The issue of vascularity in fractures and nonunion of the scaphoid

Review article THE ISSUE OF VASCULARITY IN FRACTURES UNION OF THE SCAPHOID

AND NON-

U. BUCHLER and L. NAGY

From the Division of Hand Surgery, University of Berne, Inselspital, Berne, Switzerland Journal of Hand Surgery (British and European Volume, 1995) 20B: 6." 726-735 There is obviously some variability in the arrangement of the vascular foramina along the radial to dorsal ridge. In 13% of the specimens of Obletz and Halbstein (1938), no foramina were found proximal to the waist; in 20% one arterial foramen was seen and in 67% two or more foramina were present. In 14% of Gelberman's samples, the dorsal vessels entered distal to the waist; in 59% the vessels penetrated directly over the waist and in 27% the vessels were located just proximal to the waist (Gelberman and Menon, 1980).

Existing information on ischaemia of the scaphoid is scattered in the literature and has not been comprehensively compiled. This review article collects the available knowledge, points at deficiencies in the present understanding of "avascular necrosis" of the scaphoid, and establishes a scaffold for the design of further research projects. THE BLOOD SUPPLY TO THE SCAPHO1D Development

Proximal vascular axes

During the transition from precartilage to cartilage, the substance of the scaphoid anlage is penetrated by a number of isolated arterial buds with sinusoidal endings. With the appearance of the nucleus of ossification, a delicate central arterial network develops, similar to that seen in the epiphyses of the long bones. This primitive nourishing system is gradually replaced by the final arrangement of principal arteries (Crock et al, 1980).

Travaglini (1959) noted vessels entering the proximal pole through the scapho-lunate ligament. Gelberman and Menon (1980) pointed out several small vessels in the region of the proximal pole, related to the deep radio-scapho-lunate ligament which did not truly penetrate the bone at the proximal pole. Kuhlmann and Guerin-Surville (1981), based on 50 dissections, identified an anterior vascular pedicle with a close relationship to the palmar radio-carpal ligaments and the proximal pole of the scaphoid in 40% of their specimens. Mestdagh (1982) found direct scapho-lunate branches both palmarly and dorsally, coming from the respective palmar and dorsal transverse carpal arches. This was confirmed by the injection studies of Oberlin et al (1992). Recently, Kauer (1993) stressed the potential role of the deep radio-scapho-lunate ligament as an extrinsic source of blood supply to the proximal pole of the scaphoid.

Distal vascular axes

Three main vascular axes to the scaphoid have been described by Grettve (1955), Minne et al (1973) and Taleisnik and Kelly (1966). This principal supply system is related to the ligamentous attachments around the distal two-thirds of the bone surface and encompasses: 1. The lateral palmar group, derived from the superficial palmar branch of the radial artery or the radial artery itself entering the scaphoid at the palmar lateral tubercle (Obletz and Halbstein, 1938), which Taleisnik interprets as the main contributor to the intraosseous blood supply.

Inner vascular network and venous drainage

The main arterial blood supply extends from the distal third towards the weight bearing area of the proximal pole, with several distinct small arteries traversing the proximal waist, and a number of branches running at a right-angle towards the bone surface. These end in typical subperiosteal and subchondral vascular arcades. The capillary bed is particularly abundant in the loaded subchondral areas. The venous collecting system is oriented predominantly in a parallel arrangement to the joint surface and drains towards the areas of capsular attachments and the vascular hila (Crock et al, 1980). From there, the venous blood passes into the venae commitantes of the radial artery (Handley and Pooley, 1991).

2. The dorsal group with one to three pedicles from the dorsal carpal branch of the radial artery or its main trunk, entering the scaphoid at its dorsal ridge, with foramina reaching from the distal third to the waist area. Gelberman and Menon (1980) attribute 70% to 80% of the scaphoid's blood supply to this group. 3. The distal (palmar) group, which originates from the superficial palmar branch of the radial artery and enters/exits the scaphoid at its distal, palmar and ulnar pole. While the lateral palmar and the dorsal systems anastomose freely within the scaphoid, the distal group supplies a circumscribed area of the tuberosity only, and is hence relatively unimportant. 726

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BONE ISCHAEMIA IN SCAPHOID FRACTURES Pathogenesis As most scaphoid fractures occur by forcible hyperextension and radial deviation, a mechanism of injury involving palmar gap-formation may be anticipated. Thus, a scaphoid fracture breaches the relatively avascular radial and palmar capsular attachments and inevitably disrupts the inner longitudinal axial vasculature of the proximal bone substance. The capsular attachment along the dorsal ridge and the radio-scapho-lunate interface is not necessarily ruptured. Due to the arrangement of the axial vascular supply, the distal fragment is hardly ever affected by impairment of vascularity. Whether or not a proximal fragment loses its blood supply depends on multiple factors: - - the location and spacial arrangement of the fracture with a greater risk of devascularization in proximal locations (Cooney et al, 1980a; Pennsylvania Orthopaedic Society, 1962; Stewart, 1954) - - the mechanism and violence of the traumatic impact - - the degree of dislocation at the time of injury - - the existence or non-existence of associated injury to the deep radio-scapho-lunate ligament - - the proximal reach of the nutrient vessels along the dorso-radial ridge as outlined before - - the competence of the extrinsic blood supply to the proximal pole as discussed earlier. Perhaps the general condition of microcirculation (age, presence of vascular disease, etc). Additional factors may play a role. Vascular impairment following a scaphoid fracture must be conceived as a dynamic condition, ranging from transient ischaemia to frank anoxia. Incidence The true incidence and importance of devascularization of a proximal fragment has not yet been exactly determined. Transient ischaemia probably arises frequently, but frank persisting anoxia and necrosis presumably occur in fewer than 14% of cases (Mulder, 1968; Russe, 1960). In a comprehensive analysis of the temporal evolution of T1 and T2 weighted signal intensity in acute and fresh scafghoid fractures, Imaeda et al (1992) presented eight waist fractures in which the T1 signal remained normal for the first few days, slightly decreased up to the second or third months and returned to normal within 3 to 4 months. T2 weighted signal intensity increased until the fractures had healed.

