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Surgical timing of anterior cruciate ligament reconstruction to prevent associated meniscal and cartilage lesions
Journal of Orthopaedic Science xxx (2018) 1e6
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Journal of Orthopaedic Science journal homepage: http://www.elsevier.com/locate/jos
Original Article
Surgical timing of anterior cruciate ligament reconstruction to prevent associated meniscal and cartilage lesions Shuji Taketomi a, *, Hiroshi Inui a, Ryota Yamagami a, Kohei Kawaguchi a, Keiu Nakazato a, Kenichi Kono a, Manabu Kawata a, Takumi Nakagawa b, Sakae Tanaka a a b
Department of Orthopaedic Surgery, Faculty of Medicine, The University of Tokyo, Tokyo, Japan Department of Orthopaedic Surgery, Teikyo University School of Medicine, Tokyo, Japan
a r t i c l e i n f o
a b s t r a c t
Article history: Received 23 August 2017 Received in revised form 26 January 2018 Accepted 12 February 2018 Available online xxx
Background: The purpose of this study was to analyze the association between the prevalence of meniscal and chondral lesions and the timing of surgery in patients undergoing primary anterior cruciate ligament (ACL) reconstruction to determine a safe time for surgery. Methods: This retrospective study involved 226 patients (91 females and 135 males; median age, 29 years) undergoing primary ACL reconstruction. Time interval from ACL injury to surgery (median, 4 months; range, 1e420 months) and concomitant meniscal and cartilage lesions in ACL reconstruction were reviewed. Receiver operating characteristic (ROC) curve analysis was used to determine the precise threshold interval to surgery to prevent meniscal or cartilage lesions. The risk of lesion occurrence after each cutoff period was determined using odds ratio (OR). Results: The incidences of medial meniscus (MM), lateral meniscus (LM), and cartilage lesions were 43.8%, 32.7%, and 27.4%, respectively. ROC analysis revealed that patients who waited for more than 6, 4, and 5 months for ACL reconstruction had a significantly greater risk of associated MM, LM, and chondral lesions, respectively. Patients who underwent ACL reconstruction 7 months after injury had OR of 4.1 (p < 0.001) for the presence of MM lesion as compared with those who underwent reconstruction within 6 months. Similarly, patients who underwent ACL reconstruction 5 months after injury had OR of 1.9 (p ¼ 0.023) for the presence of LM lesion as compared with those who underwent reconstruction within 4 months, and patients who underwent ACL reconstruction 6 months after injury had OR of 2.9 (p < 0.001) for chondral lesion as compared with those who underwent reconstruction within 6 months. Conclusion: ACL reconstruction should be performed within approximately 6 months after the injury to prevent associated meniscal or chondral lesions. © 2018 The Japanese Orthopaedic Association. Published by Elsevier B.V. All rights reserved.
1. Introduction Anterior cruciate ligament (ACL) rupture is one of the most common sports injuries, and ACL reconstruction has been widely performed for ACL rupture. ACL rupture is known to be associated with an increased risk of knee osteoarthritis (OA) [1,2]; therefore, the aim of ACL reconstruction is to prevent knee OA, as well as to restore normal knee kinematics and return to performing sports activities.
* Corresponding author. Department of Orthopaedic Surgery, Faculty of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-0033, Japan. Fax: þ81 3 3818 4082. E-mail address: [email protected] (S. Taketomi).
ACL reconstruction is often postponed for several weeks after injury because of inflammation, swelling, and restricted range of motion of the knee joint [3]. Some patients cannot avoid delaying ACL reconstruction because of several social situations. Delayed ACL reconstruction is considered to increase the incidence of meniscal injury or chondral lesions [4e7]. Meniscal tears and chondral injuries are often identified at the time of arthroscopic reconstruction. These lesions are considered to carry an increased risk of OA development [8]. Delaying ACL reconstruction for more than 1 year has been known to be a risk factor for knee OA [9e11]. However, there is no consensus on the ideal timing for ACL reconstruction in terms of decreasing the risk of secondary intraarticular lesions in ACL-deficient knees. In previous studies, many authors have used a particular time point as a cutoff, such as 6 or 12 months after injury, and compared the incidence of concomitant articular lesions before
https://doi.org/10.1016/j.jos.2018.02.006 0949-2658/© 2018 The Japanese Orthopaedic Association. Published by Elsevier B.V. All rights reserved.
Please cite this article in press as: Taketomi S, et al., Surgical timing of anterior cruciate ligament reconstruction to prevent associated meniscal and cartilage lesions, Journal of Orthopaedic Science (2018), https://doi.org/10.1016/j.jos.2018.02.006
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S. Taketomi et al. / Journal of Orthopaedic Science xxx (2018) 1e6
and after such a cutoff period [9,12e14]. There is a need for a more precise estimation of the appropriate interval before ACL reconstruction without increasing the risk of meniscal or cartilage lesions. In the field of surgery in recent years, receiver operating characteristic (ROC) curve has been frequently used in order to identify cutoff threshold time for surgery or other interventions [15e18]. In this study, we used ROC curve analysis in order to determine a safe time for surgery and showed a more precise cutoff period to assess the risk of meniscal or chondral lesions in delayed ACL reconstruction, instead of a particular time point as cutoff, such as 6 or 12 months after injury. The purpose of this study was to determine a safe time for surgery by analyzing the association between the prevalence of meniscal and chondral lesions and the timing of surgery in patients undergoing primary ACL reconstruction. The hypothesis of this study was that after ACL rupture, the incidence of meniscal and cartilage lesions increases after a certain time point. 2. Materials and methods This study was a retrospective case series. Medical records of 260 patients who underwent primary ACL reconstruction between August 2010 and July 2016 were reviewed. Patients were excluded from the study under the following conditions: (1) previous intraarticular surgery such as ligamentous, meniscal, or chondral surgery or previous osteotomy or fracture around the knee joint; (2) presence of posterior cruciate ligament insufficiency, abnormal varus/valgus instability, or concomitant reconstruction of other ligaments; (3) presence of OA (Kellgren and Lawrence classification [19] II); and (4) unknown time of injury. In total, 34 patients were excluded. Our final analysis included 226 patients (91 females and 135 males) with a median age of 29 years (range, 14e62 years). Baseline patient demographics are summarized in Table 1. Our local institutional review board has approved this retrospective study. Patients and their families were informed that their data would be submitted for publication, and all provided written informed consent for the same. Time to ACL reconstruction was calculated as the difference in the number of months between the date of injury and surgery. The time between ACL injury and reconstruction may have been determined by several uncontrollable factors, including misdiagnosis, nonsurgical management, patient convenience, waiting list for surgery, and financial reasons. Surgical timing was also determined by the state of the knee joint, including swelling or restriction of joint movement. A large number of patients were referred to our institute for surgery after significant delay. The presence of meniscal and cartilage lesions at the time of ACL reconstruction was collected from analysis of surgical records. Concomitant meniscal and cartilage lesions in all patients had been recorded during ACL reconstruction. Only those requiring meniscal suture, partial
