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Volume 1| Issue 2| Aug-Nov 2016

Meniscus Ramp Lesion

Bertrand Sonnery Cottet, Sanesh Tuteja, Nuno Camelo Barbosa, Mathieu Thaunat

Volume 1 | Issue 2 | Aug – Nov 2016 | Page 28-34.

Author: Bertrand Sonnery Cottet[1], Sanesh Tuteja[1], Nuno Camelo Barbosa[1], Mathieu Thaunat[1].

[1] Investigation performed at the Centre Orthopédique Santy, FIFA medical center of Excellence, Groupe Ramsay-Générale de Santé, Lyon, France

Address of Correspondence

Dr Bertrand Sonnery-Cottet
Centre Orthopédique Santy, 24 Avenue Paul Santy, Lyon, 69008, France
Email: sonnerycottet@aol.com.

Abstract

Ramp Lesions of the Medial Meniscus (MM) are associated with 9 to 17% of ACL Tears and are seldom recognized on preoperative magnetic resonance imaging (MRI) scans. They also often remain undiagnosed when viewing from the standard anterior compartment arthroscopic portals. Improved visualization is the key to achieving good meniscal repair results as it improves diagnosis of longitudinal tears in posterior horn MM, safeguards better debridement prior to repair and ensures good approximation of the torn ends under vision. A systematic posteromedial exploration allows discovery of and debridement of the hidden MM lesion and repair with a suture hook device is associated with low morbidity and must be undertaken whenever possible.
Keywords: Medial meniscus, Ramp lesion, Repair, Healing, Anterior cruciate ligament, Knee.

Introduction

Meniscal lesions of the posterior horn of medial meniscus (MM) are very often associated with an ACL rupture (16,32,49). Certain specific lesions of the Medial Meniscus (MM) such as meniscosynovial or meniscocapsular tears and meniscotibial ligament lesions are associated with 9 to 17% of ACL Tears (8,21) and are seldom recognized on preoperative magnetic resonance imaging (MRI) scans (8,38). They also often remain undiagnosed when viewing from the standard anterior compartment arthroscopic portals including a probing. They were named in the 1980s by Strobel et al (42) as ‘‘Ramp’’ lesions of the meniscus and have drawn a lot of attention over the past few years (3,8,21,38,42). The aim of this article will be to write a narrative review of this Ramp meniscal lesion.

History
Hamberg et al (15) first described “a peripheral vertical rupture in the posterior horn of the medial or lateral meniscus with an intact body” in 1983. They repaired these lesions through a postero-medial vertical arthrotomy; with the belief that the capillary blood supply from the capsule aids healing of the meniscus. They reported promising results (84% healing) in old and new lesions alike, thus providing some valuable insight into the philosophy of meniscal conservation. Morgan et al (25) in 1991 described the first arthroscopic vertical suture of the PHMM using Polydioxanone (PDS) sutures with an outside-to-inside technique. They reported a 16% failure rate occurring in patients with a concurrent ACL injury. They proposed that the rotation axis of the knee joint was altered in an ACL deficit knee thus placing excessive loads on the posterior horn of the medial meniscus. The kinematics of the posterior horn of the medial meniscus in the ACL deficient knee was therefore not conducive to meniscal healing after repair despite a peripheral blood supply. They also noted that, when combined with an ACL reconstruction, peripheral meniscal repair healing rates improved and approached those obtained in an ACL intact knee (25). Ahn et al (5) in 2004 described the first clinical series of an arthroscopic all-inside suture technique for tears in posterior horn of medial meniscus. Using a suture hook thorough 2-posteromedial portals, PHMM tears were repaired with concurrent reconstruction of the ACL. They concluded that the arthroscopic all-inside vertical suture using a hook resulted in a high healing rate even in large and complex vertical tears. Seil et al (38) in 2009 highlighted the indications for meniscal repairs based on the presence of associated ligamentous injuries and morphology of the lesion.
They advocated that Meniscal repairs be ‘‘ideally’’ carried out in:
1. Young patients (< 40 years)
2. No associated joint degeneration.
3. Vertical lesions in the peripheral third of the meniscus (3mm of the meniscosynovial junction) (4) and in conjunction with an ACL reconstruction.
4. Significantly displaced bucket-handle tear or an MMPH tear with vertical step off (5).

