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The Effect of Placing a Tensioned Graft Across Open Growth Plates A Gross and Histologic Analysis
T. Bradley Edwards, MD; Craig C. Greene, MD; Richard V. Baratta, PhD; Arthur Zieske, MD; R. Baxter Willis, MD
View Disclosures and Other Information
Investigation performed at the Bioengineering Laboratory, Department of Orthopaedic Surgery, Louisiana State University Health Sciences Center, New Orleans, Louisiana
T. Bradley Edwards, MD Craig C. Greene, MD Richard V. Baratta, PhD R. Baxter Willis, MD Department of Orthopaedic Surgery, Louisiana State University Health Sciences Center, 2025 Gravier Street, Suite 400, New Orleans, LA 70112. E-mail address for R.V. Baratta: rbarat@lsuhsc.edu
Arthur Zieske, MD Department of Pathology, Louisiana State University Health Sciences Center, 1901 Perdido Street, New Orleans, LA 70112
No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. Funds were received in total or partial support of the research or clinical study presented in this article. The funding source was the Orthopaedic Research and Education Foundation.

The Journal of Bone & Joint Surgery.  2001; 83:725-734 
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Abstract

Background: Midsubstance tears of the anterior cruciate ligament in skeletally immature patients are increasingly common and are a challenging problem. The results of nonoperative treatment are no better in children than they are in adults. Physeal-sparing reconstructive procedures have yielded poor results. Reconstructive procedures that are utilized in adults violate the physis, potentially resulting in growth abnormalities. The objective of this study was to provide a model for reconstruction of the anterior cruciate ligament in skeletally immature patients by evaluating the effects of a tensioned connective-tissue graft placed across the canine physis.

Methods: Twelve ten-week-old beagles underwent reconstruction of the anterior cruciate ligament consisting of placement of fascia lata autograft through drill-holes across the femoral and tibial physes, tensioning of the graft to 80 N, and fixing it with screws and washers. The contralateral limb served as a control. One dog was eliminated from the study secondary to a postoperative infection. Four months postoperatively, the dogs were killed and were inspected grossly, radiographically, and histologically for any evidence of growth disturbance.

Results: Significant valgus deformity of the distal part of the femur (p < 0.001) and significant varus deformity of the proximal part of the tibia (p = 0.03) developed in the treated limbs. Neither radiographic nor histologic examination demonstrated any evidence of physeal bar formation.

Conclusions: Significant growth disturbances occur with excessively tensioned transphyseal reconstruction of the anterior cruciate ligament in the canine model. These growth disturbances occur without radiographic or histologic evidence of physeal bar formation.

Clinical Relevance: This study illustrates the risk to the physis associated with transphyseal reconstruction of the anterior cruciate ligament with the use of a tensioned connective-tissue graft in skeletally immature patients. We do not recommend transphyseal reconstruction of the anterior cruciate ligament in this patient population.

Figures in this Article
    Intrasubstance rupture of the anterior cruciate ligament in patients with open physes, which is being recognized with increasing frequency, is a vexing clinical problem1,2. Nonoperative treatment of disruption of the anterior cruciate ligament has been no more successful in children than it has in adults1-8. Continuing with activities that result in episodes of knee instability risks meniscal damage and possibly early degenerative changes6,8-11.
    Primary repair of the anterior cruciate ligament has been performed in both children and adults, with suboptimal results1,2,5,8,12,13. Extra-articular reconstructions have been performed in children in an effort to restore knee stability without violating the physes; however, these procedures have not provided long-term stability or prevented meniscal damage2,9,14,15.
    Many authors who have performed transphyseal reconstruction of the anterior cruciate ligaments have not reported growth disturbances8,14-16. However, many of the patients in these series were near skeletal maturity. Additionally, many of these transphyseal reconstructions did not violate the distal femoral physis, placing the femoral attachment of the reconstruction in a nonanatomic position2,4.
    Stadelmaier et al. demonstrated bone-bridge formation after drilling through the physis of skeletally immature dogs17. However, no growth arrest occurred when an untensioned connective-tissue graft was placed through the physeal drill-hole. While the results of this study are encouraging, failure to tension the graft with use of a specific load may mask danger to the physis caused by transphyseal reconstruction of the anterior cruciate ligament. Consequently, failure to tension the graft eliminates the potential effects of the Heuter-Volkmann principle, which asserts that compression applied across a physis inhibits growth. The purpose of the current study was to provide a model for reconstruction of the anterior cruciate ligament in skeletally immature animals by evaluating the effects on growth of a tensioned connective-tissue graft placed across the canine physis.
     
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    +Fig. 1:Immediate postoperative anteroposterior radiograph of Specimen 11 (left knee), demonstrating osseous tunnels crossing the femoral and tibial physes (arrows).
     
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    +Fig. 2:Lateral photograph of the right (control) and left (grafted) femora of Specimen 11, demonstrating procurvatum and shortening of the distal part of the left femur.
     
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    +Fig. 3:Posterior photograph of the right (grafted) and left (control) femora of Specimen 12, demonstrating marked valgus angulation and shortening of the distal part of the right femur.
     
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    +Fig. 4:Photomicrograph of the grafted femoral physis of Specimen 5, demonstrating bone in the tunnel where the graft is not in close contact with the tunnel wall (arrows) but no development of a physeal bar on either side of the growth plate (magnification ¥40).
     
