THE CENTRAL GIANT CELL GRANULOMA, A CASE OF RECURRENCE AFTER 22 YEARS. SARINDER SINGH, B.D.S. Department of Oral Surgery, Guy s Hospital, London
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1 British Journal of Oral Surgery (1982) 20, The British Association of Oral Surgeons 0007-I 17x/82/ $02.00 THE CENTRAL GIANT CELL GRANULOMA, A CASE OF RECURRENCE AFTER 22 YEARS SARINDER SINGH, B.D.S. Department of Oral Surgery, Guy s Hospital, London Summary. A recurrence of giant cell granuloma of the mandible after 22 years is described. The author has been unable to find a similar case of long-term recurrence in the literature. The case also demonstrates the need for thorough surgical curettage as treatment of choice and may have a tenuous link with endocrine imbalance. A summary of the differential diagnosis of oral giant cell lesions is presented and a note added about the current thinking of giant cell formation. Introduction The term giant cell reparative granuloma of the jaws was proferred by Jaffe (1953) to distinguish the reactive lesion commonly occurring in the jaws from the giant cell tumour of long bones. He believed the former to be a local reparative reaction confined exclusively to the jaws and the latter to be a neoplastic lesion occurring mainly in long bones and rarely in the jaws. The word reparative is in general now omitted. Since Jaffe s description there have been reports of the giant cell granuloma occurring in other skull bones (Friedberg et al., 1969; Hirsch1 & Katz, 1974) and it has been suggested that the true giant cell tumour of bone occurs more often in the jaws than was first thought (Shklar & Meyer, 1961). A number of clinical and histological differences between the two entities have emerged. These have been concisely reviewed by Richter et al. (1973) and Hirsch1 & Katz (1974). The central giant cell granuloma occurs mainly in the first two decades of life and is more common in women than in men. It is seen more often in the mandible than the maxilla, rarely occurs distal to the first permanent molar and may often cross the midline. Radiographically the lesion appears as an area of rarefaction which may be faintly trabeculated and the edges are usually ill-defined but may show signs of sclerosis. Jaffe (1953) reported its appearance as nondescript and not diagnostic. Recurrences are uncommon and are generally considered to be due to inadequate initial treatment (Waldron & Shafer, 1966; Hirsch1 & Katz, 1974). The giant cell tumour of bone (osteoclastoma) occurs most often in the epiphyses of long bones and rarely in the jaws (Jaffe, 1953; Hutter et al., 1962). It is most common in the third and fourth decades of life and rarely occurs below the age of 20. This lesion may undergo malignant change and metastasises in 10 per cent of cases. Dahlin et al. (1970) reported a recurrence rate of 42 to 47 per cent of which 94 per cent recurred within three years. Hutter et al. (1962) reported its recurrence following curettage in 55 to 62 per cent of cases; of these 84 per cent recurred within two years and therefore resection would seem to be the treatment of choice. Histologically there are a number of differences. The giant cells of the giant cell granuloma are generally smaller and have fewer nuclei per cell. They tend to be clumped around areas of haemorrhage in which there are often haemosiderin deposits, especially in older lesions. The stromal cells are a mixture of oval and spindle-shaped (Received 22 September 1980; accepted 3 November 1980) 109
2 110 BRITISH JOURNAL OF ORAL SURGERY cells with few mitoses and often produce collagen. There may be foci of osteoid or new bone present. In the giant cell tumour the giant cells are larger, more rounded, have more nuclei per cell and are dispersed regularly throughout the lesion. The stroma is mainly round or oval cells with numerous mitoses present but little collagen production. There may be a rich vascular network but little haemorrhage into the lesion and very few haemosiderin deposits. New bone or osteoid is rarely seen. Although the above differences have been cited by many authors there have been reports suggesting that the giant cell granuloma is the same entity as the giant cell tumour, occurring in the jaws. Waldron & Shafer (1966) are the chief protagonists; they believe the jaws allow much quicker detection and diagnosis of the lesion and hence modify the subsequent clinical picture. The histological differential diagnosis of giant cell lesions of the jaw must also include the aneurysmal bone cyst, hyperparathyroidism, fibrous dysplasia, cherubism and the peripheral giant cell