and the other elements of the bone marrow, while the lacunat osteocytes and the osteoblasts in the trabecular seams may survive for a few days. The necrosis entails an inflammatory reaction which is well established by the 7th day. At 2 weeks, the osteocytic lacunae are empty; granulation tissue has formed in the marrow and cellular dtbris is removed. Repair starts between the 3rd and 4th Week from adjacent viable bone with an advancing front of undifferentiated connective tissue invading the necrotic area; macrophagic activity, osteoclastic removal of dead trabeculae and new bone formation are seen. D e n o v o osteogenesis seems to occur by metaplasia from woven dense fibrous tissue without the need for a pre-existing cartilagenous template. Resorptive activity of the early reparative processes reduces.the mineral content and weakens the strength of avascular bone; in the process of revascularization, the mineral content is re-enhanced, but the mechanical strength decreases further (Yu et al, 1975). In the femoral head of dogs, the decrease in mean compressive strength in the subchondral bone was 18% at 2 months, 36% at 4 months and 73% at 6 months (collapse); the decrease in mean strain energy of affected cancellous bone was 43% at 2 and at 4 months (Wang, 1993). DEFINITION, CLASSES AND TYPES OF "AVASCULAR NECROSIS" OF THE SCAPHOID Terminology In current clinical practice, the term "avascular necrosis" is used to label a wide spectrum of conditions of assumed circulatory compromise. Strictly speaking, the idiom should be reserved to designate histologically proven "death of bone substance from anoxia and its sequelae". Difficulty exists regarding the variable involvement of an affected bone segment which often displays a patchy arrangement of ischaemic lesions, and regarding the biologic dynamics of the spontaneous repair process evolving through various stages. Existing classification Based on clinical, radiographic and surgical observations, Herbert (1990) proposed a simple classification, distinguishing bone ischaemia (dense on X-ray, sclerotic at surgery, no collapse, amenable to internal fixation, healing slower) from clearcut necrosis (replacement by scar tissue, loss of trabecular framework, fragmentation, bone collapse, poor healing tendency). Our own classification

EXPERIMENTAL STUDIES ON AVASCULAR BONE NECROSIS Avascular bone necrosis has been studied in a canine model (Brody et al, 1991; Malizos et al, 1993). Within a few hours, bone anoxia leads to necrosis of the fat

For obvious reasons, comprehensive serial histological examinations of the evolution of the various classes of avascular necrosis of the carpal scaphoid are not available. The majority of procurable specimens are obtained from curettage material of proximal fragments during

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Matti-Russe type procedures, resection material during palmar wedge grafting, from excisions of very small avascular proximal pole fragments, or from whole scaphoids in cases where proximal row carpectomy was carried out. The evidence thereof, together with individual clinical and imaging data, experimental data and information gained by analogy from cases of Kienbrck's disease, justifies the following classification which we have proposed: Class I avascular necrosis"

If patency of a dorsal proximal nutrient vessel is not preserved, the break-down of the inner axial bone circulation leads to anoxia of the marrow and the trabeculae of the dependent regions and provokes necrosis as previously outlined (Berggren et al, 1982). Associated lipolysis translates into a marked decrease of MRI T1 signal intensity at that stage. The peripheral regions may undergo transient ischaemia only and may survive on the basis of random blood flow within retained capsular attachments and/or be nourished by synovial diffusion. Despite the death of osteocytes in the central regions, the physical integrity of the trabeculae is preserved and radiographs remain normal at first. Anoxia triggers an excellent stimulus for the ingrowth of neovascularization, which is promptly mediated by any viable surrounding tissue, particularly the dorsal ridge capsule, the deep radio-scapho-lunate ligament (if not significantly co-injured as sometimes seen in cases of proximal pole fractures) and the distal fracture surface (if reduced and immobilized). Ingrowing vasculature may establish connections to the remaining inner vascular network in cases of ischaemia, or form a brush of new vascular sprouts in cases of frank necrosis. Among other factors, the capacity for undisturbed vascular ingrowth resides in the relative immobility of the affected bone (fragment). With the re-establishment of a vascular network within 3 weeks at the latest, soft necrotic drbris is removed from the intertrabecular spaces of the marrow and is gradually replaced by granulation tissue. Osteoclastic action is seen, but is largely outweighed by osteoblastic activity along the surfaces of the old trabecular scaffold. The formation of osteoid and newly apposed woven bone onto the surface of the dead trabeculae is seen clearly histologically and demonstrated by supravital staining, for instance with tetracyclin labelling. Increased thickness of the trabeculae may now be demonstrated radiographically, particularly on trispiral tomograms. It is important to note that true X-ray density is not the stigma of ongoing avascular necrosis, but the sign of healing of a past ischaemic attack. With re-established vitality, a proximal scaphoid fragment affected by class 1 avascular necrosis takes up supravital staining, shows normal or diminished punctuate bleeding and is expected to consolidate almost as readily as an unaffected fragment. It will take many months before Haversian

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remodelling will have recolonized the dead central lamellae of the composite trabeculae and before a more normal-looking trabecular structure will have been rebuilt. On very long follow-up of scaphoid fractures such as that presented by D/Jppe et al (1994) with an observation time of greater than 30 years, no evidence of the sequelae of this particular osteonecrosis was seen. A case was seen of atypical De Quervain's fracturedislocation in which the proximal pole of the scaphoid was completely extruded from the carpus and found lying free in the soft tissues of the anterior forearm. Following immediate anatomical reduction, this fragment served as the perfect model of class 1 avascular necrosis: it underwent revascularization, became dense, progressed to bony union, and later developed viable integration. Class 2 avascular necrosis

If spontaneous revascularization is not established soon enough, if for undefined reasons osteoclastic activity prevails over osteoplasia, or if motion and excessive mechanical loading continue, the structural integrity of the original trabecular framework will eventually fail. This leads to compression fractures ("infraction") of dead bone material and to bone collapse, which is typically located a few mm inside the subchondral region of the load bearing area. Increased bone density is then also seen, but this time diminished radio-lucency is based on the superposition of crushed dead trabeculae. Although a scaphoid or a scaphoid fragment with a class 2 avascular lesion may become revascularized and may at least partly appear "vital", structural reconstitution is no longer possible and the chances of healing . of the fracture or the non-union are greatly diminished. By this time, the vascularity of the tissues surrounding the necrosis is usually well developed, promoting focal bone resorption and fibrosis--the typical picture of class 2 avascular pathology. In the class 2A variant, the lesion remains essentially unchanged. The affected central bone area may become fragmented, the interstices between the trabecular remnants are filled by scar tissue and cystic lesions are sometimes noted. Osteogenic activity is scant or absent. In the class 2B variant, the necrotic nidus is decompressed and comes to rest. "Healing" may occur by slow replacement of the necrotic territories by viable bone; the original shape and structure of the affected bone are never reconstituted, however, and an associated non-union does not usually consolidate.