    Anchor for JumpAnchor for JumpTABLE I:  Medial and Lateral Femoral and Tibial Measurements
    *One of the twelve dogs (Specimen 10) was eliminated from the study secondary to a postoperative infection.
    Specimen*Medial Femoral Length (mm)Lateral Femoral Length (mm)Medial Tibial Length (mm)Lateral Tibial Length (mm)
    ControlGraftedControlGraftedControlGraftedControlGrafted
    ?1133.4137.3140.4139.0140.8141.1135.6140.4
    ?2?98.0100.1104.9103.1?96.9?97.1?93.4?95.4
    ?3126.2124.7128.1124.3122.0120.7119.6121.0
    ?4135.6134.0138.9132.1138.5140.2136.4142.1
    ?5102.6102.9106.7108.1100.4?98.6?99.0102.8
    ?6102.2108.4107.3109.0101.4101.3?95.9104.3
    ?7115.9?95.6121.0?94.5119.9123.0119.5123.2
    ?8115.0104.6120.6102.4118.9110.4116.9113.0
    ?9113.7113.9120.1111.6119.8119.9118.4118.4
    11113.2?93.5117.9?94.0116.9119.0117.2121.2
    12120.1112.6124.5108.4128.8128.5126.8131.2
    Mean116.0111.6120.9111.5118.6118.2116.2119.4
    Standard deviation?12.3?14.8?11.9?14.6?14.5?15.2?14.7?15.0
     
    Anchor for JumpAnchor for JumpTABLE II:  Femoral and Tibial Valgus and Varus Measurements*
    *Valgus angles are positive; varus angles are negative. †One of the twelve dogs (Specimen 10) was eliminated from the study secondary to a postoperative infection.
    Specimen†Femoral Angulation in Anteroposterior Plane (deg)Tibial Angulation in Anteroposterior Plane (deg)
    ControlGraftedControlGrafted
    ?1-84-3-2
    ?2-2700
    ?3-55-1-5
    ?4-5550
    ?50050
    ?6077-7
    ?7-101404
    ?8-51312-7
    ?9-10150-3
    11-860-4
    12-12106-12
    Mean-5.97.82.8-3.3
    Standard deviation4.14.74.54.4
     
    Anchor for JumpAnchor for JumpTABLE III:  Results of Histologic Evaluation of the Femur
    *One of the twelve dogs (Specimen 10) was eliminated from the study secondary to a postoperative infection.
    Specimen*Peripheral Physeal Measurements (m)Central Physeal Measurements (m)Bone in Tunnel
    ControlGraftedControlGrafted
    ?1375.0312.5337.5175.0No
    ?2412.5375.0362.5400.0No
    ?3500.0225.0362.5250.0No
    ?4487.5575.0337.5487.5Yes
    ?5412.5337.5450.0350.0Yes
    ?6450.0300.0412.5287.5Yes
    ?7337.5262.5350.0175.0No
    ?8275.0312.5425.0375.0No
    ?9487.5387.5537.5400.0Yes
    11437.5450.0350.0425.0No
    12325.0400.0337.5375.0Yes
    Mean409.1358.0387.5336.4
    Standard deviation?85.0102.0?85.0109.0
     
