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Lateral meniscus allograft transplantation with platelet-rich plasma injections: A minimum two-year follow-up study
THEKNE-02598; No of Pages 8 The Knee xxx (2018) xxx–xxx
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The Knee
Lateral meniscus allograft transplantation with platelet-rich plasma injections: A minimum two-year follow-up study Hua Zhang a,1, Shiyang Chen a,1, Man Qiu b, Aiguo Zhou a, Wenlong Yan a, Jian Zhang a,⁎ a b
Department of Orthopaedics, The First Affiliated Hospital of Chongqing Medical University, Chongqing, China Department of Endoscopics, The First Affiliated Hospital of Chongqing Medical University, Chongqing, China
a r t i c l e
i n f o
Article history: Received 16 August 2017 Received in revised form 20 February 2018 Accepted 5 March 2018 Available online xxxx Keywords: Allograft Meniscus PRP Platelet-rich plasma Transplantation
a b s t r a c t Background: The aim of this study was to report the short-term clinical and imaging outcomes of lateral meniscus allograft transplantations (LMAT) combined with intra-articular platelet-rich plasma (PRP) injection. Methods: Thirty-three patients who had undergone LMAT combined with intra-articular PRP injection were evaluated. The Lysholm, International Knee Documentation Committee (IKDC), Western Ontario and McMaster Universities Osteoarthritis Index, Tegner activity level scale and visual analog scale for pain scores were used to evaluate the outcomes. Magnetic resonance imaging scans were performed postoperatively to assess graft position and chondral degeneration/damage. Results: A total of 31 of the original 33 patients were evaluated over a mean follow-up period of 37.0 months. Patients demonstrated statistically significant improvements in all scoring data from the pre-operative to two-year follow-up period. The mean postoperative extrusion was 1.59 ± 1.20 mm (range 0–3.9 mm). There were no significant differences in the distribution of the grade of chondral damage between the pre-operative and two-year follow-up periods. Three patients (9.7%) showed no improvements or had lower evaluation scores. One patient underwent matrix-induced autologous chondrocyte implantation at one year after LMAT. Conclusion: Lateral meniscus allograft transplantation combined with intra-articular PRP injection resulted in statistically significant improvements in all functions and pain scores, and clinical improvements in Tegner, IKDC, and Lysholm values during short-term follow-up. A further case–control study with a larger sample size and longer follow-up is required to obtain an overall assessment of the benefits of PRP on MAT patients. Level of evidence IV. © 2018 Published by Elsevier B.V.
1. Introduction Many studies have previously reported on the importance of the biomechanical function of the meniscus [1,2], and the high rate of osteoarthritis (OA) after total or subtotal meniscectomy [3–6]. Although arthroscopic meniscal repair techniques have been modified and improved in recent years, meniscectomy still needs to be performed on patients with insufficient meniscal tissue of sufficient quality for repairing, such as in cases of horizontal cleavage tears and meniscus re-tears. Meniscus allograft transplantation (MAT) – a surgery that aims to decrease patients' symptoms, improve function, and provide knee stability for patients who have undergone meniscectomy – has been performed since the 1980s [7,8].
⁎ Corresponding author. E-mail address: [email protected] (J. Zhang). 1 These authors contributed equally to this work and should be considered co-first authors.
https://doi.org/10.1016/j.knee.2018.03.005 0968-0160/© 2018 Published by Elsevier B.V.
Please cite this article as: Zhang H, et al, Lateral meniscus allograft transplantation with platelet-rich plasma injections: A minimum two-year follow-up study, Knee (2018), https://doi.org/10.1016/j.knee.2018.03.005
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One of the primary objectives of reconstructing the load transmission in the tibiofemoral compartment is to prevent or delay onset of knee OA in young people. Moderate to severe radiographic OA is considered to be a relative contraindication for MAT because the efficacy of the chondroprotection of this treatment remains controversial for patients with these radiographic changes [9–12]. Therefore, MAT is suitable for patients with limited cartilage degeneration. However, there are some unavoidable risks of allograft such as immunological rejection and graft disunion. This indicates that the techniques can still be optimized in many ways to avoid reintervention, increase graft survivorship, and delay knee arthroplasty in young patients. Platelet-rich plasma (PRP) contains growth factors, cytokines, chemokines, dense and lisosomal granules, and anti-inflammatory properties, which are essential for the body's response to injury [13–15]. PRP has been widely used in meniscus tears to enhance tissue repair and reduce inflammation [16–19]; however, no studies have reported the clinical or radiological results of PRP use in patients who have undergone MAT. Although the efficacy of chondroprotection remains controversial, many studies, including multiple randomized controlled trials and meta-analyses, have reported good clinical outcomes of intra-articular PRP injection, especially for younger and more active patients with limited cartilage degeneration [14,20,21]; it has also been proven effective for pain relief and functional improvement [22,23]. The aim of the current study was to report the short-term clinical and radiographic outcomes of lateral meniscus allograft transplantations (LMAT) combined with intra-articular PRP injection. It was hypothesized that patients who undergo total or subtotal meniscectomy will benefit from pain relief and functional improvement as a result of LMAT combined with PRP injection. 2. Materials and methods 2.1. Patients This retrospective study included patients who underwent LMAT (bone plug technique) combined with intra-articular PRP injection at the study authors' hospital between 2013 and 2015. Inclusion criteria were as follows: (1) unicompartmental knee pain after lateral total/subtotal meniscectomy, (2) aged b50 years, and (3) stability of the involved knee. Exclusion criteria were as follows: (1) mal-ligament or ligament deficiency of the involved knee, (2) diffuse Outerbridge grade IV cartilage damage, (3) local or systemic infections, (4) autoimmune diseases, (5) pregnancy, (6) known malignancy, and (7) bleeding disorder. 2.2. Pre-operative preparation Before the operation, detailed medical histories and comprehensive physical examinations were obtained for all patients. Radiographs and arthroscopic images of meniscectomy were reviewed when accessible (all patients' data were obtained). Standing antero-posterior, patellofemoral (30° flexion), and standing mechanical axis x-rays were obtained to exclude severe OA and malalignment. Pre-operative magnetic resonance imaging scans (MRIs) were obtained for chondral damage assessment and meniscus sizing [24]. Patients' blood was obtained during surgery, and leukocyte-poor, platelet-rich plasma was derived via a PRP centrifugal machine (WEGO Co., Shandong, China). 2.3. Surgical technique All patients underwent lateral meniscus allograft transplantation and intra-articular PRP injection performed by the same experienced surgeon (Dr. H. Z.). The allografts were fresh-frozen menisci. The transplantation used an arthroscopic double bone plug technique, as described by Shelton and Dukes [25]. In this study, the surgeon used a suture hook technique, which is widely performed in arthroscopic rotator cuff repair, to fix the posterior horn instead
Figure 1. (A) The posterior horn of the host meniscus with part of the posterior lateral capsule was pierced via a suture hook (DePuy Mitek Inc., California, USA), and one end of a PDS suture was fed into the articular though the suture hook. After the other end of the PDS was tied on a suture (Ethibond W4843), which pierced the posterior horn of the graft, (B) the end of the PDS which was in the articular was pulled out of the joint to pass the graft and W4843 in. Lastly, (C) platelet-rich plasma was injected around the allograft in the joint.
