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Osteonecrosis of the humeral head
13 Osteonecrosis of the humeral head S I M O N P. F R O S T I C K W. ANGUS WALLACE
The terms avascular necrosis of bone, aseptic necrosis of bone and osteonecrosis are all used interchangeably to define the same entity. To be pedantic, avascular necrosis of bone implies an aetiology based purely upon a loss of vascular supply to the region of bone. The loss of the blood supply to a region of bone may be the final common pathway in all causes of the disease but does not take into account any systemic disease that may be associated with it. Aseptic necrosis merely separates a form of bone necrosis which does not have an infective cause. Osteonecrosis literally means bone necrosis (death) and ignores any aetiological factor or factors. None of these terms seems to be entirely satisfactory. Some authors have further confused the situation by describing avascular osteonecrosis and idiopathic osteonecrosis. The former term refers to osteonecrosis occurring when there is a definable loss of vascularity to a region of bone as a complication of a fracture (alternatively traumatic osteonecrosis or traumatic avascular necrosis), e.g. the femoral head, humeral head, proximal pole of the scaphoid, carpal lunate, etc. Idiopathic osteonecrosis encompasses all the other causes of bone death. The pathophysiology in these forms is, at present, unknown (idiopathic). but the term idiopathic osteonecrosis is meaningless, as most of the cases will be secondary to a systemic disease or the treatment thereof. In this chapter, the term traumatic osteonecrosis will be used when referring to post-traumatic bone death. This is a loss of the blood supply to the bone without evidence of systemic disease. All the other causes of bone necrosis will be referred to as non-traumatic osteonecrosis. The authors will attempt to define aetiology, clinical presentation and approaches to treatment in osteonecrosis of the humeral head. The pathophysiology of the non-traumatic forms of osteonecrosis still remains controversial. The clinical presentation is similar in both traumatic and non-traumatic forms of the disease. Similarly, the approach to treatment is broadly the same in all cases and is dependent upon the severity of symptoms and signs. The clinical presentation will be discussed by reference to three recent cases from our Department. Baillibre's ClinicalRheumatology--Vol. 3, No. 3, December 1989
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VASCULAR SUPPLY OF THE HUMERAL HEAD
Laing (1956) injected the vessels of the humerus with either barium and formalin or a mercury turpentine emulsion. Radiographs of the excised bones demonstrated the blood supply to each region. In the 26 bones reported, nearly all had a large anterolateral vessel arising from the ascending branch of the anterior circumflex humeral artery. In most, this formed an 'arcuate artery' running posteromedially on entering the bone. There was a variable contribution to the humeral head from the posterior circumflex humeral and some minor vessels were found to enter in the region of attachment of the rotator cuff. Laing comments that the main blood
VESSELS FROM ROTATOR CUFF
ARCUATEL --
POSTERIOR t HUMERAL r~ CIRCUMFLEX TARTER, ( ANTERIOR HUMERAL CIRCUMFLEX ARTERY
ARTERY Figure 1. The blood supply of the humeral head. After Hawkins and Kiefer (1987) and Laing (1956).
supply enters above the most common sites of fracture of the surgical neck of the humerus so that an adequate blood supply is maintained. Figure 1 shows the blood supply to the humeral neck. Figure 2 shows Neer's classification of humeral neck fractures. It is evident from Figure 2 that the blood supply may indeed be disrupted in the more complex fractures, thus predisposing the humeral head to traumatic osteonecrosis. Knight and Mayne (1957) described a series of patients with various fracture and fracture-dislocation patterns of the humeral head. In all the groups reviewed, from what would appear to be 2-part fractures to the most complex fractures, the authors found a frequent occurrence of avascular necrosis. The blood supply of the humeral head is, therefore, similar to that of the femoral head. The latter bone is the most frequently involved in osteonecrosis.
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OSTEONECROSIS OF THE HUMERAL HEAD I MINIMAL DISPLACEMENT
DISPLACED 2 PART
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FRACTURES 5
PART
4 PART
:AL
NECK
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SURGICAL NECK
'Iv GREATER TUBEROSITY
~ "-..,.
LESSER TUBEROSITY
ARTICULAR SURFACE FRACTURE DISLOCATION ANT RIOR
POSteRIOR
Figure 2. Classification of h u m e r a l neck fractures. From Neer (1970), with permission.
CLASSIFICATION OF CAUSES OF OSTEONECROSIS OF THE H U M E R A L HEAD
Jones (1978) suggested that osteonecrosis from all causes has increased significantly this century. This may be true of the non-traumatic forms, particularly those related to steroid treatment and to deep-sea diving. It may not be true for traumatic osteonecrosis as systematic documentation of such sequelae of fractures has only been properly undertaken in the last 30 years or so. The classification of osteonecrosis of the humeral head is outlined in Table 1. The non-traumatic causes include treatment with steroids (especially renal
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transplantation, asthma, collagen vascular diseases, etc.), treatment with other chemotherapeutic agents and radiotherapy (e.g. in leukaemia and Hodgkin's disease), Cushing's syndrome, Gaucher's disease, sickle cell disease and its associated variants, and caisson disease. A number of rarer causes of osteonecrosis have also been reported, including one case in pregnancy (McGuigan and Fleming, 1983) and one in a scythe maker (Kovarik et al, 1987). In this latter case the authors argued that the patient should be compensated for an industrially related disease! Pancreatitis has also been implicated, as has excess alcohol intake. Kahn et al (1986) report a case of bilateral femoral and humeral head osteonecrosis in a young male without evidence of any predisposing factors. The authors suggest that this is a true idiopathic osteonecrosis. A single case of osteonecrosis has also been reported following an intrathoracic dislocation of the humeral head (Ulrich et al, 1986). Table 1. Classification of osteonecrosis. A. B.
Traumatic Non-traumatic Steroid related ?SLE (not related to the steroid therapy) O t h e r chemotherapeutic agents and radiotherapy Sickle cell a n a e m i a and genetic variants Caisson disease Alcohol
?Hyperuricaemia ?Pancreatitis Other rarities
The majority of cases of osteonecrosis will be seen in association with trauma and steroid treatment. In special circumstances other causes will be significant, such as sickle cell anaemia in areas where sickle cell disease is endemic and caisson disease where there is a large diving workforce, e.g. in and around the ports servicing the North Sea oil rigs.
INCIDENCE Osteonecrosis of all bones is mostly associated either with trauma or treatment with systemic steroids (Jones, 1978). Traumatic osteonecrosis
The true incidence of this condition is very difficult to estimate. Knight and Mayne (1957) estimated a 62.5% incidence of osteonecrosis in 40 patients. The classification of the types of humeral fractures cannot be compared with later series based on the Neer classification. Neer (1970) reported 15 cases of osteonecrosis in 117 3- and 4-part fractures. Svend-Hansen (1974) found an 8.2% incidence in 49 severe fractures. Stableforth (1984) found four patients out of 49 to have definite radiographic changes of avascular osteonecrosis.