    Anchor for JumpAnchor for JumpTABLE IV:  Results of Histologic Evaluation of the Tibia
    *One of the twelve dogs (Specimen 10) was eliminated from the study secondary to a postoperative infection.
    Specimen*Peripheral Physeal Measurements (m)Central Physeal Measurements (m)Bone in Tunnel
    ControlGraftedControlGrafted
    ?1437.5350.0437.5350.0Yes
    ?2412.5275.0437.5287.5No
    ?3412.5200.0400.0225.0Yes
    ?4300.0462.5425.0375.0Yes
    ?5237.5275.0362.5337.5Yes
    ?6362.5325.0325.0325.0No
    ?7375.0412.5275.0375.0Yes
    ?8387.5287.5412.5262.5No
    ?9512.5475.0462.5337.5Yes
    11425.0412.5350.0312.5Yes
    12350.0387.5387.5325.0Yes
    Mean383.0351.1388.6319.3
    Standard deviation?70.0?96.0?70.0?62.0
    Twelve ten-week-old purpose-bred beagles were obtained from a licensed supplier. All procedures were approved by the Institutional Animal Care and Use Committee. Each beagle underwent intra-articular reconstruction of the anterior cruciate ligament, as described by Hulse and Shires18, on a randomly selected knee, while the contralateral knee served as a control. The dogs were preanesthetized with ketamine and diazepam. A surgical plane of anesthesia was maintained with halothane. The hindquarter of the selected extremity was shaved, prepared, and draped in a sterile fashion. A skin incision was then made from approximately 1 cm distal to the greater trochanter and extending distally to the approximate midpoint of the tibial shaft. A 1-cm-wide strip of fascia lata was harvested from the proximal extent of the skin incision to the level of the lateral femoral epicondyle. The fascia lata graft was tubularized with a running number-two braided polyester suture. An additional loop of number-two suture was placed in the distal end of the graft for use in tensioning the construct immediately prior to fixation. Next, a lateral parapatellar arthrotomy was carried out, and the patella was dislocated medially, exposing the anterior cruciate ligament. No effort was made to debride the intact anterior cruciate ligament in order to minimize potentially confounding variables17. A guide-wire for a 4-mm cannulated drill-bit was placed from the tibial footprint of the anterior cruciate ligament and across the tibial physis, exiting the tibial cortex anteromedially17. A 4-mm tibial tunnel was then created by drilling over the guide-wire. Similarly, with use of the same instrumentation, a femoral tunnel was created from the footprint of the native anterior cruciate ligament and across the femoral physis, exiting the femoral cortex laterally. As it passed through the growth plate, the tunnel was most probably in the middle and/or lateral third of the physis.
    The prepared autograft was passed through the tunnels in a distal-to-proximal direction by means of the number-two suture, with use of a wire loop as a suture passer. A Synthes AO ASIF 3.5-mm bicortical small-fragment screw (Paoli, Pennsylvania) with a washer was placed in a lateral-to-medial direction just proximal to the extra-articular opening of the femoral tunnel with use of a standard insertion technique. The proximal end of the graft was secured to the screw with the number-two suture, and the screw was maximally tightened. Next, manual tension was applied to the distal aspect of the graft, and the graft was cycled by putting the knee through a full range of motion twenty-five times. An AO ASIF 3.5-mm bicortical small-fragment screw with a washer was inserted in the tibia in a medial-to-lateral direction just distal to the extra-articular opening of the tibial tunnel. An Arthrex tensiometer (Naples, Florida) was used to tension the graft to 80 N, and the graft was secured to the tibia with the same method employed in the femur19. The surgical wound was irrigated thoroughly with sterile saline solution. The defect in the fascia lata and the lateral arthrotomy site were reapproximated with 3-0 braided polyester suture in a running fashion. The skin was reapproximated with 2-0 braided polyester with a simple interrupted technique. A sterile dressing was then applied.
    Immediate postoperative anteroposterior and lateral radiographs were made with the dogs still under anesthesia. These included radiographs of both extremities with the stifle joint positioned in full extension (a 30° tibiofemoral angle)18.
    Postoperatively, the animals were allowed to use the limb as tolerated. They were given buprenorphine for pain for three days. Prophylactic antibiotics (cefadroxil, 50-mg tablets) were administered for seven days. The dogs were examined at two weeks postoperatively, at which time their sutures were removed, and monthly thereafter. The presence of any limp or complications, such as infection, was recorded.
    At four months postoperatively, the dogs were killed with an intravenous overdose of sodium pentobarbital. Prior to disarticulation of the hindquarters, postmortem radiographs were made with use of the previously described technique. The postmortem radiographs were compared with the immediate postoperative radiographs, and any qualitative changes were noted.
    Both lower extremities were disarticulated. The tibiae and femora were stripped of soft tissue. The condition of the graft was noted prior to débridement. A digital micrometer was used to measure the medial and lateral lengths of each bone in order to assess abnormalities of overall limb length. The lateral femoral length was measured from the superior aspect of the greater trochanter to the most distal aspect of the lateral femoral condyle. The medial femoral length was measured from the superior margin of the femoral head to the most distal aspect of the medial femoral condyle. The lateral tibial length was measured from the lateral tibial plateau to the tip of the lateral malleolus. The medial tibial length was measured from the medial plateau to the tip of the medial malleolus. Additionally, any angulation in the sagittal plane was recorded, although these observations were strictly subjective because we do not have a reliable measurement for evaluating procurvatum and recurvatum. The specimens were placed on white absorbent paper and photographed. Varus-valgus angulation was measured from the photographs. Since we were able to obtain true anteroposterior views of the femur and tibia, which we could not do radiographically because the stifle joint does not extend fully, we were able to measure the angulation in the anteroposterior plane with minimal effect of rotation.
    Coronal sections, 3 mm thick, were obtained in the region of the femoral and tibial physeal tunnels. Sections, 5 mm thick, were prepared from these specimens by fixing in 10% formalin, decalcifying in 5% nitric acid, and embedding in paraffin. The sections were stained with hematoxylin and eosin and were examined under light microscopy by a surgical pathologist for evidence of osseous bar formation. Additionally, the thickness of the physis was measured with a calibrated eyepiece (resolution of 25 mm). Measurements were made 2 mm from the cortical border at the medial and lateral aspects of the control and grafted specimens. Central measurements were made 2 mm from the medial and lateral aspects of the tunnel in the grafted specimens and 4 mm medial and lateral to the center of the physis in the control specimens. Because of the difficulty associated with determining the medial and lateral aspects of the histologic section, a mean of the two peripheral measurements in each specimen was calculated to yield a single value for purposes of data analysis. Central measurements were averaged to yield a single value as well.
    Differences in the lengths of the gross specimens were determined with paired t tests comparing both the medial and the lateral lengths of the femora and tibiae. Femoral and tibial varus-valgus angulation was also assessed with paired t tests; valgus angles were noted as positive and varus angles, as negative. The histologic measurements (central and peripheral for the tibia and femur) were pooled and compared with use of paired t tests.
    A knee infection requiring irrigation and débridement and antibiotics developed at six weeks postoperatively in one dog (Specimen 10). Postinfectious arthropathy developed rapidly, as demonstrated on radiographic and clinical examination, and the dog was excluded from the study. Of the remaining eleven dogs, six had the left hindlimb operated on and five had the right hindlimb operated on. No complications developed in any of these eleven dogs. All dogs limped for approximately two weeks postoperatively and had a normal gait pattern thereafter.