meniscectomy, or meniscal rasping during ACL reconstruction were considered to have meniscal lesion. The morphology of the meniscal lesion was also recorded. Cartilage lesions were classified according to the International Cartilage Repair Society (ICRS) system [20]. When grade IIeIV chondral lesion was present in medial femoral condyle, lateral femoral condyle, medial tibial plateau, lateral tibial plateau, trochlea, or patella, the site and ICRS grade of chondral lesions were recorded. 2.1. Statistical analysis Statistical analysis was performed using the EXCEL statistics 2012 software package for Microsoft Windows (SSRI Co., Ltd., Tokyo, Japan). Patient parameters were compared using the Student's t-test, ManneWhitney U test, or chi-square test. ROC curve analysis was used to determine the precise threshold interval to surgery to prevent meniscal or cartilage lesions. The risk of lesion occurrence after each cutoff period was determined using odds ratio (OR). To identify potential risk factors of meniscal or chondral lesion, age, gender, body mass index, Tegner activity scale, and time to surgery which have probably impact on these lesions were compared using multivariate logistic regression. Statistical significance was set at P < 0.05. 3. Results In total, 99 (43.8%) and 74 (32.7%) patients had medial meniscus (MM) and lateral meniscus (LM) lesions, respectively, at the time of surgery. The morphology of the meniscal lesion is described in detail in Table 2. Longitudinal tears were most commonly observed in both MM and LM lesions. Sixty-two (27.4%) patients had a chondral lesion. The location and severity of the chondral lesions are shown in Table 3. Chondral lesions were frequently observed in the medial femoral condyle and the lateral tibial plateau. 3.1. MM lesion The association between MM lesion and surgical timing is shown in Fig. 1A. The incidence of MM lesion increased with an increase in the waiting period before surgery. ROC was used to analyze the best cutoff period from ACL injury to ACL reconstruction based on the incidence of MM lesions (Fig. 1B). The best cutoff period for surgery was 7 months, with an area under curve (AUC) of 0.683. There were 45 (31.5%) MM lesions in patients who underwent ACL reconstruction before the cutoff period compared with 54 (65.1%) MM lesions in those in whom ACL reconstruction was delayed. Patients who underwent ACL reconstruction 7 months after injury had OR of 4.1 [95% confidence interval (CI), 2.3e7.2; p < 0.001] for the presence of an MM lesion compared with those Table 2 Morphology of meniscal lesion.
Table 1 Patient demographics.
Number of patients Age (years old) Gender (female/male) BMI (kg/m2) Tegner Activity Scale Time to surgery (months)
Overall
Early surgery Delayed surgery P value (6 months) (>6 months)
226 29 (14e62) 91/135 23.3 ± 4.0 7 (3e10) 4 (1e420)
143 25 (14e62) 56/87 23.3 ± 4.1 8 (3e10) 3 (1e6)
83 32 (15e61) 35/48 23.4 ± 4.0 7 (3e9) 16 (7e420)
0.003 0.657 0.837 0.001 0.000
BMI, body mass index. Data are given as mean ± standard deviation or median (range). P values between early surgery group and delayed surgery group are shown.
Longitudinal tear Bucket handle tear Radial tear Flap tear Posterior root tear Horizontal tear Complex tear Defect or partial defect Discoid meniscus tear Others Total
MM
LM
56 (56.6%) 19 (19.2%) 0 (0%) 10 (10.1%) 0 (0%) 3 (3.0%) 3 (3.0%) 4 (4.0%) 0 (0%) 4 (4.0%) 99
34 (45.9%) 7 (9.5%) 12 (16.2%) 11 (14.9%) 5 (6.8%) 1 (1.4%) 1 (1.4%) 0 (0%) 1 (1.4%) 2 (2.7%) 74
MM, medial meniscus; LM, lateral meniscus.
Please cite this article in press as: Taketomi S, et al., Surgical timing of anterior cruciate ligament reconstruction to prevent associated meniscal and cartilage lesions, Journal of Orthopaedic Science (2018), https://doi.org/10.1016/j.jos.2018.02.006
S. Taketomi et al. / Journal of Orthopaedic Science xxx (2018) 1e6 Table 3 Location and severity of chondral lesions.
Medial femoral condyle Medial tibial plateau Lateral femoral condyle Lateral tibial plateau Trochlea Patella
3
Table 4 Odds ratio of intraarticular lesions with increasing time to injury.
ICRS II
ICRS III
ICRS IV
Total
26 (11.5%) 10 (4.4%) 2 (0.9%) 22 (9.7%) 10 (4.4%) 0 (0%)
8 0 1 3 4 0
1 0 1 0 0 0
35 (15.5%) 10 (4.4%) 4 (1.8%) 25 (11.1%) 14 (6.2%) 0 (0%)
(3.5%) (0%) (0.4%) (1.3%) (1.8%) (0%)
(0.4%) (0%) (0.4%) (0%) (0%) (0%)
ICRS, International Cartilage Repair Society.
who underwent ACL reconstruction within 6 months (Table 4). In logistic regression analysis, increased time to surgery was a significant risk factor for MM lesion. The other parameters were not significant risk factors of MM lesion (Table 5). 3.2. LM lesion The association between LM lesion and surgical timing is shown in Fig. 2A. The incidence of LM lesion also increased with an increase in the waiting period before surgery. ROC was used to analyze the best cutoff period from ACL injury to ACL reconstruction based on the incidence of LM lesions (Fig. 2B). The best cutoff period for surgery was 5 months, with AUC of 0.585. There were 29 (25.7%) LM lesions in patients who underwent ACL reconstruction before the cutoff period compared with 45 (39.8%) LM lesions in those in whom ACL reconstruction was delayed. Patients who underwent ACL reconstruction 5 months after injury had OR of 1.9 (95% CI, 1.1e3.4; p ¼ 0.023) for the presence of an LM lesion compared with those who underwent ACL reconstruction within 4 months (Table 4). In logistic regression analysis, increased time to surgery was a significant risk factor for LM lesion. The other parameters were not significant risk factors of LM lesion (Table 5). 3.3. Chondral lesion The association between chondral lesion and surgical timing is shown in Fig. 3A. The number of chondral lesions increased with an increase in the waiting period before surgery. ROC was used to analyze the best cutoff period from ACL injury to ACL reconstruction based on the presence of chondral lesions (Fig. 3B). The best cutoff period for surgery was 6 months, with AUC of 0.650. There were 25 (18.8%) chondral lesions in patients who underwent surgery before the cutoff period compared with 37 (39.8%) chondral lesions in those in whom ACL reconstruction was delayed. Patients who underwent ACL reconstruction 6 months after injury had OR
MM lesion LM lesion Chondral lesion
Cutoff time
OR (95%CI)
p value
7 months 5 months 6 months
4.1 (2.3e7.2) 1.9 (1.1e3.4) 2.8 (1.6e5.2)
<0.001 0.023 <0.001
MM, medial meniscus; LM, lateral meniscus; OR, odds ratio; CI, confidence interval.
