Clinical and magnetic resonance imaging

Clinical and magnetic resonance imaging assessment of anatomical lateral ankle ligament reconstruction: comparison of tendon allograft and autograft Qianru Li, Kui Ma, Hongyue Tao, Yinghui Hua, Shuang Chen, Shiyi Chen & Yutong Zhao International Orthopaedics ISSN 0341-2695 Volume 42 Number 3 International Orthopaedics (SICOT) (2018) 42:551-557 DOI 10.1007/s00264-018-3802-5

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Author's personal copy International Orthopaedics (2018) 42:551–557 https://doi.org/10.1007/s00264-018-3802-5

ORIGINAL PAPER

Clinical and magnetic resonance imaging assessment of anatomical lateral ankle ligament reconstruction: comparison of tendon allograft and autograft Qianru Li 1 & Kui Ma 1 & Hongyue Tao 1 & Yinghui Hua 1 & Shuang Chen 1 & Shiyi Chen 1 & Yutong Zhao 2 Received: 14 October 2017 / Accepted: 23 January 2018 / Published online: 5 February 2018 # SICOT aisbl 2018

Abstract Purpose To compare the results of anatomical lateral ankle ligament (LAL) reconstruction with tendon allograft and autograft using clinical scores and ultrashort echo time (UTE) sequence of MRI. Methods A total of 26 patients with LAL reconstruction were recruited in this study, including 16 using semitendinosus allografts and 10 using semitendinosus autograft. All of them were diagnosed as chronic ankle instability and accepted anatomic reconstruction. The American Orthopedic Foot and Ankle Society (AOFAS) score, Karlsson score, and radiological evaluation using MRI UTE scanning were extracted from each patient. The comparative analysis of the clinical assessments and UTE-T2* values were performed between the patients using autografts and allografts. Results For the allograft group, the mean AOFAS score improved from 69.9 ± 13.3 to 94.8 ± 5.4 (P = 0.000), and the mean Karlsson score improved from 70.3 ± 12.2 to 93.8 ± 5.6 (P = 0.000). For the autograft group, the mean AOFAS score improved from 68.4 ± 10.0 to 94.7 ± 5.0 (P = 0.000), and the mean Karlsson score improved from 64.5 ± 14.4 to 95.0 ± 5.8 (P = 0.000). No significant differences were found between the allograft and autograft neither before (AOFAS P = 0.756, Karlsson P = 0.285) nor after (AOFAS P = 0.957, Karlsson P = 0.574) surgery. While the UTE T2* values in allograft were higher than those of autograft group both in anterior talofibular ligament (8.3 ± 1.0 vs 7.6 ± 1.1 P = 0.027) and intra-tunnel graft (7.8 ± 0.6 vs 7.2 ± 0.8 P = 0.045). Conclusion Both allograft and autograft reconstructions could get an ideal patient satisfaction and clinical functional outcomes at the follow-up. Higher T2* values were found in allograft group which indicated that autograft had some superiorities in respect of revascularization process, collagen structure, water content, and tendon properties. Keywords Lateral ankle ligament reconstruction . Ankle instability . Clinical evaluation . MRI . Ultrashort echo time

Introduction Ankle sprains are considered to be one of the commonest sports injuries with an incidence rate of 2.15 per 1000 person-years among an at-risk population [1]. Even with

proper treatment, there are still about 20–40% patients developing to chronic ankle instability (CAI) [2], a most commonly used term to describe participants who report ongoing symptoms after an initial ankle sprain [3]. The lateral ligament complex of the ankle is most likely to get hurt in an

* Yinghui Hua [email protected]

Shuang Chen [email protected]

Qianru Li [email protected]

Shiyi Chen [email protected]

Kui Ma [email protected]

Yutong Zhao [email protected]

Hongyue Tao [email protected]

1

Department of Sports Medicine, Huashan Hospital, 12 Wulumuqi Zhong Road, Shanghai 200040, China

