Clinical Anatomy 22:371–376 (2009)

ORIGINAL COMMUNICATION

The Arterial Supply of the Patellar Tendon: Anatomical Study with Clinical Implications for Knee Surgery

JACK PANG,* SARAH SHEN, WEI REN PAN, IAN R. JONES, WARREN M. ROZEN, AND G. IAN TAYLOR Jack Brockhoff Reconstructive Plastic Surgery Research Unit, Department of Anatomy and Cell Biology, University of Melbourne, Parkville, Victoria, Australia

The middle-third of the patellar tendon (PT) is well-established as a potential graft for cruciate ligament reconstruction, but there is little anatomical basis for its use. Although studies on PT vascular anatomy have focused on the risk to tendon pedicles from surgical approaches and knee pathophysiology, the significance of its blood supply to grafting has not been adequately explored previously. This investigation explores both the intrinsic and extrinsic arterial anatomy of the PT, as relevant to the PT graft. Ten fresh cadaveric lower limbs underwent angiographic injection of the common femoral artery with radio- opaque lead oxide. Each tendon was carefully dissected, underwent plain radi- ography and subsequently schematically reconstructed. The PT demonstrated a well-developed and consistent vascularity from three main sources: antero- proximally, mainly by the inferior-lateral genicular artery; antero-distally via a choke-anastomotic arch between the anterior tibial recurrent and inferior medial genicular arteries; and posteriorly via the retro-patellar anastomotic arch in Hoffa’s fat pad. Two patterns of pedicles formed this arch: inferior-lateral and descending genicular arteries (Type-I); superior-lateral, in- ferior-lateral, and superior-medial genicular arteries (Type-II). Both types sup- plied the posterior PT, with the majority of vessels descending to its middle- third. The middle-third PT has a richer intrinsic vascularity, which may enhance its ingrowth as a graft, and supports its conventional use in cruciate ligament reconstruction. The pedicles supplying the PT are endangered during procedures where Hoffa’s fat pad is removed including certain techniques of PT harvest and total knee arthroplasty. Clin. Anat. 22:371–376, 2009. VC 2009 Wiley-Liss, Inc.

Key words: patellar; tendon; cruciate; vascular; arterial

INTRODUCTION kneel and knee-walk, and significant radiological and histological abnormalities at 2 years post-operation The middle-third of the patellar tendon (PT) is (Kartus et al., 2001), as well as PT rupture commonly utilized in Orthopaedic surgery as a graft for cruciate ligament reconstruction, yet there has been little anatomical research into the basis of this *Correspondence to: Jack Pang, Jack Brockhoff Reconstructive use. There are several practical attributes that make Plastic Surgery Research Unit, Room E533, Department of Anat- it suitable including the convenience of a single inci- omy and Cell Biology, University of Melbourne, Grattan St., Park- sion to harvest the graft and access the joint space, ville 3050, Victoria, Australia. E-mail: [email protected] and well-located bone attachments to utilize as end- Received 23 September 2008; Revised 10 December 2008; plugs. A disadvantage of middle-third PT harvest is Accepted 15 December 2008 donor site morbidity, with documented problems Published online 27 January 2009 in Wiley InterScience (www. such as sensory disturbance and pain, inability to interscience.wiley.com). DOI 10.1002/ca.20770

VC 2009 Wiley-Liss, Inc. 372 Pang et al.