of 2.9 (95% CI, 1.6e5.2; p < 0.001) for the presence of a chondral lesion as compared with those who underwent ACL reconstruction within 6 months (Table 4). In logistic regression analysis, increased age and female gender were a significant risk factor for chondral lesion. Time to surgery was not significant risk factors of chondral lesion (Table 5). From the results of this study, patients were sorted into the early surgery group and the delayed surgery group. Demographic data of each group are shown in Table 1. There were significant differences in age, activity level and time to surgery. There was no significant difference in the other parameters. 4. Discussion In this study, the incidences of MM and LM lesions were 43.8% and 32.7%, respectively. In addition, the overall incidence of articular cartilage lesions was 27.4%. The incidences of MM, LM, and chondral lesions observed at the time of ACL reconstruction vary widely in previous reports, ranging from 27.1% to 56.9%, from 29.1% to 52.3%, and from 15.2% to 42.3%, respectively [4,7,9,12,13,21e23]. The incidence of concomitant intraarticular lesions in this study is consistent with that reported in previous reports. This is a unique study using ROC curve analysis to determine a safe cutoff period for ACL reconstruction to prevent associated meniscal and cartilage lesions. The ROC analysis revealed that patients who waited more than 6, 4, and 5 months to undergo ACL reconstruction had a significantly greater risk of associated MM, LM, and chondral lesions, respectively. Our results show that ACL reconstruction should be performed within preferably 4 months or within maximum 6 months after the injury to prevent associated meniscal or chondral lesions. The main strength of this study is that we used ROC analysis to calculate a cutoff period. Many previous investigators used a particular time point as cutoff, such as 6 or 12 months after injury, and compared the incidence of concomitant articular lesions before and after such a cutoff period. ROC curve analysis is often used to determine an optimal surgical timing in general surgery [15e18]. This is the first study that used ROC curve
Fig. 1. (A) Association between medial meniscal lesion and surgical timing. (B) Receiver operating characteristic curve of medial meniscal lesion. MM, medial meniscus; ROC, receiver operating characteristic; TPF, true-positive fraction; FPF, false-positive fraction.
Please cite this article in press as: Taketomi S, et al., Surgical timing of anterior cruciate ligament reconstruction to prevent associated meniscal and cartilage lesions, Journal of Orthopaedic Science (2018), https://doi.org/10.1016/j.jos.2018.02.006
analysis in order to determine a safe time for surgery and showed a more precise cutoff period to assess the risk of meniscal or cartilage lesions in delayed ACL reconstruction. Similar to previous reports, we observed a strong association between increasing surgical timing and risk of MM lesions in this study. Many previous studies have reported an increase in the incidence of MM lesions 5e12 months after an ACL injury [2,4,9,10,12e14]. A higher incidence of MM lesion due to delay in surgery is probably attributable to the function of MM as a first restraint to anterior tibial translation in the ACL-deficient situation [24]. Krutsch et al. investigated the incidence of MM lesions in patients who underwent ACL reconstruction within 6 months after trauma compared with delayed ACL reconstruction 7e12 months after trauma. They found that the incidence of repairable MM lesions was higher within the first 6 months [14]. Kennedy et al. investigated the incidence of secondary pathology within the knee
joint at the time of surgery. They divided patients into five groups according to the time from injury to surgery (<2 months, 2e6 months, 6e12 months, 12e18 months, and >18 months) and found a significant increase in MM lesions at an interval to surgery >12 months [13]. The current study using ROC analysis instead of particular time point as a cutoff time revealed the precise threshold interval to surgery for increase in the incidence of MM lesion was 7 months; in other words, the incidence of MM lesions increased if ACL reconstruction was delayed by more than 6 months. This cutoff period is similar to that reported in previous studies [9,14]. Our study revealed that the risk of LM lesions was greater in patients in whom ACL reconstruction was delayed as the risk of MM lesions. However, OR for LM lesions after a cutoff period of 4 months was less than that for MM lesions after a cutoff period of 6
S. Taketomi et al. / Journal of Orthopaedic Science xxx (2018) 1e6
There are a few reports that show an association between surgical timing and LM tears [9,12,25]. Anderson et al. reported that delayed ACL reconstruction increased the risk of LM lesions, especially in younger patients [25]. Sri-Ram et al. reported that the odds of secondary LM lesion increased when ACL reconstruction was performed more than 12 months after injury compared with <6 months, although the odds were not high [9]. It has been reported LM is frequently injured at the same time as ACL [26]. Therefore, major giving-way episodes during the period between injury and surgical timing may lead to secondary LM lesions. However, we were unable to confirm this in our study because we did not have information on patient activity and the number of giving-way episodes during the period between the injury and surgical timing. This study revealed an increase in the incidence of articular chondral lesions 6 months after an ACL injury. There is no doubt that a long delay in undergoing ACL reconstruction in patients with an unstable knee is accompanied by an increased risk of chondral damage. On the other hand, there is controversy over whether the incidence of chondral lesions is increased in the relatively early phase after ACL injury. Krutsch et al. reported that the incidence of severe chondral lesions was not increased after 7e12 months of delay in undergoing ACL reconstruction [14]. In contrast, O'Connor found that the risk of articular cartilage lesions increased when ACL reconstruction was performed more than 1 year after injury [4]. The results of our study using ROC analysis suggest the possibility of chondral damage occurring earlier than expected after injury. Early chondral damage after ACL injury may be detected using new magnetic resonance imaging techniques such as T2 or T1-rho mapping [27,28]. Not only timing of surgery but also age, gender, physique or activity of patients can have influence on meniscal or chondral lesions. From the results of logistic regression analysis, only