    The osseous tunnels crossed both physes in each operative specimen as seen on the immediate postoperative radiographs (Fig. 1). All grafted specimens demonstrated longitudinal growth in both the tibia and the femur, as evidenced by migration of the fixation screws away from the physes when immediate postoperative radiographs were compared with postmortem radiographs. No specimens showed any radiographic evidence of physeal bar formation. There was no qualitative difference in the physes between any grafted extremity and its contralateral control.
    When inspected grossly, all fascia lata autografts were noted to be in continuity. All grafts with the exception of Specimen 1 appeared to be under tension. All grafted specimens appeared to have some procurvatum of the distal part of the femur when compared with the contralateral control. This deformity was most notable in Specimens 11 and 12 (Fig. 2). No gross recurvatum or procurvatum was noted in any of the tibiae. In addition to length discrepancies, valgus deformity of the distal part of the femur was obvious in several of the specimens (Fig. 3). In general, minimal deformities were apparent on gross inspection of the tibiae.
    The medial and lateral femoral and tibial measurements of the experimental and control limbs are summarized in Table I. With the numbers available, no significant differences could be detected between the grafted and control limbs with regard to mean medial femoral length (p = 0.13) or mean medial tibial length (p = 0.67). The mean lateral femoral length in the control limbs was significantly greater than that in the grafted limbs (p < 0.01). The mean lateral tibial length in the grafted limbs was significantly greater than that in the control limbs (p = 0.009).
    Furthermore, significant valgus femoral angulation was present in the grafted extremities (p < 0.001). Coupled with the results of length measurements, this valgus reflects the relative shortening of the lateral part of the femur. The tibiae of the grafted extremities demonstrated significant varus angulation (p = 0.03). This deformity reflects the relative lengthening of the lateral part of the tibia. Data on varus and valgus angulation are summarized in Table II.
    Histologic evaluation demonstrated no osseous bar formation in any specimen. Bone was seen in the tunnel at the level of the physis in all grafted specimens in which the graft was not in tight contact with the tunnel wall. Bone was seen in five of the eleven femoral tunnels (Fig. 4) and in eight of the eleven tibial tunnels. Unpaired t tests comparing the medial and lateral lengths of the tibia and femur of specimens with bone in the tunnel with those lengths in specimens without bone in the tunnel demonstrated no relationship between the presence of bone in the tunnel and femoral or tibial growth disturbance (p > 0.05).
    The femoral physes in the control limbs showed a trend (p = 0.056) toward being thicker peripherally than those in the grafted limbs (mean, 409.1 85 compared with 358 102 mm), whereas weaker trends were found when central measurements in the control femoral physes were compared with those in their grafted counterparts (mean, 387.5 85 compared with 336.4 109 mm) (p = 0.15). The mean central physeal thickness of the control tibiae was significantly greater (p < 0.004) than that of the grafted tibiae (388.6 70 compared with 319.3 62 mm). With the numbers available, there was no significant difference between the mean peripheral thicknesses of the control and grafted tibial physes (383.0 70 mm in the control group and 351.1 96 mm in the grafted group). The results of the histologic evaluation are summarized in Tables III and IV.
    This study demonstrated growth disturbances caused by transphyseal reconstruction of the anterior cruciate ligament with a highly tensioned autograft in an immature canine model. These results suggest that similar consequences could arise if such a procedure were performed in children with substantial growth remaining.
    The increasing participation of children in competitive athletics, and increasing physician awareness, have undoubtedly contributed to an increase in the recognition of midsubstance injuries of the anterior cruciate ligament in individuals with open physes1,2. The discontinuation of sports until skeletal maturity has been attained and until standard intra-articular reconstruction of the anterior cruciate ligament can be safely performed is unacceptable to many young athletes and their parents.
    Nonoperative treatment of injuries of the anterior cruciate ligament in children yields results that are no better than those seen in adults1-8. Angel and Hall reported that, despite initially good results, knee function in these children deteriorates with time3. Of their seven patients with complete disruption of the anterior cruciate ligament, none were able to return to their preinjury level of athletic participation. Mizuta et al. reported sixteen fair or poor results in eighteen children after nonoperative treatment of an injury of the anterior cruciate ligament6. Kannus and Järvinen, in their report of twenty-five partial and seven complete tears of the anterior cruciate ligament in children, found significantly poorer results in the individuals with a complete tear (p = 0.01)20. In addition, five of the seven patients with a complete tear could not return to their preinjury level of participation.
    Another concern with nonoperative treatment of injuries of the anterior cruciate ligament is concomitant or ensuing meniscal injury, with its associated potential for development of degenerative changes. Repetitive giving-way results in a higher prevalence of meniscal injury6,8-11. Mizuta et al. found thirteen concomitant meniscal injuries and six secondary injuries in their thirty-six-month follow-up study6. In a series reported by Graf et al., seven of eight skeletally immature patients with a nonoperatively treated injury of the anterior cruciate ligament sustained secondary meniscal injury at a mean of fifteen months after ligament disruption9. In addition, concomitant meniscal tears initially treated with repair without reconstruction of the anterior cruciate ligament would seem to be at increased risk for failure secondary to residual instability21.
    Primary repair of the anterior cruciate ligament has yielded comparably poor results in both adults and children1,2,5,8,12,13. Engebretsen et al. reported that, of eight knees treated with primary repair of the anterior cruciate ligament, five were unstable postoperatively13. Two of three children treated by DeLee and Curtis with repair of the anterior cruciate ligament had clinical instability and repetitive episodes of giving-way postoperatively5.
    Extra-articular reconstruction, both alone and in combination with intra-articular procedures, has been used in the treatment of injuries of the anterior cruciate ligament in children2,9,14,15,22. Graf et al. reported continued instability and subsequent meniscal injury in both of their patients who had undergone extra-articular reconstruction9. Despite obtaining good results at a minimum of one year after extra-articular reconstruction, McCarroll et al. stated that they still preferred intra-articular procedures whenever feasible15.
    Intra-articular reconstructions that do not violate either the femoral or the tibial physis have been reported1,21,23,24. Brief reported that eight of nine patients treated with reconstruction of the anterior cruciate ligament without drill-holes exhibited no meaningful subjective or objective instability at three years postoperatively23. Parker et al. reported similar results after using the more anatomic Drez modification of Brief’s "tomato stake" procedure22. All of these reconstructions are, however, nonanatomic.
    Several authors have reported successes with various transphyseal intra-articular reconstructions8,14-16,25. However, most of the patients in these series were near skeletal maturity and may not have had substantial growth remaining. In addition, Stanitski observed that many of these studies did not properly document the degree of skeletal immaturity either radiographically or physiologically19. Furthermore, in many of these series only the tibial physis was violated, with sparing of the femoral physis, which is responsible for 40% of ultimate limb length26.