(Marumoto et al., 1996). Certain causative factors and plain radiographs, which were taken as the non- for this morbidity have been proposed, including the tendon vessels and layers of fascia were gradually interruption to the blood supply of the remaining PT removed. A splay of the tendons was created for (Marumoto et al., 1996). However such propositions, two-dimensional radiography, which was found to as well as the reason for the success of the grafted distort the normal arrangement of the tissue, and tissue itself have not been well investigated. therefore surgical clips were used to mark the ends Interest in the vascularity of the PT has mostly of separated vessels, and imaging software (Adobe arisen from concern about the risk to PT blood supply Photoshop 7.0 CS, Adobe Systems, California) from surgical procedures such as arthroscopy (Sol- allowed digital tracing of the relevant arterial dado et al., 2002), and for insight into pathology branches and annotation of the separated vessels. such as patellar tendinopathy (Soldado et al., 2002) and PT rupture (Marumoto et al., 1996). Two previ- ous studies have investigated the relevant vascular RESULTS anatomy with reference to pedicled grafting of the PT (Paulos et al., 1983; Weinstabl et al., 1986). The source vessels and extrinsic course of these These studies have described the terminal ramifica- vessels to the PT was adequately seen macroscopi- tions of the genicular arteries in Hoffa’s (infra-patel- cally and radiographically in all 10 specimens. The lar) fat pad and in the patellar rete, and used pho- intrinsic arterial anatomy was well demonstrated in tography to illustrate their contribution to the blood six specimens (from four cadavers), however in four supply of the PT (Paulos et al., 1983; Weinstabl specimens the intrinsic anatomy was inadequate for et al., 1986; Scapinelli, 1997; Soldado et al., 2002). analysis due to a combination of tissue putrification Whilst the locations of the main pedicles to the PT and poor microvascular filling. were clearly demonstrated, finer details of the The arterial supply of the anterior side of the PT source arteries and the distribution of the arterial was provided by two separate sources, at each of tree as it permeates the tendon were not adequately the PT’s proximal and distal ends, with a longitudinal demonstrated. The present study aims to further anastomosis linking the two (Fig. 1A and 1B). In all define the arterial anatomy of the PT to provide cases, the inferior-lateral genicular artery (ILGA) insight into the existing vessels of the PT graft, and provided the main pedicle to the antero-proximal the endangerment to its blood supply from certain supply, with descending branches from the superior- surgical procedures. lateral genicular artery (SLGA), superior-medial gen- icular artery (SMGA), and the musculo-articular branch of the descending genicular artery (maDGA) METHODS contributing smaller vessels (Fig. 1A). The antero- distal supply was consistently via a horizontal anas- The investigation was performed on 10 fresh tomosis between the inferior-medial genicular artery cadaveric lower limbs from six cadavers (aged 36– (IMGA) and the anterior tibial recurrent artery 82, mean age 71). None of the limbs had undergone (ATRA), shown macroscopically (Fig. 1A), and both previous knee surgery. The limbs were harvested 2 radiographically and schematically (Figs. 2 and 3A). days post-mortem, by disarticulation at the hip. The The choke-type anastomosis (connection via many common femoral artery was dissected clear of peri- smaller branches) between these antero–distal pedi- vascular tissue and cannulated. A radiopaque lead- cles has been previously referred to as the ‘‘supra- oxide mixture was prepared according to previously tubercular arch’’ (Soldado et al., 2002), discussed described techniques (Rees and Taylor, 1986), which further below. It also provided small branches to consisted of heated normal saline (to 508C), 10% supply the posterior aspect of the distal PT (Fig. 3B). weight/volume of commercial grade (96% pure) The arterial supply of the posterior PT differs lead-oxide as an orange powder, and 10% weight/ markedly with that of the anterior side, with only volume gelatine. Each limb was submerged in a one main source of vessels identified. The pedicles warm bath, and the mixture was slowly injected in formed a transversely oriented anastomosis within an anterograde fashion, with the end-point of injec- the antero-superior aspect of Hoffa’s fat pad, which tion determined when the capillaries of the toes were corresponded to the previously described ‘‘retro- deemed to be perfused by the mixture, upon distal patellar arch’’ (Soldado et al., 2002), discussed fur- incision. The specimens were then refrigerated for ther below. It was a true-type anastomosis because 24 hr to allow setting of the gelatine, before dissection. of the main connection forming from single or dual Dissection comprised the identification of feeding large vessels (Figs. 1B and 2). In each of the speci- vessels to segments of the PT, and dissection of each mens, it formed as either a: Type-I (50%), with ped- vessel back to its parent artery and then to the pop- icles from the ILGA and maDGA; or Type-II (50%), liteal artery. Once all of the major arteries had been with pedicles from the SLGA, ILGA, and SMGA with isolated, the named genicular arteries were identi- accessory input from the maDGA (Fig. 3B). fied. Upon gross inspection, the overlying anterior The retro-patellar arch provided descending ves- paratenon and Hoffa’s fat pad were noted to be sels that predominantly supplied the middle-third, richly vascularized, and thus this area was further and smaller ascending vessels to the proximal investigated using the surgical microscope. The rela- attachment (Figs. 1B and 2). Preparation in sagittal tionship of these vessels to the tendon proper was section demonstrated that descending branches thus described. The vascular anatomy was imaged from this arch also supplied the tibial periosteum (and documented) with the use of serial photographs deep to the infra-patellar bursa. As with the parate- Arterial Supply of the Patellar Tendon 373