Epidemiology
The prevalence for a meniscal lesion with an ACl tear has been reported between 47% to 61% (13,14). In 2010, S. Bollen et al (8) reported menisco-capsular lesions in 9.3% of their prospective series of 183 ACL reconstructions whereas Liu et al (21) described a prevalence of 16.6% in a series of 868 consecutive ACL reconstructions. In our series (40) on ACL deficient knees, a meniscal tears was identified in 125 out of the 302 patients. Following a systematic algorithm for exploration of the knee joint (Figure. 1), we found that; 75 (60%) medial meniscal body lesions were diagnosed through a standard anterior portal exploration, 29 (23.2%) ramp lesions were diagnosed during exploration of the posteromedial compartment, and 21 (16.8%) were discovered by probing the tear through a posteromedial portal and after minimal debridement of a superficial soft tissue layer with a motorized shaver. All-in-all, 42% (21/50) of the lesions diagnosed via inspecting the posterior compartment appeared only after superficial soft tissue debridement and were classified as ‘‘hidden lesions.’’ An ACL injury with an age at presentation above 30 years, male sex and a delay between injury and surgery are considered risk factors for concomitant meniscal lesions (8).

Biomechanical Implication on ACL
The importance of the meniscus in stabilizing the knee joint in chronically ACL-deficient knees has been validated by multiple studies (9, 39). A Peripheral posterior horn tear is caused by the recurrent trauma sustained by the Medial Meniscus, which acts as a ‘‘bumper’’ in ACL-deficient knees (2). In addition, contraction of the semimembranosus at its insertion along the posteromedial capsule may stress the peripheral meniscus, resulting in meniscocapsular tearing (17). This could occur at the time of injury or during subsequent instability episodes in the subacute or chronic situation (43). A capsular injury might also occur during the so-called medial contrecoup injury (18) after subluxation of the lateral tibial plateau and during subsequent reduction of the tibia (41). A longitudinal tear of the PHMM in ACL-deficient knees increases the anterior translation of the tibia and a repair of this lesion reduces Anteroposterior tibial translation significantly at most flexion angles (17) and most prominently at 30 degrees of flexion (12, 30). Peltier et al (30) observed that the PHMM was stabilised by the meniscotibial ligament posteriorly, which in turn inserted onto the posterior aspect of the proximal tibia. The capsule of the knee joint inserts more distally on this posterior surface. The posterior capsule hence lacks insertion onto the posterior aspect of the PHMM. Detachment of the ligament therefore results in an abnormal mobility of the entire PHMM, producing rotational instability. The authors observed that the division of the menisco-tibial ligament resulted in a statistically significant increase in internal tibial rotation. Such lesions occur either in the mid-substance (repairable) or as a bony avulsion (irreparable). Stephen et al (41) reported that the anterior tibial translation and external rotation were both significantly increased compared with the ACL-deficient knee after posterior meniscocapsular sectioning and these parameters were not restored after ACL reconstruction alone but were restored with ACL reconstruction combined with posterior meniscocapsular repair.
Classification [46] (Figure. 2)
We have proposed a classification for ramp lesions which is as follows:
Type 1: Ramp lesions. Very peripherally located in the synovial sheath. Mobility at probing is very low. (B)
Type 2: Partial superior lesions. It is stable and can be diagnosed only by trans-notch approach. Mobility at probing is low. ©
Type 3: Partial inferior or hidden lesions. It is not visible with the trans-notch approach, but it may be suspected in case of mobility at probing, which is high. (D)
Type 4: Complete tear in the red-red zone. Mobility at probing is very high. (E)
Type 5: Double tear.

figure-1-and-2

Surgical Technique (46)
With the patient supine on the operating table, a tourniquet is placed high on the thigh, and the knee placed at 90º of flexion with a foot support to allow full range of knee motion. Using standard arthroscopy portals, high lateral as viewing and medial portal for instrumentation, articular inspection is performed and we engage a probe in the posterior segment of the meniscus and force an anterior excursion of the meniscus. If the meniscus subluxates under the condyle, it is an indicator for instability and an indirect sign of a ramp lesion. Direct visualization of the posteromedial compartment is mandated to diagnose and repair these lesions. Even if the meniscus appears stable on probing, a systematic exploration of the posterior segment must be performed using the protocol in (Figure.1) Through a Guillquist maneuver, the arthroscope in the anterolateral portal is advanced in the triangle formed by the medial femoral condyle, the posterior cruciate ligament, and the tibial spines. With valgus force applied initially in flexion followed by knee extension, the arthroscope is pass through the space at the condyle border of the medial femoral condyle. Internal rotation applied to the tibia further enhances visualization; this causes subluxation of the posterior tibial plateau causing a posterior translation of the middle third segment. Almost two-thirds of peripheral lesions can be diagnosed with this maneuver. Tears of the posterior segment must be approached posteromedially. The posteromedial portal is placed superior to the hamstring tendons and posterior to the medial joint line, also trans illumination allows observation of the great saphenous vein, that is in close relation to the infra-patellar branch of the internal saphenous nerve, that must be avoided. The needle is introduced from outside to inside, in the direction of the lesion. The portal is prepared with a number 11blade scalpel under arthroscopic control. The all-inside suture is accomplished with or without a working cannula, depending on the surgeons choice. Using a shaver the lesion is debrided and the intervening fibrous tissue is excised. Suturing is carried out using a 25º curved hook (Suture Lasso, Arthrex): a left curved hook is used for a right knee and vice versa. The curved hook is loaded with a no. 2 non-absorbable braided composite suture (Fiberwire, Arthrex) or a absorbable no.1 PDS introduced through the posteromedial portal. The curved hook must penetrate the peripheral wall of the MM, and then the inner wall of the MM. The free end of the suture in the posteromedial space is grasped and brought out through the posteromedial portal. A sliding knot (fishing knot type) is applied to the most posterior part of the meniscus with the help of a knot pusher and then cut. The sutures are repeated as required depending on the length of the tear (usually we place a knot every 5 mm of the tear). During suturing, care must be taken to not splinter the meniscus that can occur with multiple failed attempts to pass the curved hook. Additionally, entangling of the sutures must be avoided. In some patients, the tear may extend to the mid-portion of the meniscus requiring further repair through the standard anterior portal with meniscal suture anchor and/or an outside-in suture. The stability of the suture is then tested with the probe.