Please cite this article as: Zhang H, et al, Lateral meniscus allograft transplantation with platelet-rich plasma injections: A minimum two-year follow-up study, Knee (2018), https://doi.org/10.1016/j.knee.2018.03.005
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of the traditional all-inside suturing technique (FasT-Fix). After transplantation, PRP was injected around the graft under arthroscopy (Figure 1). Chondral damage was evaluated directly under arthroscopy by Outerbridge (OB) classification [26]. Focal grade III or grade IV lesions b 2 cm2 were treated with concurrent microfracture; patients with focal grade IV lesions N 2 cm2 were treated with matrix-induced autologous chondrocyte implantation. 2.4. Rehabilitation The postoperative rehabilitation program included three stages: (1) protected weightbearing and range of knee motion (ROM) exercises with flexion b 90° for four weeks, (2) full-weightbearing training and ROM exercises N 90° at the fifth week, and (3) returning to sports, such as running and swimming, at six months. Muscle-strengthening exercises of the quadriceps femoris (straight leg raising and active knee extension stretching) were initiated immediately after the operation. Patients were advised to avoid contact sports and strenuous activities. Rehabilitation was individualized according to the physical condition and rehabilitation progression of each patient. 2.5. Follow-up evaluation Two orthopedic surgeons (Dr. A. Z. and Dr. S. C.), who were unrelated to the surgery, used the Lysholm, International Knee Documentation Committee (IKDC), Western Ontario and McMaster Universities Osteoarthritis Index (WOMAC), Tegner activity level scale, and visual analog scale (VAS) to evaluate patients' clinical outcomes (activity, stability, function, pain relief, and quality of life) at six months, one year, and yearly thereafter. ROM and ligament stability were followed up, and complications related to surgery were recorded during the follow-up period. Standing x-rays and MRIs were obtained at one year and yearly thereafter to assess alignment, joint space, graft position, intrameniscal signals, and chondral degeneration/damage. The absolute graft extrusion was measured as the distance between the meniscal outer edge and the outer edge of the tibial articular surface on coronal MRI slices that showed maximal extrusion. The relative extrusion was defined as [27]: ½distance of graft extrusion∕½width of graft 100%: The mechanical axial alignment of the lower extremities was evaluated by alignment deviation from the 0° mechanical axis. For the purposes of this study, LMAT failure was defined as (1) graft removal or conversion to arthroplasty, (2) graft tear, and/or (3) deterioration of clinical outcome. 2.6. Statistical analysis Statistical analysis was performed using Statistical product and service solution (SPSS) for Windows version 19 (IBM Corporation, Armonk, New York, USA). Variables had first been tested for normal distribution by the Kolmogorov–Smirnov test. Statistical comparison of the results for pre-operative and follow-up scores was performed using the paired t-test and the Wilcoxon signed rank test. Pearson's Chi-squared test was used to analyze the distribution of OB grade of chondral damage. Statistical significance was set at P b 0.05. The minimal clinically important difference (MCID) and the minimal detectable change (MDC) were used to assess clinically meaningful improvements in the outcomes. There is no report of MCID or MDC for MAT patients. Therefore, the MCID for IKDC is 9.8 [28], and the MDCs for Tegner and Lysholm are 1.0 and 8.9, respectively, in the setting of anterior cruciate ligament (ACL) injuries [29]. The MDC for WOMAC is 15.3 in the setting of focal articular cartilage defects [30]. The MCID for VAS is 2.8 in people with OA and awaiting arthroplasty [31]. These values should be considered for reference only because MCID and MDC values are affected by various patient populations, language versions of indexes or scales, and methodologies.
Table 1 Patient data. Male/female, n Mean age (range), n Meniscus transplants/patients, n Left/right knee, n Mean time from total/subtotal meniscectomy to transplant (range), years Total/subtotal meniscectomy, n Lost to follow-up, n Mean follow-up period (range), months Incomplete/complete discoid meniscus, n Concomitant surgery, n Matrix-induced autologous chondrocyte implantation Microfracture Reintervention, n Matrix-induced autologous chondrocyte implantation
14/17 32.1 (15–50) 33/31 14/17 4.7 (0.5–12) 28/3 1 37.0 (24–56) 2/7 1 1 2 1
Please cite this article as: Zhang H, et al, Lateral meniscus allograft transplantation with platelet-rich plasma injections: A minimum two-year follow-up study, Knee (2018), https://doi.org/10.1016/j.knee.2018.03.005
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3. Results Thirty-three LMAT procedures combined with intra-articular PRP injection were performed in 33 patients. One patient was lost to follow-up at one year postoperatively, and one did not consent to yearly MRI scans. A total of 31 patients were available for two-year and four-year follow-ups (mean period of 37.0 months). The patients had a mean age of 32.1 years (range 15–50). The mean time from total/subtotal meniscectomy to transplant was 4.7 years (range 0.5–12.0). Nine patients (29.0%) were diagnosed with a discoid lateral meniscus. Two of them were incomplete discoid menisci, and seven were complete discoid menisci. One patient with focal grade III lesions and one with focal grade IV lesions b2 cm2 were treated with concurrent microfracture. One patient with three square centimeter focal grade IV lesions was treated with concurrent matrixinduced autologous chondrocyte implantation (MACI) (Table 1). The mean time to full weightbearing was 6.1 postoperative weeks (range five to nine). Physical examination showed ligament stability in all patients. In addition, 90.3% of patients showed significant relief of swelling, and 93.5% of patients showed pain relief at three months. Knee flexion reached N90° with a mean time of 6.5 weeks in all patients. The mean ROM was from 0 to 136.8° pre-operatively and 0 to 135.2° three months postoperatively. There was no statistically significant difference between these ROMs (P = 0.282). Three patients (9.7%) with a mean amount of flexion loss of 8.3° were unable to restore flexion, due to a lack of flexion exercise. Seven patients (22.6%) showed mild quadriceps femoris atrophy at one month postoperatively, due to lack of muscle-strengthening exercises, but six of them recovered after following the exercises under the study authors' guidance and regained their muscle strength at the next follow-up period. Twenty-five (83.9%) of the patients returned to sporting activities (running, swimming, biking, and other noncontact athletics) at the mean time of 8.2 months (range six to 12) after transplantation (Figure 2).