Types of avascular necrosis One must distinguish between avascular changes of the proximal fragment of scaphoid fractures, which usually belong to class 1 lesions. In scaphoid non-union, larger fragments may have normal vascularity or may yield class 1 alterations; class 2 avascular necrosis rarely

s C A P H O I D VASCULARITY

occurs but may occasionally be encountered following failed attempts at scaphoid reconstruction. Small proximal fragments in non-union are more frequently affected by class 2 lesions. Rarely, avascular necrosis may be induced by bone grafting procedures as observed by Cooney et al (1980b) in Matti-Russe reconstruction and AO screw fixation. If the patient's history rules out relevant trauma, of which one is never quite sure, avascular necrosis is labelled as being "idiopathic". Typically, the entire scaphoid is involved in a class 2 lesion which is usually diagnosed at an advanced stage (Allen, 1983; Alnot et al, 1990; Bray and McCarroll, 1984; De Smet et al, 1992; Dossing and Boe 1994; Ekerot and Eiken, 1981; Ferlic and Morin, 1989; Gupta et al, 1992). Less frequently, idiopathic avascutar necrosis may involve predominantly the proximal inner zones of the proximal pole of the scaphoid, the cortex facing the capitate and the adjacent subchondral area, the remainder of the scaphoid staying more or less intact. This condition is sometimes called "osteochondritis dissecans", but is in fact identical to a localized class 2 lesion (Cook and Engber, 1993; Guelpa et al, 1980). Rarely, idiopathic avascular necrosis may involve the entire proximal pole of the scaphoid, as recently described by Herbert and Lanzetta (1993). Their eight cases demonstrated a transverse non-union separating a class 2 necrosis proximally from a normal looking fragment distally. THE ASSESSMENT OF AVASCULAR NECROSIS Viability/vascutarity of the scaphoid may be assessed by plain radiographs, trispiral tomography, radio-nuclide imaging, single photon emission computed tomography, magnetic resonance imaging, gross inspection for punctate bleeding, other surgical assessment, laser Doppler flowmetry and histology with or without supravital fluorescent labelling. Ideally, one should not rely on a single one of these methods, but combine them according to the class, the type, and the stage of the process as necessary. When using imaging techniques, repeated examinations provide a better definition of the process and its evolution.

Radiographic density Noticing "increased" bone density in standard radiographs of scaphoid fractures or non-union and interpreting this as representing the existence of avascular necrosis is common practice. Unfortunately, the specificity and accuracy of the observation of diminished radio-lucency with respect to factual avascular changes are not great. In the investigation of Perlik and Guilford (1991), hyperdensity in standard X-rays falsely predicted avascular necrosis in five out of ten cases, missed existing avascular changes in one out of ten cases and was accurate in only four out of ten cases. "Increased bone density" is normal in a scaphoid or a scaphoid fragment

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that has rotated out of normal position, and is difficult to interpret in the presence of osteoporosis/osteopenia of the surrounding bones. Density assessment in tomograms is clearly more accurate (one out of seven false positive, and none out of seven false negative predictions in Perlik's series). Trispiral tomograms are of great value for distinguishing class 1 frpm class 2 lesions.

Radio-nuclide imaging Radio-nuclide imaging yields a sensitivity of 77.5% to 81% (Beltran et al, 1988; Markisz et al, 1987) and a specificity of 18.2% to 75% (Reinus et al, 1986; Beltran et al, 1988). False positive results occur in fractures and in the presence of synovitis. Increased blood flow in the early phase 1 (radio-nuclide angiogram), increased blood pooling in hyperaemic tissues surrounding an avascular bone segment in the early phase 2 and a focal increase in delayed bone images (phase 3) are considered typical for bone infarction (Maurer, 1991). A cold centre of the necrosis p e r se is not visualized. Radio-nuclide examination helps to differentiate the active process of revascularization from the inactive residual changes seen in the late stage of avascular necrosis (Holder, 1992).

Single photon emission computed tomography SPECT has been used for the assessment of avascular necrosis in the femoral head (Collier et al, 1985; Kim et al, 1993), proving superior to bone scans, particularly in its 3-head variant. In the scaphoid, the value of this diagnostic method is not established.

Magnetic resonance imaging Magnetic resonance imaging (MRI) is highly sensitive (89%) in detecting bone ischaemia (Beltran et al, 1988; Markisz et al, 1987). It is not very specific in the early stages of avascular necrosis, since idiopathic transitory oedema, oedema from bone contusion, benign relative ischaemia, and pre-existing conditions such as granulating bone marrow reactions may produce similar images (Kulkarni et al, 1987; Robinson et al, 1989; Wenda et al, 1991). Some authors believe that a loss of signal on T1 weighted images is a non-specific finding (Dalinka et al, 1991) and therefore co-evaluation of T2 intensity has become standard practice. Gadolinium enhancement is increasingly used for detecting acute avascular changes (Cova et al, 1991; Tsukamoto et al, 1992). The negative predicting value of a comprehensive MR evaluation is excellent, and the observation of normal T1 signal intensity a few weeks after an injury is considered to rule out bone necrosis. The temporal changes in T1 and T2 signal characteristics with respect to the various classes, types and stages of avascular necrosis of the scaphoid have not been systematically assessed. Specificity was 100% in Reinus' and Beltran's material,

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when T1 and T2 sequences were used (Reinus et al, 1986; Beltran et al, 1988). MRI proved accurate in a prospective evaluation of bone viability in scaphoid fractures by Desser et al (1990). A normal T1 marrow signal was shown to correlate with the presence of osteoid and osteocytes of biopsy specimens on light microscopy and a surface layer of fluorescence reflecting tetracycline uptake in viable bone. Decreased marrow signal corresponded to non-viable trabeculae with scant osteoid, without osteocytes and with no tetracycline labelling. Trumble (1990) found a 100% consistency between decreased T1 signals and histological evidence of avascular necrosis in six out of 12 delayed or non-unions of the scaphoid. In Perlik and Guilford's study (1991), T1 signal characteristics of the proximal fragments of ten scaphoid non-unions were 100% accurate in predicting existence or non-existence of avascular changes in histological examination of curetted material (three positive, three negative). In avascular necrosis of the femoral head, the accuracy was also excellent (Neuhold et al, 1993).

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Laser Doppler flowmetry Laser Doppler flowmetry was extensively used in the evaluation of avascular necrosis of the femoral head and was found to be a reliable method for assessing residual bone blood flow (Swiontkowski et al, 1987). To our knowledge, laser Doppler flowmetry has not been used in the scaphoid.

Biopsy and histological examination Avascular changes are often present in an irregular, patchy configuration, and are thus variable within a single specimen. Therefore, random biopsy may not accurately predict the status of avascular necrosis of the entire specimen (Urban et al, 1993). As avascular changes seem to predominate in the central areas of the proximal third of the proximal fragment, this area is probably the most representative. Labelling with supravital fluorescent dyes greatly adds to the understanding of the momentary osteoblastic/osteoclastic activity and was found to be fully in agreement with plain histological assessment in five out of six specimens of Trumble's series (1990).