figure-3

Post-operative
Post operatively, active and passive range of motion is limited to 0-90º in the first six weeks. Full weight bearing is allowed by six weeks post-operatively. Jogging is permitted after 4 months, pivoting activity at 6 months, and unrestricted activities by 9 months.

Results
Ahn et al (4) in 140 patients showed complete healing in 118, incomplete healing in 17 and failure 5 repairs. The clinical success rate was 96.4% (135 of 140). Healing was associated with the type of tear and location. Incomplete healing and failures had complex tears or tears involving the red-white zone. Seventeen patients had incomplete healing at second-look arthroscopy but had no clinical sign of a meniscal tear. The mean Lysholm score and HSS scores improved post surgery (Table. 1) and 134 (95.7 %) patients had a normal (104 patients, 74.3%) or nearly normal (30 patients, 21.4%) the objective IKDC scores. In our prospective evaluation (46) of 132 patients undergoing a MM repair through a posteromedial portal in conjunction with ACL reconstruction, fifteen patients were found to be symptomatic according to Barret’s criteria on follow-up (6). The clinical failure rate was 9%, 4.9% in the subgroup “limited tear” and 15.7% in the subgroup “extended tear.” A limited tear was defined as one restricted to the posterior segment whereas those with a tear that extended to the mid-portion of the meniscus were classified as an extended tear. The extended tears required an additional repair through the standard anterior portal with meniscal suture anchor and/or an outside-in suture. The extended lesions had an increased risk of clinical failure. Out of the fifteen, 9 patients underwent revision surgery. Nine patients (6.8%) had failure of the meniscal repair; 3.7% (3/81) occurred in the subgroup of limited tears and 11.7% (6/51) in the subgroup extended tears. In the subgroup of extended tears, the cumulative survival rate did not decrease significantly and were not associated with a significant increased risk of revision of the MM. The average subjective IKDC improved at last follow-up and The Tegner activity scale at the last follow-up was slightly lower than before surgery (Table. 1).

table-1

Complications
The main complications may be related to the posteromedial portal placement. Damage to the infra-patellar branch of the saphenous nerve due to a posteromedial portal has been reported owing to the proximity of the nerve to the portal site causing hypoesthesia or paresthesia below the patella (27). Having said that, hypoesthesia resulting from harvesting the Semi-tendinous and Gracilis tendons in a concomitant ACL reconstruction may be responsible for 74% of the times (35). Transient hypoesthesia of the Sartorial branch of the saphenous nerve has also been reported probably due to an access portal situated too anteriorly (24). McGinnis et al (23) studied the neurovascular safety zone for the posteromedial access and recommended a portal through the posterior soft spot located formed by the medial head of the gastrocnemius, the tendon of the semimembranosus and the medial collateral ligament at the posterior aspect of the joint line for creation of the posteromedial portal. Hemarthrosis due to the long saphenous vein injury may occur in the postero medial approach (27). Among other complications, an iatrogenic medial meniscus tear may occur from repeated attempts at suturing the meniscus with a curved hook, rending suture impossible. Also, to our knowledge no popliteal artery, common peroneal and tibial nerve lesions has been reported, however they are at risk of damage during creation of the posterior portals. These complications may be avoided by placing the posterior portals with knee in 90 degrees of flexion. This moves the neurovascular structures posteriorly, away from the posteromedial portal site. Also, the Guillquist maneuver that provides trans-illumination may help visualize the course of the superficial veins and the accompanying nerves thus preventing inadvertent damage (35). Our series (46) also has a low complications rate with only two cases of hemarthrosis post operatively. Also, no patient developed a neuroma around the location of the posteromedial approach, although it was difficult to be accurately determining the incidence of saphenous nerve lesions due to the posteromedial approach as the hamstring tendon harvesting can cause hypoesthesia in the different territories of the saphenous nerve.