3.1. Scores There were statistically significant improvements in all scoring scales between the pre-operative and last follow-up periods (Table 2, Figures 3 and 4) and clinically meaningful improvements in Lysholm, IKDC, and Tegner activity levels according to the MDC and MCID. However, there was no clinically meaningful improvement in WOMAC or VAS between the pre-operative period and the last follow-up period, and in all scores between one-year and two-year follow-ups. Three patients showed no improvements or even lower scores in Lysholm, IKDC, Tegner, and WOMAC from the pre-operative evaluation. Two of these three patients were evaluated as Outerbridge grade III at the surgery period, and aggravated into Outerbridge grade IV cartilage damage postoperatively; one underwent MACI one year postoperatively. Another patient experienced moderate-degree quadriceps femoris atrophy at the latest follow-up period (see Table 3).
3.2. Imaging evaluation No patient underwent knee trauma postoperatively, and no MRI showed graft degeneration, graft tearing, medial meniscus tearing, ACL injury, or any other knee injury. The mean distance of absolute extrusion was 1.59 ± 1.20 mm (range 0–3.9) at the two-year follow-up. Although four knee MRIs showed absolute graft extrusion N3 mm, no significant differences in the function scores (Lysholm, Tegner, VAS, WOMAC, and IKDC) were found between these patients and others. The relative extrusion ranged from 0 to 30.9%, with a mean percentage of 15.55 ± 10.96%.
Figure 2. Trends in return to sports for all evaluated patients. The type of sports included running, swimming, biking and other non-contact athletics.
Please cite this article as: Zhang H, et al, Lateral meniscus allograft transplantation with platelet-rich plasma injections: A minimum two-year follow-up study, Knee (2018), https://doi.org/10.1016/j.knee.2018.03.005
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Table 2 Evaluation scores. Comparison Evaluation scores
Tegner Lysholm IKDC WOMAC VAS
Pre-operative
Follow-up 1 year
Follow-up 2 years
Follow-up 3 years
Pre-operative to 1 year
Pre-operative to 2 years
1 year to 2 years
(n = 31)
(n = 31)
(n = 31)
(n = 18)
% change
P
% change
P
% change
P
3.23 ± 1.15 67.68 ± 14.45 66.45 ± 12.31 58.06 ± 8.67 3.84 ± 1.79
3.87 ± 1.45 75.52 ± 17.69 72.84 + 15.34 62.00 ± 9.42 1.52 ± 1.80
4.39 ± 1.71 78.77 ± 19.92 75.13 ± 17.39 62.13 ± 9.22 1.39 ± 1.96
4.67 ± 1.88 82.56 ± 20.81 77.28 ± 18.91 61.89 ± 8.33 1.18 ± 1.91
19.8 11.6 9.6 6.8 −60.4
0.007 b0.001 b0.001 b0.001 b0.001
36.9 16.4 13.1 6.7 −63.8
0.001 b0.001 b0.001 b0.001 b0.001
13.4 4.3 3.1 0.2 −8.5
0.001 0.003 0.001 0.726 0.346
IKDC = International Knee Documentation Committee; WOMAC = Western Ontario and McMaster Universities Osteoarthritis Index; VAS = visual analog scale.
The grade of chondral damage postoperatively was recorded in a modified Outerbridge grading scale in MRI images [32,33]. There were no statistically significant differences in the distribution of the grade of chondral damage between the pre-operative period and two-year follow-up (P = 0.973) (Figure 5). The mechanical axial alignment of the lower extremities was evaluated by alignment deviation from the 0° mechanical axis. No alignment change was found at the latest follow-up. No patient had deep vein thrombosis, nerve injury, or infection postoperatively. One patient underwent MACI at one year after LMAT. No patients had undergone TKA at the latest follow-up period. No patient underwent knee trauma postoperatively, and no MRI showed graft tearing, medial meniscus tearing, ACL injury, or any other knee injury. Three patients (9.7%) showed no improvements or deteriorating scores and were considered failures. One patient who did not follow the authors' muscle-strengthening exercise guidance suffered moderate quadriceps femoris atrophy and showed no improvement in clinical outcomes postoperatively. The other two failures were possibly related to chondral damage at onset and were treated by microfracture (Table 3). 4. Discussion Although PRP injection has been widely used in sports medicine, there have been no reports of clinical or radiological results of using PRP in patients who have undergone LMAT. The aim of this study was to evaluate the short-term clinical and radiographic outcomes of LMAT (bone plug technique) with intra-articular PRP injection in 31 patients. This study demonstrated statistically significant improvements in all scores, and clinically meaningful improvements in Lysholm, IKDC, and Tegner values; however, there were no clinically meaningful improvements in WOMAC or VAS. The MCID and MDC values are affected by various patient populations, disease progression, language versions of indexes or scales, and methodologies [34]. The clinically meaningful improvement assessment should be considered for reference only in the current study because no reports have demonstrated the MCID or MDC for knee scores in Chinese on LMAT patients. Therefore, the MCID and MDC for scores on patients with ACL injury, focal cartilage lesions, or OA were used in the current study, as only the MCID for IKDC is available in Chinese. However, it was still necessary to assess the clinical relevance of these results, in case this study leads to incorrect clinical conclusions. In this study, IKDC and Lysholm showed smaller improvements than in other MAT short-term follow-up research studies, such as by Cole [35] (IKDC improved from 46.86 to 69.55; Lysholm improved from 52.77 to 75.60) and Kempshall et al. [12] (IKDC improved from 43.13 pre-operatively to 68.8 at two-year follow-up; Lysholm improved from 58.6 to 80.2). However, the postoperative score levels were similar to those obtained in the current study. The smaller improvements were caused by the higher pre-operative
Figure 3. Lysholm, WOMAC and IKDC demonstrated statistically significant improvements during the short-term follow-up period (P b 0.05). IKDC = International Knee Documentation Committee; WOMAC = Western Ontario and McMaster Universities Osteoarthritis Index.