Fig. 1. A: Anterior view photograph from a lead-ox- two indicate tibial tuberosity. B: Posterior view photo- ide injected specimen with labeled genicular arteries graph from a lead-oxide injected specimen with labeled (SLGA, superior lateral; ILGA, inferior lateral; SMGA, genicular arteries (SLGA, superior lateral; ILGA, inferior superior medial; IMGA, inferior medial; DGA, descend- lateral; SMGA, superior medial; maDGA, musculo-artic- ing geniculate; maDGA, musculo-articular part of de- ular part of descending geniculate). The complex net- scending; ATRA, anterior tibial recurrent). The ILGA is work of the retro-patellar anastomosis is evident, the main supplier of the proximal attachment, whereas receiving various genicular pedicles. Note the longitudi- a choke anastomosis of reduced caliber vessels from nal orientation of the branches from the arch to the the genicular pedicles overlies the distal attachment. tendon surface. Proximal two blue pin-heads indicate patella, and distal non, Hoffa’s fat pad contains many arterial vessels of graphically, with the current study achieving this and which only approximately half continue to supply the able to demonstrate the microscopic vascular anat- PT. Other small branches originating directly from omy of this tendon. Previous studies have largely the ATRA and SMGA contributed to the supply of the focused on the anastomoses that occur in the peri- posterior side’s lateral and medial thirds. Under the tendinous tissue and the course of the extrinsic vas- dissecting microscope, deep intra-tendinous commu- culature (Soldado et al., 2002). In the current study, nication was observed between the anterior and pos- the use of angiographic techniques enables the three terior arterial trees, however these vessels were dimensional appreciation of both the extrinsic and minor compared with the large longitudinal anasto- intrinsic arterial territories of the PT, through multi- moses that were superficial on the tendon surface planar and cross-sectional studies and well as post- (Fig. 1A and 1B). radiographic dissection studies. This provides a new perspective that allows for a more clear understand- ing of the PT’s arterial supply, and the discussion of DISCUSSION several significant clinical implications. Our study supports previous evidence of three lat- There have been no previous studies that have eral pedicles originating from the SLGA, ILGA, and demonstrated the arterial supply of the PT radio- ATRA, and the supply of the retro-patellar arch by 374 Pang et al.

Fig. 2. Radiograph of the patellar tendon vascula- proximal and distal attachments, and in the central ture, with this specimen sectioned into anterior and area. Lower: The posterior half exhibits a well-devel- posterior halves. The schematics are views of the exter- oped retro-patellar arch between the maDGA and ILGA nal tendon surfaces with labeled genicular arteries arterial pedicles. A few branches ascend to supply the (SLGA, superior lateral; ILGA, inferior lateral; SMGA, posterior half’s proximal attachment, but the richest superior medial; IMGA, inferior medial; maDGA, mus- supply is seen descending in the central third which culo-articular part of descending; ATRA, anterior tibial continues to anastomose with vessels from the ATRA recurrent). Upper: The anterior half receives supply and SMGA. from five genicular arteries, with anastomoses near the

the ILGA with additional contribution from the SLGA been only one documented anatomical study on (Soldado et al., 2002). The medial pedicles have cadavers with previous cruciate reconstruction using been described with some variability in the literature, allografts, which demonstrated revascularization in with one study highlighting the importance of the nearly the entirety of the neo-ligament (Malinin DGA in providing two pedicles, whilst suggesting the et al., 2002). Other knowledge is deduced from SMGA did not provide a tendon pedicle (Soldado post-surgical biopsy studies of the human graft, with et al., 2002). Another study reports the SMGA and both evidence of revascularization (Malinin et al., DGA to form the main superior pedicles (Kirschner 2002) and also reports of the ‘‘avascular graft’’ et al., 1996). The present study demonstrates that (Arnoczky et al., 1982). Several animal studies indi- in 50% of specimens both of these arteries contribute cate that there is an ordered sequence leading to the medially to the retro-patellar arch, and that in 50% of revascularization of the graft, from the ensheathing specimens only the maDGA supplies the retro-patellar of a synovial envelope to the ingrowth of vessels arch. Both the maDGA and SMGA were also found to from the femoral attachment, infra-patellar fat pad, consistently contribute to the antero-proximal tendon, and posterior joint (Sckell et al., 1999; Yoshikawa which was otherwise mostly supplied by the ILGA. et al., 2006). Vascular endothelial growth factor Whether the human tendon graft can revascular- expression has also been demonstrated in the animal ize as a cruciate ligament is contentious. There has neo-cruciate ligament (Yoshikawa et al., 2006). In Arterial Supply of the Patellar Tendon 375