table-2

Discussion
The forces acting on the MM increase by as much as 200% after an ACL injury. Furthermore, forces acting on the ACL replacement graft increase by 33% to 50% after a medial meniscectomy (12,28). Deficiency of the medial meniscus has therefore been proposed as a secondary cause of ACL failure. It has thus been recommended that an ACL-deficient knee be reconstructed to protect the menisci (39,50). Conversely, identification and repair of a ramp lesion during an ACL reconstruction is imperative to reduce the risk of secondary graft failures, as these lesions may increase the anterior tibial translation (2,12, 30) and subsequently the strain on the graft. The success rates for meniscal repairs have been reported to be from 70% to 90% in vascular regions (11,13,16,36). Anh et al (12) reported a clinical successful healing rate of 96.4% in PHMM repairs with concomitant ACL reconstruction. Tenuta and Arciero (45) reported higher healing rates in concomitant ACL reconstruction than for isolated repairs (90% vs 57%). Meniscal repair in conjunction with ACL reconstruction has been reported to create a favorable environment for meniscal healing because of fibrin clot formation associated with intra-articular bleeding generated during ACL reconstruction (44). Multiple techniques for suturing the meniscus are available. The indications, advantages and disadvantages of each are mentioned in (Table.2). The all-inside suture repair technique using a hook is especially useful in a ramp lesion, as the use of newer devices makes the repair procedure blind and placing a suture in the vertical configuration is technically challenging. In addition Choi et al reported that the use of meniscal devices failed to provide sufficient strength of fixation. They recommended that during suturing, the posteromedial capsule should be elevated and approximated to the PHMM to ensure precise approximation of tear site (10). In spite of the development of the newer all-inside suture devices, the failure rate of the repair of PHMM tears continues to remains high, (19) which may be attributed to various factors that include inadequate visualization and debridement of the lesions of the PHMM; failure to confirm the reduction of the lesion with the all inside technique (48) and tissue failure due suture pullout through the meniscal tissue (45).
The mechanical strength of the vertical suture is greater than that of the horizontal suture (45). Having said that, most meniscal fixators cannot facilitate meniscal repair in a vertical mattress fashion (7,34) especially in the posteromedial corner of the medial meniscus, small or tight knee joints. Sutures spaced at every 3 to 5 mm have been recommended however; the optimal number is unknown (44). Pujol et al (33) using meniscal devices reported an overall healing rate of 73.1%. van Trommel et al (47) reported similar results (76%) with the outside-in technique. (Table. 3) Both studies observed a strong trend toward a relatively lower healing rate of the posterior horn (Zone A), as compared with the body (Zone B). (Table. 4) They also observed that, partial healing in all tears extending from the posterior to the middle third of the medial meniscus. We observed similar results in our study with a higher failure rate in the extended tear subgroup (6/51) (46). Pujol et al (33) attributed this to the difficulty in performing an adequate abrasion of the posterior segment using standard anterior arthroscopic portals whereas van Trommel et al (47) attributed that same to the relatively anterior placement of the needles with the outside-in technique, making a perpendicular repair extremely difficult. This resulted in a decrease in the coaptation force of the sutures. In addition, they observed that an oblique suture placement in the posterior zone with the outside-in technique made the sutures enter more anterior than they exit. Ahn et al (5) postulated that a torn posterior menisco-capsular structure moved inferiorly against the remaining meniscus, displacing the tear during knee flexion. They suggested that this motion of the torn medial meniscus can partially explain the slow healing observed in MMPH peripheral rim tears despite a rich vascular supply to the red-red zone. Pujol et al (31) in 2011 reported a secondary meniscectomy rate of 12.5%. The authors observed that the volume of meniscus removed decreased in 35% of cases, with respect to the initial tear and noted that a secondary meniscectomy following repair can partially save the meniscus and the failure called a ‘‘partial’’ failure. They recommended that suturing a tear therefore preserved the meniscal volume in a subsequent meniscectomy performed for a failure of repair or repeat tears. Tachibana et al (44) reported newly formed meniscal tears occurring in an area different from the initial repair site, on the surface of 34.5% of the healed and incompletely healed menisci. These new injuries were 1 to 3 mm in length partial- or full-thickness lesions and located central to the peripheral repair. In our series (46), the high rate of recurrent tear was as a result of newly formed tears that were confirmed on the surface of 5 menisci. It is conceivable that these injuries were attributable to a residual cleft left by the path of the Suture Lasso and maintained by the use of a strong no. 2 non-absorbable suture.