Please cite this article as: Zhang H, et al, Lateral meniscus allograft transplantation with platelet-rich plasma injections: A minimum two-year follow-up study, Knee (2018), https://doi.org/10.1016/j.knee.2018.03.005
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Figure 4. Tegner and visual analog scale (VAS) demonstrated statistically significant improvements during the short-term follow-up period (P b 0.05).
score levels. Most patients in the current study were well introduced to the complications after total or subtotal meniscectomy, and were followed up regularly to participate in a postoperative rehabilitation program. Thus, they paid attention to mild symptoms in the involved knees and did not wait too long to perform LMAT. This may have led to high pre-operative score levels and small improvements after LMAT in the current study. Although there was no statistically significant difference in WOMAC between the one-year and three-year follow-ups, a light downtrend could be identified in the follow-up period, which was possibly related to advanced chondral damage. Although numerous studies, including the current one, have demonstrated a significant improvement at short-term follow-up compared with pre-operative status [35–38], some studies, including meta-analyses, have reported little improvement in the prevention or delay of OA progression and poor outcomes of graft survivorship. Vundelinckx et al. reported 97.8% of patients free from TKA at the five-year follow-up, 90.3% after 10 years, and 74.7% after 15 years [39]. Noyes and Barber-Westin reported that 37 of 69 patients had reoperations from 6.1 to 14.8 years postoperatively [40]. Stone et al. reported a 22.4% rate of meniscus transplant with moderate to severe cartilage damage failure at an average of 5.2 ± 4.4 years [9]. Elattar et al. reported an overall mean failure rate of 10.6% and an overall mean complication rate of 21.3% in 44 trials by meta-analysis [11]. These results indicate that MAT can only be considered as a bridging solution for many young patients. Many in-vitro and animal studies have reported that multiple growth factors in PRP have a positive effect on meniscal cell activity, and stimulate repair [19,41–43] and cartilage regeneration [44–47]. Although good clinical outcomes of PRP used in meniscus repair have been reported, the results of PRP injection in advanced chondral-damaged knees remain controversial [48–50]. The recently published meta-analyses by Lai et al. and Khoshbin et al. were inconclusive regarding the efficacy of PRP [48,49]. Kanchanatawan et al. reported that PRP injection has improved functional outcomes (WOMAC total scores, IKDC score, and EuorQol-VAS) when compared to hyaluronic acid (HA) and placebo in short-term outcomes, according to meta-regression analysis [50]. Ke-Vin et al. reported that PRP application improves function from basal evaluations in patients with knee joint cartilage degenerative pathology and tends to be more effective than HA administration, according to meta-analysis [21]. Laudy et al. found via network meta-analysis that PRP injections reduced pain and improved function more effectively than placebo and HA injections in knee OA [20]. Most studies have demonstrated that younger and more active patients with a low degree of cartilage degeneration benefit more from PRP, and most have reported a significant improvement in pain relief and functional evaluation for young, active patients [23]. The causes of graft extrusion remain unclear. Most studies, including this one, have reported a high incidence of this phenomenon [36,51,52]. There are several hypothesized causes, including surgical technique (Abat et al. [53] reported that the extrusion of bone fixation was less than that of soft tissue fixation), pre-operative sizing, non-anatomic graft fixation position, loss of fixation, and OA. Although most short-term to mid-term studies have found no association between graft extrusion and joint function, symptoms, or cartilage degeneration – even in high-degree graft extruded knees (absolute graft extrusion N 3 mm, relative extrusion N30%) – it is still necessary to pay attention to this phenomenon because the position is non-anatomic, and long-term effects are inconclusive. Long-term RCTs are required for this unsolved issue. Table 3 Failures.
Patient 1 Patient 2 Patient 3
Age
Sex
OB gradea
Concomitant
Reintervention
Cause
Deteriorative scores
45 35 37
F F F
II–II III–IV IV
– Microfracture Microfracture
– MACIb –
Quadriceps femoris atrophy Advanced chondral damage Advanced chondral damage
Lysholm, IKDC, Tegner Lysholm, IKDC, Tegner, WOMAC, VAS Lysholm, IKDC, WOMAC
IKDC = International Knee Documentation Committee; WOMAC = Western Ontario and McMaster Universities Osteoarthritis Index; VAS = visual analog scale. a Outerbridge (OB) grade at surgery and the latest follow-up. b Matrix-induced autologous chondrocyte implantation.
Please cite this article as: Zhang H, et al, Lateral meniscus allograft transplantation with platelet-rich plasma injections: A minimum two-year follow-up study, Knee (2018), https://doi.org/10.1016/j.knee.2018.03.005
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Figure 5. There were no statistically significant differences in the distribution of the grade of chondral damage during the short-term follow-up period (P N 0.05).