    Lipscomb and Anderson reported on twenty-four skeletally immature patients who underwent reconstruction of the anterior cruciate ligament with violation of the tibial physis16. Only eleven of these patients had completely open growth plates. At the time of follow-up, fourteen patients had a limb-length discrepancy, although the authors considered only one to be important. The authors concluded that their procedure did not cause major growth disturbances, but they stated that they would not recommend the procedure in patients younger than twelve years of age. McCarroll et al. performed fourteen intra-articular patellar tendon reconstructions in fourteen-year-old patients, and there were no growth arrests14. However, the intra-articular reconstructions were not done in patients who were thirteen years old or younger, had a bone age that was at least six months younger than their chronological age, had a family history of remaining growth potential after the age of fourteen, or had not attained maturity according to the Tanner classification. In a subsequent study, with patients selected with use of the same criteria, McCarroll et al. reported that sixty intra-articular reconstructions violating both physes resulted in no growth arrests15. Andrews et al. performed intra-articular allograft reconstructions violating the tibial physis in eight skeletally immature athletes; they reported a limb-length discrepancy of >10 mm secondary to a femoral length inequality in two patients25. Despite predominantly good results, the authors were reluctant to recommend the reconstruction as a routine procedure, and they believed that the femoral physis should not be violated.
    Despite the claims of some investigators that drilling across either the tibial or the femoral physis is not a problem, some surgeons have seen major growth disturbances resulting from just such a procedure. Guanche performed a standard reconstruction of the anterior cruciate ligament with drill-holes across both physes in a twelve-year-old and subsequently noted substantial distal femoral overgrowth27. Koman and Sanders reported a valgus deformity following reconstruction of the anterior cruciate ligament in a skeletally immature patient, although this disturbance could be attributed to a screw crossing the physis28. In addition, many surgeons remain hesitant to drill across an open growth plate, reasoning that a possible growth disturbance is more detrimental than deficiency of the anterior cruciate ligament. The reluctance of some surgeons to reconstruct anterior cruciate ligaments in children with substantial growth remaining has been based largely on a fear of growth disturbance caused by drilling across the growth plates. The study by Stadelmaier et al. allayed those concerns to some degree17; however, our study showed that excessively tensioned grafts can be a source of growth disturbance.
    Both rabbits and dogs have been used successfully for evaluation of the effects of surgical intervention violating the open physis, and these studies have led to several conclusions17,29-32. Surgically created physeal defects do not heal with normal physeal tissue; instead, they are bridged by cancellous bone in the absence of interposed tissue30,31. Soft-tissue interposition prevents an osseous bridge from forming in small defects19,31. Pressures applied in a direction parallel to the direction of growth inhibit longitudinal growth29. In addition, the Heuter-Volkmann principle and its corollary, the Delpech principle, uphold that compression across the physis inhibits growth, while tension across the physis accelerates growth.
    Recently, Stadelmaier et al., in an effort to study the effects of placing a soft-tissue graft across an open physis, performed transphyseal reconstruction of the anterior cruciate ligament in a canine model17. Holes were drilled across the femoral and tibial physes in eight dogs. In half of the dogs, a strip of fascia lata was placed through the tunnels and was secured with suture. Histologic evidence of an osseous bridge did not develop in the specimens with interposed autograft; however, bridge formation was seen in the animals that did not have grafting. Although these findings seemed encouraging to proponents of transphyseal procedures, it must be emphasized that no preset tension was applied to these grafts; thus, it is not possible to safely extrapolate the results to humans. Furthermore, since previous studies have demonstrated that compression across an open growth plate results in decreased growth29,32, it is reasonable to believe that compression created by excessive tensioning of a graft during reconstruction of the anterior cruciate ligament could be detrimental.
    The results of the current study suggest that excessive tensioning of an autograft used in transphyseal reconstruction of the anterior cruciate ligament can cause significant growth disturbances. The characteristic deformity seen in this series validates the Heuter-Volkmann principle in that compression provided by the autograft across the lateral femoral physis created a valgus deformity. Interestingly, in the grafted extremities a varus deformity of the tibia developed as a result of lateral tibial overgrowth and not the more readily expected decreased medial growth. This lateral tibial overgrowth may have been a compensatory growth acceleration in response to the femoral valgus caused by shortening of the lateral aspect of the femur.
    The growth disturbances observed in this study occurred without frank physeal arrest. We did find, however, deposition of bone in areas of the tunnels that the graft did not completely fill. This bone deposition was typically a few cells wide, and it was not associated with narrowing of the adjacent plate or with cellular disorganization; it certainly was not visible radiographically. In these very basic ways, the composition of bone in the tunnels was different from physeal bar formation. This was of interest because it was thought that bone formation may play a role in the observed growth disturbances. However, with the numbers available, our analysis did not show any relationship between bone in the tunnels and growth disturbances. It is conceivable that tensioning of the graft resulted in a decrease in its diameter, leaving gaps between the graft and the tunnel that led to new-bone formation. Additionally, the mean thickness of the control physes was greater in all areas measured, although the difference in the peripheral tibial measurements was not significant. These findings demonstrate that the observed deformities occur as a result of an alteration of physeal growth and not as a result of premature physeal closure.
    This study is not without limitations. First, the ability to extrapolate the results of animal studies to humans is limited; however, the dog is an accepted model for skeletal maturation32. Second, no consistent, objective measure of angulation in the sagittal plane could be calculated either radiographically or on gross examination. Third, it is also possible that the capsular or fascia lata suture, the length of which does not change with growth, may act as a lateral tether. We consider this possibility unlikely, however, since Stadelmaier et al. reported no growth disturbances attributable to the sutures17.
    The amount of initial tension placed on an autograft has been demonstrated to correlate with the amount of postoperative knee laxity33. We used a preset tension of 80 N, which corresponds to that recommended by Yasuda et al.33 for adult patients. This tension could be considered to be relatively high, and it was selected to maximize the probability of showing a tension effect if in fact there was one. Reducing the amount of initial tension applied to the autograft could certainly change the results. Grafts placed with less initial tension can stabilize the knee satisfactorily. Additional studies should be performed to examine the effects of different amounts of tension placed across an open physis and to ascertain the optimum tension likely to result in a stable knee with a minimum chance of provoking growth disturbance.
    In the current study, we utilized a 4-mm hole in the physis in all specimens as was done by Stadelmaier et al.17. The percentage of the physis destroyed by the drill was not calculated and may have contributed to the growth disturbance34.
    In summary, despite the limitations of this study, we concluded that the introduction of tension into the canine model of transphyseal reconstruction of the anterior cruciate ligament can yield significant growth disturbances. Furthermore, a similar procedure in humans could have similar consequences. At this time, we do not perform or recommend transphyseal reconstruction of the anterior cruciate ligament in individuals with substantial growth remaining. However, before this procedure is abandoned altogether, more research needs to be done in order to ascertain whether there is an optimal graft geometry and tension that would stabilize the knee without adversely affecting growth.
    Note: The authors acknowledge the technical contributions of Kenneth S. Weiss, MD, Robert Quinn, DVM, and Mrs. Merrill Frost. The authors also acknowledge the intellectual contributions of David Drez, MD.
    DeLee JC. Ligamentous injury of the knee. In: Stanitski CL, DeLee JC, Drez D, editors. Pediatric and adolescent sports medicine. Philadelphia: WB Saunders; 1994. p 406-32 
     