table-3

These clefts on the avascular meniscal substance may remain in situ without healing and would favor the recurrence of a more centrally located lesion in the white-white zone. Using a small suture hook device may therefore be desirable as it may reduce the size of the clefts created during suturing. In addition, the ‘cheese wiring effect’ due to the higher co-efficient of friction of a non-absorbable suture may contribute to a failure. We therefore decided to change our suture from a strong non-absorbable suture to a number 0 or 1 PDS suture, which are recommended to reduce the risk of these newly formed injury (37).
Nepple et al (26) observed that the time between injury and repair was the most important factor influencing healing. The zone of tear in reference to blood supply is another major factor affecting the results of a meniscal repair and ramp lesions in the red-red zone are expected to heal more readily than are those in the red-white zone (20). The criteria for healing based on follow-up arthro-CT corresponding to thickness of healing was suggested by Henning et al (36) can supplement clinical evaluation to improve diagnostic accuracy (Figure 3). The clinical failure rate in a systematic review ranged from 0% to 43.5%, with a mean failure rate of 15% (22). Failures after two years represented nearly 30% (26). Although numerous studies have reported short-term outcomes of various techniques of meniscal repair, relatively few have reported medium to long-term outcomes. The rate of meniscal repair failure appears to increase from short-term follow-up to medium to long-term follow-up regardless of the technique (26). There are limited numbers of studies assessing the outcomes of meniscal repair using the PM approach (4,5,10,46). Further prospective analysis with long – term follow-up is required to validate the promising early results of meniscal repairs performed with this approach. Finally, improved visualization is the key to achieving good meniscal repair results as it improves diagnosis of longitudinal tears in posterior horn MM (30), safeguards better debridement prior to repair and ensures good approximation of the torn ends under vision (1). It is thus important to perform a systematic exploration of the knee during an ACL reconstruction (Figure 1). A transnotch visualization combined with palpation of the meniscus with a needle or probe through the postero-medial portal aids in diagnosis of ramp lesions, which may otherwise be missed. Hidden lesions furthermore may be either very peripheral, covered by a layer of synovial or scar tissue or may not be reachable with a probe. It is therefore essential to identify these lesions during an ACL reconstruction and repair them whenever they are found to be unstable (40).

table-4

Conclusions
A systematic posteromedial exploration allows discovery of and debridement of the hidden MM lesion and repair with a suture hook device is associated with low morbidity. Failure Rates following a ramp lesion repair are low and occurs during the first 20 months. Even if a failure occurs the subsequent meniscectomy is limited and the volume of meniscal tissue debrided is reduced. An arthroscopic repair of meniscal ramp lesions should therefore be undertaken whenever possible.

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How to Cite this article:. Sonnery-Cottet B, Tuteja S, Barbosa NC, Thaunat M. Meniscus Ramp Lesion. Asian Journal of Arthroscopy Aug – Nov 2016;1(2):28-34.

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Volume 1 Issue 1 April - July 2016

Biology of Graft Incorporation

Elmar Herbst, Marcio B. V. Albers, Michaela Kopka, Humza Shaikh, Freddie H. Fu

Volume 1 | Issue 1 | April – Jun 2016 | Page 20-24

Author: Elmar Herbst [1], Marcio B. V. Albers [1], Michaela Kopka [1], Humza Shaikh [1], Freddie H. Fu [1]

[1] Department of Orthopaedic Surgery, University of Pittsburgh, 3471 Fifth Avenue, Pittsburgh, PA 15213-0802

Address of Correspondence

Prof. & Chair. Dr. Freddie H. Fu
Department of Orthopaedic Surgery, University of Pittsburgh, 3471 Fifth Avenue, Pittsburgh, PA 15213-0802.
E-mail: ffu@upmc.edu

Abstract

In order to achieve good long-term results after anterior cruciate ligament (ACL) reconstruction, appropriate graft-to-bone healing is essential. The ACL graft is most vulnerable to re-injury during the early post-reconstruction phase. This is due to the decrease in biomechanical properties that occurs throughout the remodeling and graft-to-bone healing process. These processes are highly dependent on the biological and mechanical environment of the knee. The majority of the evidence regarding graft-to-bone healing is based on animal research. However, radiographic and histologic studies in humans reveal a slow incorporation process, which must be respected in post-operative rehabilitation planning. Significant differences between the healing behavior of soft tissue and bone-tendon-bone grafts, as well as between auto- and allografts have been identified. While tendon-to-bone healing occurs with dense fibrous tissue, bone blocks become incorporated into the surrounding tunnels via primary bone healing. Consequently, bone-tendon-bone grafts reveal a different microscopic appearance and slightly faster tunnel incorporation than soft tissue grafts. In anatomic ACL reconstruction, postoperative rehabilitation protocols should be tailored to allow optimum graft-to-bone healing, thereby minimizing tunnel enlargement and risk of graft failure.
Key Words: anterior cruciate ligament, graft, healing, tendon to bone, bone to bone, biology