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Moriber and Patterson (1967) thought complications such as osteonecrosis and osteoarthritis after humeral neck fracture were rare but did occur. However, Lee and Hansen (1981) found no cases of osteonecrosis in a series of 19 4-part fractures and fracture-dislocations. The authors argued that the humeral head was rapidly revascularized and the head reconstructed by creeping substitution. Lee and Hansen describe radiographic changes in at least five patients who would be placed in stage 2 of the Ficat classification of osteonecrosis (Ficat, 1985). In the small number of patients that these authors report, none went on to develop collapse of the humeral head or osteoarthritis during the period of follow-up (6-49 months). Non-traumatic osteonecrosis
The true incidence in this category of patients is also very difficult to estimate. Jacobs (1978) examined 269 patients with femoral head necrosis. In this series, 39% were alcohol related and, in this group of 104 patients, 24 were found to have sites other than the femoral head involved, including the humeral head. In Jacobs' study, 75 patients had osteonecrosis associated with steroid therapy but no comment was made as to how many patients had sites other than the femoral head involved. The other major group comprised those associated with hyperuricaemia (58 patients) but many of these had other diseases known to be associated with osteonecrosis. Once again, no mention is made of the incidence of humeral head involvement. Three out of eight patients suffering from sickle cell disease had multifocal osteonecrosis. Overall, Jacobs found that 89% of the patients with nontraumatic osteonecrosis had a disorder of lipid metabolism. Pietrogrande and Mastromarino (1957) reported the first case of osteonecrosis associated with steroid therapy. Since that first case many others have been reported; there have been a large number of disease processes but the only common factor has been the use of steroids in the disease therapy. The published series suggest that the femoral head is the most common site of osteonecrosis in steroid therapy, followed by the humeral head. Moreover, Solomon (1973) showed that most of the 32 patients treated with corticosteroids developed the osteonecrosis between 6 and 24 months after the start of therapy. Cruess (1978) also found that patients did not suffer from osteonecrosis until 6 months after the start of the steroids but found that no new cases occurred after 18 months. Until recently, only long-term steroid therapy has been thought to be associated with osteonecrosis, but there is now evidence that short-term high-dose steroid treatment may cause multifocal osteonecrosis (Anderton and Helm, 1982; McCluskey and Gutteridge, 1982; Fast et al, 1984; Taylor, 1984). The main group of patients affected by steroid-induced osteonecrosis are those receiving immunosuppressive therapy for organ transplants. Cruess et al (1968) published the first study on osteonecrosis after renal transplantation. In 27 patients who had survived 6 months or more to the end of 1967, ten were found to have evidence of osteonecrosis. Only one patient had osteonecrosis of the humeral heads alone; two further patients had osteonecrosis in other bones as well. Cruess (1976,1978)has subsequently reported
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his further experience of this problem in renal transplantation and also a number of other conditions (systemic lupus erythematosus, glomerulonephritis, asthma hypopituitarism and Guillain-Barr6 syndrome). In the latter paper, 19 cases of osteonecrosis of the humeral head were found in 97 patients, with the total number of bones affected being 138. The humeral head was the second most common site of osteonecrosis. In only two cases was the humeral head alone affected. Harrington et al (1971) found one case of humeral head osteonecrosis in 18 patients reviewed but this patient also had osteonecrosis in both elbows, both hips, both carpal capitates, the right knee and the left talus. Potter et al (1978) found osteonecrosis in children after renal transplantation but the humeral heads were not involved in the patients they reviewed. However, in a series of 111 transplants in children from 1967 to 1977, 11 patients developed osteonecrosis, including one who 'required prosthetic replacement of the proximal humerus' (Uittenbogaart et al, 1978). Ibels et al (1978) examined 194 transplant patients, 40 of whom had evidence of osteonecrosis: only three patients had osteonecrosis of the humeral heads in their series and this was always associated with disease in the other bones. Seventy-seven patients being treated with steroids for a variety of collagen vascular, dermatological and haematological complaints, gout, pulmonary disease and other miscellaneous diseases had 142 bones affected by osteonecrosis (Fisher and Bickel, 1971); 11 humeral heads were involved. Kyd (1979) reported an isolated case of humeral head osteonecrosis; the humeral head may have been involved in other patients who had several bones affected. Osteonecrosis of the humeral heads is the second most common site in steroid-treated patients but there is usually evidence of osteonecrosis elsewhere and the disease is certainly much less common than osteonecrosis found in the femoral heads. The dosage of steroids may be the most important factor. Harrington et al (1971) found that the incidence of osteonecrosis was significantlyhigher in one group of patients whose total steroid dose was three times that of a second group. Rossleigh et al (1986) suggest that patients given steroids in combination with other chemotherapeutic agents and local radiotherapy in the treatment of Hodgkin's lymphoma are particularly at risk of developing osteonecrosis. Linus Pauling et al (1949) discovered that the haemoglobin in patients with sickle cell anaemia was abnormal. A number of variants have subsequently been described, the SC variant being one of the most important in the context of osteonecrosis. It is the SC variant, which although it is associated with fewer crises, is particularly associated with osteonecrosis of the epiphysis (Golding et al, 1959; Chung and Ralston, 1969). As with the other causes of osteonecrosis, the humeral head is less frequently affected than the femoral head. The humeral head is affected more often in adults than in children (Chung et al, 1978). Chung and Ralston (1969) found that 6 of 13 patients with femoral head osteonecrosis also had involvement of the humeral head. Unlike the causes of humeral head osteonecrosis mentioned so far, caisson disease would appear to affect the humeral head more frequently than other bones (Gregg and Walder, 1986). Amongst compressed-air workers, a rough estimate of the prevalence of osteonecrosis is 24% and in
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professional divers 6.2% (Gregg and Walder, 1986). Figures from the Medical Research Council Decompression Sickness Panel Registry, July 1972 (Davidson, 1976), found 334 men with 820 lesions (total population examined 1694), with 26% of the lesions affecting the juxta-articular region of the humeral head. In 1976, the same registry (McCallum et al, 1976) found 31% of 67 lesions in 35 divers with definite lesions (total population 1830). Ohta and Matsunga (1974) examined 301 traditional Japanese divers: 50.5% (152 individuals) had 231 lesions, of which 15% were juxta-articular humeral head. Multiple exposure to inadequate decompression may be important (Chryssanthou, 1978). In Jacobs' research (1978), pancreatitis was implicated in a small number of patients with multifocal osteonecrosis but the author did not specify the sites. Gaucher's disease is also associated with osteonecrosis; Amstutz and Carey (1966) found three definite cases of osteonecrosis of the humeral head in 20 patients reviewed. P A T H O L O G Y AND P A T H O P H Y S I O L O G Y
The pathological lesions encountered in the humeral head are consistent with bone death but are often associated with areas of revascularization. Ficat (1985) comments that, whatever the aetiology of the osteonecrosis, the end result is identical, namely 'blockage of the osseous microcirculation with intramedullary stasis'. Spencer et al (1986) described the changes found early on in a patient with osteonecrosis of the femoral head. They suggest a five stage evolution of changes: 1. 2. 3. 4. 5. 6. 7.
Normal: majority of osteocytes histologically viable. Increased numbers of empty osteocytic lacunae distributed in random fashion. Confluent areas of empty osteocytic lacunae. Medullary necrosis. Medullary fibrosis and revascularization with fibrocartilage and new bone formation. Linear fracture and separation of the necrotic focus. Collapse of the (femoral) head.
Similar pathological observations can be made in patients with osteonecrosis of the humeral head. Traumatic osteonecrosis is the direct result of a disruption of the blood supply to the affected bone. As described earlier, this is most frequently associated with displaced/complex fractures. Case 2 (see below) would also suggest that, occasionally, osteonecrosis of the humeral head can occur in undisplaced fractures. The pathophysiology of osteonecrosis secondary to sickle cell disease is similar to traumatic osteonecrosis, except that the cause of the interruption to the blood supply is due to sickling erythrocytes blocking small vessels rather than a physical interruption to the vessels, as in fractures. Osteonecrosis in sickle cell anaemia usually affects adults and can vary from an
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osteochondritis dissecans type lesion to stage 4 changes (osteoarthritis: Ficat classification, see below) (Sennara and Gorry, 1978). Based upon the observation that 89% of 269 patients with osteonecrosis of all bones had diseases or had received treatment that affected the metabolism of fats, Jacobs (1978) postulated that fat emboli were important in the aetiology of many cases of osteonecrosis (steroid therapy, alcohol, etc.). Fat emboli have not been demonstrated in human bones affected by osteonecrosis (Glimcher and Kenzora, 1979). Experimentally, fat emboli have been found in the subchondral capillaries of femoral heads in rabbits (Jones and Sakovich, 1966). Fisher (1978) reports an experiment in which bone necrosis occurred in animals treated with steroids and with the animals suffering from marked alteration of lipid metabolism. Fat emboli in bone were seen. Extrapolation of these data to humans has not been demonstrated. Solomon (1973) suggested an alternative pathophysiology in patients who were suffering from 'drug-induced arthropathy'. Many of the 'drugs' in these patients caused osteoporosis and this was thought to lead to microfractures and subsequently to collapse of the bone. Arlot et al (1983) performed extensive bone histology of iliac crest bone in patients with osteonecrosis and also found osteoporosis, reinforcing the view that microfracturing was significant. Embolization has also been implicated in the aetiology of caisson disease (nitrogen bubbles) and Gaucher's disease-associated osteonecrosis. None of the theories in the literature have explained the pathophysiological processes that are observed. For example, the majority of steroid-related osteonecrosis patients are on long-term therapy; there does not seem to be a single vascular phenomenon associated with the onset of the disease in these patients. Moreover, in order to develop osteonecrosis secondary to caisson disease, multiple exposure to inappropriate decompression regimens are required. Embolization may or may not be the physical phenomenon leading to changes in vascularity of the humeral head. However, other physical and/or biochemical changes must occur that give rise to the clinical entity of osteonecrosis. Therefore, further research is required in humans and in experimental models in order to define the changes that lead to the clinical and radiographic manifestations. CLINICAL MANIFESTATIONS The diagnosis should be suspected from the past history, particularly in relation to steroid treatment, etc. Pain, a decreasing range of movement and progressive radiographic changes are typical clinical features. The following three cases will illustrate the clinical presentation and subsequent clinical course typical of osteonecrosis of the humeral head. Case 1 (Figure 3)
A 31-year-old negro male suffering from sickle cell anaemia presented with
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OSTEONECROSIS OF THE HUMERAL HEAD
(a)
(b)
Figure 3. Case 1. Sickle cell anaemia causing osteonecrosis of the humeral head. (a) AP and lateral views of the left proximal humerus showing the 'crescent sign'. (b) Postoperative radiograph showing the Neer II prosthesis in situ, (c) Full elevation of the shoulder replacement.