2

Dunn School, 2555 Highway 154, Los Olivos, CA 93441, USA

Author's personal copy 552

ankle sprain, and it consists of the anterior talofibular ligament (ATFL), calcaneofibular ligament (CFL), and posterior talofibular ligament (PTFL) [4]. According to Broström, approximately two-thirds of ankle sprains are isolated injuries to the ATFL [5]. When patients with chronic ankle instability fail to improve through a conservative management course and physical therapy, surgery is, in most cases, the only option for them [6]. There are three main surgery methods for CAI: anatomic ligament repair, non-anatomic ligament reconstruction, and anatomic ligament reconstruction. Anatomic reconstruction has superiority as it can restore the normal ankle mechanics [7, 8] and provide a better ankle joint function [9]. In anatomic reconstruction surgery, allograft or autograft can be chosen, and a systematic review about anterior cruciate ligament concluded that short-term clinical outcomes of anterior crucial ligament (ACL) autograft reconstruction were not significantly different with allograft [10]. A study from Hong Li et al. showed that functional scores, clinical tests, and magnetic resonance imaging (MRI) measurements were not significantly different between allograft and autograft, except for the mean signal/noise quotient (SNQ) value of the graft using 3.0-T MRI scanner [11]. As known to all, the highly organized tissues such as tendons, ligaments, menisci, periosteum, and cortical bone have very short mean transverse relaxation times and show little or no signal with commonly used clinical spin echo or gradient echo sequences [12]. Unlike the conventional MRI sequences, three-dimensional ultrashort echo time (UTE) imaging can detect short T(2) components before they have decayed [13] and quantify the collagen structure, proteoglycan, and water content of tendon [14]. And as far as we know, there are no studies about the assessment of lateral ankle ligament after allograft or autograft reconstruction surgery by using UTE technology to evaluate the condition of collagen and water. The present study aimed to compare the results of clinical and MRI evaluation between the allograft and autograft postoperatively. We hypothesized that allograft tendons might have similar clinical result while inferior MRI result compared with that of autograft tendons after surgery.

International Orthopaedics (SICOT) (2018) 42:551–557

allograft ATFL reconstruction (allograft group, 11 of them combined with CFL damage) and ten with autograft ATFL reconstruction (autograft group, five of them combined with CFL damage). The demographic data of the patients are shown in Table 1. There were no significant differences in gender (P = 1.000), age (P = 0.497), and body mass index (P = 0.173) between the allograft group and the autograft group. Furthermore, no significant difference was found in the injured side (P = 1.000), the time from initial injury to surgery (P = 0.513), and the average follow-up time (P = 0.586) between two groups. Participants were excluded if they had any contraindication for MR.

Surgical technique One senior surgeon (the corresponding author) performed all the operations using anatomical reconstruction techniques. The choice of graft was made by each patient after all the potential advantages and disadvantages were stated by the senior surgeon. The patients were placed in the supine position with spinal anesthesia. A tourniquet was routinely applied at the proximal thigh. After diagnostic arthroscopy, associated intra-articular injury was treated before LAL reconstruction. A straight skin incision was made from the tip of the distal fibula to the talus insertion of the ATFL. The anterior edge of the distal fibula was exposed to show the insertion of the ATFL and CFL. A second straight incision was made posterior to the fibula, and then two oblique tunnels with diameter of 3.5 mm were made in the fibula. The distances from these two holes to the tip of fibula were 7 and 13 mm respectively, and the directions of these two tunnels were upper- and post-oriented [15]. Another two 3.5-mm converging tunnels just distal to the edge of the cartilage and 18 mm proximal to the subtalar joint were made through the talus [16]. In case of ATCL combined with CFL injury, a third straight incision was made parallel and below the first incision to expose the tubercle of the calcaneus. A Bill’s pin was drilled just at the tubercle of the calcaneus and passed to the medial aspect. And the fifth tunnel was made with a 6mm reamer 25 mm in length.

Materials and methods Table 1

Patients The study was approved by the institutional review board of Huashan Hospital, and all participants’ informed consents were obtained. A total of 26 patients who have been diagnosed with chronic ankle instability and received anatomic lateral ankle ligament (LAL) reconstruction surgery from June 2007 to September 2014 were recruited in this study retrospectively with written consent, including 16 with

Comparison of patients demographics

Variable

Allograft

Autograft

P value

Gender (male/female) Age (years) BMI (kg/m2) Injured ankle (right/left) Duration time (months) Follow-up time (months)

