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Growth Abnormalities Following Anterior Cruciate Ligament Reconstruction in the Skeletally Immature Patient: A Systematic Review
Systematic Review
Growth Abnormalities Following Anterior Cruciate Ligament Reconstruction in the Skeletally Immature Patient: A Systematic Review Michael J. Collins, M.D., Thomas A. Arns, B.S., Timothy Leroux, M.D., F.R.C.S.C., Austin Black, Randy Mascarenhas, M.D., F.R.C.S.C., Bernard R. Bach Jr., M.D., and Brian Forsythe, M.D.
Purpose: To identify all reported cases of growth disturbances after anterior cruciate ligament (ACL) reconstruction in patients with open growth plates and analyze trends with respect to different surgical techniques, graft choices, and methods of fixation. Methods: A systematic literature review was conducted using the MEDLINE, EMBASE, and SCOPUS databases with the following term: “((anterior cruciate ligament OR ACL) AND ((((immature) OR growth plates) OR physes) OR pediatric)).” Only studies that evaluated ACL reconstruction in patients with open growth plates and reported angular malformations or limb length discrepancy were included. Data were extracted, including patient characteristics, surgical technique, and postoperative growth disturbance. Results: Twenty-one studies containing 39 patients with growth abnormalities were included in the review. Mean chronological age was 13 years, and 89% of patients were male. Overall, there were 16 cases of angular malformations and 29 cases of limb length discrepancy. The most common angular malformation was genu valgum (81%, n ¼ 13; mean of 6.5 ). The most common surgical technique on the tibia and femur was transphyseal (54%, and 77% respectively), and the most common graft used was hamstring autograft (58%). Among patients with limb length discrepancy, overgrowth was most common (62%, n ¼ 18; mean of 13 mm). Interestingly, we observed that 50% of patients with overgrowth underwent a physeal-sparing technique, whereas 64% of patients with shortening underwent a transphyseal technique. Conclusions: At present, there are 21 studies reporting 39 patients with growth abnormalities in the current literature, of which 29 cases were of limb length discrepancy and 16 of angular malformation. Of the 29 cases of limb length discrepancy, limb overgrowth accounted for 62% of cases. Perhaps most interestingly, physeal-sparing techniques were performed in 25% of the cases of angular malformation and 47% cases of limb length discrepancy, despite the commonly held belief that this technique mitigates the risks of ACL reconstruction by not violating the growth plate. According to this study, it is clear that growth abnormalities after ACL reconstruction in the skeletally immature patient are underreported, and our current understanding of the etiology of these abnormalities is limited. Level of Evidence: Level IV, systematic review of Level II to IV studies.
From the Department of Orthopedic Surgery, Rush University Medical Center (M.J.C., T.A.A., T.L., A.B., B.R.B., B.F.), Chicago, Illinois; and Department of Orthopaedic Surgery, The University of Texas Health Science Center at Houston (R.M.), Houston, Texas, U.S.A. The authors report the following potential conflict of interest or source of funding: B.R.B. receives support from the American Orthopaedic Society for Sports Medicine for board membership; grants from Arthrex, CONMED Linvatec, DJ Orthopaedics, Ossur; Smith & Nephew; Tornier; royalties from SLACK. B.F. receives support from Sonoma for consultancy; grants from Stryker; payments for lecture from Arthrosurface and Sonoma; and stock/stock options in Jace Medical. This is an IRB exempt study performed at Rush University Medical Center in Chicago, Illinois, U.S.A. Received February 4, 2016; accepted February 22, 2016. Address correspondence to Brian Forsythe, M.D., Department of Orthopaedic Surgery, Rush University Medical Center, 1611 W. Harrison St., Suite 300, Chicago, IL 60612, U.S.A. E-mail: [email protected] Ó 2016 by the Arthroscopy Association of North America 0749-8063/16116/$36.00 http://dx.doi.org/10.1016/j.arthro.2016.02.025
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t has been estimated that 0.5% to 3.0% of anterior cruciate ligament (ACL) injuries arise in the pediatric skeletally immature population and controversy exists regarding optimal treatment.1,2 A 2002 survey of the Herodicus Society and the ACL Study Group of 178 international experts in sports medicine discovered 84% favored initial nonoperative treatment in an 8year-old child whereas 64% favored nonoperative treatment in a 13-year-old.3 However, more recent studies have reported poor outcomes after initial nonoperative management of ACL injuries in the pediatric population, and there has been a trend to manage these injuries operatively to improve both function and stability.4-7 Despite the increasing trend to reconstruct the injured ACL in the pediatric population, there is concern regarding the potential for growth disturbance in this
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skeletally immature population, and there is evidence that the risk of growth disturbance impacts treatment decisions.3,4,8 Guzzanti et al.9 reported on 21 skeletally immature rabbits after transphyseal ACL reconstruction, in which they observed 1 growth disturbance and 2 cases of angular malalignment. A separate study on the effect of drilling across growth plates in canines showed patterns of physeal arrest.10 However, in human subjects, cases of limb length discrepancy or angular malalignment have been infrequently reported. The purpose of this study was to identify all reported cases of growth disturbances after ACL reconstruction in patients with open growth plates and to analyze trends with respect to different surgical techniques, graft choice, and methods of fixation. We hypothesized that growth abnormalities will be more commonly observed in patients after transphyseal techniques.
discrepancy was chosen based on a study by Rush and Steiner, which discovered that 77% of normal subjects had a limb length discrepancy of 7 mm or less.34 A 3 threshold for angular malformation was chosen based on a study by Seil and Robert.35 In addition, the values 1 cm and 3 have been used in a prior analysis on outcomes of pediatric ACL reconstruction.36 From the 21 selected manuscripts, we were able to report on 39 reported individual cases of growth abnormalities after pediatric ACL surgery. These cases were then compiled into an Excel file format (Microsoft Windows, Spreadsheet, Trialware 2015) so the data could be easily summarized using mean, median, and mode statistical calculations. Other descriptive statistics used to summarize the data included ranges and measures of spread, such as variance and standard deviation.
Methods
Overall, we identified 21 studies, published between 1986 and 2015, that reported a total of 39 patients with growth abnormalities, among which were 29 cases of limb length discrepancy and 16 of angular malformation (6 cases contained both an angular malformation and limb length discrepancy). There were a total of 313 patients included across 21 case reports, case series, and cohort studies reporting on growth abnormalities, for an overall percentage of 13% (39/313) of included patients with angular malformation or limb length discrepancy. Across all included studies, demographic data and baseline characteristics were inconsistently reported. Of those studies that did report demographic data, 20 of 21 (95%) studies reported average age, which was 13.12 (SD 2.04) years, and 15 of 21 (71%) studies reported sex, which was 89% male. Demographic data from all included studies are listed in Table 2. There was wide variability in surgical technique across all included studies. The most common graft used was hamstring autograft (58%), followed by quadriceps tendon autograft (13%) and patella tendon autograft (13%). The most common surgical techniques on the femur were transphyseal (54%), over the top (18%), and all-epiphyseal (15%). On the tibia, the most common surgical techniques were transphyseal (77%), extra-articular (19%), and all-epiphyseal (10%). The most common method of fixation on the femur was suspensory (52%), whereas a screw and post was the most common fixation method on the tibia (55%).
We performed a systematic review of the literature using the MEDLINE, EMBASE, and SCOPUS databases. The search strategy employed consisted of the following keywords and phrases: “immature,” “growth plates,” “physes,” “pediatric,” “anterior cruciate ligament,” and “ACL” set into the following Boolean string formula (((((immature) OR growth plates) OR physes) OR pediatric)) AND ((anterior cruciate ligament) OR ACL). There were no restrictions placed on date of publication or Level of Evidence (Levels I to V). This search strategy generated a total of 551 articles. After excluding articles that were based on systematic reviews, meta-analyses, non-English scripts, and animal- and/or cadaver-based models, 188 articles remained to be critically evaluated. Of the remaining articles, 2 authors (M.J.C., T.A.A.) independently looked at each publication and selected those that reported limb length discrepancy and/or angular malformations after ACL reconstruction in patients with open growth plates. Based on these criteria, 163 articles were excluded, leaving a total of 25 articles reporting incidences of growth abnormalities. After selection of these 25 articles, the reference lists and citations were cross-referenced between studies to confirm that no article was missed from our initial search. There were no articles added after cross validation. Four articles were unable to be included in this study because of incomplete data, leaving 21 articles to report on (Fig 1). All 21 manuscripts (Table 1) were then investigated for data determinants pertaining to individual patient demographics (chronological age and sex), surgical technique, graft type, drilling location, and fixation method, as well as data outcomes reporting on coronal and sagittal deformities, lengthening and shortening of limbs, and reoperation rates. Our threshold to classify a limb length discrepancy and angular malformation was 1 cm and 3 between the operated and nonoperated limbs, respectively. A 1 cm threshold for limb length
Results
Limb Length Discrepancy Overall, there were 29 cases of limb length discrepancy, of which 18 cases (62%) were lengthening by an average of 13.27 mm (SD 4.83) and 11 cases (38%) were shortening by an average of 17 mm (SD 10.2). Among cases of limb lengthening, a physeal-sparing technique (n ¼ 9, 50%)2,11-13,16,25,27 and a transphyseal technique (n ¼ 8, 44%)15,25,31 were used at nearly equal rates (in 1
GROWTH ABNORMALITIES FOLLOWING ACLR
3
Fig 1. PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) diagram showing the results of application of the study algorithm to the number of studies included. (AM, angular malformation; LLD, limb length discrepancy.)
case, technique was not specified).33 On the other hand, we noted that most cases of limb shortening used a transphyseal technique on both the femur and tibia (7/ 11, 64%),17,30,31 whereas the remaining 4 cases used an all epiphyseal technique (n ¼ 1)2 or an over-the-top technique (n ¼ 3).11,28,29 Across all cases of limb length discrepancy, the most common method of fixation was suspensory (n ¼ 11, 38%) for the femur and suture and screws on the tibia (n ¼ 13, 45%). Data for all cases of limb length discrepancy are summarized in Table 3. Among 19 cases of physeal-sparing techniques used on the femur, there were 13 cases of limb length discrepancy. Limb lengthening was more common (n ¼ 9, 69%),2,11-13,16,25,27 with an average overgrowth of 14 mm (SD 3.5). Among 23 cases employing a transphyseal technique on the femur, there were 15 cases of limb length discrepancy, with overgrowth occurring in 8 patients (53%)15,25,31 and shortening in 7 patients (47%).17,30,31
Angular Malalignment Overall, there were 16 cases of angular malformation, of which 13 cases resulted in valgus malalignment with an average difference of 6.5 (SD 3.3) between the operated and nonoperated extremities. There were 3 reported cases of varus malalignment with an average difference of 8 (SD 5.8) between the operated and nonoperated extremities. The most common technique on the femur was transphyseal (n ¼ 8, 50%),17-19,21,22,30 followed by over the top (n ¼ 3, 19%),4,13,29 extraarticular (n ¼ 3, 19%),12,28 and epiphyseal (n ¼ 2, 13%).16,20 The most common graft choice was hamstring autograft (n ¼ 8, 50%), followed by patellar tendon autograft (n ¼ 3, 19%). The most common method of fixation was suspensory (n ¼ 8, 50%) for the femur, and screw and post (n ¼ 8, 50%) on the tibia. Data for all cases of angular malformation are summarized in Table 4. A summary of key data is included in Table 5.