(c)
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severe bilateral shoulder pain (left > right) and restriction of movement. The diagnosis of osteonecrosis was confirmed on plain radiographs. A core decompression was performed in February 1988 and the histology showed bone infarction and focal marrow fibrosis. Because of the severity of the pain and limitation of movement in the left shoulder, a Neer II hemiarthroplasty was performed in November 1988. The patient made an excellent postoperative recovery and has regained a near normal range of movement (fle~ion 160 ~ abduction 150 ~ external rotation 60 ~ and internal rotation to r12). Case 2 (Figure 4)
In July 1986, a 64-year-old caucasian female sustained an undisplaced humeral neck fracture of the left shoulder. The initial treatment took place in France, where she was placed into a shoulder spica cast. The spica was removed at the end of July 1986. Eighteen months after the original injury the patient continued to have significant pain, especially on movement. The range of movement was decreased. Plain radiographs at this stage showed osteonecrosis of the humeral head despite the fact that this was an undisplaced fracture (in three parts). In December 1988 a left Neer II hemiarthroplasty was performed. Good recovery of function occurred postoperatively. Case 3 (Figure 5)
In October 1987 this 58-year-old caucasian female fell downstairs and sustained multiple injuries, including a fracture-dislocation of the right shoulder. The following day an open reduction and internal fixation using 'K' wires was performed. The neck fracture was found to be impacted and the wires were used to hold fragments of the greater tuberosity. On 23 October 1987 the greater tuberosity was found to be a free fragment on radiographs. On 24 November 1987 a reconstruction of the right rotator cuff and reattachment of the greater tuberosity was performed. Between December 1987 and March 1988 an improvement in the function of the shoulder was noted. However, in March 1988 subluxation of the humeral head was found, with collapse of the humeral head indicating osteonecrosis. By July 1988 poor shoulder function was noted and the patient listed for a hemiarthroplasty. In November 1988 a Neer II hemiarthroplasty was performed. To date the patient has had poor function of the shoulder which is in part associated with postoperative scarring and contracture from previous surgery. STAGING OF SEVERITY OF OSTEONECROSIS
Ficat (1985) has classified the stages of progression of osteonecrosis affecting the femoral head. This classification is based upon clinical signs and plain radiograph changes. As the causes, pathophysiology and clinical present-
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(a)
(c)
(b) Figure 4. Case 2. Minimally displaced fracture of the humeral head. (a) Immediate post-injury radiograph showing a minimally displaced 3-part fracture of the left humeral neck. (b) Established osteonecrosis of the humeral head. (c) Almost full elevation of the shoulder is achieved after hemiarthroplasty.
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(~)
(h)
(e)
(a)
Figure 5. Case 3. Severely displaced fracture dislocation of the right humeral head. (a) The immediate post-injury radiograph shows a 4-part fracture dislocation of the right humeral head. (b) Subluxation of the humeral head is less 6 weeks after initial surgery. (e) Shows well established osteonecrosis of the humeral head. (fl) The Neer II hemiarthroplasty in situ.
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ation are similar in both femoral head and humeral head (Cruess, 1978), it seems reasonable to apply the same staging to disease of the humeral head. The Ficat staging is as follows:
Stage O. Asymptomatic osteonecrosis, suspected because of disease elsewhere.
Stage 1. Early symptoms such as pain, some limitation of movement. Possibly some early plain radiographic changes.
Stage 2. Some increase in symptoms. Radiographic changes more pronounced.
Stage 3. Characterized by a sequestrum on plain radiographs. Clinically increasing pain and marked impairment of function.
Stage 4. Osteoarthritis. RADIOGRAPHIC INVESTIGATIONS
Changes on plain radiographs occur late in the clinical course of the disease. The MRC Decompression Sickness Panel has classified the radiological changes found in caisson disease (from Heard and Schnieder, 1978). The classification is given in Table 2. Table 2. Classification of radiological changes found in caisson disease. A.
B.
Juxta-articular lesions 1. Dense areas with intact articular cortex 2. Spherical segmental opacity 3. Linear opacity 4. Structural failure a. Translucent subcortical band b. Collapse of articular cortex c. Sequestration of cortex 5. Osteoarthritis Medullary lesions of the head, neck and shaft 1. Dense areas 2. Irregular calcified areas 3. Translucent areas and cyst formation
D'Ambrosia et al (1978) used bone scintigraphy to examine the changes occurring in osteonecrosis in animals. These authors found that a 'cold spot' ( d e c r e a s e d 99myc activity) was apparent shortly after the decrease in the vascularity but this was subsequently replaced by increased activity (a 'hot spot') as revascularization and repair proceeded. Bone scintigraphy identified one patient with steroid-induced osteonecrosis before plain radiographic changes were visible and in this case the findings were compared with the early changes found on histology (Spencer et al, 1986). Gregg and Walder (1980) developed an experimental model for caisson disease that suggested that revascularization could be detected as early as 3 weeks after the avascular phenomenon, as a hot spot on bone scintigraphy. Gregg and Walder (1981) were also able to demonstrate abnormalities on
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scintigraphy in patients with normal plain radiographs but who had ceased exposure to a high-pressure environment 10 years previously. Bone scintigraphy may show relatively early lesions in patients with sickle cell disease (Epps, 1983). The investigation of choice is now magnetic resonance imaging. It has been demonstrated to be useful in diagnosing early osteonecrosis (before radiographic changes are seen) in the femoral head (Bassett et al, 1987a, 1987b) and in the talus (Sierra et al, 1986). Zlatkin et al (1988, 1989) and Aquilone et al (1988) have obtained high resolution magnetic resonance images of shoulders. Sachs (1988) suggested that osteonecrosis of the humeral head could be diagnosed with magnetic resonance imaging. TREATMENT
The initial treatment should be symptomatic, with pain relief and physiotherapy to maintain an adequate range of movement (Young and Wallace, 1985). Terrett and Molyneux (1988) suggested that physical therapy would give a favourable outcome in the long term in one patient with traumatic osteonecrosis. The treatment in established osteonecrosis with humeral head collapse and osteoarthritis is frequently by hemiarthroplasty and very occasionally with a total shoulder replacement (Neer, 1974; Neer et al, 1982; Stableforth, 1984). The results can be excellent even in young patients (e.g. Case 1 above). However, it is also evident that the functional outcome of shoulder hemiarthroplasty may be poor if previous surgery has been performed on the joint (see Case 3). Open reduction and internal fixation of humeral fractures has also been used (Hawkins and Angelo, 1987; Hawkins and Kiefer, 1987). Lee and Hansen (1981) had a zero incidence of late stage osteonecrosis using this method. Fresh osteochondral allografts with muscle pedicle have been used in the treatment of osteonecrosis of the femoral head (Meyers, 1978). Rindell (1987) has recently suggested a similar approach can be used in osteonecrosis of the humeral head. The follow-up of Rindell's single patient was only 18 months; long-term follow-up is obviously required to determine the ultimate outcome for allograft surgery. REFERENCES Amstutz HC & Carey EJ (1966) Skeletal manifestations and treatment of Gaucher's disease. Journal of Bone and Joint Surgery 48A: 670-701. Anderton JM & Helm R (1982) Multiple joint osteonecrosis following short-term steroid therapy. Journal of Bone and Joint Surgery 64A: 139-141. Aquilone LF, Burk L, Blob RD, Brown DL, Rifkin MD & Mitchell DG (1988) Technical optimization of surface coil MRI of the rotator cuff. Abstract, Society of Magnetic Resonance in Medicine 7th Annual Meeting, 41. Arlot ME, Bonjean M, Chavassieux PM & Meunier PJ (1983) Bone histology in adults with aseptic necrosis. Journal of Bone and Joint Surgery 65A: 1319-1327.