13/3 34.1 ± 11.2 24.1 ± 3.0 9/7 39.7 ± 32.0 55.9 ± 35.5

8/2 31.3 ± 8.1 26.0 ± 3.8 6/4 42.8 ± 54.6 37.7 ± 20.8

1.000 0.497 0.173 1.000 0.895 0.579

Author's personal copy International Orthopaedics (SICOT) (2018) 42:551–557

For the autograft reconstruction, the semitendinosus tendon was harvested from the ipsilateral affected limb. In the allograft group, a 20-cm semitendinosus allograft (Osteolink Biomaterial Co Ltd., Hubei, China) was thawed in sterile physiological fluid with antibiotics for 15 min at room temperature and trimmed to 3.5 mm in diameter before pretension for 15 min at a force of 15 N. And then one end of the graft was pulled into the bone tunnel of the calcaneus and fixed with a bioabsorbable screw (Smith & Nephew, Andover, MA, USA) with a diameter of 7 mm. After the graft was pulled into the holes and through the tunnels, full range ankle movements were performed 20 times to confirm the isometricity and adjust the tension of the graft. Then, the free end of the graft was sutured to the tendon itself with the ankle joint in a neutral position. The capsule was sutured back to cover the graft, and the incision was closed (Fig. 1). A short leg cast was applied to immobilize the movement of ankle after the operation. All the patients were rehabilitated according to the same protocol. From the day after surgery, rehabilitation exercises including isometric contraction of muscles functionalizing the ankle were utilized. After two weeks of the operation, the cast was placed by an ankle orthosis, and passive movement was encouraged. Partial loadbearing with crutches was permitted at four weeks, and active movement was allowed at six months post-operatively.

Clinical evaluation Clinical examination was performed on the same day the MRI examination was performed, including American Orthopedic Foot and Ankle Society (AOFAS) score and

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Karlsson score. The AOFAS score was interpreted as poor if AOFAS < 50, fair if 50 ≤ AOFAS ≤ 74, good if 75 ≤ AOFAS ≤ 89, and excellent if 90 ≤ AOFAS ≤ 100 [17]. The Karlsson score was interpreted as poor if Karlsson < 60, fair if 60 ≤ Karlsson ≤ 74, good if 75 ≤ Karlsson ≤ 84, and excellent if 85 ≤ Karlsson ≤ 100 [18].

MRI and image analysis All patients were examined in a 3.0 T horizontal magnet (Discovery MR750, GE Medical System, Milwaukee, WI) with a 60-mm-diameter gradient coil (Magtron Inc., Jiangyin, China). Four echo time images (TE = 0.03, 1.0, 7.5, and 20.0 ms) were obtained. Other parameters were set as follows: repetition time (TR) = 4000 ms, scan time = two minutes for each echo time, field of view (FOV) = 14 cm × 16.9 cm, matrix = 256,146 × 256, slice thickness (ST) = 2 mm, spatial resolution = 0.24 × 0.24 × 1.8 mm3, inter-slice distance = 2 mm, number of slices = 30. For morphological evaluation of the reconstructed ligament, the following sequences were also used: three-dimensional fat-saturated proton-density-weighted turbo-spin echo (PDTSE), axial T2weighted TSE (ax T2 TSE), and a fat-saturated sagittal T1weighted sequence (Fig. 2). For further qualitative measurement, two different regions of interests (ROIs) were manually made on the MRI UTE images (TE = 0.03 ms). The ROIs were placed on the axial, sagittal plane respectively to draw the outline of reconstructed ATFL and the graft in the fibula (Fig. 3). T2* value of each region is calculated by fitting the acquired signal at different echo time to a single exponential decay model.

Statistical methods

Fig. 1 Scheme of the route of reconstruction of the ATFL

Data analysis was performed using SPSS 24.0 software (IBM Corp, Armonk, New York, USA). Age and BMI were expressed as mean ± SD, because they were normally distributed via the Lilliefors test and were assessed with t test. The gender and number of injured side were assessed with Chi-square test. The duration and followup time were tested with Kruskal-Wallis test. The AOFAS score and Karlsson score before surgery were assessed with t test due to its normal distribution, and these two scores post-operatively were assessed with Kruskal-Wallis test because of non-normal distribution. The UTE-T2* value of ATFL was tested with Kruskal-Wallis test because of its non-normal distribution, and the value of intra-tunnel graft was assessed with t test for its normal distribution. A P value less than 0.05 was considered to be statistically significant.