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Table 1. List of Included Studies Author Andrews et al.11 Bonnard et al.12 Chotel et al.13 Cruz et al.14 Henry et al.4 Kim et al.15 Koch et al.16 Kohl et al.17 Koman et al.18 Kumar et al.19 Lawrence et al.20 Lemaitre et al.21 Liddle et al.22 Lipscomb et al.2 Lo et al.23 Mauch et al.24 McIntosh et al.25 Nakhostine et al.26 Nawabi et al.27 Robert et al.28 Rozbruch et al.29 Shifflett et al.30 Seon et al.31 Streich et al.32 Zimmerman et al.33
Journal American Journal of Sports Medicine Journal of Bone and Joint Surgery (Br) Knee Surgery, Sports Traumatology, and Arthroscopy Journal of Pediatric Orthopaedics Knee Surgery, Sports Traumatology, and Arthroscopy Knee Surgery & Related Research Knee Surgery, Sports Traumatology, and Arthroscopy The Knee Journal of Bone and Joint Surgery Journal of Bone and Joint Surgery Journal of Bone and Joint Surgery Orthopaedics & Traumatology: Surgery & Research Journal of Bone and Joint Surgery (Br) Journal of Bone and Joint Surgery Arthroscopy Sports Medicine Arthroscopy Rehabilitation Therapy Technology Arthroscopy Journal of Pediatric Orthopaedics American Journal of Sports Medicine Knee Surgery, Sports Traumatology, and Arthroscopy American Journal of Sports Medicine Journal of Pediatric Orthopaedics Journal of Korean Medical Science Knee Surgery, Sports Traumatology, and Arthroscopy Journal of Pediatric Orthopaedics
Discussion The most important findings of this study are that we identified 39 reported cases of growth abnormalities after ACL reconstruction in pediatric patients across 21 studies. Of these growth abnormalities, there were 29 cases of limb length discrepancy, of which 62% were limb lengthening. In contrast to our hypothesis, 25% of angular malformation cases and 47% of limb length discrepancy cases were observed in physeal-sparing ACL reconstructions. The incidence of growth abnormalities after ACL reconstruction in patients with open growth plates is difficult to truly assess, as many reported incidences in the literature are case series or case reports. However, prior studies have looked at growth deformities in adolescents after ACL reconstruction. A 2010 metaanalysis by Frosch et al.36 sought to analyze risks of operative treatment of ACL ruptures in adolescents. Their search yielded only 9 articles with cases of growth abnormalities in contrast to the 21 found in this study, despite using the same cut-off values of 1 cm of limb length discrepancy and 3 of angular malformation. This can be partially explained by the Frosch paper looking only at case series, cohort studies, and clinical trials between January 1980 and March 2009, whereas this analysis includes case reports and an additional 6 years of articles. Interestingly, their article discovered 8 angular malformations or limb length discrepancies out of 139 patients undergoing a physeal-sparing technique and 12 angular malformations or limb
Year of Publication 1994 2011 2010 2015 2009 2012 2014 2014 1999 2013 2011 2014 2008 1986 1997 2011 2006 1995 2014 2010 2013 2015 2005 2010 2015
Study Type Case series Retrospective cohort study Case series Case series Retrospective cohort study Case series Case series Case series Case report Case series Case report Case series Case series Case series Case series Case series Case series Case series Case series Case report Case report Case series Case series Prospective cohort study Case report
Level of Evidence IV III IV IV III IV IV IV IV IV IV IV IV IV IV IV IV IV IV IV IV IV IV II IV
length discrepancies out of 621 patients undergoing a transphyseal technique, for a relative risk of 0.34 in favor of transphyseal repair. A second article, from 2011, reviewed studies of ACL tears in skeletally immature patients with at least 6 months of follow-up.8 They only discovered 3 cases of angular malformation and 2 cases of limb length discrepancy, none of which occurred with physeal-sparing techniques. Our study was able to capture 39 incidences of angular malformation or limb length discrepancy, which represents all reported cases of growth abnormalities in the current literature. This can help to broaden our understanding of the factors that influence the occurrence of these deformities, or perhaps more importantly, address preconceived ideas regarding which surgical techniques give rise to these growth abnormalities. In this analysis, gender was reported in 27 of 39 cases (69%) of growth disturbances, with 24 patients (89%) being male. It has been reported that the incidence rate of ACL tears in females of high school age is at least 3-fold higher than their male counterparts.37 A separate study reporting gender in children aged 10 to 14 found 30 of 39 patients (76%) to be female.6 The high proportion of male patients with growth disturbances is surprising. This may be explained by a potential gender bias in reporting cases of growth disturbance versus the anecdotal nature of the report themselves. Additionally, the increased participation rates in sports, especially those that are in nature ballistic, potentially explain the disparity observed. Further research needs to be
Table 2. Summary of Data From Individual Studies Author Andrews et al.11 (1994) Bonnard et al.12 (2011)
2 103 56 25 12 15 1 32 1 13 17 24 49 16 1 23 1 1 4 11 31 1
7.0 12.1 10.0 16.4 12.1 12.8 14.3 11.3 14.0 12.0 10.0 15.0 10.5 12.0 12.6 14.5 12.0 15.0 15.5 11.0 10.0
Mean LLD Mean LLD No. of Angular Angular Femur Technique Tibia Technique No. of LLDs Shortening, cm Lengthening, cm Deformities Deformity ( ) Physeal-sparing Transphyseal 2 1.2 1.0 Physeal-sparing 1 1.5 2 4.0 (1 varus and 1 valgus) Physeal-sparing Transphyseal 2 1.3 1 6.0 valgus * * Physeal-sparing Physeal-sparing 1 Autograft/quadriceps Physeal-sparing Transphyseal 1 5.0 valgus * * Transphyseal Transphyseal 4 Allograft/hamstring Physeal-sparing 2 1.9 1 6.0 varus Autograft/quadriceps Transphyseal Transphyseal 3 1.6 1 6.0 valgus Transphyseal Transphyseal 1 14.0 valgus Transphyseal Transphyseal 1 6.2 valgus * * Allograft/tibialis Physeal-sparing Transphyseal 1 1 7.7 valgus Transphyseal Transphyseal 2 4.0 valgus Autograft/hamstring Transphyseal Transphyseal 1 5.0 valgus Physeal-sparing Transphyseal 2 2.0 1.3 Transphyseal Transphyseal * Autograft/quadriceps Transphyseal Transphyseal 1 valgus Transphyseal Transphyseal 1 1.5 Physeal-sparing Physeal-sparing 1 1.5 Autograft/hamstring Physeal-sparing Physeal-sparing 1 1.1 Physeal-sparing 1 1.0 1 13.0 valgus Allograft/Achilles Physeal-sparing Transphyseal 1 4.5 1 15.0 varus Autograft/hamstring Transphyseal Transphyseal 3 1.3 2 5.0 valgus Autograft/hamstring Transphyseal Transphyseal 4 1.0 1.0 * * Autograft/hamstring Transphyseal Transphyseal 1 1 2.8 Graft Type
GROWTH ABNORMALITIES FOLLOWING ACLR
Chotel et al.13 (2010) Cruz et al.14 (2015) Henry et al.4 (2009) Kim et al.15 (2012) Koch et al.16 (2014) Kohl et al.17 (2014) Koman et al.18 (1999) Kumar et al.19 (2013) Lawrence et al.20 (2011) Lemaitre et al.21 (2014) Liddle et al.22 (2008) Lipscomb et al.2 (1986) Lo et al.23 (1997) Mauch et al.24 (2011) McIntosh et al.25 (2006) Nakhostine et al.26 (1995) Nawabi et al.27 (2014) Robert et al.28 (2010) Rozbruch et al.29 (2013) Shifflett et al.30 (2015) Seon et al.31 (2005) Streich et al.32 (2010) Zimmerman et al.33 (2015)
No. of Mean Patients Age, y 8 13.5 57 12.2 -
LLD, limb length discrepancy. *Incomplete and/or missing data.