granuloma. The diagnostic features of the aneurysmal bone cyst are the numerous vascular spaces lined by flattened spindle-shaped cells and separated by thin fibrous septa. Giant cells are found in the connective tissue stroma (Bhaskar et al., 1959; Austin et al., 1959). The brown tumour of hyperparathyroidism may histologically be indistinguishable from the central giant cell granuloma. Early in the disease, bone is resorbed from areas around the blood vessels, often leaving islands of osteoid surrounded by osteoclasts. As the disease progresses, lesions develop that are histologically similar to those of the central giant cell granuloma. Normal serum calcium, inorganic phosphate and alkaline phosphatase estimations should exclude hyperparathyroidism from the diagnosis. The criteria put forward by Reed and Hagy (1965) should distinguish true fibrous dyplasia from all other fibro-osseous lesions of bone, namely, the persistence of woven bone pattern with a complete lack of lamellar bone formation. Cherubism is a rare disease confined to children. The clinical and radiographic appearance should be diagnostic although histologically the lesions may be indistinguishable from the giant cell granuloma. The peripheral giant cell granuloma occurs on the gingiva or alveolar ridge as a bluish haemorrhagic swelling, often pedunculated and rarely exceeding 2 cm in diameter. Bony involvement is limited to superficial erosion (Giasanti & Waldron, 1969). Much has been written about giant cells in central and peripheral giant cell granulomas. Stones (1941) originally described two types of giant cells in the central giant cell granuloma which Bhaskar et al. (1971) in their review of the peripheral giant cell granuloma describe as Type I and Type II cells. Type I cells are the most prevalent. They have multiple nuclei which are large, ovoid, vesicular and translucent with prominent nucleoli. The general morphology of the nuclei corresponds to those of the surrounding stromal cells. The cytoplasm is palely basophilic, translucent and occasionally vacuolated. Their size varies but are often over 100 pm in diameter. Type II cells have eosinophilic staining cytoplasm. Vacuolation is rarely seen and the nucleoli are difficult to observe. Type II cells are generally smaller than Type I. The nuclei in both types are randomly scattered throughout the cytoplasm. Both Stones (1941) and Shklar & Cataldo (1967), who had also noted the two types of cell, concluded that the more reactive and intensely staining Type II cell represented an older cell in the process of degeneration. Bhasker et al. (1971) thought this unlikely as both types appeared in nearly equal numbers (Type I slightly more often than Type II); both are seen in, and arising from, adjacent vascular channels. The origin of giant cells in these lesions remains uncertain. Cooke (1952) suggested that the giant cells of peripheral giant cell granulomas are osteoclasts. Soskolne (1972) suggested that the giant cells are not phagocytic and arise from the fusion of undifferentiated stromal cells. In a report of the ultrastructure of giant cells
3 THE CENTRAL GIANT CELL GRANIJLOMA 111 Adkins et al. (1969) found similarities between some stromal mononuclear cells and giant cells. Andersen et al. (1973) concluded that the similar histochemical activities in giant cells and pericytes of the vascular granulation tissue lend support to the assumption that pericytes are the precursors of giant cells. Mariano and Spector (1974) and Chambers (1977) have observed that macrophage fusion in vitro has not been achieved with substances in inflammatory exudates, or by ageing macrophages before adding fresh monocytes. They have attempted to explain macrophage fusion by the alteration of surface properties of the cell to overcome electrostatic forces of repulsion or the presence of intercellular material. Chambers (1977) noted that the macrophage surface membrane undergoes fusion during endocytosis. Hence there is no need for a change in the surface properties except for the attachment of endocytogenic material to the macrophage surface (that is, material which attaches to and is endocytosed by the macrophage, for example, erythrocytes and insoluble foreign material). He suggests that in the densely packed environment of a granuloma, endocytogenic material may attach simultaneously to more than one macrophage thereby leading to fusion. This needs a particle that is strongly adherent to both macrophages. Galindo et al. (1974) and Warfel(l978) have shown that fusion of rabbit alveolar macrophages is mediated by a molecular weight lymphokine they have called