increased time to surgery was a significant risk factor for MM and LM lesion. On the other hand, increased age and female gender were a significant risk factor for chondral lesion. BMI and activity level were not significant risk factors for meniscal or chondral lesions. Influence of these factors on meniscal or chondral lesions differ depending on the study. Kluczynski et al. reported that male sex and sports type predicted MM tears and age predicted chondral injuries [22]. Brambilla et al. stated that the close association between BMI and prevalence of associated lesion suggested that attention be paid to patients with anelevated BMI when considering the timing of ACL surgery [7]. Moreover, Tandogan et al. found that age was important predictor of LM tears and chondral lesions. Female generally have weaker muscles supporting the knees, higher joint laxity, and a different leg axis, which may be one explanation for our results [12]. This study has several limitations. First, it was a retrospective study and the sample size was small. It is desirable to conduct a prospective cohort study with a larger sample size. Second, no randomization was performed because it was neither practical nor ethical to do so. Third, it was impossible to differentiate initial trauma from secondary lesions because meniscal and chondral lesions occurred as part of the initial injury. Fourth, this study does not include information on meniscus or cartilage treatment or its prognosis. Fifth, it is known that there is interobserver error in ICRS grading of chondral lesions. In recent literature, Dwyer reported the arthroscopic ICRS classification system did not have excellent but good interobserver reliability [29]. Sixth, when meniscal or chondral lesions were arthroscopically confirmed at the time of ACL reconstruction, they were determined to be existed in this study. Therefore, there is a possibility that they had existed earlier than assessment time. Finally, data on patient activity, usage of orthosis, or number of giving-way episodes during
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the period between injury and surgery were unknown. Some patients may have been involved in vigorous physical activity, whereas others may have had restricted physical activity during this period. 5. Conclusion ACL reconstruction should be performed within approximately 6 months after injury from the perspective of preventing associated meniscal or chondral lesions. Conflict of interest The authors declare there are no conflicts of interest directly relevant to the content of this article. References [1] Jomha NM, Borton DC, Clingeleffer AJ, Pinczewski LA. Long-term osteoarthritic changes in anterior cruciate ligament reconstructed knees. Clin Orthop Relat Res 1999 Jan;(358):188e93. [2] Chhadia AM, Inacio MC, Maletis GB, Csintalan RP, Davis BR, Funahashi TT. Are meniscus and cartilage injuries related to time to anterior cruciate ligament reconstruction? Am J Sports Med 2011 Sep;39(9):1894e9. [3] Shelbourne KD, Wilckens JH, Mollabashy A, DeCarlo M. Arthrofibrosis in acute anterior cruciate ligament reconstruction. The effect of timing of reconstruction and rehabilitation. Am J Sports Med 1991 JuleAug;19(4):332e6. [4] O'Connor DP, Laughlin MS, Woods GW. Factors related to additional knee injuries after anterior cruciate ligament injury. Arthroscopy 2005 Apr;21(4): 431e8. [5] Bottoni CR, Liddell TR, Trainor TJ, Freccero DM, Lindell KK. Postoperative range of motion following anterior cruciate ligament reconstruction using autograft hamstrings: a prospective, randomized clinical trial of early versus delayed reconstructions. Am J Sports Med 2008 Apr;36(4):656e62. [6] Anstey DE, Heyworth BE, Price MD, Gill TJ. Effect of timing of ACL reconstruction in surgery and development of meniscal and chondral lesions. Phys Sportsmed 2012 Feb;40(1):36e40. [7] Brambilla L, Pulici L, Carimati G, Quaglia A, Prospero E, Bait C, Morenghi E, Portinaro N, Denti M, Volpi P. Prevalence of associated lesions in anterior cruciate ligament reconstruction: correlation with surgical timing and with patient age, sex, and mody mass index. Am J Sports Med 2015 Dec;43(12): 2966e73. [8] Øiestad BE, Engebretsen L, Storheim K, Risberg MA. Knee osteoarthritis after anterior cruciate ligament injury: a systematic review. Am J Sports Med 2009 Jul;37(7):1434e43. [9] Sri-Ram K, Salmon LJ, Pinczewski LA, Roe JP. The incidence of secondary pathology after anterior cruciate ligament rupture in 5086 patients requiring ligament reconstruction. Bone Joint J 2013 Jan;95-B(1):59e64. [10] Church S, Keating JF. Reconstruction of the anterior cruciate ligament: timing of surgery and the incidence of meniscal tears and degenerative change. J Bone Joint Surg Br 2005 Dec;87(12):1639e42. [11] Foster A, Butcher C, Turner PG. Changes in arthroscopic findings in the anterior cruciate ligament deficient knee prior to reconstructive surgery. Knee 2005 Jan;12(1):33e5. [12] Tandogan RN, Tas¸er O, Kayaalp A, Tas¸kiran E, Pinar H, Alparslan B, Alturfan A. Analysis of meniscal and chondral lesions accompanying anterior cruciate ligament tears: relationship with age, time from injury, and level of sport. Knee Surg Sports Traumatol Arthrosc 2004 Jul;12(4):262e70. [13] Kennedy J, Jackson MP, O'Kelly P, Moran R. Timing of reconstruction of the anterior cruciate ligament in athletes and the incidence of secondary pathology within the knee. J Bone Joint Surg Br 2010 Mar;92(3):362e6. [14] Krutsch W, Zellner J, Baumann F, Pfeifer C, Nerlich M, Angele P. Timing of anterior cruciate ligament reconstruction within the first year after trauma and its influence on treatment of cartilage and meniscus pathology. Knee Surg Sports Traumatol Arthrosc 2017 Feb;25(2):418e25. [15] Cunningham ME, Donofrio MT, Peer SM, Zurakowski D, Jonas RA, Sinha P. Optimal timing for elective early primary repair of tetralogy of fallot: analysis of intermediate term outcomes. Ann Thorac Surg 2017 Mar;103(3): 845e52. [16] Jin M, Zhang H, Lu B, Li Y, Wu D, Qian J, Yang H. The optimal timing of enteral nutrition and its effect on the prognosis of acute pancreatitis: a propensity score matched cohort study. Pancreatology 2017 SepeOct;17(5):651e7. [17] Li S, Tian B. Acute pancreatitis in patients with pancreatic cancer: timing of surgery and survival duration. Medicine (Baltimore) 2017 Jan;96(3):e5908. [18] Kimura H, Kunisaki R, Tatsumi K, Koganei K, Sugita A, Endo I. Prolonged medical therapy increases the risk of surgical complications in patients with severe ulcerative colitis. Dig Surg 2016;33(3):182e9. [19] Kellgren JH, Lawrence JS. Radiological assessment of osteo-arthrosis. Ann Rheum Dis 1957 Dec;16(4):494e502.