5
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Table 3. Data From Cases of Limb Length Discrepancies Author, Subject No. Andrews,11 1 Andrews,11 2 Bonnard,12 3 Chotel,13 1 Chotel,13 2 Kim,15 1
Graft Type Patella Iliotibial band Iliotibial band -
Kim,15 2
-
Kim,15 3
Femur Fixation Staples Staples Interference screw Suspensory
Transphyseal
Transphyseal
Suspensory
-
Transphyseal
Transphyseal
Suspensory
Kim,15 4
-
Transphyseal
Transphyseal
Suspensory
Koch,16 1 Koch,16 2 Kohl,17 1 Kohl,17 2 Kohl,17 3 Lipscomb,2 1 Lipscomb,2 2 McIntosh25 Nakhostine26 Nawabi27 Robert28 Rozbruch29 Schifflett,30 1
Hamstring Hamstring Quadriceps Quadriceps Quadriceps Hamstring Hamstring Hamstring Patella Achilles Hamstring
Physeal-sparing Physeal-sparing Transphyseal Transphyseal Transphyseal Physeal-sparing Physeal-sparing Transphyseal Physeal-sparing Physeal-sparing Physeal-sparing Physeal-sparing Transphyseal
Physeal-sparing Physeal-sparing Transphyseal Transphyseal Transphyseal Transphyseal Transphyseal Transphyseal Physeal-sparing Physeal-sparing Physeal-sparing Transphyseal Transphyseal
Suspensory Suspensory Screw and suture post Screw and suture post Screw and suture post Screw and suture post Screw and suture post Suspensory Screw and suture post Interference screw Staples Suspensory
Schifflett,30 2
Hamstring
Transphyseal
Transphyseal
Suspensory
Schifflett,30 4
Hamstring
Transphyseal
Transphyseal
Suspensory
Seon,31 1
Hamstring
Transphyseal
Transphyseal
Seon,31 2
Hamstring
Transphyseal
Transphyseal
Seon,31 3
Hamstring
Transphyseal
Transphyseal
Seon,31 4
Hamstring
Transphyseal
Transphyseal
Zimmerman33
Tibialis
-
-
Staples or interference screw Staples or interference screw Staples or interference screw Staples or interference screw Screw and suture post
Tibia Fixation Staples Staples Screw and suture post Staples Staples Staples or interference screw Staples or interference screw Staples or interference screw Staples or interference screw Screw and suture post Screw and suture post Screw and suture post Screw and suture post Screw and suture post Screw and suture post Screw and suture post Screw and suture post Staples Screw and suture post Screw and suture post Screw and suture post Suture and interference screw Suture and interference screw Suture and interference screw Staples or interference screw Staples or interference screw Staples or interference screw Staples or interference screw Screw and suture post
LLD Shortening, cm 1.2 -
LLD Lengthening, cm 1.0 1.5 1.5 1.0 1.0
-
1.0
-
-
1.0
-
-
1.0
1.8 1.0 2.0 2.0 1.0 4.5 1.4
2.1 1.6 1.3
1.4
-
-
1.0
-
7 valgus
-
1.0
-
-
1.0
-
-
1.0
-
1.0
-
-
-
2.8
-
1.5 1.5 1.1 -
Angular Deformity ( ) 6 valgus -
6 varus 6 valgus 13 valgus 15 varus -
M. J. COLLINS ET AL.
Tibia Technique Transphyseal Transphyseal Physeal-sparing Transphyseal Transphyseal Transphyseal
LLD, limb length discrepancy.
Femur Technique Physeal-sparing Physeal-sparing Physeal-sparing Physeal-sparing Physeal-sparing Transphyseal
Table 4. Data From Cases of Angular Deformities Graft Type Patella Patella Iliotibial band Quadriceps Hamstring Quadriceps Hamstring Hamstring Tibialis Hamstring Hamstring Hamstring Patella Achilles Hamstring Hamstring
Femur Technique Physeal-sparing Physeal-sparing Physeal-sparing Physeal-sparing Physeal-sparing Transphyseal Transphyseal Transphyseal Physeal-sparing Transphyseal Transphyseal Transphyseal Physeal-sparing Physeal-sparing Transphyseal Transphyseal
Tibia Technique Physeal-sparing Physeal-sparing Transphyseal Transphyseal Physeal-sparing Transphyseal Transphyseal Transphyseal Transphyseal Transphyseal Transphyseal Transphyseal Physeal-sparing Transphyseal Transphyseal Transphyseal
Femur Fixation Interference screw Interference screw Suspensory Screw and suture post Interference screw Suspensory Suspensory Suspensory Suspensory Suspensory Interference screw Staples Suspensory Suspensory
Tibia Fixation Screw and suture post Screw and suture post Staples Staples Screw and suture post Screw and suture post Staples Screw and suture post Staples Staples and interference screw Staples and interference screw Screw and suture post Screw and suture post Screw and suture post Suture and interference screw Suture and interference Screw
Degrees Valgus ( ) 4.0 6.0 5.0 6.0 14.0 6.2 7.7 4.0 4.0 5.0 13.0 3.1 6.9
Degrees Varus ( ) 4.0 6.0 15.0 -
Location of Angular Deformity Unspecified Unspecified Tibia Tibia Mainly femoral Unspecified Femur Femur Femur Femur Femur Unspecified Femur Tibia Femur and tibia Femur and tibia
Table 5. Summary of Key Data
Limb overgrowth
Number of Cases 18
Limb shortening
11
Varus malformation
3
Valgus malformation
13
Most Common TechniquedFemur Physeal-sparing (n ¼ 9)
Most Common TechniquedTibia Transphyseal (n ¼ 12)
Most Common FixationdFemur Suspensory (n ¼ 7)
Transphyseal (n ¼ 7)
Transphyseal (n ¼ 10)
Screw and suture post (n ¼ 4)
Physeal-sparing (n ¼ 3)
Physeal-sparing (n ¼ 2)
Transphyseal (n ¼ 8)
Transphyseal (n ¼ 11)
Interference screw, suspensory, staples (n ¼ 1 each) Suspensory (n ¼ 7)
Most Common FixationdTibia Screw and suture post (n ¼ 7) Screw and suture post (n ¼ 6) Screw and suture post (n ¼ 3) Screw and suture post (n ¼ 5)
Average Limb Length Discrepancy, mm 13.27
Average Angular Malformation ( ) -
17.0
-
-
8.3
-
6.5
GROWTH ABNORMALITIES FOLLOWING ACLR
Author, Subject No. Bonnard,12 1 Bonnard,12 2 Chotel,13 2 Henry4 Koch,16 1 Kohl,17 1 Koman18 Kumar19 Lawrence20 Lemaitre,21 1 Lemaitre,21 2 Liddle22 Robert28 Rozbruch29 Schifflett,30 3 Schifflett,30 4
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performed to investigate if males do indeed have a higher risk of growth disturbance after ACL reconstruction than females. In this analysis, 18 of 29 cases (62%) of limb length discrepancy were due to limb overgrowth after ACL reconstruction. In pediatric femoral shaft fractures, there is a risk of limb lengthening which is well documented.38-40 This has been attributed to increased vascularity in the distal femoral shaft as well as an increase in mitotic activity within the growth plates after mid-diaphyseal fractures.38 The theory is thought to be due to periosteal disruption, which occurs during ACL reconstruction with both physeal-sparing and transphyseal techniques. In this analysis, one study exploring limb overgrowth attributed this phenomenon as a possible explanation for the observed overgrowth.13 Importantly, periosteal disruption and increased vascularity occurs irrespective of surgical technique. In this analysis, physeal-sparing techniques, thought by many surgeons to be a safe alternative to transphyseal techniques, produced a similar number of limb overgrowth cases as did transphyseal techniques. Among 18 cases of limb overgrowth, physeal-sparing techniques were used in 9 cases (50%) and transphyseal was used in 8 cases (44%) (in 1 case, technique was not specified). Limb shortening was noted in 11 of 29 cases (38%) of limb length discrepancy within this analysis. A wellreported and potential cause of limb shortening has been the malplacement of bone blocks or hardware across the physis, resulting in premature growth arrest. In this analysis, Lipscomb et al.2 reported on a case of limb length discrepancy attributed to staples being placed across the femoral physis. Koman et al.18 attributed a case of angular malalignment to a cannulated screw crossing the femoral physis. Additionally, Mauch et al.24 attributed a case of procurvatum to malplacement of a bone block within the posterolateral femoral physis. Although this is a well-known potential cause of growth deformity after pediatric ACL reconstruction, in this analysis we only discovered 3 cases attributed to such causes. Although malplacement of hardware or bone blocks across the physis appears to be a factor that may lead to growth deformity, alternative reasons are more likely, such as drilling across the physis. In a study of 44 rabbits, it was discovered by Makela et al.41 that destruction of 7% of the crosssectional area of femoral growth plates (3.2-mm drill hole) lead to permanent growth disturbance and shortening of the limb. Results of this study have not been tested in humans, although drilling of the femoral tunnel at an oblique angle has been cited as a cause of growth disturbance after ACL reconstruction. Kohl et al.17 theorized that a likely cause of the growth disturbances in their study was due to the tunnel crossing the growth plate at an oblique angle, affecting a greater percentage of the physis. Unfortunately, few studies
report on the obliquity of their femoral tunnel. Perhaps more striking is our finding that just over half of the studies with limb shortening (8/11, 73%) had transphyseal femoral tunnels, used grafts with bone blocks, and/or used interference screws. This suggests that the current theories regarding tunnel placement and size, graft type and placement, and fixation type may not account for all of the causes of limb shortening. Future studies should be aimed at expanding our understanding of the risks associated with limb shortening after ACL reconstruction in skeletally immature patients. In this analysis, we identified 16 cases of angular malformation after ACL reconstruction on skeletally immature patients. The most common deformity seen was valgus malalignment (n ¼ 13, 81%; the remaining cases were varus deformity). Across all studies reporting on angular malformation, physeal-sparing techniques on the femur were employed equally as often as a transphyseal techniques. Many of the same risk factors that have been attributed to limb length discrepancy in the literature have also been reported in association with angular malformation deformities after ACL reconstruction in skeletally immature patients. Of the 16 cases with angular malformation, 4 cases were attributed to the tibial side and 8 to the femoral side, and the remaining 4 cases did not specify location of the partial growth arrest. Interestingly, of the 4 cases of angular malformation centered about the tibia, all employed a transphyseal technique on the tibia. On the other hand, among the 8 cases of angular malformation centered about the femur, 5 used a transphyseal technique on the femur whereas the remaining 3 used physeal-sparing techniques. Although we did observe that most of the cases of angular malformation arose in conjunction with a transphyseal technique, this was not exclusive as a quarter of all cases arose when a physealsparing technique was employed. Irrespective of technique, our findings suggest that surgeons must remain mindful of the physis to minimize secondary growth abnormalities. Limitations This analysis has several limitations. First, a survey of the Herodicus Society and ACL Study Group reported that 11% of respondents saw a growth abnormality after ACL reconstruction in a skeletally immature patient.3 However, given that only 39 cases were identified in the literature, it is likely that many cases may go unreported, which also suggests that there is a void in clinical research to enhance our understanding as to the etiology and risk factors for the development of these deformities. Second, there is no consensus in the literature as to what constitutes a clinically significant limb length discrepancy or angular malformation after ACL reconstruction in a skeletally immature patient. Variation in what is considered clinically significant would
GROWTH ABNORMALITIES FOLLOWING ACLR
impact the number of patients we included in this study; however, we attempted to set our inclusion parameters in line with past studies on this topic. Third, there were 4 studies comprising an additional 8 cases of limb length discrepancy reported in the literature that we were unable to include in this study due to incomplete data. These cases, indicated with an asterisk, are outlined in Table 2. Lastly, given the heterogeneity in the data we obtained from the current literature, we were unable to perform any meaningful statistics to identify risk factors and determine causality. As such, most of our current understanding pertaining to the etiology of growth abnormalities after ACL reconstruction in skeletally immature patients is based on theories generated from anatomic or animal studies, and future prospective studies are needed to enhance our understanding so that these devastating complications can be avoided.