Assessment of bone structure during surgery By definition, class 1 lesions present with bone or a bone fragment of normal shape (except for possible loss of bone substance at a non-union site), normal cartilagenous surface and normal physical properties of cancellous bone substance. In longer-standing lesions, the freshened cancellous surface may appear harder than normal. In class 2A lesions, collapse of bone substance is noted, the affected zone is softened and under loupe observation of the freshened surface, fibrosis and/or cyst formation may be seen; the cartilagenous surface may appear normal or show the typical floating plaque phenomenon with cartilage degeneration and/or fracture along the border of the destabilized osteochondral fragment.

Observation of punctate bleeding Observation of the quantity and quality of punctate bleeding during d6bridement of scaphoid non-union sites was evaluated as a parameter of avascular changes by Green in 1985. The correlation to histology was not convincing: "Isolated areas of avascular bone were seen in many proximal poles, in which punctate bleeding points were grossly visible; conversely, bones with relatively poor gross vascularity frequently had areas of viable osteocytes". Nevertheless, Green demonstrated a drastic drop in the healing capacity of non-m~ion in which the proximal scaphoid pole was devoid of bleeding points (see below). In Trumble's material (1990), five out of six scaphoids with established avascular necrosis demonstrated only sparce punctate bleeding points.

AVASCULAR NECROSIS IN FRESH SCAPHOID FRACTURES

Incidence The incidence of avascular changes with respect to the various types of scaphoid fracture is not yet clear. Transient ischaemia is believed to be frequent and essentially without detriment to healing capacity. Frank necrosis probably occurs in less than 14% of cases (Mulder, 1968; Russe, 1960).

Healing capacity Union rates of adequately treated acute and fresh scaphold fractures are between 94% and 98.5% (Russe, 1960; Cooney et al, 1980a; Morgan and Waiters, 1984; Barton, 1992). Failure to unite is related to many parameters (location of fracture, type of fracture, instability, treatment modalities, avascular necrosis, etc) and hence the relative impact of avascular changes is difficult to establish. A proximal scaphoid fragment with increased radiographic density as a sign of class 1 avascular necrosis may take slightly longer to achieve union, but seems to proceed uninhibitedly towards union (Morgan and Waiters, 1984). AVASCULAR NECROSIS IN SCAPHOID NONUNION Each cohort of cases of scaphoid non-union is a heterogenous group. With respect to avascular necrosis it contains cases of missed fracture diagnosis in which the

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lack of immobilization hindered timely revascularization of a primarily necrotized proximal pole fragment, cases of inadequate primary reduction in which poor contact of the fragments impeded endosteal revascularization and repair of an ischaemic proximal pole, cases of unfavourable biology, represented by the small proximal fragment group and in retrospect, proximal poles proceeding to class 2 lesions, cases of improper primary treatment such as inadequate immobilization, devascularization from extensive or gross dissection, heat necrosis from repeated K-wire drilling and damage from inappropriate implants, and cases due to high-energy lesions. Incidence Judged by increased radiographic density, the incidence of avascular necrosis ranges from 16% in Cooney's series of 110 cases of scaphoid non-union (Cooney et al, 1980b) to 39% in the 73 cases of non-union collected in Pennsylvania (Pennsylvania Orthopaedic Society, 1962) or 40% in Mulder's (1968) series of 100 cases of scaphoid non-union. From observation of bleeding points, Green (1985) determined the incidence of impaired vascularity to the proximal pole at 42%, with a range of 50% to 70% depending on the location of non-union. In his material of 45 cases of non-union, 14 showed sparse bleeding points and five had none. The correlation of poor "vascularity" with the location of non-union is shown in Table 1. Perlik and Guilford (1991) found histological evidence of avascular changes in seven out of ten cases of non-union. In a comprehensive viability assessment, Trumble (1990) had an incidence of six of 12 of avascular changes in the proximal fragments of three delayed and nine randomly selected cases of non-union. Classes of avascular necrosis in scaphoid non-union A clear distinction between class 1 and class 2 avascular necrosis is not made in the literature. From our own observations, the majority fall into class 1; class 2a lesions were almost exclusively seen in longstanding instances of proximal non-union and class 2b variants were extremely rare."

Table 1--Correlation of poor vascolarity with the location of scaphoid non-union

Proximal to waist At the waist Distal to the waist

Number

Avaseular

Diminished "vascularity'"

Good "vaseularity'"

10 32 3

10% 12% 0%

60% 38% 67%

30% 50% 33%

Healing of scaphoid non-union in the face of avascular changes In the context of avascular necrosis, true healing must imply not only bony union of the pseudarthrotic area, but also healing of the bone necrosis. In a class 1 lesion this means creeping substitution of the original trabecular substance, and in class 2 lesions, the transition towards el'ass 2b as a minimal requirement. Conventional bone grafting of scaphoid non-union in the face of avascular necrosis The osteogenic potential of conventional autologous bone grafts is well established experimentally and clinically. It is not clearly understood, however, why widespread initial necrosis of cells within the grafts can be compatible with osteogenic activity starting as early as 6 days after transplantation. Once viability has been restored, the quality of osteogenic repair is influenced by many factors, such as the site of implantation, the status of the recipient bed (type of trauma, vascularity), the size of the defect/transplant, the condition of the red bone marrow, the inflammatory response, physical forces and other factors (Stringa, 1957; Enneking et al, 1975; Goldberg and Stevenson, 1987). Autologous cancellous bone grafts are revascularized at an amazing speed of 2mm to 4 mm/day under ideal circumstances. After revitalization of the intertrabecular marrow, osteogenesis is immediately induced (Stringa, 1957) and leads to deposition of osteoid and new bone on the framework of old necrotic trabeculae (Enneking et al 1975; Shaffer et al, 1985). By 3 months, the majority of the original spongiosa has been replaced by creeping substitution (Goldberg and Stevenson, 1987). Under an enveloping callus, the cortical/trabecular substance of a cortical transplant is also gradually replaced by Haversian remodelling. As resorption necessarily precedes bone apposition, substantial structural weakening occurs. By 8 weeks, a third of the transplant is replaced by new bone, a sixth consists of holes and cavities and half of the substance is composed of remnants of the necrotic matrix. Bony consolidation following conventional grafting of scaphoid pseud-arthrosis with avascular changes In the absence of strict criteria for the diagnosis and classification of "avascular necrosis", conclusions regarding the healing of scaphoid non-union in the face of avascular changes have been inaccurate. The healing capacity of a scaphoid non-union is governed by a multitude of interrelated factors: the location of the non-union; its displacement; its mobility or fibrous coherence; the presence of cystic changes; the presence of sclerosis of the surfaces of the fragments; the amount of bone loss; the class, type and stage of "avascular necrosis", the association of carpal instability, the