Fig. 2 Comparison of the visualization of ATFL using PD and UTE respectively. a Axial plane in PD TSE sequences, the relatively low signal intensity part between the white arrows is ATFL. b The same plane in UTE sequences, the high signal intensity part between the black arrows is ATFL

Results Clinical assessment All the participants returned to normal sports activities at the follow-up time point, as all of them acquired full functional ankle strength and stability. No infection and no synovitis were found in all the participants. For the allograft group, the mean AOFAS score improved from 69.9 ± 13.3 to 94.8 ± 5.4 (P = 0.000), and the mean Karlsson score improved from 70.3 ± 12.2 to 93.8 ± 5.6 (P = 0.000) (Fig. 4). For the autograft group, the mean AOFAS score improved from 68.4 ± 10.0 to 94.7 ± 5.0 (P = 0.000), and the mean Karlsson score improved from 64.5 ± 14.4 to 95.0 ± 5.8 (P = 0.000) (Fig. 4). According to the AOFAS grading criteria, there were 13 graded as excellent and three graded as good in the allograft groups, and there were eight graded as excellent and two graded as good in the autograft group. In the point of Karlsson grading criteria, all the patients (16 and 10) in both groups were graded as excellent. Moreover, in terms of AOFAS and Karlsson score, there were no significant differences between the allograft and

Fig. 3 Two different regions of interests (ROIs) were manually made on the MRI UTE images. a The first ROI was placed on the axial plane to draw the outline of reconstructed ATFL. b The second ROI was placed on the sagittal plane to draw the outline of intra-tunnel graft. T talus, F fibula

autograft neither before (AOFAS P = 0.756, Karlsson P = 0.285) nor after (AOFAS P = 0.957, Karlsson P = 0.574) surgery (Table 2).

MRI UTE-T2* value The UTE-T2* value of ATFL showed a significant difference between the allograft group and autograft group (P = 0.027). Furthermore, the value of graft in the fibula tunnel also presented a significant difference between these two groups (P = 0.045) (Fig. 5).

Discussion In this study, we found that the surgical intervention significantly improved the patient satisfaction and clinical outcome of the patients with chronic ankle instability regarding the AOFAS score (P = 0.000) and Karlsson score (P = 0.000). No difference of AOFAS score nor Karlsson score was found in two groups of patients who share the same level pre-


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Fig. 4 Comparison of AOFAS score and Karlsson score before surgery and at follow-up time in allograft and autograft group respectively. a In the allograft group, the mean AOFAS score improved from 69.9 ± 13.3 to 94.8 ± 5.4 (P = 0.000). b In the autograft group, the mean AOFAS score improved from 68.4 ± 10.0 to 94.7 ± 5.0 (P = 0.000). c In the allograft group, the mean Karlsson score improved from 70.3 ± 12.2 to 93.8 ± 5.6 (P = 0.000). d In the allograft group, the mean Karlsson score improved from 64.5 ± 14.4 to 95.0 ± 5.8 (P = 0.000)

operative clinical assessment, regardless of which graft they received (Table 2). A study about minimally invasive reconstruction of the lateral ankle ligaments summed that using semitendinosus autograft or tendon allograft had no difference at the point of AOFAS score, but the patients in autograft group went through longer surgery time and shorter time to

Table 2 Comparison of AOFAS score and Karlsson score between allograft and autograft group before surgery and at follow-up time

AOFAS score Pre-operative Final follow-up P value Karlsson score Pre-operative Final follow-up P value

Allograft

Autograft

P value

69.9 ± 13.3 94.8 ± 5.4 0.000

68.4 ± 10.0 94.7 ± 5.0 0.000

0.756 0.957

70.3 ± 12.2 93.8 ± 5.6 0.000

64.5 ± 14.4 95.0 ± 5.8 0.000

0.285 0.574

heal [19]. James L. Carey et al. pointed that the short-term clinical outcomes of ACL reconstruction with allograft were not significantly different from those with autograft after reviewing nine articles comparing the outcomes of allograft and autograft [10]. There was also a long-term prospective, randomized controlled clinical study about ACL with an average 7.8 years follow-up showed no difference between allograft and autograft [20]. Although there was no significant difference at the aspect of clinical assessment, with the help of MRI UTE scanning, we found that the difference of graft (autograft vs allograft) leaded to different value of T2*. The mean T2* value of ATFL and intra-tunnel in allograft were significantly higher than that of autograft. Although the UTE T2* is sensitive to the movement and the magic angle and needs long scanning time [21]. Given that the surgery procedure, graft standard and graft placement, orientation at scanning time were same in two groups, in our study the deviation of T2* brought by magic angle effect can be ignored because of its appearance equally in allograft group and autograft group. Evaluation of the graft by MRI is much better and proper at two years post-