Conclusions At present, there are 21 studies reporting 39 patients with growth abnormalities in the current literature, of which 29 cases of limb length discrepancy and 16 cases of angular malformation. Of the 29 cases of limb length discrepancy, limb overgrowth accounted for 62% of cases. Perhaps most interestingly, physeal-sparing techniques were performed in 25% of the cases of angular malformation and 47% cases of limb length discrepancy, despite the commonly held belief that this technique mitigates the risks of ACL reconstruction by not violating the growth plate. Based on this study, it is clear that growth abnormalities after ACL reconstruction in the skeletally immature patient are underreported, and our current understanding of the etiology of these abnormalities is limited.
References 1. McConkey MO, Bonasia DE, Amendola A. Pediatric anterior cruciate ligament reconstruction. Curr Rev Musculoskelet Med 2011;4:37-44. 2. Lipscomb AB, Anderson AF. Tears of the anterior cruciate ligament in adolescents. J Bone Joint Surg Am 1986;68: 19-28. 3. Kocher MS, Saxon HS, Hovis WD, Hawkins RJ. Management and complications of anterior cruciate ligament injuries in skeletally immature patients: survey of the Herodicus Society and The ACL Study Group. J Pediatr Orthop 2002;22:452-457. 4. Henry J, Chotel F, Chouteau J, Fessy MH, Berard J, Moyen B. Rupture of the anterior cruciate ligament in children: Early reconstruction with open physes or delayed reconstruction to skeletal maturity? Knee Surg Sports Traumatol Arthrosc 2009;17:748-755. 5. Smith TO, Davies L, Hing CB. Early versus delayed surgery for anterior cruciate ligament reconstruction: A systematic review and meta-analysis. Knee Surg Sports Traumatol Arthrosc 2010;18:304-311.
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6. Millett PJ, Willis AA, Warren RF. Associated injuries in pediatric and adolescent anterior cruciate ligament tears: Does a delay in treatment increase the risk of meniscal tear? Arthroscopy 2002;18:955-959. 7. Cassard X, Cavaignac E, Maubisson L, Bowen M. Anterior cruciate ligament reconstruction in children with a quadrupled semitendinosus graft: Preliminary results with minimum 2 years of follow-up. J Pediatr Orthop 2014;34: 70-77. 8. Vavken P, Murray MM. Treating anterior cruciate ligament tears in skeletally immature patients. Arthroscopy 2011;27:704-716. 9. Guzzanti V, Falciglia F, Gigante A, Fabbriciani C. The effect of intra-articular ACL reconstruction on the growth plates of rabbits. J Bone Joint Surg Br 1994;76:960-963. 10. Stadelmaier DM, Arnoczky SP, Dodds J, Ross H. The effect of drilling and soft tissue grafting across open growth plates. A histologic study. Am J Sports Med 1995;23: 431-435. 11. Andrews M, Noyes FR, Barber-Westin SD. Anterior cruciate ligament allograft reconstruction in the skeletally immature athlete. Am J Sports Med 1994;22:48-54. 12. Bonnard C, Fournier J, Babusiaux D, Planchenault M, Bergerault F, de Courtivron B. Physeal-sparing reconstruction of anterior cruciate ligament tears in children: Results of 57 cases using patellar tendon. J Bone Joint Surg Br 2011;93:542-547. 13. Chotel F, Henry J, Seil R, Chouteau J, Moyen B, Berard J. Growth disturbances without growth arrest after ACL reconstruction in children. Knee Surg Sports Traumatol Arthrosc 2010;18:1496-1500. 14. Cruz AI Jr, Fabricant PD, McGraw M, Rozell JC, Ganley TJ, Wells L. All-epiphyseal ACL reconstruction in children: Review of safety and early complications. J Pediatr Orthop July 17, 2015 [Epub ahead of print]. 15. Kim SJ, Shim DW, Park KW. Functional outcome of transphyseal reconstruction of the anterior cruciate ligament in skeletally immature patients. Knee Surg Relat Res 2012;24:173-179. 16. Koch PP, Fucentese SF, Blatter SC. Complications after epiphyseal reconstruction of the anterior cruciate ligament in prepubescent children. Knee Surg Sports Traumatol Arthrosc October 26, 2014 [Epub ahead of print]. 17. Kohl S, Stutz C, Decker S, et al. Mid-term results of transphyseal anterior cruciate ligament reconstruction in children and adolescents. Knee 2014;21:80-85. 18. Koman JD, 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;81:711-715. 19. Kumar S, Ahearne D, Hunt DM. Transphyseal anterior cruciate ligament reconstruction in the skeletally immature: Follow-up to a minimum of sixteen years of age. J Bone Joint Surg Am 2013;95:e1. 20. Lawrence JT, West RL, Garrett WE. Growth disturbance following ACL reconstruction with use of an epiphyseal femoral tunnel: A case report. J Bone Joint Surg Am 2011;93:e39. 21. Lemaitre G, Salle de Chou E, Pineau V, et al. ACL reconstruction in children: A transphyseal technique. Orthop Traumatol Surg Res 2014;100:S261-S265 (suppl).
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22. Liddle AD, Imbuldeniya AM, Hunt DM. Transphyseal reconstruction of the anterior cruciate ligament in prepubescent children. J Bone Joint Surg Br 2008;90: 1317-1322. 23. Lo IK, Kirkley A, Fowler PJ, Miniaci A. The outcome of operatively treated anterior cruciate ligament disruptions in the skeletally immature child. Arthroscopy 1997;13: 627-634. 24. Mauch C, Arnold MP, Wirries A, Mayer RR, Friederich NF, Hirschmann MT. Anterior cruciate ligament reconstruction using quadriceps tendon autograft for adolescents with open physesdA technical note. Sports Med Arthrosc Rehabil Ther Technol 2011;3:7. 25. McIntosh AL, Dahm DL, Stuart MJ. Anterior cruciate ligament reconstruction in the skeletally immature patient. Arthroscopy 2006;22:1325-1330. 26. Nakhostine M, Bollen SR, Cross MJ. Reconstruction of mid-substance anterior cruciate rupture in adolescents with open physes. J Pediatr Orthop 1995;15:286-287. 27. Nawabi DH, Jones KJ, Lurie B, Potter HG, Green DW, Cordasco FA. All-inside, physeal-sparing anterior cruciate ligament reconstruction does not significantly compromise the physis in skeletally immature athletes: A postoperative physeal magnetic resonance imaging analysis. Am J Sports Med 2014;42:2933-2940. 28. Robert HE, Casin C. Valgus and flexion deformity after reconstruction of the anterior cruciate ligament in a skeletally immature patient. Knee Surg Sports Traumatol Arthrosc 2010;18:1369-1373. 29. Rozbruch SR, Fryman C, Schachter LF, Bigman D, Marx RG. Growth arrest of the tibia after anterior cruciate ligament reconstruction: Lengthening and deformity correction with the Taylor Spatial Frame. Am J Sports Med 2013;41:1636-1641. 30. Shifflett GD, Green DW, Widmann RF, Marx RG. Growth arrest following ACL reconstruction with hamstring autograft in skeletally immature patients: A review of 4 cases. J Pediatr Orthop April 6, 2015 [Epub ahead of print].
31. Seon JK, Song EK, Yoon TR, Park SJ. Transphyseal reconstruction of the anterior cruciate ligament using hamstring autograft in skeletally immature adolescents. J Korean Med Sci 2005;20:1034-1038. 32. Streich NA, Barie A, Gotterbarm T, Keil M, Schmitt H. Transphyseal reconstruction of the anterior cruciate ligament in prepubescent athletes. Knee Surg Sports Traumatol Arthrosc 2010;18:1481-1486. 33. Zimmerman LJ, Jauregui JJ, Riis JF, Tuten HR. Symmetric limb overgrowth following anterior cruciate ligament reconstruction in a skeletally immature patient. J Pediatr Orthop B 2015;24:530-534. 34. Rush WA, Steiner HA. A study of lower extremity length inequality. Am J Roentgenol Radium Ther 1946;56:616-623. 35. Seil PDR, Robert H. VKB-Plastik bei offenen Wachstumsfugen. Arthroskopie 2005;18:48-52. 36. Frosch KH, Stengel D, Brodhun T, et al. Outcomes and risks of operative treatment of rupture of the anterior cruciate ligament in children and adolescents. Arthroscopy 2010;26:1539-1550. 37. Prodromos CC, Han Y, Rogowski J, Joyce B, Shi K. A metaanalysis of the incidence of anterior cruciate ligament tears as a function of gender, sport, and a knee injury-reduction regimen. Arthroscopy 2007;23:1320-1325. e1326. 38. Ashraf N, Meyer MH, Frick S, Meyer RA Jr. Evidence for overgrowth after midfemoral fracture via increased RNA for mitosis. Clin Orthop Relat Res 2007;454:214-222. 39. Sulaiman AR, Joehaimy J, Iskandar MA, Anwar Hau M, Ezane AM, Faisham WI. Femoral overgrowth following plate fixation of the fractured femur in children. Singapore Med J 2006;47:684-687. 40. Jawish R, Kahwaji A, Dagher G. Overgrowth of femoral fractures in childhood. Rev Chir Orthop Reparatrice Appar Mot 2003;89:404-406 [in French]. 41. Makela EA, Vainionpaa S, Vihtonen K, Mero M, Rokkanen P. The effect of trauma to the lower femoral epiphyseal plate. An experimental study in rabbits. J Bone Joint Surg Br 1988;70:187-191.