The incidence of discoid meniscus in Asia is much higher than in Europe and America, and most discoid menisci are found on the lateral side in patients of Asian descent [54,55]. According to the medical records and radiology/arthroscopic images, nine patients (29.0%) examined in this study were diagnosed with discoid lateral meniscus. Two of them were incomplete discoid menisci and seven were complete discoid menisci. Discoid meniscus entails disordered structural morphology and myxoid degeneration in the intrameniscal substance; therefore, it is more frequently associated with horizontal cleavage tears and meniscus re-tears. Subtotal or total meniscectomy is usually performed in these cases [56,57], and this may be the cause of the high rate of discoid meniscus in the current study. 4.1. Limitations There were several limitations to the present study. First, it was an evidence level IV study, and there was no control group. Second, the sample size was small, and the follow-up period was not long enough to fully assess the effects of PRP on the condition of cartilage damage and graft survivorship. Additionally, there was no second-look arthroscopic surgery or histological examination performed to directly evaluate graft healing. Therefore, a further case–control study with a larger sample size and longer follow-up term will facilitate overall assessment of the effects of PRP on LMAT patients. 5. Conclusion Lateral meniscus allograft transplantation combined with intra-articular PRP injection resulted in statistically significant improvements in all functions and pain scores, and clinical improvement in Tegner, IKDC, and Lysholm values during short-term follow-up. Considerable graft extrusion was observed. A further case–control study with a larger sample size and longer follow-up term is needed in order to obtain an overall assessment of the benefits of PRP on LMAT patients. Acknowledgments Authors declare no funding, grant, financial benefit, or competing interest involved in this study. References [1] [2] [3] [4] [5] [6] [7] [8] [9] [10] [11]
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The Knee
Lateral meniscus allograft transplantation with platelet-rich plasma injections: A minimum two-year follow-up study Hua Zhang a,1, Shiyang Chen a,1, Man Qiu b, Aiguo Zhou a, Wenlong Yan a, Jian Zhang a,⁎ a b
Department of Orthopaedics, The First Affiliated Hospital of Chongqing Medical University, Chongqing, China Department of Endoscopics, The First Affiliated Hospital of Chongqing Medical University, Chongqing, China
a r t i c l e
i n f o
Article history: Received 16 August 2017 Received in revised form 20 February 2018 Accepted 5 March 2018 Available online xxxx Keywords: Allograft Meniscus PRP Platelet-rich plasma Transplantation
a b s t r a c t Background: The aim of this study was to report the short-term clinical and imaging outcomes of lateral meniscus allograft transplantations (LMAT) combined with intra-articular platelet-rich plasma (PRP) injection. Methods: Thirty-three patients who had undergone LMAT combined with intra-articular PRP injection were evaluated. The Lysholm, International Knee Documentation Committee (IKDC), Western Ontario and McMaster Universities Osteoarthritis Index, Tegner activity level scale and visual analog scale for pain scores were used to evaluate the outcomes. Magnetic resonance imaging scans were performed postoperatively to assess graft position and chondral degeneration/damage. Results: A total of 31 of the original 33 patients were evaluated over a mean follow-up period of 37.0 months. Patients demonstrated statistically significant improvements in all scoring data from the pre-operative to two-year follow-up period. The mean postoperative extrusion was 1.59 ± 1.20 mm (range 0–3.9 mm). There were no significant differences in the distribution of the grade of chondral damage between the pre-operative and two-year follow-up periods. Three patients (9.7%) showed no improvements or had lower evaluation scores. One patient underwent matrix-induced autologous chondrocyte implantation at one year after LMAT. Conclusion: Lateral meniscus allograft transplantation combined with intra-articular PRP injection resulted in statistically significant improvements in all functions and pain scores, and clinical improvements in Tegner, IKDC, and Lysholm values during short-term follow-up. A further case–control study with a larger sample size and longer follow-up is required to obtain an overall assessment of the benefits of PRP on MAT patients. Level of evidence IV. © 2018 Published by Elsevier B.V.
1. Introduction Many studies have previously reported on the importance of the biomechanical function of the meniscus [1,2], and the high rate of osteoarthritis (OA) after total or subtotal meniscectomy [3–6]. Although arthroscopic meniscal repair techniques have been modified and improved in recent years, meniscectomy still needs to be performed on patients with insufficient meniscal tissue of sufficient quality for repairing, such as in cases of horizontal cleavage tears and meniscus re-tears. Meniscus allograft transplantation (MAT) – a surgery that aims to decrease patients' symptoms, improve function, and provide knee stability for patients who have undergone meniscectomy – has been performed since the 1980s [7,8].
⁎ Corresponding author. E-mail address: [email protected] (J. Zhang). 1 These authors contributed equally to this work and should be considered co-first authors.
https://doi.org/10.1016/j.knee.2018.03.005 0968-0160/© 2018 Published by Elsevier B.V.
Please cite this article as: Zhang H, et al, Lateral meniscus allograft transplantation with platelet-rich plasma injections: A minimum two-year follow-up study, Knee (2018), https://doi.org/10.1016/j.knee.2018.03.005
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One of the primary objectives of reconstructing the load transmission in the tibiofemoral compartment is to prevent or delay onset of knee OA in young people. Moderate to severe radiographic OA is considered to be a relative contraindication for MAT because the efficacy of the chondroprotection of this treatment remains controversial for patients with these radiographic changes [9–12]. Therefore, MAT is suitable for patients with limited cartilage degeneration. However, there are some unavoidable risks of allograft such as immunological rejection and graft disunion. This indicates that the techniques can still be optimized in many ways to avoid reintervention, increase graft survivorship, and delay knee arthroplasty in young patients. Platelet-rich plasma (PRP) contains growth factors, cytokines, chemokines, dense and lisosomal granules, and anti-inflammatory properties, which are essential for the body's response to injury [13–15]. PRP has been widely used in meniscus tears to enhance tissue repair and reduce inflammation [16–19]; however, no studies have reported the clinical or radiological results of PRP use in patients who have undergone MAT. Although the efficacy of chondroprotection remains controversial, many studies, including multiple randomized controlled trials and meta-analyses, have reported good clinical outcomes of intra-articular PRP injection, especially for younger and more active patients with limited cartilage degeneration [14,20,21]; it has also been proven effective for pain relief and functional improvement [22,23]. The aim of the current study was to report the short-term clinical and radiographic outcomes of lateral meniscus allograft transplantations (LMAT) combined with intra-articular PRP injection. It was hypothesized that patients who undergo total or subtotal meniscectomy will benefit from pain relief and functional improvement as a result of LMAT combined with PRP injection. 2. Materials and methods 2.1. Patients This retrospective study included patients who underwent LMAT (bone plug technique) combined with intra-articular PRP injection at the study authors' hospital between 2013 and 2015. Inclusion criteria were as follows: (1) unicompartmental knee pain after lateral total/subtotal meniscectomy, (2) aged b50 years, and (3) stability of the involved knee. Exclusion criteria were as follows: (1) mal-ligament or ligament deficiency of the involved knee, (2) diffuse Outerbridge grade IV cartilage damage, (3) local or systemic infections, (4) autoimmune diseases, (5) pregnancy, (6) known malignancy, and (7) bleeding disorder. 2.2. Pre-operative preparation Before the operation, detailed medical histories and comprehensive physical examinations were obtained for all patients. Radiographs and arthroscopic images of meniscectomy were reviewed when accessible (all patients' data were obtained). Standing antero-posterior, patellofemoral (30° flexion), and standing mechanical axis x-rays were obtained to exclude severe OA and malalignment. Pre-operative magnetic resonance imaging scans (MRIs) were obtained for chondral damage assessment and meniscus sizing [24]. Patients' blood was obtained during surgery, and leukocyte-poor, platelet-rich plasma was derived via a PRP centrifugal machine (WEGO Co., Shandong, China). 2.3. Surgical technique All patients underwent lateral meniscus allograft transplantation and intra-articular PRP injection performed by the same experienced surgeon (Dr. H. Z.). The allografts were fresh-frozen menisci. The transplantation used an arthroscopic double bone plug technique, as described by Shelton and Dukes [25]. In this study, the surgeon used a suture hook technique, which is widely performed in arthroscopic rotator cuff repair, to fix the posterior horn instead
Figure 1. (A) The posterior horn of the host meniscus with part of the posterior lateral capsule was pierced via a suture hook (DePuy Mitek Inc., California, USA), and one end of a PDS suture was fed into the articular though the suture hook. After the other end of the PDS was tied on a suture (Ethibond W4843), which pierced the posterior horn of the graft, (B) the end of the PDS which was in the articular was pulled out of the joint to pass the graft and W4843 in. Lastly, (C) platelet-rich plasma was injected around the allograft in the joint.