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Bassett LW, Gold RH, Reicher MA, Bennett LR & Tooke SM (1987a) Magnetic resonance imaging in the early diagnosis of ischemic necrosis of the femoral head. Clinical Orthopaedics 214: 237-248. Bassett LW, Mirra JM, Crachiolo A & Gold RH (1987b) Ischemic necrosis of the femoral head: correlation of MRI and histologic sections. Clinical Orthopaedics 223: 181-187. Chrysannthou CP (1978) Dysbaric osteonecrosis. Clinical Orthopaedics 130: 94-106. Chung SMK & Ralston EL (1969) Necrosis of the femoral head associated with sickle cell anemia and its genetic variants. Journal of Bone and Joint Surgery 51A: 33-58. Chung SMK, Alavi A & Russell MO (1978) Management of osteonecrosis in sickle-cell anemia and its genetic variants. Clinical Orthopaedics 130: 158-174. Cruess RL (1976) Steroid-induced avascular necrosis of the head of the humerus. Journal of Bone and Joint Surgery 58B: 313-317. Cruess RL (1978) Experience with steroid-induced avascular necrosis of the shoulder and etiologic considerations regarding osteonecrosis of the hip. Clinical Orthopaedics 130: 86-93. Cruess RL, Blennerhassett J, MacDonald FR, Maclean LD & Dossetor J (1968) Aseptic necrosis following renal transplantation. Journal of Bone and Joint Surgery 50A: 15771590. D'A.mbrosia RD, Shoji H, Riggins RS, Staddalink RC & Dennardo GL (1978) Scimigraphy in the diagnosis of osteonecrosis. Clinical Orthopaedics 130: 139-143. Davidson JK (1976) Aseptic Necrosis of Bone. Amsterdam, Excerpta Medica. Epps CH (1983) Painful haematologic conditions affecting the shoulder. ClinicalOrthopaedics 173: 38-43. Fast A., Alon M, Weiss S & Zer-A.viv FR (1984) A.vascular necrosis of bone following short-term dexamethasone therapy for brain edema. Case report. Journal of Neurosurgery 61: 983-985. Ficat RP (1985) Idiopathic bone necrosis of the femoral head. Journal of Bone and Joint Surgery 67B: 3-9. Fisher DT (1978) The role of fat embolism in the etiology of corticosteroid-induced avascular necrosis. Clinical Orthopaedics 130: 51-67. Fisher DT & Bickel WH (1971) Corticosteroid-induced avascular necrosis. Journal of Bone and Joint Surgery 53A: 859-873. Glimcher MJ & Kenzora JE (1979) The biology of osteonecrosis of the human femoral head and its clinical implications. Clinical Orthopaedics 140: 273-312. Golding JSK, Maclver JE & Went LN (1959) The bone changes in sickle cell anaemia and its genetic variants. Journal of Bone and Joint Surgery 41B: 711-718. Gregg PJ & Walder DN (1980) Scintigraphy versus radiography in the early diagnosis of experimental bone necrosis. Journal of Bone and Joint Surgery 62B: 214-221. Gregg PJ & Walder DN (1981) A. study of old lesions of caisson disease by radiography and bone scintigraphy. Journal of Bone and Joint Surgery 63B: 132-137. Gregg PJ & Walder DN (1986) Caisson disease of bone. Clinical Orthopaedics 210: 43-54. Harrington KD, Murray WR, Kountz SL & Belzer FO (1971) A_vascular necrosis of bone after transplantation. Journal of Bone and Joint Surgery 53A: 203-215. Hawkins RJ & Angelo RL (1987) Displaced proximal humeral fractures: selecting treatment, avoiding pitfalls. Orthopedic Clinics of North America 18: 421-431. Hawkins RJ & Kiefer GN (1987) Internal fixation techniques for proximal humeral fractures. Clinical Orthopaedics 223: 77-85. Heard JL & Schneider CS (1978) Radiographic findings in commercial divers. Clinical Orthopaedics 130: 129-138. Ibels LS, A.lfrey AC, Huffer WE & Well R (1978) Aseptic necrosis of bone following renal transplantation: experience in 194 transplant recipients and review of the literature. Medicine 57: 25-45. Jacobs B (1978) Epidemiology of traumatic and non-traumatic osteonecrosis. Clinical Orthopaedics 130: 51-67. Jones JP (1978) Editorial comment: Osteonecrosis. Clinical Orthopaedics 130: 2-4. Jones JP & Sakovich L (1966) Fat embolism in bone: A roentgenographic and histological investigation with use of intra-arterial lipiodol in rabbits. JournalofBone andJointSurgery 48A: 149-164. Kahn T, Reiser M, Heimhuber B & Jager R (1986) Die Kombination von beid seitiger
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idiopathischer Hfift- und Humeruskopfnekrose-erster Bericht fiber ein Krankenheitsbild. ROntgenbli~tter 39: 130-132. Knight RA & Mayne JA (1957) Comminuted fractures and fracture-dislocations involving the articular surface of the humeral head. Journal of Bone and Joint Surgery 39A: 1343-1355. Kovarik J, Niebauer B, Fruhwald F & Seidl G (1987) Probleme der aseptischen Humeruskopfnekrose--irrwege eines Senienschmiedes in der Begutactungsmedizin. Wiener Klinische Wochenschrifi 99: 462-466. Kyd RJ (1979) Bone and joint complications of maintenance haemodialysis and renal transplantation. New Zealand Journal of Medicine January 10: 4-6. Laing PG (1956) The arterial supply of the adult humerus. Journal of Bone and Joint Surgery 38A: 1105-1116. Lee CK & Hansen HR (1981) Post-traumatic avascular necrosis of the humeral head in displaced proximal humeral fractures. Journal of Trauma 21: 788-791. McCallum RI, Walder DW & Thickett VB (1976) Bone necrosis in commercial divers. Undersea Biomedical Research 3: A41. McCluskey J & Gutteridge DH (1982) Avascular necrosis of bone after high doses of dexamethasone during neurosurgery. British Journal of Medicine 284(6312): 333-334. McGuigan L & Fleming A (1983) Osteonecrosis of the humerus related to pregnancy. Annals of the Rheumatic Diseases 42: 59%599. Meyers MH (1978) The treatment of osteonecrosis of the hip with fresh osteochondral allografts and the muscle pedicle graft technique. Clinical Orthopaedics 130: 202-209. Moriber LA & Patterson RL (1967) Fractures of the proximal end of the humerus. Journal of Bone and Joint Surgery 49A: 1018. Neer CS (1970a) Displaced proximal humeral fractures Part I: Classification and evaluation. Journal of Bone and Joint Surgery 52A: 1077-1089. Neer CS (1970b) Displaced proximal humeral fractures Part II: Treatment of three-part and four-part displacement. Journal of Bone and Joint Surgery 52A: 1090-1103. Neer CS (1974) Replacement arthroplasty for glenohumeral osteoarthritis. Journal of Bone and Joint Surgery 56A: 1-13. Neer CS, Watson KC & Stanton JF (1982) Recent experience in total shoulder replacement. Journal of Bone and Joint Surgery 64A: 319-337. Ohta Y & Matsunga H (1974) Bone lesions in divers. Journal of Bone and Joint Surgery 56B: 3-16. Pauling L, Itano HA, Singer SJ & Wells IC (1949) Sickle cell anemia, a molecular disease. Science 110: 543-548. Pietrogrande V & Mastromarino R (1957) Osteopatia da prolungato trattamento cortisono. Ortopedica Traumatologia 25: 791. Potter DE, Genant HK & Salvatierra O (1978) Avascular necrosis of bone after renal transplantation. American Journal of Diseases of Children 132: 1125-1129. RindeU K (1987) Muscle pedicled bone graft in revascularization of aseptic necrosis of the humeral head. Annales Chirurgiae et Gynaecologiae 76: 283-285. Rossleigh MA, Smith J, Straus DJ & Engel H (1986) Osteonecrosis in patients with malignant lymphoma. A review of 31 cases. Cancer 58: 1112-1116. Sachs L (1988) MR of the shoulder. Abstract, Society of Magnetic Resonance in Medicine 7th Annual Meeting, 40. Sennara H & Gorry F (1978) Orthopaedic aspects of sickle cell anaemia and allied haemoglobinopathies. Clinical Orthopaedics 130: 154-157. Sierra A, Potchen EJ, Moore J & Smith GH (1986) High field magnetic resonance imaging of aseptic necrosis of the talus. Journal of Bone and Joint Surgery 68A: 927-928. Solomon L (1973) Drug-induced arthropathy and necrosis of the femoral head. Journal of Bone and Joint Surgery 55B: 246-261. Spencer JD, Humphreys S, Tighe JR & Cummings RK (1986) Early avascular necrosis of the femoral head. Journal of Bone and Joint Surgery 68B: 414-417. Stableforth PG (1984) Four part fractures of the neck of the humerus. Journal of Bone and Joint Surgery 66B: 104-108. Svend-I-Iansen H (1974) Displaced proximal humeral fractures: a review of 49 cases. Acta Orthopaedica Scandinavica 45: 359-364. Taylor LJ (1984) Multifocal avascular necrosis after short-term high dose steroid therapy. Journal of Bone and Joint Surgery 66B: 431-433.
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Terrett A G & Molyneux TP (1988) Hass' disease. Journal of Manipulation and Physical Therapy 11: 43-47. Uittenbogaart EH, Isaacson AS, Stanley P e t al (1978) Aseptic necrosis after renal transplantation in children. American Journal of Diseases in Children 132: 765-767. Ulrich C, Helbing G, Worsdorfer O & Lampl LH (1986) Intrathorakale Humeruskopfluxation. Langenbecks Archiv fur Chirurgie 367: 197-202. Young TB & Wallace WA (1985) Conservative treatment of fractures and fracture dislocations of the upper end of the humerus. Journal of Bone and Joint Surgery 67B: 373-377. Zlatkin MB, Iannotti JR, Esterhai J & Dalinka MK (1988) Magnetic resonance imaging of rotator cuff disease. Abstract, Society of Magnetic Resonance in Medicine 7th Annual Meeting, 140. Zlatkin MB, Dalinka MK & Kressel HY (1989) Magnetic resonance imaging of the shoulder. Magnetic Resonance Quarterly 5: 3-22.
