaired amid control ligaments. DISCUSSION Miltnicn-, Him, anmd Fang show cd that after a mild ligament sprain in which 5(IIiiC fibers ar-c ton-ni i)ut the higanncnnt n-emaimis functionally intact, healing follow s a (lefinute patter-ri. Inn expcriminents on the knee ligaments of rabbits, they found that clun-inig the fir-st week imnflamniminatory cells predominate; during the latter part of the finst week arid pant of the second w eek, there is a gradually developing predominance (If fibm-oblasts. This stage persists during the second and third weeks, after- w hich collagen hl)ers appear and increase during the fourth and fifth weeks as the hl)roblasts decrcase. By the sixth w eek after a mild:sprain, the ligament is appam-enntly completely healed. After complete tear of a ligament, Miltner amid associates shiowe(l that the process of repair was much slower. Each step was prolonged to the poirnt that complete healing was delayed up to eight to tern w eeks. It. Could be surnniscd fronn this that complete healing in an unrepaired ligament w hich n as completely ruptured or avulsed from the bone would be delayed for at least tern w ccks arid pen-haps longer. Jack, inn his won-k on the collateral ligament of the knee in cats, showed that healing was good if the ligament ends wem-e inn close approximation. However, if a gap remained after m-uptun-e, healing between the ends of the ligament ns as i)y diffuse, poom-ly omgannizcd scam- tissue with very little tensile stremigth, with the i-esult that the involved joint was gm-ossly unnstablc. Inn their studies of the healing (If knee ligannicnits in dogs, Claytonn amid Weimcanine to conclusions sinnilar to our own. Oum- experimnnennts have shown that tine cham-acter of the scar, the speed of healing, amid the strength of the healing ligamucnnt vary quite consistently according to the type of treatnnemnt given. The outstamndinng finding was that close approxmmatiomi of the torn ligannemnt impi-oves tine chances fom- complete repair. SUMMARY AND CONCLUSION The experiment was umndertakeni inn n-espomnse to the three questionis previously VOL. 43-A, NO. 8, DECEMBER 1961

1178 D. H. O DONOGHUE, C. A. ROCKWOOD, JR., B. ZARICZNYJ, AND R. KENYON posed. We believe that these questions have been satisfactorily if inot completely answered: 1. When the ends of a i-uptun-ed ligament are inn approximation, healing occur-s by an orderly process: first, by necrosis and cellular infiltration, then by fibroblastic invasion, and finally, by collagenization. If the ligament ends are not inn close approximation, this orderly process does not occur and healing is by diffuse extensive scar formation. As time passes, the scar at the site of rupture beconies more orderly and its structure begins to resemble that of a normal ligament. Up to ten weeks, however, this scar had not become normal ligament even under the most favorable circumstances. Possibly, normal ligament would have developed if the process had been followed longer. 2. The most favorable circumstance for repair is end-to-end direct apposition of ligament fibers. This minimizes scarring, accelerates repair, hastens collagenization, and produces the most normal-appearing healed ligament. 3. Tests of the tensile strength of the divided lateral collateral ligament in our dogs suggest that after six or more weeks of immobilization, the strength of the attachment of the ligamemit to bone is diminished, presumably as the result of the atrophy of disuse. It would appear that during the first few weeks after such immobilization, care should be taken to prevent damage to this weakened area. This will need further confirmatory work. REFERENCES 1. CLAYTON, M. L., and \\EIR, 0. J., JR. : Experimental Investigations of Ligamentous Healing. Am. J. Surg., 98: 373-378, 1959. 2. JACK, E. A. : Experimental Rupture of the Medial Collateral Ligament of the Knee. J. Bone and Joint Surg., 32-B: 396-402, Aug. 1950. 3. MILTNER, L. J.; Hu, C. H.; and FANG, H. C.: Experimental Joint Sprain. Pathologic Study. Arch. Surg., 35: 234-240, 1937. 4. O DONOGHUE, D. H. : Surgical Treatment of Fresh Injuries to the Major Ligaments of the Knee. J. Bone and Joint Surg., 32-A: 721-738, Oct. 1950. 5. O DONOGHUE, D. H.: An Analysis of End Results of Surgical Treatment of Major Injuries to tie Ligaments of the Knee. J. Bone and Joint Surg., 37-A: 1-13, Jan. 1955. THE JOURNAL OF BONE AND JOINT SURGERY