Introduction

The bony insertion of the anterior cruciate ligament (ACL) is comprised of four distinct zones: ligamentous tissue, non-calcified fibrocartilage, calcified fibrocartilage, and bone. This “enthesis” is responsible for effectively transmitting the forces from the elastic ligament to the stiff bone. Despite its well organized structure, the enthesis has limited vascularity and thereby poor healing capacity(16, 40). As a result, primary repair of a torn ACL has been shown to be ineffective in restoring knee kinematics and stability, and reconstruction of the ligament (with autogenous or allogenous tissue) has become the standard of care. Although the outcomes following ACL reconstruction are generally good, there remains a 7-10 % overall re-rupture rate which warrants further evaluation(11). Technical errors (most frequently malposition of the femoral tunnel) are the most common cause of graft failure(18). However, 3 – 27% of ACL re-ruptures are considered “biologic” graft failures, which occur due to inappropriate graft ligamentization and inadequate graft-to-bone tunnel healing(18).
In the early post-operative phase, the primary strength of an ACL graft is afforded by the means of femoral and tibial fixation. However, long-term stability and the ultimate success of ACL reconstruction are dependent mainly on the secondary mechanical properties of the graft – instilled through the remodeling and graft-to-bone incorporation processes28. The purpose of this review is to discuss the important aspects of graft-to-bone healing and highlight their clinical relevance in anatomic ACL reconstruction.

Figure 1: Magnetic resonance imaging (MRI) of a left knee of a 21-years old male patient one year after ACL reconstruction with an autologous quadriceps tendon grafts. A) Coronal T2-weighted coronal image with the arrow indicating the fibrous interface between the soft tissue graft and the bone tunnel. B) T1-weighted coronal cut with a homogenous intra-tunnel portion of the graft (arrow). C) T1-weighted sagittal image. At the distal part of the tibial bone tunnel the interference screw is visible. The arrow proximal to the interference screw highlights the fibrous interface in the anterior part of the bone tunnel.

The four stages of graft incorporation
Analogous to the intra-articular graft remodeling process, graft-to-bone healing can be subdivided into four stages: 1) inflammatory phase, 2) proliferative phase, 3) matrix synthesis, and 4) matrix remodeling(16). The similarity ends there, however, as each stage is distinctly different between the two processes. During the initial inflammatory response, the ACL graft undergoes partial necrosis. This stimulates the release of a cocktail of growth factors, which induce the proliferative phase and promote neovascularization and nerve ingrowth. The matrix synthesis and remodeling phases result in bone or collagen fiber formation at the bone-tendon-bone (BTB) and soft tissue graft-tunnel interface, respectively(6, 16, 28, 39). This complex process is affected by a variety of biologic and technical factors. Of the technical – and thereby controllable – factors, graft type and tunnel position are likely the most important(5, 37).

The influence of different graft types
Animal studies
In general, both the ACL graft remodeling and incorporation processes are different and faster in animals compared to humans. Therefore, histologic and biomechanical data from animal studies cannot be directly transferred to humans and must be interpreted in the appropriate context.

Soft tissue graft incorporation
Incorporation of soft tissue ACL grafts begins with the development of granulation tissue and perpendicular collagen (Sharpey-like) fibers at the tendon-bone interface. This process usually occurs during the first 3-4 weeks. The granulation tissue surrounding the graft expresses high levels of vascular endothelial growth factor (VEGF) and basic fibroblast growth factor (b-FGF), which leads to an increase in the amount of fibroblasts and blood vessels(14, 23). This rudimentary scar tissue is characterized by loose and poorly organized collagen types I, II, and III fibers. Over time, the amount of type II collagen decreases, and the remaining type I and III fibers become more dense and organized(14, 16, 26, 33).
The biology of the later stages of graft incorporation is less consistently reported in the literature. Some authors suggest that the graft becomes incorporated into the tunnel by woven bone as early as six weeks(19), while others have shown that dense collagen fibers predominate at the interface during this time33. The majority of the studies agree that bony ingrowth begins between 6-8 weeks(19, 23, 26). However, despite the formation of distinct cartilaginous (type-II collagen) tissue at the graft-tunnel interface, no direct insertion of fibrocartilaginous tissue is present at this time. Furthermore, the expression of VEGF, b-FGF, and collagen types II and III remains similar to the earlier stages of the incorporation process(13, 15, 26). At 12 weeks, a calcified cartilage zone similar to the native ACL insertion can be observed at the intra-articular tunnel aperture(19). This was demonstrated by Weiler et al., who showed that a mature fibrocartilaginous tendon-to-bone junction was present at 12 weeks in an interference-fit fixation study(29, 35). Others have disputed these findings, suggesting instead that the fibrocartilaginous tissue becomes more dense leading to bone tunnel sclerosis(33). The late stages of soft tissue graft incorporation are characterized by a decrease in cartilage metaplasia and resultant bony ingrowth (26). At six months following ACL reconstruction, significant ossification and formation of a four phase insertion can be observed at the graft-bone interface(19,35). This process continues along the length of the tunnel well beyond one year post-operatively. In a sheep model, Hunt et al. demonstrated that the intra-tunnel portion of the soft tissue ACL graft loses its tendinous structure and begins to show evidence of bony ingrowth at 2 years following reconstruction(10).