Please cite this article as: Zhang H, et al, Lateral meniscus allograft transplantation with platelet-rich plasma injections: A minimum two-year follow-up study, Knee (2018), https://doi.org/10.1016/j.knee.2018.03.005
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of the traditional all-inside suturing technique (FasT-Fix). After transplantation, PRP was injected around the graft under arthroscopy (Figure 1). Chondral damage was evaluated directly under arthroscopy by Outerbridge (OB) classification [26]. Focal grade III or grade IV lesions b 2 cm2 were treated with concurrent microfracture; patients with focal grade IV lesions N 2 cm2 were treated with matrix-induced autologous chondrocyte implantation. 2.4. Rehabilitation The postoperative rehabilitation program included three stages: (1) protected weightbearing and range of knee motion (ROM) exercises with flexion b 90° for four weeks, (2) full-weightbearing training and ROM exercises N 90° at the fifth week, and (3) returning to sports, such as running and swimming, at six months. Muscle-strengthening exercises of the quadriceps femoris (straight leg raising and active knee extension stretching) were initiated immediately after the operation. Patients were advised to avoid contact sports and strenuous activities. Rehabilitation was individualized according to the physical condition and rehabilitation progression of each patient. 2.5. Follow-up evaluation Two orthopedic surgeons (Dr. A. Z. and Dr. S. C.), who were unrelated to the surgery, used the Lysholm, International Knee Documentation Committee (IKDC), Western Ontario and McMaster Universities Osteoarthritis Index (WOMAC), Tegner activity level scale, and visual analog scale (VAS) to evaluate patients' clinical outcomes (activity, stability, function, pain relief, and quality of life) at six months, one year, and yearly thereafter. ROM and ligament stability were followed up, and complications related to surgery were recorded during the follow-up period. Standing x-rays and MRIs were obtained at one year and yearly thereafter to assess alignment, joint space, graft position, intrameniscal signals, and chondral degeneration/damage. The absolute graft extrusion was measured as the distance between the meniscal outer edge and the outer edge of the tibial articular surface on coronal MRI slices that showed maximal extrusion. The relative extrusion was defined as [27]: ½distance of graft extrusion∕½width of graft 100%: The mechanical axial alignment of the lower extremities was evaluated by alignment deviation from the 0° mechanical axis. For the purposes of this study, LMAT failure was defined as (1) graft removal or conversion to arthroplasty, (2) graft tear, and/or (3) deterioration of clinical outcome. 2.6. Statistical analysis Statistical analysis was performed using Statistical product and service solution (SPSS) for Windows version 19 (IBM Corporation, Armonk, New York, USA). Variables had first been tested for normal distribution by the Kolmogorov–Smirnov test. Statistical comparison of the results for pre-operative and follow-up scores was performed using the paired t-test and the Wilcoxon signed rank test. Pearson's Chi-squared test was used to analyze the distribution of OB grade of chondral damage. Statistical significance was set at P b 0.05. The minimal clinically important difference (MCID) and the minimal detectable change (MDC) were used to assess clinically meaningful improvements in the outcomes. There is no report of MCID or MDC for MAT patients. Therefore, the MCID for IKDC is 9.8 [28], and the MDCs for Tegner and Lysholm are 1.0 and 8.9, respectively, in the setting of anterior cruciate ligament (ACL) injuries [29]. The MDC for WOMAC is 15.3 in the setting of focal articular cartilage defects [30]. The MCID for VAS is 2.8 in people with OA and awaiting arthroplasty [31]. These values should be considered for reference only because MCID and MDC values are affected by various patient populations, language versions of indexes or scales, and methodologies.
Table 1 Patient data. Male/female, n Mean age (range), n Meniscus transplants/patients, n Left/right knee, n Mean time from total/subtotal meniscectomy to transplant (range), years Total/subtotal meniscectomy, n Lost to follow-up, n Mean follow-up period (range), months Incomplete/complete discoid meniscus, n Concomitant surgery, n Matrix-induced autologous chondrocyte implantation Microfracture Reintervention, n Matrix-induced autologous chondrocyte implantation
14/17 32.1 (15–50) 33/31 14/17 4.7 (0.5–12) 28/3 1 37.0 (24–56) 2/7 1 1 2 1
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3. Results Thirty-three LMAT procedures combined with intra-articular PRP injection were performed in 33 patients. One patient was lost to follow-up at one year postoperatively, and one did not consent to yearly MRI scans. A total of 31 patients were available for two-year and four-year follow-ups (mean period of 37.0 months). The patients had a mean age of 32.1 years (range 15–50). The mean time from total/subtotal meniscectomy to transplant was 4.7 years (range 0.5–12.0). Nine patients (29.0%) were diagnosed with a discoid lateral meniscus. Two of them were incomplete discoid menisci, and seven were complete discoid menisci. One patient with focal grade III lesions and one with focal grade IV lesions b2 cm2 were treated with concurrent microfracture. One patient with three square centimeter focal grade IV lesions was treated with concurrent matrixinduced autologous chondrocyte implantation (MACI) (Table 1). The mean time to full weightbearing was 6.1 postoperative weeks (range five to nine). Physical examination showed ligament stability in all patients. In addition, 90.3% of patients showed significant relief of swelling, and 93.5% of patients showed pain relief at three months. Knee flexion reached N90° with a mean time of 6.5 weeks in all patients. The mean ROM was from 0 to 136.8° pre-operatively and 0 to 135.2° three months postoperatively. There was no statistically significant difference between these ROMs (P = 0.282). Three patients (9.7%) with a mean amount of flexion loss of 8.3° were unable to restore flexion, due to a lack of flexion exercise. Seven patients (22.6%) showed mild quadriceps femoris atrophy at one month postoperatively, due to lack of muscle-strengthening exercises, but six of them recovered after following the exercises under the study authors' guidance and regained their muscle strength at the next follow-up period. Twenty-five (83.9%) of the patients returned to sporting activities (running, swimming, biking, and other noncontact athletics) at the mean time of 8.2 months (range six to 12) after transplantation (Figure 2).