    Nottage WM, and Matsuura PA: Management of complete traumatic anterior cruciate ligament tears in the skeletally immature patient: current concepts and review of the literature. Arthroscopy,1994.10: 569-73, 10569  1994  [PubMed]
     
    Angel KR, and Hall DJ: Anterior cruciate ligament injury in children and adolescents. Arthroscopy,1989.5: 197-200, 5197  1989  [PubMed]
     
    Bisson LJ; Wickiewicz T; Levinson M; and Warren R: ACL reconstruction in children with open physes. Orthopedics,1998.21: 659-63, 21659  1998  [PubMed]
     
    DeLee JC, and Curtis R: Anterior cruciate ligament insufficiency in children. Clin Orthop,1983.172: 112-8, 172112  1983  [PubMed]
     
    Mizuta H; Kubota K; Shiraishi M; Otsuka Y; Nagamoto N; and Takagi K: The conservative treatment of complete tears of the anterior cruciate ligament in skeletally immature patients. J Bone Joint Surg Br,1995.77: 890-4, 77890  1995  [PubMed]
     
    Pressman AE; Letts RM; and Jarvis JG: Anterior cruciate ligament tears in children: an analysis of operative versus nonoperative treatment. J Pediatr Orthop,1997.17: 505-11, 17505  1997  [PubMed]
     
    Shelbourne KD, Foulk DA, Nitz PA. Anterior cruciate ligament injuries. In: Reider B, editor. Sports medicine: the school-age athlete. 2nd ed. Philadelphia: WB Saunders; 1996. p 329-47 
     
    Graf BK; Lange RH; Fujisaki CK; Landry GL; and Saluja RK: Anterior cruciate ligament tears in skeletally immature patients: meniscal pathology at presentation and after attempted conservative treatment. Arthroscopy,1992.8: 229-33, 8229  1992  [PubMed]
     
    Hawkins RJ; Misamore GW; and Merritt TR: Followup of the acute nonoperated isolated anterior cruciate ligament tear. Am J Sports Med,1986.14: 205-10, 14205  1986  [PubMed]
     
    Irvine GB, and Glasgow MM: The natural history of the meniscus in anterior cruciate insufficiency. J Bone Joint Surg Br,1992.74: 403-5, 74403  1992  [PubMed]
     
    Clanton TO; DeLee JC; Sanders B; and Neidre A: Knee ligament injuries in children. J Bone Joint Surg Am,1979.61: 1195-201, 611195  1979  [PubMed]
     
    Engebretsen L; Svenningsen S; and Benum P: Poor results of anterior cruciate ligament repair in adolescence. Acta Orthop Scand,1988.59: 684-6, 59684  1988  [PubMed]
     
    McCarroll JR; Rettig AC; and Shelbourne KD: Anterior cruciate ligament injuries in the young athlete with open physes. Am J Sports Med,1988.16: 44-7, 1644  1988  [PubMed]
     
    McCarroll JR; Shelbourne KD; Porter DA; Rettig AC; and Murray S: Patellar tendon graft reconstruction for midsubstance anterior cruciate ligament rupture in junior high school athletes. An algorithm for management. Am J Sports Med,1994.22: 478-84, 22478  1994  [PubMed]
     
    Lipscomb AB, and Anderson AF: Tears of the anterior cruciate ligament in adolescents. J Bone Joint Surg Am,1986.68: 19-28, 6819  1986  [PubMed]
     
    Stadelmaier DM; Arnoczky SP; Dodds J; and Ross H: The effect of drilling and soft tissue grafting across open growth plates. A histologic study. Am J Sports Med,1995.23: 431-5, 23431  1995  [PubMed]
     
    Hulse DA, Shires PK. The stifle joint. In: Slatter D, editor. Textbook of small animal surgery. Philadelphia: WB Saunders; 1993. p 2203-4 
     
    Stanitski CL: Surgical reconstruction for symptomatic ACL insufficiency in skeletally immature athletes [letter]. Am J Sports Med,1994.22: 433, 22433  1994  [PubMed]
     
    Kannus P, and Järvinen M: Knee ligament injuries in adolescents. Eight year follow-up of conservative management. J Bone Joint Surg Br. ,1988.70: 772-6, 70772  1988  [PubMed]
     
    Janarv P; Nyström A; Werner S; and Hirsch G: Anterior cruciate ligament injuries in skeletally immature patients. J Pediatr Orthop,1996.16: 673-7, 16673  1996  [PubMed]
     
    Parker AW; Drez D Jr; and Cooper JL: Anterior cruciate ligament injuries in patients with open physes. Am J Sports Med,1994.22: 44-7, 2244  1994  [PubMed]
     
    Brief LP: Anterior cruciate ligament reconstruction without drill holes. Arthroscopy,1991.7: 350-7, 7350  1991  [PubMed]
     
    Nakhostine M; Bollen SR; and Cross MJ: Reconstruction of mid-substance anterior rupture in adolescents with open physes. J Pediatr Orthop,1995.15: 286-7, 15286  1995  [PubMed]
     
    Andrews M; Noyes FR; and Barber-Westin SD: Anterior cruciate ligament allograft reconstruction in the skeletally immature athlete. Am J Sports Med,1994.22: 48-54, 2248  1994  [PubMed]
     
    Ogden JA. The uniqueness of growing bones. In: Rockwood CA Jr, Wilkins KE, King RE, editors. Fractures in children. 3rd ed. Philadelphia: JB Lippincott; 1984. p 1-86 
     
    Guanche CA. Personal communication, 1997 
     
    Koman JD, and Sanders JO: Valgus deformity after reconstruction of the anterior cruciate ligament in a skeletally immature patient. A case report. J Bone Joint Surg Am,1999.81: 711-5, 81711  1999  [PubMed]
     
    Arkin AM, and Katz JF: The effects of pressure on epiphyseal growth. The mechanism of plasticity of growing bone. J Bone Joint Surg Am,1956.38: 1056-76, 381056  1956  [PubMed]
     
    Campbell CJ; Grisolia A; and Zanconato G: The effects produced in the cartilaginous epiphyseal plate of immature dogs by experimental surgical traumata. J Bone Joint Surg Am,1959.41: 1221-42, 411221  1959  [PubMed]
     
    Österman K: Healing of large surgical defects of the epiphyseal plate. An experimental study. Clin Orthop,1994.300: 264-8, 300264  1994  [PubMed]
     
    Siffert RS: The effect of staples and longitudinal wires on epiphyseal growth. An experimental study. J Bone Joint Surg Am,1956.38: 1077-88, 381077  1956  [PubMed]
     
    Yasuda K; Tsujino J; Tanabe Y; and Kaneda K: Effects of initial graft tension on clinical outcome after anterior cruciate ligament reconstruction. Autogenous doubled hamstring tendons connected in series with polyester tapes. Am J Sports Med,1997.25: 99-106, 2599  1997  [PubMed]
     
    Guzzanti V; Falciglia F; Gigante A; and Fabbriciani C: The effect of intra-articular ACL reconstruction on the growth plates of rabbits. J Bone Joint Surg Br,1994.76: 960-3, 76960  1994  [PubMed]
     