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sequelae of lesser or greater arch injuries; the duration of non-union; the method of treatment; the adequacy of reduction; and other elements (Fisk, 1970; Cooney et al, 1980b; Leslie and Dickson, 1981; Nakamura et al, 1993). In statistical terms, the relative importance of the aforementioned parameters, and specifically of avascular necrosis, could only be determined by a comprehensive multivariate analysis, which has not yet been done. There is no unanimous opinion in the literature about the union rates of "avascular" proximal scaphoid fragments following conventional bone grafting of pseudarthrosis. In a series of anterior wedge grafts in 21 cases of scaphoid non-union, Cooney et al (1988) achieved a union rate of 81%. Non-unions were related to incorrect Herbert screw placement, failure of compression at the site of reconstruction, resorption of bone graft, or persistent avascular necrosis. Carrozella et al (1989) dealt with ten cases of scaphoid non-union which had failed to heal after a first grafting procedure. Six united after a second grafting and one united after a third. The rate of union was not affected by fracture location, instability, or the presence of "avascular changes" in the proximal pole. Admitting an incidence of 16% to 70% of avascular changes in scaphoid non-union (see above), and accepting an over-all union rate for scaphoid pseudarthrosis of 80% to 97% (Mulder 1968; Barton 1992), necrosis does not seem to rule out healing. With avascular necrosis defined on the basis of increased radiographic density, the literature contains several reports. Hull et al (1976) achieved union in only 36% of graftings for small ununited dense proximal pole fragments. Nakamnra et al (1993) found a reduced healing tendency when grafting non-union with a "sclerotic" proximal fragment. A more positive outcome was reported by Cooney et al (1980b) who achieved union in 11 out of 13 cases of non-union with increased density of the proximal fragment. 40 of Mulder's 100 scaphoid non-unions showed increased density of the proximal fragment and 97 consolidated following a Matti-Russe type procedure (Mulder, 1968). Three out of four cases of proximal pole non-union with avascular necrosis that had failed to unite after a first bone grafting procedure united following regrafting by Carrozella et al (1989), leading the authors to believe that the "presence of avascular necrosis did not appear to adversely affect ultimate union". The amount and quality of punctate bleeding correlated with the bone healing potential in Green's investigation (1985). Following Matti-Russe grafting in 26 patients, 92% of scaphoids with good vascularity united, and the success rate dropped to 71% in scaphoids with diminished blood supply, falling to 0% in scaphoids whose proximal pole was devoid of bleeding points. Using MRI and histology (Trumble, 1990), only three out of six patients with established avascular changes of the proximal fragment went on to healing, while six with normal MRI and histology united.

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It is safe to assume that the majority of the above information concerns class 1 lesions; the union rates in the presence of aggressive avascular changes (Herbert and Lanzetta, 1993; the class 2 lesions of our proposed classification) are presumably minimal, but their percentage is not known.

REVASCULARIZATION AS AN ADJUNCT IN TREATING SCAPHOID NON2UNION WITH BONE NECROSIS

Rationale and indications Based on MRI and direct surgical assessment, the class, type and stage of avascular necrosis must be identified before a treatment plan is developed. With a relatively large, radiographically dense proximal fragment in which abundant bleeding points are detected, conventional inlay or wedge bone grafting (selection according to the characteristics of a particular non-union) is probably sufficient and should initiate healing in about 90% of the cases. To enhance revascularization and bony union, it seems important to provide rigid fixation of the two scaphoid fragments and the bone graft, either by special methods of inlay grafting, K-wire splinting, applications of K-wires plus an external fixator, or screw fixation. Vascularized bone grafting appears logical for small proximal pole fragments, class 1 lesions of larger fragments yielding scant or absent bleeding points, nonunion persisting after conventional grafting, and perhaps long-standing non-union. Whether or not minor class 2 avascular necrosis can yield adequate surface properties, normal shape, good load-bearing capacity and bony union is as yet questionable. At the extreme, advanced class 2 avascular proximal pole fragments that are deformed and contain just bone d~bris and scar tissue are not reasonably amenable to reconstructive surgical means. Research into the healing capacity of vascularized bone grafts in these instances would be reasonable, or the use of more predictable therapeutic alternatives such as four corner arthrodesis or proximal row carpectomy.

Vascular pedicle implantation Vascular pedicle implantation into necrotic carpal bone has been used in the treatment of Kienb~ck's disease (Hori et al, 1979; Foucher and Saffar, 1982). Active proliferation of new blood vessels and formation of new bone occurred in all instances where the vascular bundle was used, but this method was unable to induce significant revascularization in the peripheral portion of an avascular bone segment (Gartsman et al, 1985). There are no reports in the literature regarding its use in scaphoid pole fragments.

SCAPHOID VASCULARITY

Vascularized bone grafts It has been shown that the viability and strength of a vascularized bone graft are well preserved and that the union at the contact site to normal bone occurs faster (Dell et al, 1985; Shaffer et al, 1985). Vascularized bone grafting places viable bone in close contact with the necrotic fragment and thus eliminates the stacking-up of non-viable tissue as occurs with conventional grafting methods. Vascularized bone grafts are believed to deploy osteogenic potential even in a poorly vascularized bed (Chacha, 1984), but the revascularizing effect of a vascularized bone graft on an adjacent necrotic bone fragment is not inevitable (Uchida and Sugioka, 1990). A number of questions regarding vascularized bone grafts have not been clarified. Is it a circulatory hazard to shape a vascularized bone to the size of a window created in the scaphoid? Is it detrimental to add plain cancellous bone grafts around the vascularized graft component? May adequacy of circulation be monitored in a vascularized bone graft? Do vascularized bone grafts truly encourage neocolonization by osteoblasts/ osteocytes in an otherwise biologically dormant situation? If the entire necrotic d6bris were removed from a class 2 lesion, do vascularized bone grafts become integrated into the remaining viable outer shell? Do they facilitate and expedite bone union and do they assist in the maintenance of the shape and the physical strength of the proximal fragment? We just do not know. Available vascularized bone grafts Roy-Camille (1965) was probably the first to use vascularized bone grafting in the scaphoid. He employed part of the palmar tubercle of the scaphoid on the pedicle of the lateral head of the abductor pollicis brevis for grafting scaphoid non-union. In 1971, Beck identified a vascular axis from the ulnar artery and its venae commitantes to the pisiform and described the transfer of the decorticated pisiform to the lunate. Saffar later found the pisiform's second supply system from a branch of the ulnar artery that follows the dorsal sensory branch of the ulnar nerve; the pedicle is sufficiently long to carry the pisiform to the palmar aspect of the scaphoid. Braun (1983) described a bone graft from the distal radius on the pedicle of part of the pronator quadratus muscle and presented one case of Preiser's disease and five cases of scaphoid delayed union, all of which healed. Kawai and Yamamoto (1988) presented eight cases of pronator quadratus radial bone grafts to the scaphoid (one in the proximal third, one with presumed avascular necrosis), all of which were successful. Kuhlmann et al (1987) proposed a vascularized bone graft from the palmar aspect of the distal radial epiphysis, based on the radial branch of the palmar carpal arterial arch, which spans the epiphysis of the radius close to the radio-carpal joint. Three cases of scaphoid