The terms avascular necrosis of bone, aseptic necrosis of bone and osteonecrosis are all used interchangeably to define the same entity. To be pedantic, avascular necrosis of bone implies an aetiology based purely upon a loss of vascular supply to the region of bone. The loss of the blood supply to a region of bone may be the final common pathway in all causes of the disease but does not take into account any systemic disease that may be associated with it. Aseptic necrosis merely separates a form of bone necrosis which does not have an infective cause. Osteonecrosis literally means bone necrosis (death) and ignores any aetiological factor or factors. None of these terms seems to be entirely satisfactory. Some authors have further confused the situation by describing avascular osteonecrosis and idiopathic osteonecrosis. The former term refers to osteonecrosis occurring when there is a definable loss of vascularity to a region of bone as a complication of a fracture (alternatively traumatic osteonecrosis or traumatic avascular necrosis), e.g. the femoral head, humeral head, proximal pole of the scaphoid, carpal lunate, etc. Idiopathic osteonecrosis encompasses all the other causes of bone death. The pathophysiology in these forms is, at present, unknown (idiopathic). but the term idiopathic osteonecrosis is meaningless, as most of the cases will be secondary to a systemic disease or the treatment thereof. In this chapter, the term traumatic osteonecrosis will be used when referring to post-traumatic bone death. This is a loss of the blood supply to the bone without evidence of systemic disease. All the other causes of bone necrosis will be referred to as non-traumatic osteonecrosis. The authors will attempt to define aetiology, clinical presentation and approaches to treatment in osteonecrosis of the humeral head. The pathophysiology of the non-traumatic forms of osteonecrosis still remains controversial. The clinical presentation is similar in both traumatic and non-traumatic forms of the disease. Similarly, the approach to treatment is broadly the same in all cases and is dependent upon the severity of symptoms and signs. The clinical presentation will be discussed by reference to three recent cases from our Department. Baillibre's ClinicalRheumatology--Vol. 3, No. 3, December 1989
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VASCULAR SUPPLY OF THE HUMERAL HEAD
Laing (1956) injected the vessels of the humerus with either barium and formalin or a mercury turpentine emulsion. Radiographs of the excised bones demonstrated the blood supply to each region. In the 26 bones reported, nearly all had a large anterolateral vessel arising from the ascending branch of the anterior circumflex humeral artery. In most, this formed an 'arcuate artery' running posteromedially on entering the bone. There was a variable contribution to the humeral head from the posterior circumflex humeral and some minor vessels were found to enter in the region of attachment of the rotator cuff. Laing comments that the main blood
VESSELS FROM ROTATOR CUFF
ARCUATEL --
POSTERIOR t HUMERAL r~ CIRCUMFLEX TARTER, ( ANTERIOR HUMERAL CIRCUMFLEX ARTERY
ARTERY Figure 1. The blood supply of the humeral head. After Hawkins and Kiefer (1987) and Laing (1956).
supply enters above the most common sites of fracture of the surgical neck of the humerus so that an adequate blood supply is maintained. Figure 1 shows the blood supply to the humeral neck. Figure 2 shows Neer's classification of humeral neck fractures. It is evident from Figure 2 that the blood supply may indeed be disrupted in the more complex fractures, thus predisposing the humeral head to traumatic osteonecrosis. Knight and Mayne (1957) described a series of patients with various fracture and fracture-dislocation patterns of the humeral head. In all the groups reviewed, from what would appear to be 2-part fractures to the most complex fractures, the authors found a frequent occurrence of avascular necrosis. The blood supply of the humeral head is, therefore, similar to that of the femoral head. The latter bone is the most frequently involved in osteonecrosis.
653
OSTEONECROSIS OF THE HUMERAL HEAD I MINIMAL DISPLACEMENT
DISPLACED 2 PART
ANAT(
FRACTURES 5
PART
4 PART
:AL
NECK
rrr
SURGICAL NECK
'Iv GREATER TUBEROSITY
~ "-..,.
LESSER TUBEROSITY
ARTICULAR SURFACE FRACTURE DISLOCATION ANT RIOR
POSteRIOR
Figure 2. Classification of h u m e r a l neck fractures. From Neer (1970), with permission.
CLASSIFICATION OF CAUSES OF OSTEONECROSIS OF THE H U M E R A L HEAD
Jones (1978) suggested that osteonecrosis from all causes has increased significantly this century. This may be true of the non-traumatic forms, particularly those related to steroid treatment and to deep-sea diving. It may not be true for traumatic osteonecrosis as systematic documentation of such sequelae of fractures has only been properly undertaken in the last 30 years or so. The classification of osteonecrosis of the humeral head is outlined in Table 1. The non-traumatic causes include treatment with steroids (especially renal
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transplantation, asthma, collagen vascular diseases, etc.), treatment with other chemotherapeutic agents and radiotherapy (e.g. in leukaemia and Hodgkin's disease), Cushing's syndrome, Gaucher's disease, sickle cell disease and its associated variants, and caisson disease. A number of rarer causes of osteonecrosis have also been reported, including one case in pregnancy (McGuigan and Fleming, 1983) and one in a scythe maker (Kovarik et al, 1987). In this latter case the authors argued that the patient should be compensated for an industrially related disease! Pancreatitis has also been implicated, as has excess alcohol intake. Kahn et al (1986) report a case of bilateral femoral and humeral head osteonecrosis in a young male without evidence of any predisposing factors. The authors suggest that this is a true idiopathic osteonecrosis. A single case of osteonecrosis has also been reported following an intrathoracic dislocation of the humeral head (Ulrich et al, 1986). Table 1. Classification of osteonecrosis. A. B.
Traumatic Non-traumatic Steroid related ?SLE (not related to the steroid therapy) O t h e r chemotherapeutic agents and radiotherapy Sickle cell a n a e m i a and genetic variants Caisson disease Alcohol
?Hyperuricaemia ?Pancreatitis Other rarities
The majority of cases of osteonecrosis will be seen in association with trauma and steroid treatment. In special circumstances other causes will be significant, such as sickle cell anaemia in areas where sickle cell disease is endemic and caisson disease where there is a large diving workforce, e.g. in and around the ports servicing the North Sea oil rigs.
INCIDENCE Osteonecrosis of all bones is mostly associated either with trauma or treatment with systemic steroids (Jones, 1978). Traumatic osteonecrosis
The true incidence of this condition is very difficult to estimate. Knight and Mayne (1957) estimated a 62.5% incidence of osteonecrosis in 40 patients. The classification of the types of humeral fractures cannot be compared with later series based on the Neer classification. Neer (1970) reported 15 cases of osteonecrosis in 117 3- and 4-part fractures. Svend-Hansen (1974) found an 8.2% incidence in 49 severe fractures. Stableforth (1984) found four patients out of 49 to have definite radiographic changes of avascular osteonecrosis.