Fig. 3. A: Arterial territory of the anterior surface patellar arch (50% of specimens), whereas Type II of the patellar tendon. The supply of the anterior side derives the main supply from a three-artery retro-patel- was found to be consistent in all specimens, with one lar arch with a further accessory artery (50% of speci- type of conformation depicted. B: Arterial territory of mens). Main arteries: superficial femoral (yellow); de- the posterior surface of the patellar tendon. Two types scending genicular (purple); popliteal (red); and ante- of conformation are depicted for the posterior side. rior tibial (blue). Type I derives the main supply from a two-artery retro- the specimens of the present study, the middle-third struction and total knee arthroplasty involve partial of the PT contained a greater number of arterial ves- or total resection of the fat pad. Several studies sug- sels compared to the lateral and medial thirds, with gest that when Hoffa’s fat pad is preserved, it plays vessels descending from the retro-patellar arch to a key role in the regeneration of the middle-third course longitudinally with the tendon fibers. As stud- defect (Sanchis-Alfonso et al., 1996; Atkinson et al., ies with other tissues indicate, angiogenesis occurs 1998; Sanchis-Alfonso et al., 1999), in addition to from a pre-existing endothelium (Folkman, 1985; the contribution from the anterior paratenon (San- Yoshikawa et al., 2006), and as such the richer vas- chis-Alfonso et al., 1999). However, it has been cular bed of the middle-third PT may theoretically shown in the animal model that when the fat pad is act as a better scaffold for revascularization and in- preserved (albeit with incision) during PT harvesting, growth as a graft. there are proliferative changes in the remaining ten- Our anatomical findings suggest that the insult to don and a fibrotic thickening of Hoffa’s fat pad. It is both the intrinsic and extrinsic vasculature after mid- therefore suggested that these processes may be dle-third PT harvest, may significantly interrupt the implicated in the pathogenesis of infra-patellar con- blood supply to the residual tendon. PT rupture is a tracture syndrome and anterior knee pain (Atkinson rare but significant surgical complication of middle- et al., 1998, 1999). In theory, removal of paratendi- third PT harvest, with one case-report suggesting nous tissue (e.g., Hoffa’s fat pad) in addition to har- that devascularization may be a cause (Marumoto vest of the middle-third PT, may correspond to re- et al., 1996). Certain techniques of open ACL recon- moval of important arterial anastomoses and supply- 376 Pang et al. ing vessels, and this may compromise the PT’s re- Atkinson PJ, Oyen-Tiesma M, Zukosky DK, DeCamp CE, MacKenzie generative ability. Other knee approaches that CD, Haut RC. 1999. Patellar tendon augmentation after removal endanger this vasculature include double para-patal- of its central third limits joint tissue changes. J Orthop Res 17: lar incisions, lateral retinacular release and postero- 28–36. Atkinson TS, Atkinson PJ, Mendenhall HV, Haut RC. 1998. Patellar lateral corner repair, as appreciated in other publica- tendon and infrapatellar fat pad healing after harvest of an ACL tions (Vialle et al., 1997; Soldado et al., 2002). The graft. J Surg Res 79:25–30. surgeon need have an awareness of the course of Folkman J. 1985. Tumor angiogenesis. Adv Cancer Res 43:175–203. the tendon pedicles, and have caution when expos- Kartus J, Movin T, Karlsson J. 2001. Donor-site morbidity and ante- ing the surrounds of the PT during such procedures. rior knee problems after anterior cruciate ligament reconstruc- tion using autografts. Arthroscopy 17:971–980. Kirschner MH, Menck J, Hofmann GO. 1996. Anatomic bases of a CONCLUSION vascularized allogenic knee joint transplantation: arterial blood supply of the human knee joint. Surg Radiol Anat 18:263–269. The