733

non-union with unknown presence of avascular necrosis were healed by this method. In 1987, Pechlaner et al advocated the use of a microvascular bone graft from the iliac crest, nourished by the horizontal branches of the deep circumflex iliac artery. Scaphoid grafting was accomplished from a palmar approach, similar to a Matti-Russe procedure, with vascular anastomoses of the pedicle to the radial artery system. 25 patients were reported, but the results were not given. Guimberteau and Panconi (1990) harvested a vascularized bone graft from the distal ulna, a few centimetres proximal to the head, based on the distal postero-medial branch of the ulnar artery (or the branch travelling with the dorsal branch of the ulnar nerve when the former was absent); pedicted transport of the bone graft to the palmar aspect of the scaphoid required division and vein grafting of the ulnar artery. Eight cases of scaphoid non-union, most of which had had two failed treatment attempts and two of which demonstrated avascular changes, proceeded to union. Today's most logical choice is a bone graft from the dorso-radial aspect of the distal radius on the pedicle of a recurrent branch of the adjacent radial vascular axis, as published by Zaidemberg et al (1991), which is ideally suited to dorsal grafting of proximal avascular nonunion. Saint-Cast et al (1994) studied the consistency of the feeding artery and defined four types of anatomical arrangement. The first comprehensive clinical series was presented by Hastings in 1993 and achieved union in 15 out of 17 cases, in which the incidence of avascular necrosis is not stated. In conclusion, despite a wealth of existing knowledge, we have not yet come very far in the understanding of avascular necrosis of the scaphoid, and further research is needed. This must reside on a clearer definition and classification of avascular "necrosis" by a more systematic application of MRI investigative techniques, better peroperative assessment of blood flow, supravital staining, and histology. The potential therapeutic role of vascularized bone grafting has not been fully determined and should be clarified. References ALLEN, P. R. (1983). Idiopathic avascular necrosis of the scaphoid. Journal of Bone and Joint Surgery, 65B: 333-335. ALNOT, J. Y., FRAJMAN, J. M. and BOCQUET, L. (1990). Les ost~on6croses aseptiques primitives totales du scaphoide: Apropos de trois cas. Annales de Chirurgie de la Main et du Membre Sup6rieur, 9:221 225. BARTON, N. J. (1992). Twenty questions about scaphoid fractures. Journal of Hand Surgery, 17B: 289-310. BECK, E. (1971). Die Verpflanzung des Os pisiforme am Gef~.ssstiel zur Behandlung der Lunatummalazie. Handchirurgie, 3: 64-67. BELTRAN, J., HERMAN, L. J., BURK, J. M. et al. (1988). Femoral head avascular necrosis: MR imaging with clinical-pathologic and radionuclide correlation. Radiology, 166: 215-220. BERGGREN, A., WEILAND, A. J. and DORFMAN, H. (1982). The effect of prolonged ischemia time on osteocyte and osteoblast survival in composite bone grafts revascularized by microvascular anastomoses. Plastic and Reconstructive Surgery, 69:290 298. BRAUN, R. N. (1983). Pronator pedicle bone grafting in the forearm and proximal carpal row. Journal of Hand Surgery, 8: 612-613.

734 BRAY, T. J. and McCARROLL, H. R. (1984). Preiser's disease: A case report. Journal of Hand Surgery, 9A: 730-732. BRODY, A. S., STRONG, M., BABIKIAN, G. et al. (1991). Avascular necrosis: Early MR imaging and histologic findings in a canine model. American Journal of Roentgenology, 157: 341-345. CARROZZELLA, J. C., STERN, P. J. and MURDOCK, P, A. (1989). The fate of failed bone graft surgery for scaphoid nonunions. Journal of Hand Surgery, 14A: 800-806. CHACHA, P. B. (1984). Vascularized pedicular bone grafts. International Orthopaedics, 8:117-138. COLLIER, B. D., CARRERA, G. F., JOHNSON, R. P. et al. (1985). Detection of femoral head avascular necrosis in adults by SPECT. Journal of Nuclear Medicine, 26: 979-987. COOK, D. A. and ENGBER, W. D. (1993). Osteocbondritis dissecans of the scaphoid: Preiser's disease? Orthopaedics, 16:705 707. COONEY, W. P., DOBYNS, J. H. and LINSCHEID, R. L. (1980a). Fractures of the scaphoid: A rational approach to management. Clinical Orthopaedics and Related Research 149: 9~98. COONEY, W. P., DOBYNS, J. H. and LINSCHEID, R. L. (1980b). Nonunion of the scaphoid: Analysis of the results fi'om bone grafting. Journal of Hand Surgery, 5:343 354. COONEY, W. P.0 LINSCHEID, R. L., DOBYNS, J. H. and WOOD, M. B. (1988). Seaphoid nonunion: Role of anterior interpositional bone grafts. Journal of Hand Surgery, 13A: 635-650. COVA, M., KANG, Y. S., TSUKAMOTO, H. ct al. (1991). Bone marrow perfusion evaluated with gadolinium-enhanced dynamic fast MR imaging in a dog model. Radiology, 179: 535-539. CROCK, H. V., CHARI, P. R. and CROCK, M. C. La Vascularisation des os du Poignet et de la Main chez l'Homme. In: Tubiana, R. (Ed): TraitO de Chirurgie de la Main, Paris, Masson, 1980 Tome premier, 361-371. DALINKA, M. K., MEYER, S., KRICUN, M. E. and VANEL, D. (1991). Magnetic resonance imaging of the wrist. Hand Clinics, 7: 87-98. DE SMET, L., AERTS, P. and FABRY, G. (1992). Avascular necrosis of the scaphoid: Report of three cases treated with a proximal row carpectomy. Journal of Hand Surgery, 17A: 907 909. DELL, P. C., BURCHARDT, H. and GLOWCZEWSKIE, F. P. (1985). A roantgenographic, biomechanical, and histological evaluation of vascularized and non-vascularized segmental fibular canine antografts. Journal of Bone and Joint Surgery, 67A: 105-112. DESSER, T. S., McCARTHY, S. and TRUMBLE, T. (1990). Scapboid fractures and Kienbock's disease of the lunate: MR imaging with histopathologic correlation. Magnetic Resonance Imaging, 8:357 361. DOSSING, K. and BOE, S. (1994). Idiopathic avascular necrosis of the scaphold. Scandinavian Journal of Plastic, Reconstructive and Hand Surgery, 28: 155-156. DIS/PpE, H., JOHNELL, O., LUNDBORG, G., KARLSSON, M. and REDLUND-JOHNELL I. (1994). Long-term results of fracture of the scaphoid. Journal of Bone and Joint Surgery, 76A: 249-252. EKEROT, L. and EIKEN, O. (1981). Idiopathic avascular necrosis of the scaphoid, Scandinavian Journal of Plastic, Reconstructive and Hand Surgery, 15: 69-72. ENNEKING, W. F., BURCHARDT, H., PUHL, J. J. and PIOTROWSKI, G. (1975). Physical and biological aspects of repair in dog cortical-bone transplants. Journal of Bone and Joint Surgery, 57A: 237-251. FERLIC, D. C. and MORIN, P. (1989). Idiopathic avascular necrosis of the scaphoid: Preiser's disease? Journal of Hand Surgery, 14A: 13-16. FISK, G. R. (1970). Carpal instability and the fractured scaphoid. Annals of the Royal College of Surgeons of England, 46: 63-76. FOUCHER, G. and SAFFAR, P. (1982). Revascalarization of the necrosed lunate, stages I and II, with a dorsal intermetacarpal arteriovenous pedicle. Annales de Chirnrgie de la Main, I: 259. GARTSMAN, G. M., WEILAND, A. J., MOORE, J. R. and RANDOLPH, M. A. (1985). Blood vessel implantation into ischemic bone. Journal of Reconstructive Microsurgery, 1:215 222. GELBERMAN, R. H. and MENON, J. (1980). The vascularity of the scaphoid bone. Journal of Hand Surgery, 5: 508-513. GOLDBERG, V. M. and STEVENSON, S. (1987). Natural history of autografts and allografts. Clinical Orthopaedics and Related Research, 225: 7-16. GREEN, D. P. (1985). The effect of avascular necrosis on Russe bone grafting for scaphoid nonunion. Journal of Hand Surgery, 10A: 597-605. GRETTVE, S. (1955). Arterial anatomy of the carpal bones. Acta Anatatomica, 25: 331-345. GUELPA, G., CHAMAY, A. and LAGIER, R. (1980). Bilateral osteochondritis dissecans of the carpal scaphoid. International Orthopaedics, 4: 25-30. GUIMBERTEAU, J. C. and PANCONI, B. (1990). Recalcitrant non-union of the scaphoid treated with a vascniarized bone graft based on the ulnar artery. Journal of Bone and Joint Surgery, 72A: 88-97. GUPTA, A., BIQCHLER, U. and MAZZUCCHELLI, L. (1992). Idiopathic avascular necrosis of the scaphoid. A case report. Annales de Chirurgie de la Main et du Membre Suprrieur, 11: 406-410.