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Contents lists available at ScienceDirect
Journal of Orthopaedic Science journal homepage: http://www.elsevier.com/locate/jos
Original Article
Surgical timing of anterior cruciate ligament reconstruction to prevent associated meniscal and cartilage lesions Shuji Taketomi a, *, Hiroshi Inui a, Ryota Yamagami a, Kohei Kawaguchi a, Keiu Nakazato a, Kenichi Kono a, Manabu Kawata a, Takumi Nakagawa b, Sakae Tanaka a a b
Department of Orthopaedic Surgery, Faculty of Medicine, The University of Tokyo, Tokyo, Japan Department of Orthopaedic Surgery, Teikyo University School of Medicine, Tokyo, Japan
a r t i c l e i n f o
a b s t r a c t
Article history: Received 23 August 2017 Received in revised form 26 January 2018 Accepted 12 February 2018 Available online xxx
Background: The purpose of this study was to analyze the association between the prevalence of meniscal and chondral lesions and the timing of surgery in patients undergoing primary anterior cruciate ligament (ACL) reconstruction to determine a safe time for surgery. Methods: This retrospective study involved 226 patients (91 females and 135 males; median age, 29 years) undergoing primary ACL reconstruction. Time interval from ACL injury to surgery (median, 4 months; range, 1e420 months) and concomitant meniscal and cartilage lesions in ACL reconstruction were reviewed. Receiver operating characteristic (ROC) curve analysis was used to determine the precise threshold interval to surgery to prevent meniscal or cartilage lesions. The risk of lesion occurrence after each cutoff period was determined using odds ratio (OR). Results: The incidences of medial meniscus (MM), lateral meniscus (LM), and cartilage lesions were 43.8%, 32.7%, and 27.4%, respectively. ROC analysis revealed that patients who waited for more than 6, 4, and 5 months for ACL reconstruction had a significantly greater risk of associated MM, LM, and chondral lesions, respectively. Patients who underwent ACL reconstruction 7 months after injury had OR of 4.1 (p < 0.001) for the presence of MM lesion as compared with those who underwent reconstruction within 6 months. Similarly, patients who underwent ACL reconstruction 5 months after injury had OR of 1.9 (p ¼ 0.023) for the presence of LM lesion as compared with those who underwent reconstruction within 4 months, and patients who underwent ACL reconstruction 6 months after injury had OR of 2.9 (p < 0.001) for chondral lesion as compared with those who underwent reconstruction within 6 months. Conclusion: ACL reconstruction should be performed within approximately 6 months after the injury to prevent associated meniscal or chondral lesions. © 2018 The Japanese Orthopaedic Association. Published by Elsevier B.V. All rights reserved.
1. Introduction Anterior cruciate ligament (ACL) rupture is one of the most common sports injuries, and ACL reconstruction has been widely performed for ACL rupture. ACL rupture is known to be associated with an increased risk of knee osteoarthritis (OA) [1,2]; therefore, the aim of ACL reconstruction is to prevent knee OA, as well as to restore normal knee kinematics and return to performing sports activities.
* Corresponding author. Department of Orthopaedic Surgery, Faculty of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-0033, Japan. Fax: þ81 3 3818 4082. E-mail address: [email protected] (S. Taketomi).
ACL reconstruction is often postponed for several weeks after injury because of inflammation, swelling, and restricted range of motion of the knee joint [3]. Some patients cannot avoid delaying ACL reconstruction because of several social situations. Delayed ACL reconstruction is considered to increase the incidence of meniscal injury or chondral lesions [4e7]. Meniscal tears and chondral injuries are often identified at the time of arthroscopic reconstruction. These lesions are considered to carry an increased risk of OA development [8]. Delaying ACL reconstruction for more than 1 year has been known to be a risk factor for knee OA [9e11]. However, there is no consensus on the ideal timing for ACL reconstruction in terms of decreasing the risk of secondary intraarticular lesions in ACL-deficient knees. In previous studies, many authors have used a particular time point as a cutoff, such as 6 or 12 months after injury, and compared the incidence of concomitant articular lesions before
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Please cite this article in press as: Taketomi S, et al., Surgical timing of anterior cruciate ligament reconstruction to prevent associated meniscal and cartilage lesions, Journal of Orthopaedic Science (2018), https://doi.org/10.1016/j.jos.2018.02.006
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and after such a cutoff period [9,12e14]. There is a need for a more precise estimation of the appropriate interval before ACL reconstruction without increasing the risk of meniscal or cartilage lesions. In the field of surgery in recent years, receiver operating characteristic (ROC) curve has been frequently used in order to identify cutoff threshold time for surgery or other interventions [15e18]. In this study, we used ROC curve analysis in order to determine a safe time for surgery and showed a more precise cutoff period to assess the risk of meniscal or chondral lesions in delayed ACL reconstruction, instead of a particular time point as cutoff, such as 6 or 12 months after injury. The purpose of this study was to determine a safe time for surgery by analyzing the association between the prevalence of meniscal and chondral lesions and the timing of surgery in patients undergoing primary ACL reconstruction. The hypothesis of this study was that after ACL rupture, the incidence of meniscal and cartilage lesions increases after a certain time point. 2. Materials and methods This study was a retrospective case series. Medical records of 260 patients who underwent primary ACL reconstruction between August 2010 and July 2016 were reviewed. Patients were excluded from the study under the following conditions: (1) previous intraarticular surgery such as ligamentous, meniscal, or chondral surgery or previous osteotomy or fracture around the knee joint; (2) presence of posterior cruciate ligament insufficiency, abnormal varus/valgus instability, or concomitant reconstruction of other ligaments; (3) presence of OA (Kellgren and Lawrence classification [19] II); and (4) unknown time of injury. In total, 34 patients were excluded. Our final analysis included 226 patients (91 females and 135 males) with a median age of 29 years (range, 14e62 years). Baseline patient demographics are summarized in Table 1. Our local institutional review board has approved this retrospective study. Patients and their families were informed that their data would be submitted for publication, and all provided written informed consent for the same. Time to ACL reconstruction was calculated as the difference in the number of months between the date of injury and surgery. The time between ACL injury and reconstruction may have been determined by several uncontrollable factors, including misdiagnosis, nonsurgical management, patient convenience, waiting list for surgery, and financial reasons. Surgical timing was also determined by the state of the knee joint, including swelling or restriction of joint movement. A large number of patients were referred to our institute for surgery after significant delay. The presence of meniscal and cartilage lesions at the time of ACL reconstruction was collected from analysis of surgical records. Concomitant meniscal and cartilage lesions in all patients had been recorded during ACL reconstruction. Only those requiring meniscal suture, partial