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    Anchor for JumpAnchor for Jump
    +Fig. 1:Immediate postoperative anteroposterior radiograph of Specimen 11 (left knee), demonstrating osseous tunnels crossing the femoral and tibial physes (arrows).
    Anchor for JumpAnchor for Jump
    +Fig. 2:Lateral photograph of the right (control) and left (grafted) femora of Specimen 11, demonstrating procurvatum and shortening of the distal part of the left femur.
    Anchor for JumpAnchor for Jump
    +Fig. 3:Posterior photograph of the right (grafted) and left (control) femora of Specimen 12, demonstrating marked valgus angulation and shortening of the distal part of the right femur.
    Anchor for JumpAnchor for Jump
    +Fig. 4:Photomicrograph of the grafted femoral physis of Specimen 5, demonstrating bone in the tunnel where the graft is not in close contact with the tunnel wall (arrows) but no development of a physeal bar on either side of the growth plate (magnification ¥40).
    Anchor for JumpAnchor for JumpTABLE I:  Medial and Lateral Femoral and Tibial Measurements
    *One of the twelve dogs (Specimen 10) was eliminated from the study secondary to a postoperative infection.
    Specimen*Medial Femoral Length (mm)Lateral Femoral Length (mm)Medial Tibial Length (mm)Lateral Tibial Length (mm)
    ControlGraftedControlGraftedControlGraftedControlGrafted
    ?1133.4137.3140.4139.0140.8141.1135.6140.4
    ?2?98.0100.1104.9103.1?96.9?97.1?93.4?95.4
    ?3126.2124.7128.1124.3122.0120.7119.6121.0
    ?4135.6134.0138.9132.1138.5140.2136.4142.1
    ?5102.6102.9106.7108.1100.4?98.6?99.0102.8
    ?6102.2108.4107.3109.0101.4101.3?95.9104.3
    ?7115.9?95.6121.0?94.5119.9123.0119.5123.2
    ?8115.0104.6120.6102.4118.9110.4116.9113.0
    ?9113.7113.9120.1111.6119.8119.9118.4118.4
    11113.2?93.5117.9?94.0116.9119.0117.2121.2
    12120.1112.6124.5108.4128.8128.5126.8131.2
    Mean116.0111.6120.9111.5118.6118.2116.2119.4
    Standard deviation?12.3?14.8?11.9?14.6?14.5?15.2?14.7?15.0
    Anchor for JumpAnchor for JumpTABLE II:  Femoral and Tibial Valgus and Varus Measurements*
    *Valgus angles are positive; varus angles are negative. †One of the twelve dogs (Specimen 10) was eliminated from the study secondary to a postoperative infection.
    Specimen†Femoral Angulation in Anteroposterior Plane (deg)Tibial Angulation in Anteroposterior Plane (deg)
    ControlGraftedControlGrafted
    ?1-84-3-2
    ?2-2700
    ?3-55-1-5
    ?4-5550
    ?50050
    ?6077-7
    ?7-101404
    ?8-51312-7
    ?9-10150-3
    11-860-4
    12-12106-12
    Mean-5.97.82.8-3.3
    Standard deviation4.14.74.54.4
    Anchor for JumpAnchor for JumpTABLE III:  Results of Histologic Evaluation of the Femur
    *One of the twelve dogs (Specimen 10) was eliminated from the study secondary to a postoperative infection.
    Specimen*Peripheral Physeal Measurements (m)Central Physeal Measurements (m)Bone in Tunnel
    ControlGraftedControlGrafted
    ?1375.0312.5337.5175.0No
    ?2412.5375.0362.5400.0No
    ?3500.0225.0362.5250.0No
    ?4487.5575.0337.5487.5Yes
    ?5412.5337.5450.0350.0Yes
    ?6450.0300.0412.5287.5Yes
    ?7337.5262.5350.0175.0No
    ?8275.0312.5425.0375.0No
    ?9487.5387.5537.5400.0Yes
    11437.5450.0350.0425.0No
    12325.0400.0337.5375.0Yes
    Mean409.1358.0387.5336.4
    Standard deviation?85.0102.0?85.0109.0
    Anchor for JumpAnchor for JumpTABLE IV:  Results of Histologic Evaluation of the Tibia
    *One of the twelve dogs (Specimen 10) was eliminated from the study secondary to a postoperative infection.
    Specimen*Peripheral Physeal Measurements (m)Central Physeal Measurements (m)Bone in Tunnel
    ControlGraftedControlGrafted
    ?1437.5350.0437.5350.0Yes
    ?2412.5275.0437.5287.5No
    ?3412.5200.0400.0225.0Yes
    ?4300.0462.5425.0375.0Yes
    ?5237.5275.0362.5337.5Yes
    ?6362.5325.0325.0325.0No
    ?7375.0412.5275.0375.0Yes
    ?8387.5287.5412.5262.5No
    ?9512.5475.0462.5337.5Yes
    11425.0412.5350.0312.5Yes
    12350.0387.5387.5325.0Yes
    Mean383.0351.1388.6319.3
    Standard deviation?70.0?96.0?70.0?62.0
    DeLee JC. Ligamentous injury of the knee. In: Stanitski CL, DeLee JC, Drez D, editors. Pediatric and adolescent sports medicine. Philadelphia: WB Saunders; 1994. p 406-32 
     
    Nottage WM, and Matsuura PA: Management of complete traumatic anterior cruciate ligament tears in the skeletally immature patient: current concepts and review of the literature. Arthroscopy,1994.10: 569-73, 10569  1994  [PubMed]
     
    Angel KR, and Hall DJ: Anterior cruciate ligament injury in children and adolescents. Arthroscopy,1989.5: 197-200, 5197  1989  [PubMed]
     
    Bisson LJ; Wickiewicz T; Levinson M; and Warren R: ACL reconstruction in children with open physes. Orthopedics,1998.21: 659-63, 21659  1998  [PubMed]
     
    DeLee JC, and Curtis R: Anterior cruciate ligament insufficiency in children. Clin Orthop,1983.172: 112-8, 172112  1983  [PubMed]
     
    Mizuta H; Kubota K; Shiraishi M; Otsuka Y; Nagamoto N; and Takagi K: The conservative treatment of complete tears of the anterior cruciate ligament in skeletally immature patients. J Bone Joint Surg Br,1995.77: 890-4, 77890  1995  [PubMed]
     