THE JOURNAL OF HAND SURGERY VOL. 20B No. 6 DECEMBER 1995 HANDLEY, R. C. and POOLEY, J. (1991). The venous anatomy of the scaphoid. Journal of Anatomy, 178:1 t5-118. HASTINGS, H. (1993). Vascularized bone grafting for scaphoid non-union. Unpublished, presented at American Academy of Orthopaedic Surgeons, New Orleans, HERBERT, T. (1990). Avascular Necrosis of the Scaphoid. In: The Fractured Scaphoid, St Louis, Quality Medical Publishing, 1990: 121-138. HERBERT, T. J. and LANZETTA, M. (1993). Idiopathic avascular necrosis of the scaphoid. Journal of Hand Surgery, 19B: 174-182. HOLDER, L. E. (1992). Radionuclide Bone Imaging in Surgical Problems of the Hand. In: Gilula, L. A. (Ed): The Traumatized Hand and Wrist, Philadelphia, Saunders, 1992: 19-43. HORI, Y., TAMAI, S., OKUDA, H. et al. (1979). Blood vessel transplantation to bone. Journal of Hand Surgery, 4: 23-33. HULL, W. J., HOUSE, J. H., GUSTILLO, R. B., KLEVEN, L. and THOMPSON, W. (1976). The surgical approach and source of bone graft for symptomatic nonunion of the scaphoid. Clinical Orthopaedics and Related Research, I15: 241-247. IMAEDA, T., NAKAMURA, R., MIURA, T. and MAKINO, N. (1992). Magnetic resonance imaging in scaphoid fractures. Journal of Hand Surgery, 17B: 20-27. KAUER, J. Personal communication, 1993. KAWAI, H. and YAMAMOTO, K. (1988). Pronator quadrams pedicled bone graft for old scaphoid fractures. Journal of Bone and Joint Surgery, 70B: 829-831. K/M, K. Y., LEE, S. H., MOON, D. H. and NAH, H. Y. (1993). The diagnostic value of triple head single photon emission computed tomography (3H-SPECT) in avascular necrosis of the femoral head. International Orthopaedics, 17: 132-138. KUHLMANN, J. N. and GUERIN-SURVILLE, H. (1981). Vascularisation extrins~que et intrins~que du scaphoide et de l'os lunaire. Bulletin de l'Association d'Anatomie (Nancy), 65:433 446. KUHLMANN, J. N., MIMOUN, M., BOABIGHI, A. and BAUX, S. (1987). Vascularized bone graft pedicled on the volar carpal artery for non-union of the scaphoid. Journal of Hand Surgery, 12B: 203-210. KULKARNI, M. V., TARR, R. R., K/M, E. E., McARDLE, C. B. and PARTAIN, C. L. (1987). Potential pitfalls of magnetic resonance imaging in the diagnosis of avascular necrosis. Journal of Nuclear Medicine, 28: 1052-1054. LESLIE, L J. and DICKSON, R. A. (1981). The fractured carpal scaphoid: Natural history and factors influencing outcome. Joumal of Bone and Joint Surgery, 63B: 225-230. MALIZOS, K. N., QUARLES, L. D., SEABER, A. V., R1ZK, W. S. and URBANIAK, J. R. (1993). An experimental canine model of osteonecrosis: Characterization of the repair process. Journal of Orthopaedic Research 11: 350-357. MARKISZ, J. A., KNOWLES, R. J. R., ALTCHEK, D. W. et al. (1987). Segmental patterns of avascular necrosis of the femoral heads: Early detection with MR imaging. Radiology, 162: 717-720. MAURER, A. H. (1991). Nuclear medicine in evaluation of the hand and wrist. Hand Clinics, 7:183 200. MESTDAGH, H. (1982). Vascularisation artrrielle du semi-lunaire. Annales de Chirnrgie de la Main, 1: 246548. MINNE, J., DEPREUX, R,, MESTDAGH, H. and LECLUSE P. (1973). Les prdicules artrriels du massif carpien. Lille Mrdical, l 8:1174-1185. MORGAN, D. A. F. and WALTERS, J. W. (1984). A prospective study of 100 consecutive carpal scaphoid fractures. Australian and New Zealand Journal of Surgery, 54: 233-241. MULDER, J. D. (1968). The results of 100 cases of pseudarthrosis in the scaphold bone treated by the Matti-Russe operation. Journal of Bone and Joint Surgery, 50B: 110-115. NAKAMURA, R., HORII, E., WATANABE, K., TSUNODA, K. and MIURA, T. (1993). Scaphoid non-union: Factors affecting the functional outcome of open reduction and wedge grafting with Herbert screw fixation. Journal of Hand Surgery, 18B: 219-224. NEUHOLD, VON A., HOFMANN, S., ENGEL, A. et al. (1993). Bone marrow oedema: An early form of femoral head necrosis. Fortschritte auf dem Gebiet der Rrntgenstrahlen und der Neuen Bildgebenden Verfahren, 159: 120-125. OBERLIN, C., SALON, A., PIGEAU, Let al. (1992). Three-dimensional reconstruction of the carpus and its vasculature: An anatomic study. Journal of Hand Surgery, 17A: 767 772. OBLETZ, B. E. and HALBSTEIN, B. M. (1938). Non-union of fractures of the carpal navicular. Journal of Bone and Joint Sttrgery, 20: 424-428. PECHLANER, S., HUSSL, H. and K~)NZEL, K. H. (1987). Alternative Operationsmethode bei Kahnbeinpseudarthrosen: Prospektive Studie. Handchirurgie, Plastisehe Chirurgie, Mikrochirnrgie, 19: 302-305. Pennsylvania Orthopaedic Society. (1962). Evaluation of treatment for nonunion of the carpal navicular. Journal of Bone and Joint Surgery, 44A: 169-174.