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Moriber and Patterson (1967) thought complications such as osteonecrosis and osteoarthritis after humeral neck fracture were rare but did occur. However, Lee and Hansen (1981) found no cases of osteonecrosis in a series of 19 4-part fractures and fracture-dislocations. The authors argued that the humeral head was rapidly revascularized and the head reconstructed by creeping substitution. Lee and Hansen describe radiographic changes in at least five patients who would be placed in stage 2 of the Ficat classification of osteonecrosis (Ficat, 1985). In the small number of patients that these authors report, none went on to develop collapse of the humeral head or osteoarthritis during the period of follow-up (6-49 months). Non-traumatic osteonecrosis
The true incidence in this category of patients is also very difficult to estimate. Jacobs (1978) examined 269 patients with femoral head necrosis. In this series, 39% were alcohol related and, in this group of 104 patients, 24 were found to have sites other than the femoral head involved, including the humeral head. In Jacobs' study, 75 patients had osteonecrosis associated with steroid therapy but no comment was made as to how many patients had sites other than the femoral head involved. The other major group comprised those associated with hyperuricaemia (58 patients) but many of these had other diseases known to be associated with osteonecrosis. Once again, no mention is made of the incidence of humeral head involvement. Three out of eight patients suffering from sickle cell disease had multifocal osteonecrosis. Overall, Jacobs found that 89% of the patients with nontraumatic osteonecrosis had a disorder of lipid metabolism. Pietrogrande and Mastromarino (1957) reported the first case of osteonecrosis associated with steroid therapy. Since that first case many others have been reported; there have been a large number of disease processes but the only common factor has been the use of steroids in the disease therapy. The published series suggest that the femoral head is the most common site of osteonecrosis in steroid therapy, followed by the humeral head. Moreover, Solomon (1973) showed that most of the 32 patients treated with corticosteroids developed the osteonecrosis between 6 and 24 months after the start of therapy. Cruess (1978) also found that patients did not suffer from osteonecrosis until 6 months after the start of the steroids but found that no new cases occurred after 18 months. Until recently, only long-term steroid therapy has been thought to be associated with osteonecrosis, but there is now evidence that short-term high-dose steroid treatment may cause multifocal osteonecrosis (Anderton and Helm, 1982; McCluskey and Gutteridge, 1982; Fast et al, 1984; Taylor, 1984). The main group of patients affected by steroid-induced osteonecrosis are those receiving immunosuppressive therapy for organ transplants. Cruess et al (1968) published the first study on osteonecrosis after renal transplantation. In 27 patients who had survived 6 months or more to the end of 1967, ten were found to have evidence of osteonecrosis. Only one patient had osteonecrosis of the humeral heads alone; two further patients had osteonecrosis in other bones as well. Cruess (1976,1978)has subsequently reported
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his further experience of this problem in renal transplantation and also a number of other conditions (systemic lupus erythematosus, glomerulonephritis, asthma hypopituitarism and Guillain-Barr6 syndrome). In the latter paper, 19 cases of osteonecrosis of the humeral head were found in 97 patients, with the total number of bones affected being 138. The humeral head was the second most common site of osteonecrosis. In only two cases was the humeral head alone affected. Harrington et al (1971) found one case of humeral head osteonecrosis in 18 patients reviewed but this patient also had osteonecrosis in both elbows, both hips, both carpal capitates, the right knee and the left talus. Potter et al (1978) found osteonecrosis in children after renal transplantation but the humeral heads were not involved in the patients they reviewed. However, in a series of 111 transplants in children from 1967 to 1977, 11 patients developed osteonecrosis, including one who 'required prosthetic replacement of the proximal humerus' (Uittenbogaart et al, 1978). Ibels et al (1978) examined 194 transplant patients, 40 of whom had evidence of osteonecrosis: only three patients had osteonecrosis of the humeral heads in their series and this was always associated with disease in the other bones. Seventy-seven patients being treated with steroids for a variety of collagen vascular, dermatological and haematological complaints, gout, pulmonary disease and other miscellaneous diseases had 142 bones affected by osteonecrosis (Fisher and Bickel, 1971); 11 humeral heads were involved. Kyd (1979) reported an isolated case of humeral head osteonecrosis; the humeral head may have been involved in other patients who had several bones affected. Osteonecrosis of the humeral heads is the second most common site in steroid-treated patients but there is usually evidence of osteonecrosis elsewhere and the disease is certainly much less common than osteonecrosis found in the femoral heads. The dosage of steroids may be the most important factor. Harrington et al (1971) found that the incidence of osteonecrosis was significantlyhigher in one group of patients whose total steroid dose was three times that of a second group. Rossleigh et al (1986) suggest that patients given steroids in combination with other chemotherapeutic agents and local radiotherapy in the treatment of Hodgkin's lymphoma are particularly at risk of developing osteonecrosis. Linus Pauling et al (1949) discovered that the haemoglobin in patients with sickle cell anaemia was abnormal. A number of variants have subsequently been described, the SC variant being one of the most important in the context of osteonecrosis. It is the SC variant, which although it is associated with fewer crises, is particularly associated with osteonecrosis of the epiphysis (Golding et al, 1959; Chung and Ralston, 1969). As with the other causes of osteonecrosis, the humeral head is less frequently affected than the femoral head. The humeral head is affected more often in adults than in children (Chung et al, 1978). Chung and Ralston (1969) found that 6 of 13 patients with femoral head osteonecrosis also had involvement of the humeral head. Unlike the causes of humeral head osteonecrosis mentioned so far, caisson disease would appear to affect the humeral head more frequently than other bones (Gregg and Walder, 1986). Amongst compressed-air workers, a rough estimate of the prevalence of osteonecrosis is 24% and in
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professional divers 6.2% (Gregg and Walder, 1986). Figures from the Medical Research Council Decompression Sickness Panel Registry, July 1972 (Davidson, 1976), found 334 men with 820 lesions (total population examined 1694), with 26% of the lesions affecting the juxta-articular region of the humeral head. In 1976, the same registry (McCallum et al, 1976) found 31% of 67 lesions in 35 divers with definite lesions (total population 1830). Ohta and Matsunga (1974) examined 301 traditional Japanese divers: 50.5% (152 individuals) had 231 lesions, of which 15% were juxta-articular humeral head. Multiple exposure to inadequate decompression may be important (Chryssanthou, 1978). In Jacobs' research (1978), pancreatitis was implicated in a small number of patients with multifocal osteonecrosis but the author did not specify the sites. Gaucher's disease is also associated with osteonecrosis; Amstutz and Carey (1966) found three definite cases of osteonecrosis of the humeral head in 20 patients reviewed. P A T H O L O G Y AND P A T H O P H Y S I O L O G Y
The pathological lesions encountered in the humeral head are consistent with bone death but are often associated with areas of revascularization. Ficat (1985) comments that, whatever the aetiology of the osteonecrosis, the end result is identical, namely 'blockage of the osseous microcirculation with intramedullary stasis'. Spencer et al (1986) described the changes found early on in a patient with osteonecrosis of the femoral head. They suggest a five stage evolution of changes: 1. 2. 3. 4. 5. 6. 7.
Normal: majority of osteocytes histologically viable. Increased numbers of empty osteocytic lacunae distributed in random fashion. Confluent areas of empty osteocytic lacunae. Medullary necrosis. Medullary fibrosis and revascularization with fibrocartilage and new bone formation. Linear fracture and separation of the necrotic focus. Collapse of the (femoral) head.
Similar pathological observations can be made in patients with osteonecrosis of the humeral head. Traumatic osteonecrosis is the direct result of a disruption of the blood supply to the affected bone. As described earlier, this is most frequently associated with displaced/complex fractures. Case 2 (see below) would also suggest that, occasionally, osteonecrosis of the humeral head can occur in undisplaced fractures. The pathophysiology of osteonecrosis secondary to sickle cell disease is similar to traumatic osteonecrosis, except that the cause of the interruption to the blood supply is due to sickling erythrocytes blocking small vessels rather than a physical interruption to the vessels, as in fractures. Osteonecrosis in sickle cell anaemia usually affects adults and can vary from an
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S. P. FROSTICK A N D W . A . W A L L A C E
osteochondritis dissecans type lesion to stage 4 changes (osteoarthritis: Ficat classification, see below) (Sennara and Gorry, 1978). Based upon the observation that 89% of 269 patients with osteonecrosis of all bones had diseases or had received treatment that affected the metabolism of fats, Jacobs (1978) postulated that fat emboli were important in the aetiology of many cases of osteonecrosis (steroid therapy, alcohol, etc.). Fat emboli have not been demonstrated in human bones affected by osteonecrosis (Glimcher and Kenzora, 1979). Experimentally, fat emboli have been found in the subchondral capillaries of femoral heads in rabbits (Jones and Sakovich, 1966). Fisher (1978) reports an experiment in which bone necrosis occurred in animals treated with steroids and with the animals suffering from marked alteration of lipid metabolism. Fat emboli in bone were seen. Extrapolation of these data to humans has not been demonstrated. Solomon (1973) suggested an alternative pathophysiology in patients who were suffering from 'drug-induced arthropathy'. Many of the 'drugs' in these patients caused osteoporosis and this was thought to lead to microfractures and subsequently to collapse of the bone. Arlot et al (1983) performed extensive bone histology of iliac crest bone in patients with osteonecrosis and also found osteoporosis, reinforcing the view that microfracturing was significant. Embolization has also been implicated in the aetiology of caisson disease (nitrogen bubbles) and Gaucher's disease-associated osteonecrosis. None of the theories in the literature have explained the pathophysiological processes that are observed. For example, the majority of steroid-related osteonecrosis patients are on long-term therapy; there does not seem to be a single vascular phenomenon associated with the onset of the disease in these patients. Moreover, in order to develop osteonecrosis secondary to caisson disease, multiple exposure to inappropriate decompression regimens are required. Embolization may or may not be the physical phenomenon leading to changes in vascularity of the humeral head. However, other physical and/or biochemical changes must occur that give rise to the clinical entity of osteonecrosis. Therefore, further research is required in humans and in experimental models in order to define the changes that lead to the clinical and radiographic manifestations. CLINICAL MANIFESTATIONS The diagnosis should be suspected from the past history, particularly in relation to steroid treatment, etc. Pain, a decreasing range of movement and progressive radiographic changes are typical clinical features. The following three cases will illustrate the clinical presentation and subsequent clinical course typical of osteonecrosis of the humeral head. Case 1 (Figure 3)
A 31-year-old negro male suffering from sickle cell anaemia presented with
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OSTEONECROSIS OF THE HUMERAL HEAD
(a)
(b)
Figure 3. Case 1. Sickle cell anaemia causing osteonecrosis of the humeral head. (a) AP and lateral views of the left proximal humerus showing the 'crescent sign'. (b) Postoperative radiograph showing the Neer II prosthesis in situ, (c) Full elevation of the shoulder replacement.