Macrophage Fusion Factor (M.F.F.). Hence giant cell formation reflects an alteration of macrophages during cellular immune reaction and is dependent on T-lymphocytes. The purpose of this paper is to present a case of recurrence of the central giant cell granuloma after 22 years. A recurrence after this length of time had not previously been reported. Case report The patient, a 13-year-old girl, was originally referred to the Regional Oral Surgery Service in August 1956, by her general dental practitioner, who had noted a swelling of the mandible in the left mental region. She presented with a 5 x2 cm swelling, extending from the premolar region to the midline with buccal expansion. Radiographs revealed a 4 x 3 cm radiolucent area in the same region. This radiolucency extended from the alveolar margin almost to the lower border of the mandible with a poorly dehned margin. The roots of 145 extended into the radiolucency but there was no record of mobility of these teeth. Incisional biopsy of the swelling revealed a lesion containing multinucleate giant cells distributed throughout a fibroblastic background. This was consistent with a diagnosis of either central giant cell granuloma of bone or hyperparathyroidism. Serum calcium estimations were carried out on two separate occasions with the following results : Sept. Oct Normal Values Serum Calcium (m.mol/litre) Serum Inorganic Phosphate Serum Alkaline Phosphatase (Units/litre) (m.mol/litre) The elevated serum calcium raised the possibility of hyperparathyroidism and the neck was surgically explored in November 1956, but no obvious parathyroid enlargement or ectopic parathyroid tissue found. Although the serum calcium was elevated
4 112 BRITISH JOURNAL OF ORAL SURGERY the diagnosis of hyperparathyroidism was finally excluded as the serum inorganic phosphate was not lowered. This was confirmed later as serum calcium and phosphate estimations proved to be within normal limits. The patient was treated with 2800 rads of 4MeV X-radiation over a period of 14 days during December One year postirradiation the swelling was reduced to 3 x2 cm, and was clinically normal two years post-irradiation. Four years post-irradiation the area appeared radiologically normal. The patient was reviewed biannually until November 1965 and then discharged. The patient remained symptom-free until 1979 except for the extraction of in 1975 due to dental abscesses, since when she had worn a lower partial denture. In January 1979 the patient now aged 36 presented with a 1.5 cm diameter bluish swelling on the lingual aspect of the lower left premolars which extended on to the alveolar ridge in the incisor region (Fig. 1). Radiographically there was an irregularly defined rarefaction from the midline to the left premolar region (Fig. 2). An excisional biopsy which removed the soft tissue lesion only, revealed a similar histological picture to the 1956 biopsy. The biopsy site healed but the soft tissue lesion recurred three months later and the patient was readmitted in May On readmission the swelling was similar to that of January 1979; a haemorrhagic bluish lesion now extending along the alveolar ridge in the 21)12 region and prolific lingually in the vregion. The lesion was causing mobility of the and radiographs revealed a diffuse radiolucency from31 to 13: Blood chemistry revealed: Serum Calcium Serum Phosphate Serum Alkaline Phosphatase 2.53 mmol/litre 0.98 mmol/litre 47 units/litre Haematology revealed a red blood cell count of 3.69 x lolz/litre and haemoglobin of 8.7g/dl. This microcytic, hypochromic anaemia was due to menorrhagia which had occurred after withdrawal of the contraceptive pill following sterilisation. There were no other gynaecological symptoms. The patient was transfused with 2 units of packed FIG. 1. Clinical presentation in January 1979 showing a bluish haemorrhagic swelling.
5 THE CENTRAL GIANT CELL GRANULOMA 113.:..I FIG. 2. Orthopantomogram, January 1979, showing a diffuse ill-defined radiolucency from [rregion to the midline. red cells pre-operatively to bring her red blood cell count to 4.67 x lolz/litre and haemoglobin to 12.4g/dl. The haemoglobin and red cell count have remained normal 1 year post-operatively. At operation the were extracted and the lesion excised. The underlying bone was thoroughly curetted and the area allowed to granulate. By July 1980 the area had healed satisfactorily (Fig. 3) and the radiolucency markedly reduced. Further serum calcium, inorganic phosphate, alkaline phosphatase, haemoglobin and red cell counts proved to be within normal limits. FIG. 3. Satisfactory post-operative healing, July 1980.