Growth Abnormalities Following Anterior Cruciate Ligament Reconstruction in the Skeletally Immature Patient: A Systematic Review Michael J. Collins, M.D., Thomas A. Arns, B.S., Timothy Leroux, M.D., F.R.C.S.C., Austin Black, Randy Mascarenhas, M.D., F.R.C.S.C., Bernard R. Bach Jr., M.D., and Brian Forsythe, M.D.
Purpose: To identify all reported cases of growth disturbances after anterior cruciate ligament (ACL) reconstruction in patients with open growth plates and analyze trends with respect to different surgical techniques, graft choices, and methods of fixation. Methods: A systematic literature review was conducted using the MEDLINE, EMBASE, and SCOPUS databases with the following term: “((anterior cruciate ligament OR ACL) AND ((((immature) OR growth plates) OR physes) OR pediatric)).” Only studies that evaluated ACL reconstruction in patients with open growth plates and reported angular malformations or limb length discrepancy were included. Data were extracted, including patient characteristics, surgical technique, and postoperative growth disturbance. Results: Twenty-one studies containing 39 patients with growth abnormalities were included in the review. Mean chronological age was 13 years, and 89% of patients were male. Overall, there were 16 cases of angular malformations and 29 cases of limb length discrepancy. The most common angular malformation was genu valgum (81%, n ¼ 13; mean of 6.5 ). The most common surgical technique on the tibia and femur was transphyseal (54%, and 77% respectively), and the most common graft used was hamstring autograft (58%). Among patients with limb length discrepancy, overgrowth was most common (62%, n ¼ 18; mean of 13 mm). Interestingly, we observed that 50% of patients with overgrowth underwent a physeal-sparing technique, whereas 64% of patients with shortening underwent a transphyseal technique. Conclusions: At present, there are 21 studies reporting 39 patients with growth abnormalities in the current literature, of which 29 cases were of limb length discrepancy and 16 of angular malformation. Of the 29 cases of limb length discrepancy, limb overgrowth accounted for 62% of cases. Perhaps most interestingly, physeal-sparing techniques were performed in 25% of the cases of angular malformation and 47% cases of limb length discrepancy, despite the commonly held belief that this technique mitigates the risks of ACL reconstruction by not violating the growth plate. According to this study, it is clear that growth abnormalities after ACL reconstruction in the skeletally immature patient are underreported, and our current understanding of the etiology of these abnormalities is limited. Level of Evidence: Level IV, systematic review of Level II to IV studies.
From the Department of Orthopedic Surgery, Rush University Medical Center (M.J.C., T.A.A., T.L., A.B., B.R.B., B.F.), Chicago, Illinois; and Department of Orthopaedic Surgery, The University of Texas Health Science Center at Houston (R.M.), Houston, Texas, U.S.A. The authors report the following potential conflict of interest or source of funding: B.R.B. receives support from the American Orthopaedic Society for Sports Medicine for board membership; grants from Arthrex, CONMED Linvatec, DJ Orthopaedics, Ossur; Smith & Nephew; Tornier; royalties from SLACK. B.F. receives support from Sonoma for consultancy; grants from Stryker; payments for lecture from Arthrosurface and Sonoma; and stock/stock options in Jace Medical. This is an IRB exempt study performed at Rush University Medical Center in Chicago, Illinois, U.S.A. Received February 4, 2016; accepted February 22, 2016. Address correspondence to Brian Forsythe, M.D., Department of Orthopaedic Surgery, Rush University Medical Center, 1611 W. Harrison St., Suite 300, Chicago, IL 60612, U.S.A. E-mail: [email protected] Ó 2016 by the Arthroscopy Association of North America 0749-8063/16116/$36.00 http://dx.doi.org/10.1016/j.arthro.2016.02.025
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t has been estimated that 0.5% to 3.0% of anterior cruciate ligament (ACL) injuries arise in the pediatric skeletally immature population and controversy exists regarding optimal treatment.1,2 A 2002 survey of the Herodicus Society and the ACL Study Group of 178 international experts in sports medicine discovered 84% favored initial nonoperative treatment in an 8year-old child whereas 64% favored nonoperative treatment in a 13-year-old.3 However, more recent studies have reported poor outcomes after initial nonoperative management of ACL injuries in the pediatric population, and there has been a trend to manage these injuries operatively to improve both function and stability.4-7 Despite the increasing trend to reconstruct the injured ACL in the pediatric population, there is concern regarding the potential for growth disturbance in this
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skeletally immature population, and there is evidence that the risk of growth disturbance impacts treatment decisions.3,4,8 Guzzanti et al.9 reported on 21 skeletally immature rabbits after transphyseal ACL reconstruction, in which they observed 1 growth disturbance and 2 cases of angular malalignment. A separate study on the effect of drilling across growth plates in canines showed patterns of physeal arrest.10 However, in human subjects, cases of limb length discrepancy or angular malalignment have been infrequently reported. The purpose of this study was to identify all reported cases of growth disturbances after ACL reconstruction in patients with open growth plates and to analyze trends with respect to different surgical techniques, graft choice, and methods of fixation. We hypothesized that growth abnormalities will be more commonly observed in patients after transphyseal techniques.
discrepancy was chosen based on a study by Rush and Steiner, which discovered that 77% of normal subjects had a limb length discrepancy of 7 mm or less.34 A 3 threshold for angular malformation was chosen based on a study by Seil and Robert.35 In addition, the values 1 cm and 3 have been used in a prior analysis on outcomes of pediatric ACL reconstruction.36 From the 21 selected manuscripts, we were able to report on 39 reported individual cases of growth abnormalities after pediatric ACL surgery. These cases were then compiled into an Excel file format (Microsoft Windows, Spreadsheet, Trialware 2015) so the data could be easily summarized using mean, median, and mode statistical calculations. Other descriptive statistics used to summarize the data included ranges and measures of spread, such as variance and standard deviation.
Methods
Overall, we identified 21 studies, published between 1986 and 2015, that reported a total of 39 patients with growth abnormalities, among which were 29 cases of limb length discrepancy and 16 of angular malformation (6 cases contained both an angular malformation and limb length discrepancy). There were a total of 313 patients included across 21 case reports, case series, and cohort studies reporting on growth abnormalities, for an overall percentage of 13% (39/313) of included patients with angular malformation or limb length discrepancy. Across all included studies, demographic data and baseline characteristics were inconsistently reported. Of those studies that did report demographic data, 20 of 21 (95%) studies reported average age, which was 13.12 (SD 2.04) years, and 15 of 21 (71%) studies reported sex, which was 89% male. Demographic data from all included studies are listed in Table 2. There was wide variability in surgical technique across all included studies. The most common graft used was hamstring autograft (58%), followed by quadriceps tendon autograft (13%) and patella tendon autograft (13%). The most common surgical techniques on the femur were transphyseal (54%), over the top (18%), and all-epiphyseal (15%). On the tibia, the most common surgical techniques were transphyseal (77%), extra-articular (19%), and all-epiphyseal (10%). The most common method of fixation on the femur was suspensory (52%), whereas a screw and post was the most common fixation method on the tibia (55%).
We performed a systematic review of the literature using the MEDLINE, EMBASE, and SCOPUS databases. The search strategy employed consisted of the following keywords and phrases: “immature,” “growth plates,” “physes,” “pediatric,” “anterior cruciate ligament,” and “ACL” set into the following Boolean string formula (((((immature) OR growth plates) OR physes) OR pediatric)) AND ((anterior cruciate ligament) OR ACL). There were no restrictions placed on date of publication or Level of Evidence (Levels I to V). This search strategy generated a total of 551 articles. After excluding articles that were based on systematic reviews, meta-analyses, non-English scripts, and animal- and/or cadaver-based models, 188 articles remained to be critically evaluated. Of the remaining articles, 2 authors (M.J.C., T.A.A.) independently looked at each publication and selected those that reported limb length discrepancy and/or angular malformations after ACL reconstruction in patients with open growth plates. Based on these criteria, 163 articles were excluded, leaving a total of 25 articles reporting incidences of growth abnormalities. After selection of these 25 articles, the reference lists and citations were cross-referenced between studies to confirm that no article was missed from our initial search. There were no articles added after cross validation. Four articles were unable to be included in this study because of incomplete data, leaving 21 articles to report on (Fig 1). All 21 manuscripts (Table 1) were then investigated for data determinants pertaining to individual patient demographics (chronological age and sex), surgical technique, graft type, drilling location, and fixation method, as well as data outcomes reporting on coronal and sagittal deformities, lengthening and shortening of limbs, and reoperation rates. Our threshold to classify a limb length discrepancy and angular malformation was 1 cm and 3 between the operated and nonoperated limbs, respectively. A 1 cm threshold for limb length
Results
Limb Length Discrepancy Overall, there were 29 cases of limb length discrepancy, of which 18 cases (62%) were lengthening by an average of 13.27 mm (SD 4.83) and 11 cases (38%) were shortening by an average of 17 mm (SD 10.2). Among cases of limb lengthening, a physeal-sparing technique (n ¼ 9, 50%)2,11-13,16,25,27 and a transphyseal technique (n ¼ 8, 44%)15,25,31 were used at nearly equal rates (in 1
GROWTH ABNORMALITIES FOLLOWING ACLR
3
Fig 1. PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) diagram showing the results of application of the study algorithm to the number of studies included. (AM, angular malformation; LLD, limb length discrepancy.)
case, technique was not specified).33 On the other hand, we noted that most cases of limb shortening used a transphyseal technique on both the femur and tibia (7/ 11, 64%),17,30,31 whereas the remaining 4 cases used an all epiphyseal technique (n ¼ 1)2 or an over-the-top technique (n ¼ 3).11,28,29 Across all cases of limb length discrepancy, the most common method of fixation was suspensory (n ¼ 11, 38%) for the femur and suture and screws on the tibia (n ¼ 13, 45%). Data for all cases of limb length discrepancy are summarized in Table 3. Among 19 cases of physeal-sparing techniques used on the femur, there were 13 cases of limb length discrepancy. Limb lengthening was more common (n ¼ 9, 69%),2,11-13,16,25,27 with an average overgrowth of 14 mm (SD 3.5). Among 23 cases employing a transphyseal technique on the femur, there were 15 cases of limb length discrepancy, with overgrowth occurring in 8 patients (53%)15,25,31 and shortening in 7 patients (47%).17,30,31
Angular Malalignment Overall, there were 16 cases of angular malformation, of which 13 cases resulted in valgus malalignment with an average difference of 6.5 (SD 3.3) between the operated and nonoperated extremities. There were 3 reported cases of varus malalignment with an average difference of 8 (SD 5.8) between the operated and nonoperated extremities. The most common technique on the femur was transphyseal (n ¼ 8, 50%),17-19,21,22,30 followed by over the top (n ¼ 3, 19%),4,13,29 extraarticular (n ¼ 3, 19%),12,28 and epiphyseal (n ¼ 2, 13%).16,20 The most common graft choice was hamstring autograft (n ¼ 8, 50%), followed by patellar tendon autograft (n ¼ 3, 19%). The most common method of fixation was suspensory (n ¼ 8, 50%) for the femur, and screw and post (n ¼ 8, 50%) on the tibia. Data for all cases of angular malformation are summarized in Table 4. A summary of key data is included in Table 5.