Fig. 5 Comparison of UTE-T2* value of ATFL and intra-tunnel graft between allograft group and autograft group

operatively, for the graft usually looks like a normal one [22]. In our study, 9/16 (56.25%) patients’ follow-up time longer than five years, 11/16 (68.75%) longer than two years in allograft, and 10/10 (100%) longer than two years in autograft group. The long healing time allowed the remodeling process: initial avascular necrosis, revascularization, cellular repopulation, and finally remodeling to complete adequately [20]. The different UTE values between groups might be leaded by other factors. During this healing process, revascularization plays a critical role by acting as a prerequisite for the other phases to be conducted and ensuring the long-term viability of the graft [23]. Muramatsu et al. applied serial contrast-enhanced MRI to point that allogenic tendons become established and revascularize more slowly than autologous tendons do [24]. Given the different intensity of UTE signals between groups in our results, the difference in the revascularization between allograft and autograft tendons might have an influence on the graft remodeling process. These higher T2* value may due to the disorganization of collagen structure and water content in allograft group [12]. In a study of Achilles tendon, pathologic changes in the tendon are represented by an increase in water content with a corresponding increase in signal intensity that can be recognized by MRI, and tears of the tendon show increased signal intensity [14]. In our study, the higher UTE T2* values may be explained as the poorer situation of collagen structure and much water content. Even if these differences were not reflected by AOFAS and Karlsson score, one impossible interpretation may be these functional assessments are too subtle to unveil the tiny histological changes. More pathological investigation and large-scale long-term follow-up study should be performed to identify the relationship between histological characteristics and clinical outcomes. Meanwhile, the cryopreservation and thawing temperature may affect the tendon’s properties of allograft. Thawing at room temperature as we did in this study reduced the

maximum stress [25], which may cause higher recurrence after surgical reconstruction in allograft group, whereas the autograft group would not be faced with. This factor may also contribute to the high T2* value in allograft. There were some limitations in our study. At first, the recruited sample size is relatively small which would lead to decreased power and increased statistical deviation. But all the test statistics applied to each statistic obeyed the application condition strictly. In other word, the bias that may brought in by the data were controlled to the minimal level. Given the fact that this study was prospectively designed, implication that the different MRI T2* values were caused by the choice of graft was unveiled. While a more convinced conclusion about cause and effect should be drew via further study with more patients. In addition, only semitendinosus autografts or semitendinosus allografts were used in this cohort. It is unclear if there is any difference regarding other kinds of autografts or allografts. More studies about different grafts and surgical techniques are supp o s e d t o b e d o n e i n t he f u t u r e [2 6 ] . T h i r d l y, monoexponential calculation of T2* reflects the mean value of all the components of relaxation time, which may lead to an underrate of T2*. Finally, from 2007 to 2014, the time span was too long to avoid unpredictable factor which may affect the accuracy of outcomes.

Conclusion In conclusion, both allograft and autograft reconstructions gain an ideal patient satisfaction and clinical functional outcomes. Higher T2*values were found allograft group when evaluated by UTE-T2* sequence, which indicated that autograft had some superiorities in respect of revascularization process, collagen structure, water content, and tendon properties, while the histological changes seem not to have apparent effect on clinical prognosis.


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Authors’ contributions Qianru Li and Kui Ma contributed equally to this work. 12. Funding National Natural Science Foundation of China (8157090042).

Compliance with ethical standards Conflict of interest The authors declare that they have no conflict of interest.

13. 14.

Ethical approval The study was approved by the institutional review board of Huashan Hospital. 15. Informed consent Informed consent was obtained from all individual participants included in the study. 16.

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