(c)
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S. P. FROSTICK A N D W . A. W A L L A C E
severe bilateral shoulder pain (left > right) and restriction of movement. The diagnosis of osteonecrosis was confirmed on plain radiographs. A core decompression was performed in February 1988 and the histology showed bone infarction and focal marrow fibrosis. Because of the severity of the pain and limitation of movement in the left shoulder, a Neer II hemiarthroplasty was performed in November 1988. The patient made an excellent postoperative recovery and has regained a near normal range of movement (fle~ion 160 ~ abduction 150 ~ external rotation 60 ~ and internal rotation to r12). Case 2 (Figure 4)
In July 1986, a 64-year-old caucasian female sustained an undisplaced humeral neck fracture of the left shoulder. The initial treatment took place in France, where she was placed into a shoulder spica cast. The spica was removed at the end of July 1986. Eighteen months after the original injury the patient continued to have significant pain, especially on movement. The range of movement was decreased. Plain radiographs at this stage showed osteonecrosis of the humeral head despite the fact that this was an undisplaced fracture (in three parts). In December 1988 a left Neer II hemiarthroplasty was performed. Good recovery of function occurred postoperatively. Case 3 (Figure 5)
In October 1987 this 58-year-old caucasian female fell downstairs and sustained multiple injuries, including a fracture-dislocation of the right shoulder. The following day an open reduction and internal fixation using 'K' wires was performed. The neck fracture was found to be impacted and the wires were used to hold fragments of the greater tuberosity. On 23 October 1987 the greater tuberosity was found to be a free fragment on radiographs. On 24 November 1987 a reconstruction of the right rotator cuff and reattachment of the greater tuberosity was performed. Between December 1987 and March 1988 an improvement in the function of the shoulder was noted. However, in March 1988 subluxation of the humeral head was found, with collapse of the humeral head indicating osteonecrosis. By July 1988 poor shoulder function was noted and the patient listed for a hemiarthroplasty. In November 1988 a Neer II hemiarthroplasty was performed. To date the patient has had poor function of the shoulder which is in part associated with postoperative scarring and contracture from previous surgery. STAGING OF SEVERITY OF OSTEONECROSIS
Ficat (1985) has classified the stages of progression of osteonecrosis affecting the femoral head. This classification is based upon clinical signs and plain radiograph changes. As the causes, pathophysiology and clinical present-
661
OSTEONECROSIS OF THE HUMERAL HEAD
(a)
(c)
(b) Figure 4. Case 2. Minimally displaced fracture of the humeral head. (a) Immediate post-injury radiograph showing a minimally displaced 3-part fracture of the left humeral neck. (b) Established osteonecrosis of the humeral head. (c) Almost full elevation of the shoulder is achieved after hemiarthroplasty.
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S. P. FROSTICK AND W. A. WALLACE
(~)
(h)
(e)
(a)
Figure 5. Case 3. Severely displaced fracture dislocation of the right humeral head. (a) The immediate post-injury radiograph shows a 4-part fracture dislocation of the right humeral head. (b) Subluxation of the humeral head is less 6 weeks after initial surgery. (e) Shows well established osteonecrosis of the humeral head. (fl) The Neer II hemiarthroplasty in situ.
OSTEONECROSIS OF THE HUMERAL HEAD
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ation are similar in both femoral head and humeral head (Cruess, 1978), it seems reasonable to apply the same staging to disease of the humeral head. The Ficat staging is as follows:
Stage O. Asymptomatic osteonecrosis, suspected because of disease elsewhere.
Stage 1. Early symptoms such as pain, some limitation of movement. Possibly some early plain radiographic changes.
Stage 2. Some increase in symptoms. Radiographic changes more pronounced.
Stage 3. Characterized by a sequestrum on plain radiographs. Clinically increasing pain and marked impairment of function.
Stage 4. Osteoarthritis. RADIOGRAPHIC INVESTIGATIONS
Changes on plain radiographs occur late in the clinical course of the disease. The MRC Decompression Sickness Panel has classified the radiological changes found in caisson disease (from Heard and Schnieder, 1978). The classification is given in Table 2. Table 2. Classification of radiological changes found in caisson disease. A.
B.
Juxta-articular lesions 1. Dense areas with intact articular cortex 2. Spherical segmental opacity 3. Linear opacity 4. Structural failure a. Translucent subcortical band b. Collapse of articular cortex c. Sequestration of cortex 5. Osteoarthritis Medullary lesions of the head, neck and shaft 1. Dense areas 2. Irregular calcified areas 3. Translucent areas and cyst formation
D'Ambrosia et al (1978) used bone scintigraphy to examine the changes occurring in osteonecrosis in animals. These authors found that a 'cold spot' ( d e c r e a s e d 99myc activity) was apparent shortly after the decrease in the vascularity but this was subsequently replaced by increased activity (a 'hot spot') as revascularization and repair proceeded. Bone scintigraphy identified one patient with steroid-induced osteonecrosis before plain radiographic changes were visible and in this case the findings were compared with the early changes found on histology (Spencer et al, 1986). Gregg and Walder (1980) developed an experimental model for caisson disease that suggested that revascularization could be detected as early as 3 weeks after the avascular phenomenon, as a hot spot on bone scintigraphy. Gregg and Walder (1981) were also able to demonstrate abnormalities on
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S. P. FROSTICK AND W. A. WALLACE
scintigraphy in patients with normal plain radiographs but who had ceased exposure to a high-pressure environment 10 years previously. Bone scintigraphy may show relatively early lesions in patients with sickle cell disease (Epps, 1983). The investigation of choice is now magnetic resonance imaging. It has been demonstrated to be useful in diagnosing early osteonecrosis (before radiographic changes are seen) in the femoral head (Bassett et al, 1987a, 1987b) and in the talus (Sierra et al, 1986). Zlatkin et al (1988, 1989) and Aquilone et al (1988) have obtained high resolution magnetic resonance images of shoulders. Sachs (1988) suggested that osteonecrosis of the humeral head could be diagnosed with magnetic resonance imaging. TREATMENT
The initial treatment should be symptomatic, with pain relief and physiotherapy to maintain an adequate range of movement (Young and Wallace, 1985). Terrett and Molyneux (1988) suggested that physical therapy would give a favourable outcome in the long term in one patient with traumatic osteonecrosis. The treatment in established osteonecrosis with humeral head collapse and osteoarthritis is frequently by hemiarthroplasty and very occasionally with a total shoulder replacement (Neer, 1974; Neer et al, 1982; Stableforth, 1984). The results can be excellent even in young patients (e.g. Case 1 above). However, it is also evident that the functional outcome of shoulder hemiarthroplasty may be poor if previous surgery has been performed on the joint (see Case 3). Open reduction and internal fixation of humeral fractures has also been used (Hawkins and Angelo, 1987; Hawkins and Kiefer, 1987). Lee and Hansen (1981) had a zero incidence of late stage osteonecrosis using this method. Fresh osteochondral allografts with muscle pedicle have been used in the treatment of osteonecrosis of the femoral head (Meyers, 1978). Rindell (1987) has recently suggested a similar approach can be used in osteonecrosis of the humeral head. The follow-up of Rindell's single patient was only 18 months; long-term follow-up is obviously required to determine the ultimate outcome for allograft surgery. REFERENCES Amstutz HC & Carey EJ (1966) Skeletal manifestations and treatment of Gaucher's disease. Journal of Bone and Joint Surgery 48A: 670-701. Anderton JM & Helm R (1982) Multiple joint osteonecrosis following short-term steroid therapy. Journal of Bone and Joint Surgery 64A: 139-141. Aquilone LF, Burk L, Blob RD, Brown DL, Rifkin MD & Mitchell DG (1988) Technical optimization of surface coil MRI of the rotator cuff. Abstract, Society of Magnetic Resonance in Medicine 7th Annual Meeting, 41. Arlot ME, Bonjean M, Chavassieux PM & Meunier PJ (1983) Bone histology in adults with aseptic necrosis. Journal of Bone and Joint Surgery 65A: 1319-1327.