meniscectomy, or meniscal rasping during ACL reconstruction were considered to have meniscal lesion. The morphology of the meniscal lesion was also recorded. Cartilage lesions were classified according to the International Cartilage Repair Society (ICRS) system [20]. When grade IIeIV chondral lesion was present in medial femoral condyle, lateral femoral condyle, medial tibial plateau, lateral tibial plateau, trochlea, or patella, the site and ICRS grade of chondral lesions were recorded. 2.1. Statistical analysis Statistical analysis was performed using the EXCEL statistics 2012 software package for Microsoft Windows (SSRI Co., Ltd., Tokyo, Japan). Patient parameters were compared using the Student's t-test, ManneWhitney U test, or chi-square test. ROC curve analysis was used to determine the precise threshold interval to surgery to prevent meniscal or cartilage lesions. The risk of lesion occurrence after each cutoff period was determined using odds ratio (OR). To identify potential risk factors of meniscal or chondral lesion, age, gender, body mass index, Tegner activity scale, and time to surgery which have probably impact on these lesions were compared using multivariate logistic regression. Statistical significance was set at P < 0.05. 3. Results In total, 99 (43.8%) and 74 (32.7%) patients had medial meniscus (MM) and lateral meniscus (LM) lesions, respectively, at the time of surgery. The morphology of the meniscal lesion is described in detail in Table 2. Longitudinal tears were most commonly observed in both MM and LM lesions. Sixty-two (27.4%) patients had a chondral lesion. The location and severity of the chondral lesions are shown in Table 3. Chondral lesions were frequently observed in the medial femoral condyle and the lateral tibial plateau. 3.1. MM lesion The association between MM lesion and surgical timing is shown in Fig. 1A. The incidence of MM lesion increased with an increase in the waiting period before surgery. ROC was used to analyze the best cutoff period from ACL injury to ACL reconstruction based on the incidence of MM lesions (Fig. 1B). The best cutoff period for surgery was 7 months, with an area under curve (AUC) of 0.683. There were 45 (31.5%) MM lesions in patients who underwent ACL reconstruction before the cutoff period compared with 54 (65.1%) MM lesions in those in whom ACL reconstruction was delayed. Patients who underwent ACL reconstruction 7 months after injury had OR of 4.1 [95% confidence interval (CI), 2.3e7.2; p < 0.001] for the presence of an MM lesion compared with those Table 2 Morphology of meniscal lesion.
Table 1 Patient demographics.
Number of patients Age (years old) Gender (female/male) BMI (kg/m2) Tegner Activity Scale Time to surgery (months)
Overall
Early surgery Delayed surgery P value (6 months) (>6 months)
226 29 (14e62) 91/135 23.3 ± 4.0 7 (3e10) 4 (1e420)
143 25 (14e62) 56/87 23.3 ± 4.1 8 (3e10) 3 (1e6)
83 32 (15e61) 35/48 23.4 ± 4.0 7 (3e9) 16 (7e420)
0.003 0.657 0.837 0.001 0.000
BMI, body mass index. Data are given as mean ± standard deviation or median (range). P values between early surgery group and delayed surgery group are shown.
Longitudinal tear Bucket handle tear Radial tear Flap tear Posterior root tear Horizontal tear Complex tear Defect or partial defect Discoid meniscus tear Others Total
MM
LM
56 (56.6%) 19 (19.2%) 0 (0%) 10 (10.1%) 0 (0%) 3 (3.0%) 3 (3.0%) 4 (4.0%) 0 (0%) 4 (4.0%) 99
34 (45.9%) 7 (9.5%) 12 (16.2%) 11 (14.9%) 5 (6.8%) 1 (1.4%) 1 (1.4%) 0 (0%) 1 (1.4%) 2 (2.7%) 74
MM, medial meniscus; LM, lateral meniscus.
Please cite this article in press as: Taketomi S, et al., Surgical timing of anterior cruciate ligament reconstruction to prevent associated meniscal and cartilage lesions, Journal of Orthopaedic Science (2018), https://doi.org/10.1016/j.jos.2018.02.006
S. Taketomi et al. / Journal of Orthopaedic Science xxx (2018) 1e6 Table 3 Location and severity of chondral lesions.
Medial femoral condyle Medial tibial plateau Lateral femoral condyle Lateral tibial plateau Trochlea Patella
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Table 4 Odds ratio of intraarticular lesions with increasing time to injury.
ICRS II
ICRS III
ICRS IV
Total
26 (11.5%) 10 (4.4%) 2 (0.9%) 22 (9.7%) 10 (4.4%) 0 (0%)
8 0 1 3 4 0
1 0 1 0 0 0
35 (15.5%) 10 (4.4%) 4 (1.8%) 25 (11.1%) 14 (6.2%) 0 (0%)
(3.5%) (0%) (0.4%) (1.3%) (1.8%) (0%)
(0.4%) (0%) (0.4%) (0%) (0%) (0%)
ICRS, International Cartilage Repair Society.
who underwent ACL reconstruction within 6 months (Table 4). In logistic regression analysis, increased time to surgery was a significant risk factor for MM lesion. The other parameters were not significant risk factors of MM lesion (Table 5). 3.2. LM lesion The association between LM lesion and surgical timing is shown in Fig. 2A. The incidence of LM lesion also increased with an increase in the waiting period before surgery. ROC was used to analyze the best cutoff period from ACL injury to ACL reconstruction based on the incidence of LM lesions (Fig. 2B). The best cutoff period for surgery was 5 months, with AUC of 0.585. There were 29 (25.7%) LM lesions in patients who underwent ACL reconstruction before the cutoff period compared with 45 (39.8%) LM lesions in those in whom ACL reconstruction was delayed. Patients who underwent ACL reconstruction 5 months after injury had OR of 1.9 (95% CI, 1.1e3.4; p ¼ 0.023) for the presence of an LM lesion compared with those who underwent ACL reconstruction within 4 months (Table 4). In logistic regression analysis, increased time to surgery was a significant risk factor for LM lesion. The other parameters were not significant risk factors of LM lesion (Table 5). 3.3. Chondral lesion The association between chondral lesion and surgical timing is shown in Fig. 3A. The number of chondral lesions increased with an increase in the waiting period before surgery. ROC was used to analyze the best cutoff period from ACL injury to ACL reconstruction based on the presence of chondral lesions (Fig. 3B). The best cutoff period for surgery was 6 months, with AUC of 0.650. There were 25 (18.8%) chondral lesions in patients who underwent surgery before the cutoff period compared with 37 (39.8%) chondral lesions in those in whom ACL reconstruction was delayed. Patients who underwent ACL reconstruction 6 months after injury had OR
MM lesion LM lesion Chondral lesion
Cutoff time
OR (95%CI)
p value
7 months 5 months 6 months
4.1 (2.3e7.2) 1.9 (1.1e3.4) 2.8 (1.6e5.2)
<0.001 0.023 <0.001
MM, medial meniscus; LM, lateral meniscus; OR, odds ratio; CI, confidence interval.