3.1. Scores There were statistically significant improvements in all scoring scales between the pre-operative and last follow-up periods (Table 2, Figures 3 and 4) and clinically meaningful improvements in Lysholm, IKDC, and Tegner activity levels according to the MDC and MCID. However, there was no clinically meaningful improvement in WOMAC or VAS between the pre-operative period and the last follow-up period, and in all scores between one-year and two-year follow-ups. Three patients showed no improvements or even lower scores in Lysholm, IKDC, Tegner, and WOMAC from the pre-operative evaluation. Two of these three patients were evaluated as Outerbridge grade III at the surgery period, and aggravated into Outerbridge grade IV cartilage damage postoperatively; one underwent MACI one year postoperatively. Another patient experienced moderate-degree quadriceps femoris atrophy at the latest follow-up period (see Table 3).
3.2. Imaging evaluation No patient underwent knee trauma postoperatively, and no MRI showed graft degeneration, graft tearing, medial meniscus tearing, ACL injury, or any other knee injury. The mean distance of absolute extrusion was 1.59 ± 1.20 mm (range 0–3.9) at the two-year follow-up. Although four knee MRIs showed absolute graft extrusion N3 mm, no significant differences in the function scores (Lysholm, Tegner, VAS, WOMAC, and IKDC) were found between these patients and others. The relative extrusion ranged from 0 to 30.9%, with a mean percentage of 15.55 ± 10.96%.
Figure 2. Trends in return to sports for all evaluated patients. The type of sports included running, swimming, biking and other non-contact athletics.
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Table 2 Evaluation scores. Comparison Evaluation scores
Tegner Lysholm IKDC WOMAC VAS
Pre-operative
Follow-up 1 year
Follow-up 2 years
Follow-up 3 years
Pre-operative to 1 year
Pre-operative to 2 years
1 year to 2 years
(n = 31)
(n = 31)
(n = 31)
(n = 18)
% change
P
% change
P
% change
P
3.23 ± 1.15 67.68 ± 14.45 66.45 ± 12.31 58.06 ± 8.67 3.84 ± 1.79
3.87 ± 1.45 75.52 ± 17.69 72.84 + 15.34 62.00 ± 9.42 1.52 ± 1.80
4.39 ± 1.71 78.77 ± 19.92 75.13 ± 17.39 62.13 ± 9.22 1.39 ± 1.96
4.67 ± 1.88 82.56 ± 20.81 77.28 ± 18.91 61.89 ± 8.33 1.18 ± 1.91
19.8 11.6 9.6 6.8 −60.4
0.007 b0.001 b0.001 b0.001 b0.001
36.9 16.4 13.1 6.7 −63.8
0.001 b0.001 b0.001 b0.001 b0.001
13.4 4.3 3.1 0.2 −8.5
0.001 0.003 0.001 0.726 0.346
IKDC = International Knee Documentation Committee; WOMAC = Western Ontario and McMaster Universities Osteoarthritis Index; VAS = visual analog scale.
The grade of chondral damage postoperatively was recorded in a modified Outerbridge grading scale in MRI images [32,33]. There were no statistically significant differences in the distribution of the grade of chondral damage between the pre-operative period and two-year follow-up (P = 0.973) (Figure 5). The mechanical axial alignment of the lower extremities was evaluated by alignment deviation from the 0° mechanical axis. No alignment change was found at the latest follow-up. No patient had deep vein thrombosis, nerve injury, or infection postoperatively. One patient underwent MACI at one year after LMAT. No patients had undergone TKA at the latest follow-up period. No patient underwent knee trauma postoperatively, and no MRI showed graft tearing, medial meniscus tearing, ACL injury, or any other knee injury. Three patients (9.7%) showed no improvements or deteriorating scores and were considered failures. One patient who did not follow the authors' muscle-strengthening exercise guidance suffered moderate quadriceps femoris atrophy and showed no improvement in clinical outcomes postoperatively. The other two failures were possibly related to chondral damage at onset and were treated by microfracture (Table 3). 4. Discussion Although PRP injection has been widely used in sports medicine, there have been no reports of clinical or radiological results of using PRP in patients who have undergone LMAT. The aim of this study was to evaluate the short-term clinical and radiographic outcomes of LMAT (bone plug technique) with intra-articular PRP injection in 31 patients. This study demonstrated statistically significant improvements in all scores, and clinically meaningful improvements in Lysholm, IKDC, and Tegner values; however, there were no clinically meaningful improvements in WOMAC or VAS. The MCID and MDC values are affected by various patient populations, disease progression, language versions of indexes or scales, and methodologies [34]. The clinically meaningful improvement assessment should be considered for reference only in the current study because no reports have demonstrated the MCID or MDC for knee scores in Chinese on LMAT patients. Therefore, the MCID and MDC for scores on patients with ACL injury, focal cartilage lesions, or OA were used in the current study, as only the MCID for IKDC is available in Chinese. However, it was still necessary to assess the clinical relevance of these results, in case this study leads to incorrect clinical conclusions. In this study, IKDC and Lysholm showed smaller improvements than in other MAT short-term follow-up research studies, such as by Cole [35] (IKDC improved from 46.86 to 69.55; Lysholm improved from 52.77 to 75.60) and Kempshall et al. [12] (IKDC improved from 43.13 pre-operatively to 68.8 at two-year follow-up; Lysholm improved from 58.6 to 80.2). However, the postoperative score levels were similar to those obtained in the current study. The smaller improvements were caused by the higher pre-operative
Figure 3. Lysholm, WOMAC and IKDC demonstrated statistically significant improvements during the short-term follow-up period (P b 0.05). IKDC = International Knee Documentation Committee; WOMAC = Western Ontario and McMaster Universities Osteoarthritis Index.