finer details of the intrinsic and extrinsic arte- Malinin TI, Levitt RL, Bashore C, Temple HT, Mnaymneh W. 2002. A rial supply of the PT have been demonstrated in the study of retrieved allografts used to replace anterior cruciate lig- current study. The use of angiographic techniques, aments. Arthroscopy 18:163–170. not previously described, present radiographic evi- Marumoto JM, Mitsunaga MM, Richardson AB, Medoff RJ, Mayfield GW. 1996. Late patellar tendon ruptures after removal of the dence of the pedicles and the intra-tendinous course central third for anterior cruciate ligament reconstruction. A of their branches, and we have ultimately described report of two cases. Am J Sports Med 24:698–701. this supply by arterial territories. The consistent find- Paulos LE, Butler DL, Noyes FR, Grood ES. 1983. Intra-articular cru- ings between all specimens, demonstrating the ten- ciate reconstruction. II. Replacement with vascularized patellar don vessels arising from three main sources, show ligament. Clin Orthop Relat Res 172:78–84. that the anterior side is consistently supplied by the Rees MJ, Taylor GI. 1986. A simplified lead oxide cadaver injection ILGA proximally, and that the supra-tubercular arch technique. Plast Reconstr Surg 77:141–145. distally forms from the ATRA and the IMGA. The ped- Sanchis-Alfonso V, Monteagudo-Castro C, Rosello´-Sastre E, Carda C, Subı´as-Lo´pez A, Gil-Santos L, Peydro´ A. 1996. Value of the icles to the retro-patellar arch were variable, with Hoffa fat pad in recellularization of allografts used to replace the two configurations identified and described. This ACL. Orthopedics 4:281–290. study invites further investigation of the PT vascular- Sanchis-Alfonso V, Subı´as-Lo´pez A, Monteagudo-Castro C, Rosello´- ity to strengthen our understanding of the anatomi- Sastre E. 1999. Healing of the patellar tendon donor defect cre- cal variability. ated after central-third patellar tendon autograft harvest. A These findings have implications for current long-term histological evaluation in the lamb model. Knee Surg reconstructive and orthopedic techniques, including Sports Traumatol Arthrosc 7:340–348. supporting the conventional use of the middle-third Scapinelli R. 1997. Vascular anatomy of the human cruciate liga- PT for cruciate ligament reconstruction, and high- ments and surrounding structures. Clin Anat 10:151–162. Sckell A, Leunig M, Fraitzl CR, Ganz R, Ballmer FT. 1999. The con- lighting the vessels that may be endangered in surgi- nective-tissue envelope in revascularisation of patellar tendon cal approaches to the knee. grafts. J Bone Joint Surg Br 81:915–920. Soldado F, Reina F, Yuguero M, Rodrı´guez-Baeza A. 2002. Clinical anatomy of the arterial supply of the human patellar ligament. ACKNOWLEDGMENTS Surg Radiol Anat 24:177–182. Vialle R, Beddouk A, Cronier P, Fournier D, Papon X, Mercier P. The authors thank Mrs. Prue Dodwell, Dr. Hiroo 1997. Prevention of hemorrhagic complications in the lateral ret- Suami, Associate Professor Mark Ashton, and Associ- inacular section of the patella. A study of the lateral arteries of ate Professor Martin Richardson for their support and the knee applied to the prevention of knee hemarthrosis. Rev advice. Chir Orthop Reparatrice Appar Mot 83:665–669. Weinstabl R, Wagner M, Schabus R, Firbas W. 1986. Anatomical bases of patellar tendon grafts used in anterior cruciate ligament reconstruction. Surg Radiol Anat 8:163–167. REFERENCES Yoshikawa T, Tohyama H, Enomoto H, Matsumoto H, Toyama Y, Yasuda K. 2006. Expression of vascular endothelial growth factor Arnoczky SP, Tarvin GB, Marshall JL. 1982. Anterior cruciate liga- and angiogenesis in patellar tendon grafts in the early phase af- ment replacement using patellar tendon. An evaluation of graft ter anterior ligament reconstruction. Knee Surg Sports Trauma- revascularization in the dog. J Bone Joint Surg Am 64:217–224. tol Arthrosc 14:804–810.