Bone-tendon-bone graft incorporation
Bone-to-bone healing is a different and much faster process than tendon-to-bone healing. During the first four weeks, granulation tissue develops at the bone graft-tunnel interface, and partial necrosis of the bone block occurs due to increased osteoclast activity(23, 33). Unlike soft tissue graft incorporation, only a small amount of fibrous tissue is formed(23). Studies have shown that BTB ACL grafts are at least partially incorporated into the tunnels after only 6 weeks(19, 23, 33). At 24 weeks, a fibrocartilaginous ligament-like insertion develops at the tunnel aperture, and by 6 months the graft is completely incorporated into the surrounding bone(38,19, 29).

Allograft incorporation
The intra-articular remodeling as well as the graft incorporation processes are much slower in allografts compared to autografts(3). Harris et al. investigated the graft-to-bone incorporation of BTB allografts in goats. At 18 weeks following surgery, they found no evidence of bony incorporation and only a connective tissue interface at the graft-tunnel junction. Not until 36 weeks did the bone blocks become fully incorporated(9).

Biomechanical consequences of graft incorporation and remodeling
Several studies have shown that the biomechanical properties of ACL grafts decrease steadily during the first few months following reconstruction(19). It is well documented that the intra-articular portion of the graft undergoes a distinct remodeling process that results in an initial decrease in strength and load to failure. However, the graft-to-bone incorporation must also be considered as a contributing factor to the overall decrease in the biomechanical properties seen in the early stages of graft healing.
In a canine model, the load to failure at three weeks following surgery was significantly lower in soft tissue compared to BTB grafts (p = 0.021). No significant difference was identified at six weeks. Interestingly, at 12 weeks, the soft tissue grafts exhibited a higher load to failure than the BTB grafts(33). Mayr et al. showed that all failures occurred in the mid-substance at six weeks and at the graft-tunnel junction at 3-6 months, regardless of graft type(19). These findings are supported by other studies, and suggest that intra-articular graft remodeling is more important early on, while graft incorporation becomes significant at the later stages of healing(23, 33). Given that graft remodeling and incorporation continue well beyond one year following surgery, the biomechanical properties correspondingly increase in this later time frame(14, 36).

Figure 2: Sagittal and coronal computed tomography image of a left knee of a patient six months after ACL reconstruction with an aoutologous quadriceps tendon with a patellar bone block in the femoral tunnel. The bone block is partially integrated in the surrounding bone (arrow). The bone tunnel is surrounded by a thin sclerotic wall (arrow).

Figure 3: T2-weighted MRI of a left knee of a patients four years following ACL revision with soft tissue allograft and a bony reaction with consecutive tibial bone tunnel widening due to a fixation device. The graft in the bone tunnel is not homogenous and surrounded by irregular fibrous tissue. At the proximal part of the bone tunnel an evident synovial influx is visible.

Histological findings in humans
The evidence surrounding graft-to-bone healing in humans is limited to a few case series, and therefore it is difficult to draw definitive conclusion from the data. Nevertheless, it is important to consider some of the key differences observed in human patients.

Hamstring tendon grafts
The process of soft tissue autograft incorporation into the surrounding bone tunnel is through formation of woven bone, which is penetrated by type I and III collagen fibers(24). In the first three months following reconstruction, the graft-bone interface consists primarily of dense, vascularized fibrous tissue surrounded by a layer of calcified osteoid. In this early phase, the fibrous tissue has no direct contact to the surrounding lamellar bone(25). At 5-6 months, the graft becomes surrounded by irregular fibrovascular granulation tissue with some areas of woven bone. Sharpey-like fibers begin to connect the graft to the bone, however, there is no evidence of bony ingrowth at this time(20, 25). Histological analyses of the graft-bone interface at 8-12 months following ACL reconstruction with hamstring tendon autograft show a firm attachment of the tendinous graft to the bone in some studies, and a persistent fibrous attachment in others(25,20). At one year following surgery, histological analyses show ongoing maturation of the graft-bone interface with an increase in Sharpey-like fibers and some evidence of peripheral bony ingrowth(20, 25).