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Bassett LW, Gold RH, Reicher MA, Bennett LR & Tooke SM (1987a) Magnetic resonance imaging in the early diagnosis of ischemic necrosis of the femoral head. Clinical Orthopaedics 214: 237-248. Bassett LW, Mirra JM, Crachiolo A & Gold RH (1987b) Ischemic necrosis of the femoral head: correlation of MRI and histologic sections. Clinical Orthopaedics 223: 181-187. Chrysannthou CP (1978) Dysbaric osteonecrosis. Clinical Orthopaedics 130: 94-106. Chung SMK & Ralston EL (1969) Necrosis of the femoral head associated with sickle cell anemia and its genetic variants. Journal of Bone and Joint Surgery 51A: 33-58. Chung SMK, Alavi A & Russell MO (1978) Management of osteonecrosis in sickle-cell anemia and its genetic variants. Clinical Orthopaedics 130: 158-174. Cruess RL (1976) Steroid-induced avascular necrosis of the head of the humerus. Journal of Bone and Joint Surgery 58B: 313-317. Cruess RL (1978) Experience with steroid-induced avascular necrosis of the shoulder and etiologic considerations regarding osteonecrosis of the hip. Clinical Orthopaedics 130: 86-93. Cruess RL, Blennerhassett J, MacDonald FR, Maclean LD & Dossetor J (1968) Aseptic necrosis following renal transplantation. Journal of Bone and Joint Surgery 50A: 15771590. D'A.mbrosia RD, Shoji H, Riggins RS, Staddalink RC & Dennardo GL (1978) Scimigraphy in the diagnosis of osteonecrosis. Clinical Orthopaedics 130: 139-143. Davidson JK (1976) Aseptic Necrosis of Bone. Amsterdam, Excerpta Medica. Epps CH (1983) Painful haematologic conditions affecting the shoulder. ClinicalOrthopaedics 173: 38-43. Fast A., Alon M, Weiss S & Zer-A.viv FR (1984) A.vascular necrosis of bone following short-term dexamethasone therapy for brain edema. Case report. Journal of Neurosurgery 61: 983-985. Ficat RP (1985) Idiopathic bone necrosis of the femoral head. Journal of Bone and Joint Surgery 67B: 3-9. Fisher DT (1978) The role of fat embolism in the etiology of corticosteroid-induced avascular necrosis. Clinical Orthopaedics 130: 51-67. Fisher DT & Bickel WH (1971) Corticosteroid-induced avascular necrosis. Journal of Bone and Joint Surgery 53A: 859-873. Glimcher MJ & Kenzora JE (1979) The biology of osteonecrosis of the human femoral head and its clinical implications. Clinical Orthopaedics 140: 273-312. Golding JSK, Maclver JE & Went LN (1959) The bone changes in sickle cell anaemia and its genetic variants. Journal of Bone and Joint Surgery 41B: 711-718. Gregg PJ & Walder DN (1980) Scintigraphy versus radiography in the early diagnosis of experimental bone necrosis. Journal of Bone and Joint Surgery 62B: 214-221. Gregg PJ & Walder DN (1981) A. study of old lesions of caisson disease by radiography and bone scintigraphy. Journal of Bone and Joint Surgery 63B: 132-137. Gregg PJ & Walder DN (1986) Caisson disease of bone. Clinical Orthopaedics 210: 43-54. Harrington KD, Murray WR, Kountz SL & Belzer FO (1971) A_vascular necrosis of bone after transplantation. Journal of Bone and Joint Surgery 53A: 203-215. Hawkins RJ & Angelo RL (1987) Displaced proximal humeral fractures: selecting treatment, avoiding pitfalls. Orthopedic Clinics of North America 18: 421-431. Hawkins RJ & Kiefer GN (1987) Internal fixation techniques for proximal humeral fractures. Clinical Orthopaedics 223: 77-85. Heard JL & Schneider CS (1978) Radiographic findings in commercial divers. Clinical Orthopaedics 130: 129-138. Ibels LS, A.lfrey AC, Huffer WE & Well R (1978) Aseptic necrosis of bone following renal transplantation: experience in 194 transplant recipients and review of the literature. Medicine 57: 25-45. Jacobs B (1978) Epidemiology of traumatic and non-traumatic osteonecrosis. Clinical Orthopaedics 130: 51-67. Jones JP (1978) Editorial comment: Osteonecrosis. Clinical Orthopaedics 130: 2-4. Jones JP & Sakovich L (1966) Fat embolism in bone: A roentgenographic and histological investigation with use of intra-arterial lipiodol in rabbits. JournalofBone andJointSurgery 48A: 149-164. Kahn T, Reiser M, Heimhuber B & Jager R (1986) Die Kombination von beid seitiger
666
S. P. FROSTICK AND W, A, WALLACE
idiopathischer Hfift- und Humeruskopfnekrose-erster Bericht fiber ein Krankenheitsbild. ROntgenbli~tter 39: 130-132. Knight RA & Mayne JA (1957) Comminuted fractures and fracture-dislocations involving the articular surface of the humeral head. Journal of Bone and Joint Surgery 39A: 1343-1355. Kovarik J, Niebauer B, Fruhwald F & Seidl G (1987) Probleme der aseptischen Humeruskopfnekrose--irrwege eines Senienschmiedes in der Begutactungsmedizin. Wiener Klinische Wochenschrifi 99: 462-466. Kyd RJ (1979) Bone and joint complications of maintenance haemodialysis and renal transplantation. New Zealand Journal of Medicine January 10: 4-6. Laing PG (1956) The arterial supply of the adult humerus. Journal of Bone and Joint Surgery 38A: 1105-1116. Lee CK & Hansen HR (1981) Post-traumatic avascular necrosis of the humeral head in displaced proximal humeral fractures. Journal of Trauma 21: 788-791. McCallum RI, Walder DW & Thickett VB (1976) Bone necrosis in commercial divers. Undersea Biomedical Research 3: A41. McCluskey J & Gutteridge DH (1982) Avascular necrosis of bone after high doses of dexamethasone during neurosurgery. British Journal of Medicine 284(6312): 333-334. McGuigan L & Fleming A (1983) Osteonecrosis of the humerus related to pregnancy. Annals of the Rheumatic Diseases 42: 59%599. Meyers MH (1978) The treatment of osteonecrosis of the hip with fresh osteochondral allografts and the muscle pedicle graft technique. Clinical Orthopaedics 130: 202-209. Moriber LA & Patterson RL (1967) Fractures of the proximal end of the humerus. Journal of Bone and Joint Surgery 49A: 1018. Neer CS (1970a) Displaced proximal humeral fractures Part I: Classification and evaluation. Journal of Bone and Joint Surgery 52A: 1077-1089. Neer CS (1970b) Displaced proximal humeral fractures Part II: Treatment of three-part and four-part displacement. Journal of Bone and Joint Surgery 52A: 1090-1103. Neer CS (1974) Replacement arthroplasty for glenohumeral osteoarthritis. Journal of Bone and Joint Surgery 56A: 1-13. Neer CS, Watson KC & Stanton JF (1982) Recent experience in total shoulder replacement. Journal of Bone and Joint Surgery 64A: 319-337. Ohta Y & Matsunga H (1974) Bone lesions in divers. Journal of Bone and Joint Surgery 56B: 3-16. Pauling L, Itano HA, Singer SJ & Wells IC (1949) Sickle cell anemia, a molecular disease. Science 110: 543-548. Pietrogrande V & Mastromarino R (1957) Osteopatia da prolungato trattamento cortisono. Ortopedica Traumatologia 25: 791. Potter DE, Genant HK & Salvatierra O (1978) Avascular necrosis of bone after renal transplantation. American Journal of Diseases of Children 132: 1125-1129. RindeU K (1987) Muscle pedicled bone graft in revascularization of aseptic necrosis of the humeral head. Annales Chirurgiae et Gynaecologiae 76: 283-285. Rossleigh MA, Smith J, Straus DJ & Engel H (1986) Osteonecrosis in patients with malignant lymphoma. A review of 31 cases. Cancer 58: 1112-1116. Sachs L (1988) MR of the shoulder. Abstract, Society of Magnetic Resonance in Medicine 7th Annual Meeting, 40. Sennara H & Gorry F (1978) Orthopaedic aspects of sickle cell anaemia and allied haemoglobinopathies. Clinical Orthopaedics 130: 154-157. Sierra A, Potchen EJ, Moore J & Smith GH (1986) High field magnetic resonance imaging of aseptic necrosis of the talus. Journal of Bone and Joint Surgery 68A: 927-928. Solomon L (1973) Drug-induced arthropathy and necrosis of the femoral head. Journal of Bone and Joint Surgery 55B: 246-261. Spencer JD, Humphreys S, Tighe JR & Cummings RK (1986) Early avascular necrosis of the femoral head. Journal of Bone and Joint Surgery 68B: 414-417. Stableforth PG (1984) Four part fractures of the neck of the humerus. Journal of Bone and Joint Surgery 66B: 104-108. Svend-I-Iansen H (1974) Displaced proximal humeral fractures: a review of 49 cases. Acta Orthopaedica Scandinavica 45: 359-364. Taylor LJ (1984) Multifocal avascular necrosis after short-term high dose steroid therapy. Journal of Bone and Joint Surgery 66B: 431-433.
OSTEONECROSIS OF THE HUMERAL HEAD
667
Terrett A G & Molyneux TP (1988) Hass' disease. Journal of Manipulation and Physical Therapy 11: 43-47. Uittenbogaart EH, Isaacson AS, Stanley P e t al (1978) Aseptic necrosis after renal transplantation in children. American Journal of Diseases in Children 132: 765-767. Ulrich C, Helbing G, Worsdorfer O & Lampl LH (1986) Intrathorakale Humeruskopfluxation. Langenbecks Archiv fur Chirurgie 367: 197-202. Young TB & Wallace WA (1985) Conservative treatment of fractures and fracture dislocations of the upper end of the humerus. Journal of Bone and Joint Surgery 67B: 373-377. Zlatkin MB, Iannotti JR, Esterhai J & Dalinka MK (1988) Magnetic resonance imaging of rotator cuff disease. Abstract, Society of Magnetic Resonance in Medicine 7th Annual Meeting, 140. Zlatkin MB, Dalinka MK & Kressel HY (1989) Magnetic resonance imaging of the shoulder. Magnetic Resonance Quarterly 5: 3-22.