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Table 1. List of Included Studies Author Andrews et al.11 Bonnard et al.12 Chotel et al.13 Cruz et al.14 Henry et al.4 Kim et al.15 Koch et al.16 Kohl et al.17 Koman et al.18 Kumar et al.19 Lawrence et al.20 Lemaitre et al.21 Liddle et al.22 Lipscomb et al.2 Lo et al.23 Mauch et al.24 McIntosh et al.25 Nakhostine et al.26 Nawabi et al.27 Robert et al.28 Rozbruch et al.29 Shifflett et al.30 Seon et al.31 Streich et al.32 Zimmerman et al.33
Journal American Journal of Sports Medicine Journal of Bone and Joint Surgery (Br) Knee Surgery, Sports Traumatology, and Arthroscopy Journal of Pediatric Orthopaedics Knee Surgery, Sports Traumatology, and Arthroscopy Knee Surgery & Related Research Knee Surgery, Sports Traumatology, and Arthroscopy The Knee Journal of Bone and Joint Surgery Journal of Bone and Joint Surgery Journal of Bone and Joint Surgery Orthopaedics & Traumatology: Surgery & Research Journal of Bone and Joint Surgery (Br) Journal of Bone and Joint Surgery Arthroscopy Sports Medicine Arthroscopy Rehabilitation Therapy Technology Arthroscopy Journal of Pediatric Orthopaedics American Journal of Sports Medicine Knee Surgery, Sports Traumatology, and Arthroscopy American Journal of Sports Medicine Journal of Pediatric Orthopaedics Journal of Korean Medical Science Knee Surgery, Sports Traumatology, and Arthroscopy Journal of Pediatric Orthopaedics
Discussion The most important findings of this study are that we identified 39 reported cases of growth abnormalities after ACL reconstruction in pediatric patients across 21 studies. Of these growth abnormalities, there were 29 cases of limb length discrepancy, of which 62% were limb lengthening. In contrast to our hypothesis, 25% of angular malformation cases and 47% of limb length discrepancy cases were observed in physeal-sparing ACL reconstructions. The incidence of growth abnormalities after ACL reconstruction in patients with open growth plates is difficult to truly assess, as many reported incidences in the literature are case series or case reports. However, prior studies have looked at growth deformities in adolescents after ACL reconstruction. A 2010 metaanalysis by Frosch et al.36 sought to analyze risks of operative treatment of ACL ruptures in adolescents. Their search yielded only 9 articles with cases of growth abnormalities in contrast to the 21 found in this study, despite using the same cut-off values of 1 cm of limb length discrepancy and 3 of angular malformation. This can be partially explained by the Frosch paper looking only at case series, cohort studies, and clinical trials between January 1980 and March 2009, whereas this analysis includes case reports and an additional 6 years of articles. Interestingly, their article discovered 8 angular malformations or limb length discrepancies out of 139 patients undergoing a physeal-sparing technique and 12 angular malformations or limb
Year of Publication 1994 2011 2010 2015 2009 2012 2014 2014 1999 2013 2011 2014 2008 1986 1997 2011 2006 1995 2014 2010 2013 2015 2005 2010 2015
Study Type Case series Retrospective cohort study Case series Case series Retrospective cohort study Case series Case series Case series Case report Case series Case report Case series Case series Case series Case series Case series Case series Case series Case series Case report Case report Case series Case series Prospective cohort study Case report
Level of Evidence IV III IV IV III IV IV IV IV IV IV IV IV IV IV IV IV IV IV IV IV IV IV II IV
length discrepancies out of 621 patients undergoing a transphyseal technique, for a relative risk of 0.34 in favor of transphyseal repair. A second article, from 2011, reviewed studies of ACL tears in skeletally immature patients with at least 6 months of follow-up.8 They only discovered 3 cases of angular malformation and 2 cases of limb length discrepancy, none of which occurred with physeal-sparing techniques. Our study was able to capture 39 incidences of angular malformation or limb length discrepancy, which represents all reported cases of growth abnormalities in the current literature. This can help to broaden our understanding of the factors that influence the occurrence of these deformities, or perhaps more importantly, address preconceived ideas regarding which surgical techniques give rise to these growth abnormalities. In this analysis, gender was reported in 27 of 39 cases (69%) of growth disturbances, with 24 patients (89%) being male. It has been reported that the incidence rate of ACL tears in females of high school age is at least 3-fold higher than their male counterparts.37 A separate study reporting gender in children aged 10 to 14 found 30 of 39 patients (76%) to be female.6 The high proportion of male patients with growth disturbances is surprising. This may be explained by a potential gender bias in reporting cases of growth disturbance versus the anecdotal nature of the report themselves. Additionally, the increased participation rates in sports, especially those that are in nature ballistic, potentially explain the disparity observed. Further research needs to be
Table 2. Summary of Data From Individual Studies Author Andrews et al.11 (1994) Bonnard et al.12 (2011)
2 103 56 25 12 15 1 32 1 13 17 24 49 16 1 23 1 1 4 11 31 1
7.0 12.1 10.0 16.4 12.1 12.8 14.3 11.3 14.0 12.0 10.0 15.0 10.5 12.0 12.6 14.5 12.0 15.0 15.5 11.0 10.0
Mean LLD Mean LLD No. of Angular Angular Femur Technique Tibia Technique No. of LLDs Shortening, cm Lengthening, cm Deformities Deformity ( ) Physeal-sparing Transphyseal 2 1.2 1.0 Physeal-sparing 1 1.5 2 4.0 (1 varus and 1 valgus) Physeal-sparing Transphyseal 2 1.3 1 6.0 valgus * * Physeal-sparing Physeal-sparing 1 Autograft/quadriceps Physeal-sparing Transphyseal 1 5.0 valgus * * Transphyseal Transphyseal 4 Allograft/hamstring Physeal-sparing 2 1.9 1 6.0 varus Autograft/quadriceps Transphyseal Transphyseal 3 1.6 1 6.0 valgus Transphyseal Transphyseal 1 14.0 valgus Transphyseal Transphyseal 1 6.2 valgus * * Allograft/tibialis Physeal-sparing Transphyseal 1 1 7.7 valgus Transphyseal Transphyseal 2 4.0 valgus Autograft/hamstring Transphyseal Transphyseal 1 5.0 valgus Physeal-sparing Transphyseal 2 2.0 1.3 Transphyseal Transphyseal * Autograft/quadriceps Transphyseal Transphyseal 1 valgus Transphyseal Transphyseal 1 1.5 Physeal-sparing Physeal-sparing 1 1.5 Autograft/hamstring Physeal-sparing Physeal-sparing 1 1.1 Physeal-sparing 1 1.0 1 13.0 valgus Allograft/Achilles Physeal-sparing Transphyseal 1 4.5 1 15.0 varus Autograft/hamstring Transphyseal Transphyseal 3 1.3 2 5.0 valgus Autograft/hamstring Transphyseal Transphyseal 4 1.0 1.0 * * Autograft/hamstring Transphyseal Transphyseal 1 1 2.8 Graft Type
GROWTH ABNORMALITIES FOLLOWING ACLR
Chotel et al.13 (2010) Cruz et al.14 (2015) Henry et al.4 (2009) Kim et al.15 (2012) Koch et al.16 (2014) Kohl et al.17 (2014) Koman et al.18 (1999) Kumar et al.19 (2013) Lawrence et al.20 (2011) Lemaitre et al.21 (2014) Liddle et al.22 (2008) Lipscomb et al.2 (1986) Lo et al.23 (1997) Mauch et al.24 (2011) McIntosh et al.25 (2006) Nakhostine et al.26 (1995) Nawabi et al.27 (2014) Robert et al.28 (2010) Rozbruch et al.29 (2013) Shifflett et al.30 (2015) Seon et al.31 (2005) Streich et al.32 (2010) Zimmerman et al.33 (2015)
No. of Mean Patients Age, y 8 13.5 57 12.2 -
LLD, limb length discrepancy. *Incomplete and/or missing data.