6 114 BRITISH JOURNAL OF ORAL SURGERY Histology Sections from the original 1956 and both 1979 lesions were examined. They were all essentially similar, with numerous multinucleate giant cells scattered throughout a highly fibroblastic background. All 3 biopsies contained Type I and Type II giant cells which were found as foci around effete red blood cells. The giant cells often contained cytoplasmic vacuoles and rarely haemosiderin pigment. The stromal cells were mainly oval or spindle-shaped fibroblasts producing collagen. Few mitoses were seen. In the collagenous connective tissue were scattered foci of effete red blood cells, haemosiderin granules and occasional siderophages. There were also many inflammatory cells and occasional small foci of bone. Some minor differences were found in the sections examined. Both 1979 biopsies were covered with keratinised, stratified squamous epithelium, typical of a peripheral extension of a central giant cell granuloma. In the 1979 sections there appeared to be more Type I giant cells than Type II whilst in the 1956 sections their numbers were roughly equal. The features were consistent with a diagnosis of central giant cell granuloma of bone. FIG. 4. Histological section of lesion curetted, May Note the mixture of Type I and Type II giant cells in the fibroblastic stroma containing effete red blood cells. (x 100.) Discussion The diagnosis of central giant cell granuloma was arrived at after excluding hyperparathyroidism. This was done after considering the nondiagnostic blood chemistry associated with a lack of parathyroid hyperplasia or adenoma. In hyperparathyroidism the serum levels of calcium and alkaline phosphatase are raised and inorganic phosphates depressed. The central giant cell tumour was excluded on the clinical and histological grounds reviewed above. A span of 22 years elapsed from the diagnosis of the original lesion to a recurrence
7 THE CENTRAL GIANT CELL GRANULOMA 115 of the same histological entity at the same site. A search of the major American and British journals failed to reveal a case of recurrence of the same magnitude. Most cases had no recurrence at the time of reporting, and of those that did recur, the majority were within five years. Littler (1979) reviewed a case of recurrence during pregnancy six years after the removal of the original lesion. McGowan (1969) reported a similar case of giant cell granuloma appearing in pregnancy and recurring two years later during another pregnancy. He quoted other cases from the literature of lesions occurring in pregnancy and proposed a hormonal influence on the development of these lesions. It would seem that puberty may have been associated with the 1956 lesion and menorrhagia with the recurrence in 1979, both of which are linked with endocrine changes. Unfortunately hormonal assays were not performed on the patient reported in this paper. Surgical curettage must remain the treatment of choice in the central giant cell granuloma. The use of radiotherapy is contraindicated in an area that is so easily accessible to surgery. Irradiation has been successfully carried out but its use should be confined to surgically inaccessible giant cell granulomas in other facial and long bones. Attention must be drawn to the radiation-induced sarcoma reported as long ago as 1956 by Sabanas et al. (1956). The present case demonstrates the need for thorough surgical curettage. Simple excision in January 1979 proved ineffective without removal of the underlying softened bone. This case has drawn attention to an unusually long term recurrence of a central giant cell granuloma of the mandible which may have an association with hormonal imbalance as suggested by McGowan (1969). It has also demonstrated the need for thorough surgical curettage in the treatment of this condition. I would like to thank Professors J. C. Southam and W. D. MacLennan for their advice and encouragement in the preparation of this paper. I would also like to thank Dr J. F. Gould and Mr