of 2.9 (95% CI, 1.6e5.2; p < 0.001) for the presence of a chondral lesion as compared with those who underwent ACL reconstruction within 6 months (Table 4). In logistic regression analysis, increased age and female gender were a significant risk factor for chondral lesion. Time to surgery was not significant risk factors of chondral lesion (Table 5). From the results of this study, patients were sorted into the early surgery group and the delayed surgery group. Demographic data of each group are shown in Table 1. There were significant differences in age, activity level and time to surgery. There was no significant difference in the other parameters. 4. Discussion In this study, the incidences of MM and LM lesions were 43.8% and 32.7%, respectively. In addition, the overall incidence of articular cartilage lesions was 27.4%. The incidences of MM, LM, and chondral lesions observed at the time of ACL reconstruction vary widely in previous reports, ranging from 27.1% to 56.9%, from 29.1% to 52.3%, and from 15.2% to 42.3%, respectively [4,7,9,12,13,21e23]. The incidence of concomitant intraarticular lesions in this study is consistent with that reported in previous reports. This is a unique study using ROC curve analysis to determine a safe cutoff period for ACL reconstruction to prevent associated meniscal and cartilage lesions. The ROC analysis revealed that patients who waited more than 6, 4, and 5 months to undergo ACL reconstruction had a significantly greater risk of associated MM, LM, and chondral lesions, respectively. Our results show that ACL reconstruction should be performed within preferably 4 months or within maximum 6 months after the injury to prevent associated meniscal or chondral lesions. The main strength of this study is that we used ROC analysis to calculate a cutoff period. Many previous investigators used a particular time point as cutoff, such as 6 or 12 months after injury, and compared the incidence of concomitant articular lesions before and after such a cutoff period. ROC curve analysis is often used to determine an optimal surgical timing in general surgery [15e18]. This is the first study that used ROC curve
Fig. 1. (A) Association between medial meniscal lesion and surgical timing. (B) Receiver operating characteristic curve of medial meniscal lesion. MM, medial meniscus; ROC, receiver operating characteristic; TPF, true-positive fraction; FPF, false-positive fraction.
Please cite this article in press as: Taketomi S, et al., Surgical timing of anterior cruciate ligament reconstruction to prevent associated meniscal and cartilage lesions, Journal of Orthopaedic Science (2018), https://doi.org/10.1016/j.jos.2018.02.006
analysis in order to determine a safe time for surgery and showed a more precise cutoff period to assess the risk of meniscal or cartilage lesions in delayed ACL reconstruction. Similar to previous reports, we observed a strong association between increasing surgical timing and risk of MM lesions in this study. Many previous studies have reported an increase in the incidence of MM lesions 5e12 months after an ACL injury [2,4,9,10,12e14]. A higher incidence of MM lesion due to delay in surgery is probably attributable to the function of MM as a first restraint to anterior tibial translation in the ACL-deficient situation [24]. Krutsch et al. investigated the incidence of MM lesions in patients who underwent ACL reconstruction within 6 months after trauma compared with delayed ACL reconstruction 7e12 months after trauma. They found that the incidence of repairable MM lesions was higher within the first 6 months [14]. Kennedy et al. investigated the incidence of secondary pathology within the knee
joint at the time of surgery. They divided patients into five groups according to the time from injury to surgery (<2 months, 2e6 months, 6e12 months, 12e18 months, and >18 months) and found a significant increase in MM lesions at an interval to surgery >12 months [13]. The current study using ROC analysis instead of particular time point as a cutoff time revealed the precise threshold interval to surgery for increase in the incidence of MM lesion was 7 months; in other words, the incidence of MM lesions increased if ACL reconstruction was delayed by more than 6 months. This cutoff period is similar to that reported in previous studies [9,14]. Our study revealed that the risk of LM lesions was greater in patients in whom ACL reconstruction was delayed as the risk of MM lesions. However, OR for LM lesions after a cutoff period of 4 months was less than that for MM lesions after a cutoff period of 6
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There are a few reports that show an association between surgical timing and LM tears [9,12,25]. Anderson et al. reported that delayed ACL reconstruction increased the risk of LM lesions, especially in younger patients [25]. Sri-Ram et al. reported that the odds of secondary LM lesion increased when ACL reconstruction was performed more than 12 months after injury compared with <6 months, although the odds were not high [9]. It has been reported LM is frequently injured at the same time as ACL [26]. Therefore, major giving-way episodes during the period between injury and surgical timing may lead to secondary LM lesions. However, we were unable to confirm this in our study because we did not have information on patient activity and the number of giving-way episodes during the period between the injury and surgical timing. This study revealed an increase in the incidence of articular chondral lesions 6 months after an ACL injury. There is no doubt that a long delay in undergoing ACL reconstruction in patients with an unstable knee is accompanied by an increased risk of chondral damage. On the other hand, there is controversy over whether the incidence of chondral lesions is increased in the relatively early phase after ACL injury. Krutsch et al. reported that the incidence of severe chondral lesions was not increased after 7e12 months of delay in undergoing ACL reconstruction [14]. In contrast, O'Connor found that the risk of articular cartilage lesions increased when ACL reconstruction was performed more than 1 year after injury [4]. The results of our study using ROC analysis suggest the possibility of chondral damage occurring earlier than expected after injury. Early chondral damage after ACL injury may be detected using new magnetic resonance imaging techniques such as T2 or T1-rho mapping [27,28]. Not only timing of surgery but also age, gender, physique or activity of patients can have influence on meniscal or chondral lesions. From the results of logistic regression analysis, only increased time to surgery was a significant risk factor for MM and LM lesion. On the other hand, increased age and female gender were a significant risk factor