5
6
Table 3. Data From Cases of Limb Length Discrepancies Author, Subject No. Andrews,11 1 Andrews,11 2 Bonnard,12 3 Chotel,13 1 Chotel,13 2 Kim,15 1
Graft Type Patella Iliotibial band Iliotibial band -
Kim,15 2
-
Kim,15 3
Femur Fixation Staples Staples Interference screw Suspensory
Transphyseal
Transphyseal
Suspensory
-
Transphyseal
Transphyseal
Suspensory
Kim,15 4
-
Transphyseal
Transphyseal
Suspensory
Koch,16 1 Koch,16 2 Kohl,17 1 Kohl,17 2 Kohl,17 3 Lipscomb,2 1 Lipscomb,2 2 McIntosh25 Nakhostine26 Nawabi27 Robert28 Rozbruch29 Schifflett,30 1
Hamstring Hamstring Quadriceps Quadriceps Quadriceps Hamstring Hamstring Hamstring Patella Achilles Hamstring
Physeal-sparing Physeal-sparing Transphyseal Transphyseal Transphyseal Physeal-sparing Physeal-sparing Transphyseal Physeal-sparing Physeal-sparing Physeal-sparing Physeal-sparing Transphyseal
Physeal-sparing Physeal-sparing Transphyseal Transphyseal Transphyseal Transphyseal Transphyseal Transphyseal Physeal-sparing Physeal-sparing Physeal-sparing Transphyseal Transphyseal
Suspensory Suspensory Screw and suture post Screw and suture post Screw and suture post Screw and suture post Screw and suture post Suspensory Screw and suture post Interference screw Staples Suspensory
Schifflett,30 2
Hamstring
Transphyseal
Transphyseal
Suspensory
Schifflett,30 4
Hamstring
Transphyseal
Transphyseal
Suspensory
Seon,31 1
Hamstring
Transphyseal
Transphyseal
Seon,31 2
Hamstring
Transphyseal
Transphyseal
Seon,31 3
Hamstring
Transphyseal
Transphyseal
Seon,31 4
Hamstring
Transphyseal
Transphyseal
Zimmerman33
Tibialis
-
-
Staples or interference screw Staples or interference screw Staples or interference screw Staples or interference screw Screw and suture post
Tibia Fixation Staples Staples Screw and suture post Staples Staples Staples or interference screw Staples or interference screw Staples or interference screw Staples or interference screw Screw and suture post Screw and suture post Screw and suture post Screw and suture post Screw and suture post Screw and suture post Screw and suture post Screw and suture post Staples Screw and suture post Screw and suture post Screw and suture post Suture and interference screw Suture and interference screw Suture and interference screw Staples or interference screw Staples or interference screw Staples or interference screw Staples or interference screw Screw and suture post
LLD Shortening, cm 1.2 -
LLD Lengthening, cm 1.0 1.5 1.5 1.0 1.0
-
1.0
-
-
1.0
-
-
1.0
1.8 1.0 2.0 2.0 1.0 4.5 1.4
2.1 1.6 1.3
1.4
-
-
1.0
-
7 valgus
-
1.0
-
-
1.0
-
-
1.0
-
1.0
-
-
-
2.8
-
1.5 1.5 1.1 -
Angular Deformity ( ) 6 valgus -
6 varus 6 valgus 13 valgus 15 varus -
M. J. COLLINS ET AL.
Tibia Technique Transphyseal Transphyseal Physeal-sparing Transphyseal Transphyseal Transphyseal
LLD, limb length discrepancy.
Femur Technique Physeal-sparing Physeal-sparing Physeal-sparing Physeal-sparing Physeal-sparing Transphyseal
Table 4. Data From Cases of Angular Deformities Graft Type Patella Patella Iliotibial band Quadriceps Hamstring Quadriceps Hamstring Hamstring Tibialis Hamstring Hamstring Hamstring Patella Achilles Hamstring Hamstring
Femur Technique Physeal-sparing Physeal-sparing Physeal-sparing Physeal-sparing Physeal-sparing Transphyseal Transphyseal Transphyseal Physeal-sparing Transphyseal Transphyseal Transphyseal Physeal-sparing Physeal-sparing Transphyseal Transphyseal
Tibia Technique Physeal-sparing Physeal-sparing Transphyseal Transphyseal Physeal-sparing Transphyseal Transphyseal Transphyseal Transphyseal Transphyseal Transphyseal Transphyseal Physeal-sparing Transphyseal Transphyseal Transphyseal
Femur Fixation Interference screw Interference screw Suspensory Screw and suture post Interference screw Suspensory Suspensory Suspensory Suspensory Suspensory Interference screw Staples Suspensory Suspensory
Tibia Fixation Screw and suture post Screw and suture post Staples Staples Screw and suture post Screw and suture post Staples Screw and suture post Staples Staples and interference screw Staples and interference screw Screw and suture post Screw and suture post Screw and suture post Suture and interference screw Suture and interference Screw
Degrees Valgus ( ) 4.0 6.0 5.0 6.0 14.0 6.2 7.7 4.0 4.0 5.0 13.0 3.1 6.9
Degrees Varus ( ) 4.0 6.0 15.0 -
Location of Angular Deformity Unspecified Unspecified Tibia Tibia Mainly femoral Unspecified Femur Femur Femur Femur Femur Unspecified Femur Tibia Femur and tibia Femur and tibia
Table 5. Summary of Key Data
Limb overgrowth
Number of Cases 18
Limb shortening
11
Varus malformation
3
Valgus malformation
13
Most Common TechniquedFemur Physeal-sparing (n ¼ 9)
Most Common TechniquedTibia Transphyseal (n ¼ 12)
Most Common FixationdFemur Suspensory (n ¼ 7)
Transphyseal (n ¼ 7)
Transphyseal (n ¼ 10)
Screw and suture post (n ¼ 4)
Physeal-sparing (n ¼ 3)
Physeal-sparing (n ¼ 2)
Transphyseal (n ¼ 8)
Transphyseal (n ¼ 11)
Interference screw, suspensory, staples (n ¼ 1 each) Suspensory (n ¼ 7)
Most Common FixationdTibia Screw and suture post (n ¼ 7) Screw and suture post (n ¼ 6) Screw and suture post (n ¼ 3) Screw and suture post (n ¼ 5)
Average Limb Length Discrepancy, mm 13.27
Average Angular Malformation ( ) -
17.0
-
-
8.3
-
6.5
GROWTH ABNORMALITIES FOLLOWING ACLR
Author, Subject No. Bonnard,12 1 Bonnard,12 2 Chotel,13 2 Henry4 Koch,16 1 Kohl,17 1 Koman18 Kumar19 Lawrence20 Lemaitre,21 1 Lemaitre,21 2 Liddle22 Robert28 Rozbruch29 Schifflett,30 3 Schifflett,30 4
7
8
M. J. COLLINS ET AL.
performed to investigate if males do indeed have a higher risk of growth disturbance after ACL reconstruction than females. In this analysis, 18 of 29 cases (62%) of limb length discrepancy were due to limb overgrowth after ACL reconstruction. In pediatric femoral shaft fractures, there is a risk of limb lengthening which is well documented.38-40 This has been attributed to increased vascularity in the distal femoral shaft as well as an increase in mitotic activity within the growth plates after mid-diaphyseal fractures.38 The theory is thought to be due to periosteal disruption, which occurs during ACL reconstruction with both physeal-sparing and transphyseal techniques. In this analysis, one study exploring limb overgrowth attributed this phenomenon as a possible explanation for the observed overgrowth.13 Importantly, periosteal disruption and increased vascularity occurs irrespective of surgical technique. In this analysis, physeal-sparing techniques, thought by many surgeons to be a safe alternative to transphyseal techniques, produced a similar number of limb overgrowth cases as did transphyseal techniques. Among 18 cases of limb overgrowth, physeal-sparing techniques were used in 9 cases (50%) and transphyseal was used in 8 cases (44%) (in 1 case, technique was not specified). Limb shortening was noted in 11 of 29 cases (38%) of limb length discrepancy within this analysis. A wellreported and potential cause of limb shortening has been the malplacement of bone blocks or hardware across the physis, resulting in premature growth arrest. In this analysis, Lipscomb et al.2 reported on a case of limb length discrepancy attributed to staples being placed across the femoral physis. Koman et al.18 attributed a case of angular malalignment to a cannulated screw crossing the femoral physis. Additionally, Mauch et al.24 attributed a case of procurvatum to malplacement of a bone block within the posterolateral femoral physis. Although this is a well-known potential cause of growth deformity after pediatric ACL reconstruction, in this analysis we only discovered 3 cases attributed to such causes. Although malplacement of hardware or bone blocks across the physis appears to be a factor that may lead to growth deformity, alternative reasons are more likely, such as drilling across the physis. In a study of 44 rabbits, it was discovered by Makela et al.41 that destruction of 7% of the crosssectional area of femoral growth plates (3.2-mm drill hole) lead to permanent growth disturbance and shortening of the limb. Results of this study have not been tested in humans, although drilling of the femoral tunnel at an oblique angle has been cited as a cause of growth disturbance after ACL reconstruction. Kohl et al.17 theorized that a likely cause of the growth disturbances in their study was due to the tunnel crossing the growth plate at an oblique angle, affecting a greater percentage of the physis. Unfortunately, few studies
report on the obliquity of their femoral tunnel. Perhaps more striking is our finding that just over half of the studies with limb shortening (8/11, 73%) had transphyseal femoral tunnels, used grafts with bone blocks, and/or used interference screws. This suggests that the current theories regarding tunnel placement and size, graft type and placement, and fixation type may not account for all of the causes of limb shortening. Future studies should be aimed at expanding our understanding of the risks associated with limb shortening after ACL reconstruction in skeletally immature patients. In this analysis, we identified 16 cases of angular malformation after ACL reconstruction on skeletally immature patients. The most common deformity seen was valgus malalignment (n ¼ 13, 81%; the remaining cases were varus deformity). Across all studies reporting on angular malformation, physeal-sparing techniques on the femur were employed equally as often as a transphyseal techniques. Many of the same risk factors that have been attributed to limb length discrepancy in the literature have also been reported in association with angular malformation deformities after ACL reconstruction in skeletally immature patients. Of the 16 cases with angular malformation, 4 cases were attributed to the tibial side and 8 to the femoral side, and the remaining 4 cases did not specify location of the partial growth arrest. Interestingly, of the 4 cases of angular malformation centered about the tibia, all employed a transphyseal technique on the tibia. On the other hand, among the 8 cases of angular malformation centered about the femur, 5 used a transphyseal technique on the femur whereas the remaining 3 used physeal-sparing techniques. Although we did observe that most of the cases of angular malformation arose in conjunction with a transphyseal technique, this was not exclusive as a quarter of all cases arose when a physealsparing technique was employed. Irrespective of technique, our findings suggest that surgeons must remain mindful of the physis to minimize secondary growth abnormalities. Limitations This analysis has several limitations. First, a survey of the Herodicus Society and ACL Study Group reported that 11% of respondents saw a growth abnormality after ACL reconstruction in a skeletally immature patient.3 However, given that only 39 cases were identified in the literature, it is likely that many cases may go unreported, which also suggests that there is a void in clinical research to enhance our understanding as to the etiology and risk factors for the development of these deformities. Second, there is no consensus in the literature as to what constitutes a clinically significant limb length discrepancy or angular malformation after ACL reconstruction in a skeletally immature patient. Variation in what is considered clinically significant would
GROWTH ABNORMALITIES FOLLOWING ACLR
impact the number of patients we included in this study; however, we attempted to set our inclusion parameters in line with past studies on this topic. Third, there were 4 studies comprising an additional 8 cases of limb length discrepancy reported in the literature that we were unable to include in this study due to incomplete data. These cases, indicated with an asterisk, are outlined in Table 2. Lastly, given the heterogeneity in the data we obtained from the current literature, we were unable to perform any meaningful statistics to identify risk factors and determine causality. As such, most of our current understanding pertaining to the etiology of growth abnormalities after ACL reconstruction in skeletally immature patients is based on theories generated from anatomic or animal studies, and future prospective studies are needed to enhance our understanding so that these devastating complications can be avoided.