SCAPHOID VASCULARITY PERLIK, P. C. and GUILFORD, W. B. (1991). Magnetic resonance imaging to assess vascularity of scaphoid nonunions. Journal of Hand Surgery, 16A: 479 484. REINUS, W. R., CONWAY, W. F., TOTTY, W. G. et al. (1986). Carpal avascular necrosis: MR imaging. Radiology, 160:689 693. ROBINSON, H. J., HARTLEBEN, P. D., LUND, G. and SCHREIMAN, J. (1989). Evaluation of magnetic resonance imaging in the diagnosis of osteonecrosis of the femoral head: Accuracy compared with radiographs, core biopsy, and intraosseous pressure measurements. Journal of Bone and Joint Surgery, 71A: 650-663. ROY-CAMILLE, R. (1965). Fractures et pseudarthroses du scaphoide moyen. Utilisation d'un gr6ffon p6dicul6. Actualit6s de Chirurgie Orthop6dique Raymond Poincar6, 4:197 214. RUSSE, O. (1960). Fracture of the carpal navicular: Diagnosis, non-operative treatment and operative treatment. Journal of Bone and Joint Surgery, 42A: 759 768. SAFFAR, P. (1985). Traitement de la maladie de Kienb6ck par le transfert du pisiforme p6dicul6 sur les vaissaux et le cubital anterieur. Revue de Chirurgie Orthop6dique, 71:66 71. SAINT-CAST, J., DAGREGORIO, G., RAIMBEAU, G. and FOUQUE, P. A. (1994). Le greffon vascularis6 par l'art6re du processus stylolde radial. Presented at and contained in the book of abstracts, 30me Congr6s de la Soci6t6 Francaise de Chirurgie de la Main, Paris. SHAFFER, J. W., FIELD, G. A., GOLDBERG, V. M. and DAVY, D. T. (1985). Fate of vascularized and nonvascularized autografts. Clinical Orthopedics and Related Research, 197:32 43. STEWART, M. J. (1954). Fractures of the carpal navicular (scaphoid): A report of 436 cases. Journal of Bone and Joint Surgery, 36A: 998-1005. STRINGA, G. (1957). Studies of the vascularisation of bone grafts. Journal of Bone and Joint Surgery, 39B: 395-420. SWIONTKOWSKI, M. F., GANZ, R., SCHLEGEL, U. and PERREN, S. M. (1987). Laser Doppler flowmetry for clinical evaluation of femoral head osteonecrosis: Preliminary experience. Clinical Orthopaedics and Related Research, 218: 181-185. TALEISNIK, J. and KELLY, P. J. (1966). The extraosseous and intraosseous

735 blood supply of the scaphoid bone. Journal of Bone and Joint Surgery, 48A: 1125-1137. TRAVAGLINI, F. (1959). Arterial circulation of the carpal bones. Bulletin of the Hospital of Joint Disease, 20: 19-26. TRUMBLE, T. E. (t990). Avascular necrosis after scaphoid fracture: A correlation of magnetic resonance imaging and histology. Journal of Hand Surgery, 15A: 557-564. TSUKAMOTO, H., KANG, Y. S., JONES, L. C. et al. (1992). Evaluation of marrow perfusion in the femoral head by dynamic magnetic resonance imaging: Effect of venous occlusion in a dog model. Investigative Radiology, 27:275 781. UCHIDA, Y_and SUGIOKA, Y. (1990). Effects of vascularized bone graft on surrounding necrotic bone: An experimental study. Journal of Reconstructive Microsurgery, 6: 101-107. URBAN, M. A., GREEN, D. P. and AUFDEMORTE, T. B. (1993). The patchy configuration of scaphoid avascular necrosis. Journal of Hand Surgery, 18A: 669-674. WANG, J. X. (1993). A biomechanical study in the repairing process of avascular necrosis of the femoral head in dogs. Chung Hua Wai Ko Tsa Chih, 31: 374-377. WENDA, K., RITTER, G., PEDROSA, P. et al. (1991). Interpretation of MR tomography findings in tranma surgery. UnfaUchirurg, 94: 302-307. YU, W. Y., SIU, C. M., SHIM, S. S., HAWTHORNE, H. M. and DUNBAR, J. S. (1975). Mechanical properties and mineral content of avascular and revascularizing cortical bone. Journal of Bone and Joint Surgery, 57A: 692-695. ZAIDEMBERG, C., SIEBERT, J. W. and ANGRIGIANI, C. (t991). A new vascularized bone graft for scaphoid nonunion. Journal of Hand Surgery, 16A: 474-478.

Professor Dr med. Ueli B0.chler, Division of Hand Surgery, University of Bern, Inselspital, CH-3010 Bern, Switzerland. © 1995 The British Society for Surgery of the Hand