A. C. Buchan for access to the clinical material, and Miss Y. Stables, Mr J. Mitchell, Mr R. Renton, Dr G. Sclare and Mr W. Franklin for their assistance. References Adkins, K. F., Martinez, M. G. & Hartley, M. W. (1969). Ultrastructure of giant-cell lesions. Oral Surgery, Oral Medicine and Oral Pathology, 28, 713. Andersen, L., Arwill, T., Fejerskov, O., Heyden, G., & Philipsen, H. P. (1973). Oral giant cell granulomas. Acta Pathologica et MicrobioIogica Scandinauica, 81a, 617. Austin, L. T., Dahlin, D. C. & Royer, R. Q. (1959). Giant-cell reparative granuloma and related conditions affecting the jawbones. Oral Surgery, Oral Medicine and Oral Pathology, 12, Bhaskar, S. N., Cutright, 0. E., Beasley, J. D. & Perez, B. (1971). Giant cell reparative granuloma (peripheral): report of 50 cases. Journal of Oral Surgery, 29, 110. Bhaskar, S. N., Bernier, J. L. & Godby, F. (1959). Aneurysmal bone cyst and other giant-cell lesions of the jaws. Journal of Oral Surgery, 17, 30. Chambers. T. J. (1977). Fusion of macrophages following simultaneous phagosytosis of glutaraldehyde-fixed red cells. Journal of Pathology, 122, 71. Cooke, B. E. D. (1952). Giant-cell epulis; histogenesis and natural history. British Dental Journal, 93, 13. Dahlin, D. C., Cupps, R. E. & Johnson, E. W. (1970). Giant cell tumour: a study of 195 cases. Cancer, 25, Friedberg, S. A., Eisenstein, R. & Wallner, L. J. (1969). Giant cell lesions involving the nasal accessory sinuses. Laryngoscope, 79,763. Galindo, B., Lazdins, J., & Castillo, R. (1974). Fusion of normal rabbit alveolar macrophages induced by supernatant fluids from BCG-sensitised lymph node cells after elicitation by antigen. Infection and Immunity, 9,212.
8 116 BRITISH JOURNAL OF ORAL SURGERY Giasanti, J. S. & Waldron, C. A. (1969). Peripheral giant-cell granuloma; review of 720 cases. Journal of Oral Surgery, 27, 787. Hirschl, S. & Katz, A. (1974). Giant-cell reparative granuloma outside the jaw bone. Human Pathology, 5, 171. Hutter, R. V. P., Worcester, J. N., Francis, K. C., Foote, F. W., & Stewart, F. S. (1962). Benign and malignant giant cell tumours of bone. Cancer, 15, 653. Jaffe, H. L. (1953). Giant-cell reparative granuloma, traumatic bone cyst and fibrous (fibro-osseous) dysplasia of the jaw bones. Oral Surgery, Oral Medicine and Oral Pathology, 6, 159. Littler, B. 0. (1979). Central giant-cell granuloma of the jaw - a hormonal influence. British Journal of Oral Surgery, 17,43. McGowan, D. A. (1969). Central giant-cell tumours of the mandible occurring in pregnancy. British Journal of Oral Surgery, 7, 131. Mariano, M. & Spector, W. G. (1974). The formation and properties of macrophage karyons (Inflammatory giant cells). Journal of Pathology, 113, 1. Reed, R. J. P. & Hagy, D. H. (1965). Benign non-odontogenic fibro-osseous lesions of the skull. Oral Surgery, Oral Medicine and Oral Pathology, 19,214. Richter, J. K., Grammer, F. C. & Boies, L. (1973). Central giant-cell lesion in the angle of the mandible; review of the literature and report of a case. Journal of Oral Surgery, 31, 26. Sabanas. A. 0.. Dahlin. D. C. & Childs. D. S. (1956). Post-radiation sarcoma of bone. Cancer Shklar, G. & Cataldo; E. (1967). The gingival giant-cell granuloma, histochemical observations. Periodontics, 5, 303. Shklar, G. & Meyer, I. (1961). Giant-cell tumours of the mandible and maxilla. Oral Surgery, Oral Medicine and Oral Pathology, 14, 809. Soskolne, W. A. (1972). Some observations of the pathogenesis and morphology of giant-cell Granulomas. Proceedings of the Royal Society of Medicine, 65, Stones, H. H. (1941). The more frequent benign connective tissue tumours of the mouth. British Dental Journal, 71,49. Waldron, C. A. & Shafer, W. G. (1966). The central giant-cell reparative granuloma of the jaws. The American Journal of Clinical Pathology, 45,437. Warfel, A. H. (1978). Macrophage fusion and multinucleate giant-cell formation, surface morphology. Experimental and Molecular Pathology, 28, 163.
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