Conclusions At present, there are 21 studies reporting 39 patients with growth abnormalities in the current literature, of which 29 cases of limb length discrepancy and 16 cases of angular malformation. Of the 29 cases of limb length discrepancy, limb overgrowth accounted for 62% of cases. Perhaps most interestingly, physeal-sparing techniques were performed in 25% of the cases of angular malformation and 47% cases of limb length discrepancy, despite the commonly held belief that this technique mitigates the risks of ACL reconstruction by not violating the growth plate. Based on this study, it is clear that growth abnormalities after ACL reconstruction in the skeletally immature patient are underreported, and our current understanding of the etiology of these abnormalities is limited.
References 1. McConkey MO, Bonasia DE, Amendola A. Pediatric anterior cruciate ligament reconstruction. Curr Rev Musculoskelet Med 2011;4:37-44. 2. Lipscomb AB, Anderson AF. Tears of the anterior cruciate ligament in adolescents. J Bone Joint Surg Am 1986;68: 19-28. 3. Kocher MS, Saxon HS, Hovis WD, Hawkins RJ. Management and complications of anterior cruciate ligament injuries in skeletally immature patients: survey of the Herodicus Society and The ACL Study Group. J Pediatr Orthop 2002;22:452-457. 4. Henry J, Chotel F, Chouteau J, Fessy MH, Berard J, Moyen B. Rupture of the anterior cruciate ligament in children: Early reconstruction with open physes or delayed reconstruction to skeletal maturity? Knee Surg Sports Traumatol Arthrosc 2009;17:748-755. 5. Smith TO, Davies L, Hing CB. Early versus delayed surgery for anterior cruciate ligament reconstruction: A systematic review and meta-analysis. Knee Surg Sports Traumatol Arthrosc 2010;18:304-311.
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6. Millett PJ, Willis AA, Warren RF. Associated injuries in pediatric and adolescent anterior cruciate ligament tears: Does a delay in treatment increase the risk of meniscal tear? Arthroscopy 2002;18:955-959. 7. Cassard X, Cavaignac E, Maubisson L, Bowen M. Anterior cruciate ligament reconstruction in children with a quadrupled semitendinosus graft: Preliminary results with minimum 2 years of follow-up. J Pediatr Orthop 2014;34: 70-77. 8. Vavken P, Murray MM. Treating anterior cruciate ligament tears in skeletally immature patients. Arthroscopy 2011;27:704-716. 9. Guzzanti V, Falciglia F, Gigante A, Fabbriciani C. The effect of intra-articular ACL reconstruction on the growth plates of rabbits. J Bone Joint Surg Br 1994;76:960-963. 10. Stadelmaier DM, Arnoczky SP, Dodds J, Ross H. The effect of drilling and soft tissue grafting across open growth plates. A histologic study. Am J Sports Med 1995;23: 431-435. 11. Andrews M, Noyes FR, Barber-Westin SD. Anterior cruciate ligament allograft reconstruction in the skeletally immature athlete. Am J Sports Med 1994;22:48-54. 12. Bonnard C, Fournier J, Babusiaux D, Planchenault M, Bergerault F, de Courtivron B. Physeal-sparing reconstruction of anterior cruciate ligament tears in children: Results of 57 cases using patellar tendon. J Bone Joint Surg Br 2011;93:542-547. 13. Chotel F, Henry J, Seil R, Chouteau J, Moyen B, Berard J. Growth disturbances without growth arrest after ACL reconstruction in children. Knee Surg Sports Traumatol Arthrosc 2010;18:1496-1500. 14. Cruz AI Jr, Fabricant PD, McGraw M, Rozell JC, Ganley TJ, Wells L. All-epiphyseal ACL reconstruction in children: Review of safety and early complications. J Pediatr Orthop July 17, 2015 [Epub ahead of print]. 15. Kim SJ, Shim DW, Park KW. Functional outcome of transphyseal reconstruction of the anterior cruciate ligament in skeletally immature patients. Knee Surg Relat Res 2012;24:173-179. 16. Koch PP, Fucentese SF, Blatter SC. Complications after epiphyseal reconstruction of the anterior cruciate ligament in prepubescent children. Knee Surg Sports Traumatol Arthrosc October 26, 2014 [Epub ahead of print]. 17. Kohl S, Stutz C, Decker S, et al. Mid-term results of transphyseal anterior cruciate ligament reconstruction in children and adolescents. Knee 2014;21:80-85. 18. Koman JD, 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;81:711-715. 19. Kumar S, Ahearne D, Hunt DM. Transphyseal anterior cruciate ligament reconstruction in the skeletally immature: Follow-up to a minimum of sixteen years of age. J Bone Joint Surg Am 2013;95:e1. 20. Lawrence JT, West RL, Garrett WE. Growth disturbance following ACL reconstruction with use of an epiphyseal femoral tunnel: A case report. J Bone Joint Surg Am 2011;93:e39. 21. Lemaitre G, Salle de Chou E, Pineau V, et al. ACL reconstruction in children: A transphyseal technique. Orthop Traumatol Surg Res 2014;100:S261-S265 (suppl).
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22. Liddle AD, Imbuldeniya AM, Hunt DM. Transphyseal reconstruction of the anterior cruciate ligament in prepubescent children. J Bone Joint Surg Br 2008;90: 1317-1322. 23. Lo IK, Kirkley A, Fowler PJ, Miniaci A. The outcome of operatively treated anterior cruciate ligament disruptions in the skeletally immature child. Arthroscopy 1997;13: 627-634. 24. Mauch C, Arnold MP, Wirries A, Mayer RR, Friederich NF, Hirschmann MT. Anterior cruciate ligament reconstruction using quadriceps tendon autograft for adolescents with open physesdA technical note. Sports Med Arthrosc Rehabil Ther Technol 2011;3:7. 25. McIntosh AL, Dahm DL, Stuart MJ. Anterior cruciate ligament reconstruction in the skeletally immature patient. Arthroscopy 2006;22:1325-1330. 26. Nakhostine M, Bollen SR, Cross MJ. Reconstruction of mid-substance anterior cruciate rupture in adolescents with open physes. J Pediatr Orthop 1995;15:286-287. 27. Nawabi DH, Jones KJ, Lurie B, Potter HG, Green DW, Cordasco FA. All-inside, physeal-sparing anterior cruciate ligament reconstruction does not significantly compromise the physis in skeletally immature athletes: A postoperative physeal magnetic resonance imaging analysis. Am J Sports Med 2014;42:2933-2940. 28. Robert HE, Casin C. Valgus and flexion deformity after reconstruction of the anterior cruciate ligament in a skeletally immature patient. Knee Surg Sports Traumatol Arthrosc 2010;18:1369-1373. 29. Rozbruch SR, Fryman C, Schachter LF, Bigman D, Marx RG. Growth arrest of the tibia after anterior cruciate ligament reconstruction: Lengthening and deformity correction with the Taylor Spatial Frame. Am J Sports Med 2013;41:1636-1641. 30. Shifflett GD, Green DW, Widmann RF, Marx RG. Growth arrest following ACL reconstruction with hamstring autograft in skeletally immature patients: A review of 4 cases. J Pediatr Orthop April 6, 2015 [Epub ahead of print].
31. Seon JK, Song EK, Yoon TR, Park SJ. Transphyseal reconstruction of the anterior cruciate ligament using hamstring autograft in skeletally immature adolescents. J Korean Med Sci 2005;20:1034-1038. 32. Streich NA, Barie A, Gotterbarm T, Keil M, Schmitt H. Transphyseal reconstruction of the anterior cruciate ligament in prepubescent athletes. Knee Surg Sports Traumatol Arthrosc 2010;18:1481-1486. 33. Zimmerman LJ, Jauregui JJ, Riis JF, Tuten HR. Symmetric limb overgrowth following anterior cruciate ligament reconstruction in a skeletally immature patient. J Pediatr Orthop B 2015;24:530-534. 34. Rush WA, Steiner HA. A study of lower extremity length inequality. Am J Roentgenol Radium Ther 1946;56:616-623. 35. Seil PDR, Robert H. VKB-Plastik bei offenen Wachstumsfugen. Arthroskopie 2005;18:48-52. 36. Frosch KH, Stengel D, Brodhun T, et al. Outcomes and risks of operative treatment of rupture of the anterior cruciate ligament in children and adolescents. Arthroscopy 2010;26:1539-1550. 37. Prodromos CC, Han Y, Rogowski J, Joyce B, Shi K. A metaanalysis of the incidence of anterior cruciate ligament tears as a function of gender, sport, and a knee injury-reduction regimen. Arthroscopy 2007;23:1320-1325. e1326. 38. Ashraf N, Meyer MH, Frick S, Meyer RA Jr. Evidence for overgrowth after midfemoral fracture via increased RNA for mitosis. Clin Orthop Relat Res 2007;454:214-222. 39. Sulaiman AR, Joehaimy J, Iskandar MA, Anwar Hau M, Ezane AM, Faisham WI. Femoral overgrowth following plate fixation of the fractured femur in children. Singapore Med J 2006;47:684-687. 40. Jawish R, Kahwaji A, Dagher G. Overgrowth of femoral fractures in childhood. Rev Chir Orthop Reparatrice Appar Mot 2003;89:404-406 [in French]. 41. Makela EA, Vainionpaa S, Vihtonen K, Mero M, Rokkanen P. The effect of trauma to the lower femoral epiphyseal plate. An experimental study in rabbits. J Bone Joint Surg Br 1988;70:187-191.