Bone-tendon-bone grafts
In bone-tendon-bone grafts, the four-phase insertion of fibrocartilage can be preserved by ensuring that the bone plug rests flush with the intra-articular tunnel aperture. In this instance, the BTB graft becomes incorporated into the tunnel by direct bone healing. When the bone plug is recessed within the tunnel, the tendon-bone interface becomes incorporated via fibrocartilage(24). Ishibashi et al. performed histological analyses on the BTB graft-tunnel interface in patients who had undergone primary ACL reconstruction. Prior to one year from the time of surgery, granulation tissue was present between the tendinous portion of the graft and the bone tunnel. After one year, the granulation tissue was replaced by fibrous tissue containing collagen fibers, but without an obvious fibrocartilaginous insertion. The bone block, in contrast, was completely incorporated and could not be distinguished from the surrounding bone by one year postoperatively(12).

Imaging of graft incorporation
The incorporation of BTB grafts into the surrounding bone can be readily evaluated by computed tomography (CT) and magnetic resonance imaging (MRI) (Fig. 1, Fig. 2). Suzuki et al. used CT scans to show that the majority of BTB grafts were near-completely incorporated within the bone tunnel by eight weeks post-operatively(31). In contrast, the use of imaging to assess graft-to-bone healing of soft tissue grafts is much more demanding. A high resolution MRI can often be helpful in visualizing the remodelling and bone incorporation process8. However, accurate assessment of graft revascularization requires the use of contrast-enhaced MRI or MR angiography.
MRI studies have shown that the revascularization process peaks at two months following ACL reconstruction and then decreases steadily over time(32). Interestingly, revascularization of BTB grafts is significantly faster in the intra-articular portion of the graft compared to the intra-tunnel segment. A recent MRI study revealed that revascularization of the intra-tunnel portion of the BTB graft persists beyond one year after surgery, suggesting that bone-to-bone incorporation may be slower than initially demonstrated by histological studies(21). Similar results were obtained when investigating the revascularization of soft tissue autografts(22, 27).

Clinical implications of incomplete graft incorporation
Early return to function is a common goal following ACL reconstruction and modern rehabilitation protocols have been tailored accordingly. Range of motion exercises and gentle strengthening are important to maintain quadriceps function and mitigate the risk of arthrofibrosis. While femoral and tibial fixation techniques are responsible for maintaining graft strength in the early postoperative period, it is the graft remodeling and graft-to-bone incorporation processes that determine the long-term stability success of an ACL reconstruction4.
An important clinical problem in graft-to-bone incorporation is tunnel enlargement (Figure 3). Although this is a multi-factorial issue, one contributing factor is the discrepancy of the healing process across different segments of the bone tunnel. Studies show that the number of osteoclasts as well as their activity level is higher at the intra-articular bone tunnel aperture1. Consequently, bony ingrowth occurs preferentially at the peripheral end of the bone tunnel(2). This in combination with an increased graft motion near the intra-articular tunnel aperture can result in tunnel widening and impaired graft-to-bone healing(26). This finding is corroborated by a number of clinical studies(34), whereas others found that bone tunnel widening does not influence graft incorporation(17).
Another issue which may predispose to tunnel enlargement is the graft bending angle. In anatomic ACL reconstruction, a bend develops as the graft transitions from the intra-articular portion into the tunnel. Particularly with soft tissue grafts, this results in an asymmetric position of the graft at the tunnel aperture and formation of a gap between the graft and the tunnel wall(7). Synovial fluid and osteoclasts can enter this space and stimulate tunnel widening.
Finally, the position of the bone socket plays a critical role in the motion of the graft within the tunnel(30). This was demonstrated by Ekdahl et al., who showed that bone tunnel enlargement is significantly decreased in anatomic ACL reconstruction compared to non-anatomic tunnel placement. The non-anatomic reconstructions revealed an increased amount of osteoclasts and a decreased amount of vascularization compared to the anatomic reconstructions(5).

Conclusions

Successful graft-to-bone incorporation plays an integral role in the long-term outcomes following ACL reconstruction. Animal studies provide some understanding of this complex process and highlight the differences between graft and tissue types. However, the results of animal studies are not analogous to human data, which reveals a distinct and much slower incorporation process. The available evidence suggests that anatomic ACL reconstruction and likely a less aggressive rehabilitation protocol are both important variables in optimizing graft incorporation and improving patient outcomes.

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How to Cite this article:. Herbst E, Albers M, Kopka M, Shaikh H, Fu FH, . Biology of Graft Incorporation. Asian Journal of Arthroscopy Apr- June 2016;1(1):20-24 .