for chondral lesion. BMI and activity level were not significant risk factors for meniscal or chondral lesions. Influence of these factors on meniscal or chondral lesions differ depending on the study. Kluczynski et al. reported that male sex and sports type predicted MM tears and age predicted chondral injuries [22]. Brambilla et al. stated that the close association between BMI and prevalence of associated lesion suggested that attention be paid to patients with anelevated BMI when considering the timing of ACL surgery [7]. Moreover, Tandogan et al. found that age was important predictor of LM tears and chondral lesions. Female generally have weaker muscles supporting the knees, higher joint laxity, and a different leg axis, which may be one explanation for our results [12]. This study has several limitations. First, it was a retrospective study and the sample size was small. It is desirable to conduct a prospective cohort study with a larger sample size. Second, no randomization was performed because it was neither practical nor ethical to do so. Third, it was impossible to differentiate initial trauma from secondary lesions because meniscal and chondral lesions occurred as part of the initial injury. Fourth, this study does not include information on meniscus or cartilage treatment or its prognosis. Fifth, it is known that there is interobserver error in ICRS grading of chondral lesions. In recent literature, Dwyer reported the arthroscopic ICRS classification system did not have excellent but good interobserver reliability [29]. Sixth, when meniscal or chondral lesions were arthroscopically confirmed at the time of ACL reconstruction, they were determined to be existed in this study. Therefore, there is a possibility that they had existed earlier than assessment time. Finally, data on patient activity, usage of orthosis, or number of giving-way episodes during
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the period between injury and surgery were unknown. Some patients may have been involved in vigorous physical activity, whereas others may have had restricted physical activity during this period. 5. Conclusion ACL reconstruction should be performed within approximately 6 months after injury from the perspective of preventing associated meniscal or chondral lesions. Conflict of interest The authors declare there are no conflicts of interest directly relevant to the content of this article. References [1] Jomha NM, Borton DC, Clingeleffer AJ, Pinczewski LA. Long-term osteoarthritic changes in anterior cruciate ligament reconstructed knees. Clin Orthop Relat Res 1999 Jan;(358):188e93. [2] Chhadia AM, Inacio MC, Maletis GB, Csintalan RP, Davis BR, Funahashi TT. Are meniscus and cartilage injuries related to time to anterior cruciate ligament reconstruction? Am J Sports Med 2011 Sep;39(9):1894e9. [3] Shelbourne KD, Wilckens JH, Mollabashy A, DeCarlo M. Arthrofibrosis in acute anterior cruciate ligament reconstruction. The effect of timing of reconstruction and rehabilitation. Am J Sports Med 1991 JuleAug;19(4):332e6. [4] O'Connor DP, Laughlin MS, Woods GW. Factors related to additional knee injuries after anterior cruciate ligament injury. Arthroscopy 2005 Apr;21(4): 431e8. [5] Bottoni CR, Liddell TR, Trainor TJ, Freccero DM, Lindell KK. Postoperative range of motion following anterior cruciate ligament reconstruction using autograft hamstrings: a prospective, randomized clinical trial of early versus delayed reconstructions. Am J Sports Med 2008 Apr;36(4):656e62. [6] Anstey DE, Heyworth BE, Price MD, Gill TJ. Effect of timing of ACL reconstruction in surgery and development of meniscal and chondral lesions. Phys Sportsmed 2012 Feb;40(1):36e40. [7] Brambilla L, Pulici L, Carimati G, Quaglia A, Prospero E, Bait C, Morenghi E, Portinaro N, Denti M, Volpi P. Prevalence of associated lesions in anterior cruciate ligament reconstruction: correlation with surgical timing and with patient age, sex, and mody mass index. Am J Sports Med 2015 Dec;43(12): 2966e73. [8] Øiestad BE, Engebretsen L, Storheim K, Risberg MA. Knee osteoarthritis after anterior cruciate ligament injury: a systematic review. Am J Sports Med 2009 Jul;37(7):1434e43. [9] Sri-Ram K, Salmon LJ, Pinczewski LA, Roe JP. The incidence of secondary pathology after anterior cruciate ligament rupture in 5086 patients requiring ligament reconstruction. Bone Joint J 2013 Jan;95-B(1):59e64. [10] Church S, Keating JF. Reconstruction of the anterior cruciate ligament: timing of surgery and the incidence of meniscal tears and degenerative change. J Bone Joint Surg Br 2005 Dec;87(12):1639e42. [11] Foster A, Butcher C, Turner PG. Changes in arthroscopic findings in the anterior cruciate ligament deficient knee prior to reconstructive surgery. Knee 2005 Jan;12(1):33e5. [12] Tandogan RN, Tas¸er O, Kayaalp A, Tas¸kiran E, Pinar H, Alparslan B, Alturfan A. Analysis of meniscal and chondral lesions accompanying anterior cruciate ligament tears: relationship with age, time from injury, and level of sport. Knee Surg Sports Traumatol Arthrosc 2004 Jul;12(4):262e70. [13] Kennedy J, Jackson MP, O'Kelly P, Moran R. Timing of reconstruction of the anterior cruciate ligament in athletes and the incidence of secondary pathology within the knee. J Bone Joint Surg Br 2010 Mar;92(3):362e6. [14] Krutsch W, Zellner J, Baumann F, Pfeifer C, Nerlich M, Angele P. Timing of anterior cruciate ligament reconstruction within the first year after trauma and its influence on treatment of cartilage and meniscus pathology. Knee Surg Sports Traumatol Arthrosc 2017 Feb;25(2):418e25. [15] Cunningham ME, Donofrio MT, Peer SM, Zurakowski D, Jonas RA, Sinha P. Optimal timing for elective early primary repair of tetralogy of fallot: analysis of intermediate term outcomes. Ann Thorac Surg 2017 Mar;103(3): 845e52. [16] Jin M, Zhang H, Lu B, Li Y, Wu D, Qian J, Yang H. The optimal timing of enteral nutrition and its effect on the prognosis of acute pancreatitis: a propensity score matched cohort study. Pancreatology 2017 SepeOct;17(5):651e7. [17] Li S, Tian B. Acute pancreatitis in patients with pancreatic cancer: timing of surgery and survival duration. Medicine (Baltimore) 2017 Jan;96(3):e5908. [18] Kimura H, Kunisaki R, Tatsumi K, Koganei K, Sugita A, Endo I. Prolonged medical therapy increases the risk of surgical complications in patients with severe ulcerative colitis. Dig Surg 2016;33(3):182e9. [19] Kellgren JH, Lawrence JS. Radiological assessment of osteo-arthrosis. Ann Rheum Dis 1957 Dec;16(4):494e502.
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Please cite this article in press as: Taketomi S, et al., Surgical timing of anterior cruciate ligament reconstruction to prevent associated meniscal and cartilage lesions, Journal of Orthopaedic Science (2018), https://doi.org/10.1016/j.jos.2018.02.006