    Pressman AE; Letts RM; and Jarvis JG: Anterior cruciate ligament tears in children: an analysis of operative versus nonoperative treatment. J Pediatr Orthop,1997.17: 505-11, 17505  1997  [PubMed]
     
    Shelbourne KD, Foulk DA, Nitz PA. Anterior cruciate ligament injuries. In: Reider B, editor. Sports medicine: the school-age athlete. 2nd ed. Philadelphia: WB Saunders; 1996. p 329-47 
     
    Graf BK; Lange RH; Fujisaki CK; Landry GL; and Saluja RK: Anterior cruciate ligament tears in skeletally immature patients: meniscal pathology at presentation and after attempted conservative treatment. Arthroscopy,1992.8: 229-33, 8229  1992  [PubMed]
     
    Hawkins RJ; Misamore GW; and Merritt TR: Followup of the acute nonoperated isolated anterior cruciate ligament tear. Am J Sports Med,1986.14: 205-10, 14205  1986  [PubMed]
     
    Irvine GB, and Glasgow MM: The natural history of the meniscus in anterior cruciate insufficiency. J Bone Joint Surg Br,1992.74: 403-5, 74403  1992  [PubMed]
     
    Clanton TO; DeLee JC; Sanders B; and Neidre A: Knee ligament injuries in children. J Bone Joint Surg Am,1979.61: 1195-201, 611195  1979  [PubMed]
     
    Engebretsen L; Svenningsen S; and Benum P: Poor results of anterior cruciate ligament repair in adolescence. Acta Orthop Scand,1988.59: 684-6, 59684  1988  [PubMed]
     
    McCarroll JR; Rettig AC; and Shelbourne KD: Anterior cruciate ligament injuries in the young athlete with open physes. Am J Sports Med,1988.16: 44-7, 1644  1988  [PubMed]
     
    McCarroll JR; Shelbourne KD; Porter DA; Rettig AC; and Murray S: Patellar tendon graft reconstruction for midsubstance anterior cruciate ligament rupture in junior high school athletes. An algorithm for management. Am J Sports Med,1994.22: 478-84, 22478  1994  [PubMed]
     
    Lipscomb AB, and Anderson AF: Tears of the anterior cruciate ligament in adolescents. J Bone Joint Surg Am,1986.68: 19-28, 6819  1986  [PubMed]
     
    Stadelmaier DM; Arnoczky SP; Dodds J; and Ross H: The effect of drilling and soft tissue grafting across open growth plates. A histologic study. Am J Sports Med,1995.23: 431-5, 23431  1995  [PubMed]
     
    Hulse DA, Shires PK. The stifle joint. In: Slatter D, editor. Textbook of small animal surgery. Philadelphia: WB Saunders; 1993. p 2203-4 
     
    Stanitski CL: Surgical reconstruction for symptomatic ACL insufficiency in skeletally immature athletes [letter]. Am J Sports Med,1994.22: 433, 22433  1994  [PubMed]
     
    Kannus P, and Järvinen M: Knee ligament injuries in adolescents. Eight year follow-up of conservative management. J Bone Joint Surg Br. ,1988.70: 772-6, 70772  1988  [PubMed]
     
    Janarv P; Nyström A; Werner S; and Hirsch G: Anterior cruciate ligament injuries in skeletally immature patients. J Pediatr Orthop,1996.16: 673-7, 16673  1996  [PubMed]
     
    Parker AW; Drez D Jr; and Cooper JL: Anterior cruciate ligament injuries in patients with open physes. Am J Sports Med,1994.22: 44-7, 2244  1994  [PubMed]
     
    Brief LP: Anterior cruciate ligament reconstruction without drill holes. Arthroscopy,1991.7: 350-7, 7350  1991  [PubMed]
     
    Nakhostine M; Bollen SR; and Cross MJ: Reconstruction of mid-substance anterior rupture in adolescents with open physes. J Pediatr Orthop,1995.15: 286-7, 15286  1995  [PubMed]
     
    Andrews M; Noyes FR; and Barber-Westin SD: Anterior cruciate ligament allograft reconstruction in the skeletally immature athlete. Am J Sports Med,1994.22: 48-54, 2248  1994  [PubMed]
     
    Ogden JA. The uniqueness of growing bones. In: Rockwood CA Jr, Wilkins KE, King RE, editors. Fractures in children. 3rd ed. Philadelphia: JB Lippincott; 1984. p 1-86 
     
    Guanche CA. Personal communication, 1997 
     
    Koman JD, and Sanders JO: Valgus deformity after reconstruction of the anterior cruciate ligament in a skeletally immature patient. A case report. J Bone Joint Surg Am,1999.81: 711-5, 81711  1999  [PubMed]
     
    Arkin AM, and Katz JF: The effects of pressure on epiphyseal growth. The mechanism of plasticity of growing bone. J Bone Joint Surg Am,1956.38: 1056-76, 381056  1956  [PubMed]
     
    Campbell CJ; Grisolia A; and Zanconato G: The effects produced in the cartilaginous epiphyseal plate of immature dogs by experimental surgical traumata. J Bone Joint Surg Am,1959.41: 1221-42, 411221  1959  [PubMed]
     
    Österman K: Healing of large surgical defects of the epiphyseal plate. An experimental study. Clin Orthop,1994.300: 264-8, 300264  1994  [PubMed]
     
    Siffert RS: The effect of staples and longitudinal wires on epiphyseal growth. An experimental study. J Bone Joint Surg Am,1956.38: 1077-88, 381077  1956  [PubMed]
     
    Yasuda K; Tsujino J; Tanabe Y; and Kaneda K: Effects of initial graft tension on clinical outcome after anterior cruciate ligament reconstruction. Autogenous doubled hamstring tendons connected in series with polyester tapes. Am J Sports Med,1997.25: 99-106, 2599  1997  [PubMed]
     
    Guzzanti V; Falciglia F; Gigante A; and Fabbriciani C: The effect of intra-articular ACL reconstruction on the growth plates of rabbits. J Bone Joint Surg Br,1994.76: 960-3, 76960  1994  [PubMed]
     
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