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Figure 4. Tegner and visual analog scale (VAS) demonstrated statistically significant improvements during the short-term follow-up period (P b 0.05).
score levels. Most patients in the current study were well introduced to the complications after total or subtotal meniscectomy, and were followed up regularly to participate in a postoperative rehabilitation program. Thus, they paid attention to mild symptoms in the involved knees and did not wait too long to perform LMAT. This may have led to high pre-operative score levels and small improvements after LMAT in the current study. Although there was no statistically significant difference in WOMAC between the one-year and three-year follow-ups, a light downtrend could be identified in the follow-up period, which was possibly related to advanced chondral damage. Although numerous studies, including the current one, have demonstrated a significant improvement at short-term follow-up compared with pre-operative status [35–38], some studies, including meta-analyses, have reported little improvement in the prevention or delay of OA progression and poor outcomes of graft survivorship. Vundelinckx et al. reported 97.8% of patients free from TKA at the five-year follow-up, 90.3% after 10 years, and 74.7% after 15 years [39]. Noyes and Barber-Westin reported that 37 of 69 patients had reoperations from 6.1 to 14.8 years postoperatively [40]. Stone et al. reported a 22.4% rate of meniscus transplant with moderate to severe cartilage damage failure at an average of 5.2 ± 4.4 years [9]. Elattar et al. reported an overall mean failure rate of 10.6% and an overall mean complication rate of 21.3% in 44 trials by meta-analysis [11]. These results indicate that MAT can only be considered as a bridging solution for many young patients. Many in-vitro and animal studies have reported that multiple growth factors in PRP have a positive effect on meniscal cell activity, and stimulate repair [19,41–43] and cartilage regeneration [44–47]. Although good clinical outcomes of PRP used in meniscus repair have been reported, the results of PRP injection in advanced chondral-damaged knees remain controversial [48–50]. The recently published meta-analyses by Lai et al. and Khoshbin et al. were inconclusive regarding the efficacy of PRP [48,49]. Kanchanatawan et al. reported that PRP injection has improved functional outcomes (WOMAC total scores, IKDC score, and EuorQol-VAS) when compared to hyaluronic acid (HA) and placebo in short-term outcomes, according to meta-regression analysis [50]. Ke-Vin et al. reported that PRP application improves function from basal evaluations in patients with knee joint cartilage degenerative pathology and tends to be more effective than HA administration, according to meta-analysis [21]. Laudy et al. found via network meta-analysis that PRP injections reduced pain and improved function more effectively than placebo and HA injections in knee OA [20]. Most studies have demonstrated that younger and more active patients with a low degree of cartilage degeneration benefit more from PRP, and most have reported a significant improvement in pain relief and functional evaluation for young, active patients [23]. The causes of graft extrusion remain unclear. Most studies, including this one, have reported a high incidence of this phenomenon [36,51,52]. There are several hypothesized causes, including surgical technique (Abat et al. [53] reported that the extrusion of bone fixation was less than that of soft tissue fixation), pre-operative sizing, non-anatomic graft fixation position, loss of fixation, and OA. Although most short-term to mid-term studies have found no association between graft extrusion and joint function, symptoms, or cartilage degeneration – even in high-degree graft extruded knees (absolute graft extrusion N 3 mm, relative extrusion N30%) – it is still necessary to pay attention to this phenomenon because the position is non-anatomic, and long-term effects are inconclusive. Long-term RCTs are required for this unsolved issue. Table 3 Failures.
Patient 1 Patient 2 Patient 3
Age
Sex
OB gradea
Concomitant
Reintervention
Cause
Deteriorative scores
45 35 37
F F F
II–II III–IV IV
– Microfracture Microfracture
– MACIb –
Quadriceps femoris atrophy Advanced chondral damage Advanced chondral damage
Lysholm, IKDC, Tegner Lysholm, IKDC, Tegner, WOMAC, VAS Lysholm, IKDC, WOMAC
IKDC = International Knee Documentation Committee; WOMAC = Western Ontario and McMaster Universities Osteoarthritis Index; VAS = visual analog scale. a Outerbridge (OB) grade at surgery and the latest follow-up. b Matrix-induced autologous chondrocyte implantation.
Please cite this article as: Zhang H, et al, Lateral meniscus allograft transplantation with platelet-rich plasma injections: A minimum two-year follow-up study, Knee (2018), https://doi.org/10.1016/j.knee.2018.03.005
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Figure 5. There were no statistically significant differences in the distribution of the grade of chondral damage during the short-term follow-up period (P N 0.05).
The incidence of discoid meniscus in Asia is much higher than in Europe and America, and most discoid menisci are found on the lateral side in patients of Asian descent [54,55]. According to the medical records and radiology/arthroscopic images, nine patients (29.0%) examined in this study were diagnosed with discoid lateral meniscus. Two of them were incomplete discoid menisci and seven were complete discoid menisci. Discoid meniscus entails disordered structural morphology and myxoid degeneration in the intrameniscal substance; therefore, it is more frequently associated with horizontal cleavage tears and meniscus re-tears. Subtotal or total meniscectomy is usually performed in these cases [56,57], and this may be the cause of the high rate of discoid meniscus in the current study. 4.1. Limitations There were several limitations to the present study. First, it was an evidence level IV study, and there was no control group. Second, the sample size was small, and the follow-up period was not long enough to fully assess the effects of PRP on the condition of cartilage damage and graft survivorship. Additionally, there was no second-look arthroscopic surgery or histological examination performed to directly evaluate graft healing. Therefore, a further case–control study with a larger sample size and longer follow-up term will facilitate overall assessment of the effects of PRP on LMAT patients. 5. Conclusion Lateral meniscus allograft transplantation combined with intra-articular PRP injection resulted in statistically significant improvements in all functions and pain scores, and clinical improvement in Tegner, IKDC, and Lysholm values during short-term follow-up. Considerable graft extrusion was observed. A further case–control study with a larger sample size and longer follow-up term is needed in order to obtain an overall assessment of the benefits of PRP on LMAT patients. Acknowledgments Authors declare no funding, grant, financial benefit, or competing interest involved in this study. References [1] [2] [3] [4] [5] [6] [7] [8] [9] [10] [11]
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Please cite this article as: Zhang H, et al, Lateral meniscus allograft transplantation with platelet-rich plasma injections: A minimum two-year follow-up study, Knee (2018), https://doi.org/10.1016/j.knee.2018.03.005