British Dental Journal V205 N8

Orofacial presentations of IN BRIEF • Demonstrates the wide spectrum of orofacial manifestations of sarcoidosis PRACTICE above and beyond the ‘classical’ features sarcoidosis – a case series of the disease. • Serves as an aide memoire for junior hospital clinicians, general dental and review of the literature practitioners and dental students. • Highlights the dental aspects of this 1 2 3 4 systemic condition and is beneﬁ cial when T. W. J. Poate, R. Sharma, K. A. Moutasim, M. P. Escudier formulating treatment plans for patients and S. Warnakulasuriya5 affected by the disorder.

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Sarcoidosis is a multi-system disease of unknown aetiology characterised by the presence of non-caseating granulomas, the lungs and lymph nodes being the most affected sites. Orofacial manifestations of the condition are increasingly rec ognised, with several recent case reports where the initial presentation of the disease is in the region. Here, we report six cases of orofacial sarcoidosis which help to illustrate the wide spectrum of the condition.

INTRODUCTION The lungs are often affected and in such prick in the distribution of all three Sarcoidosis is a systemic granulomatous cases the patient may present with a dry branches of the left trigeminal nerve. condition of unknown cause affecting cough, dyspnoea or chest pain. Other The left corneal reflex was also reduced. multiple organs.1 The disease is char common symptoms include a fl u-like The motor component of the nerve was acterised by the presence of non-case illness with fever, night sweats, fatigue spared and neurological examination ating granulomas and whilst any organ and arthralgia. Ocular discomfort and was otherwise normal. There was a 6 x 7 may be affected the most common sites reduced visual acuity due to uveitis mm firm swelling on the left lateral bor are the lungs and lymph nodes.2 More may occur as may lymphadenopathy der of the tongue. An excisional biopsy than 3,000 new cases of sarcoidosis are and enlargement of the liver and spleen. of the lingual swelling demonstrated the diagnosed in the UK each year with a Cutaneous lesions may also be present presence of non-caseating granulomas higher incidence among young adults and include a macular papular rash and suggestive of sarcoidosis (Fig. 1). Her aged 20–40.2,3 It occurs in all races but erythema nodosum.2 serum angiotensin converting enzyme appears to be more common in people of Oral involvement has been noted as (SACE) was raised at 110 U/L (normal African-American, Afro-Caribbean or the initial manifestation in several case level 27-82 U/L). Scandinavian origin.2,4,5 reports of sarcoidosis.6-8 A diagnosis of sarcoidosis was made It has been suggested that sarcoido We report six cases of orofacial sar and she was referred for chest and neu sis is due to an immunological response coidosis that have attended the oral med rology opinions. Clinical examination to an infective trigger in a genetically icine department in this dental institute of the chest was unremarkable whilst a predisposed individual, with the most in London in the past 24 months which chest X-ray revealed slight hilar promi likely candidates being mycobacteria help to illustrate the spectr um of the oro nence. Tuberculosis was excluded by and propionibacteria.5 facial presentations of this condition. the mantoux test. An MRI scan dem Affected patients may be asymp onstrated a mass adjacent to the left tomatic or have a wide range of non CASE 1: TRIGEMINAL NEUROPATHY trigeminal ganglion. Treatment was specific symptoms depending on the A 33-year-old Caucasian lady was commenced with prednisolone at a dose organs affected and stage of the disease. referred to the oral medicine department of 40 mg with appropriate prophylaxis by her general dental practitioner with including a bisphosphonate. a one year history of numbness of the At her subsequent review by a car left side of the face and forehead. She diologist it was felt that her cardiac 1Consultant in Oral Medicine; 2Senior House had also noticed an asymptomatic lump disease was probably a further mani Officer in Oral Medicine; 3*Speciality Dentist in Oral Medicine, Barts & The London NHS Trust, on the left side of her tongue which had festation of the sarcoidosis. Over the London; 4Consultant in Oral Medicine; 5Professor been present for the last three months. next four months her facial sensation of Oral Medicine, Dental Institute at Guy’s, King’s and St. Thomas’ Hospitals, London She had also recently been diagnosed improved. A repeat MRI showed the *Correspondence to: Dr Karwan Moutasim with hypertrophic cardiomyopathy but mass in the trigeminal ganglion to have Email: [email protected] had no other relevant medical history. reduced in size and her prednisolone was Refereed Paper She had no chest symptoms. therefore gradually reduced and then Accepted 11 July 2008 DOI: 10.1038/sj.bdj.2008.892 On examination she was found to have stopped over the following six months ©British Dental Journal 2008; 205: 437-442 reduced sensation to light touch and pin without relapse.

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CASE 2: SALIVARY AND LACRIMAL GLAND SWELLING A 43-year-old Indian female developed bilateral parotid and submandibular swelling. This was initially diagnosed by her general medical practitioner (GMP) as mumps and was managed conservatively. She subsequently developed a right sided lower motor neurone lesion of the sev enth cranial nerve for which she was pre scribed a two week course of prednisolone with good effect. However, three weeks after the cessation of the prednisolone the bilateral parotid and submandibular swelling recurred. On this occasion she was also noted to have bilateral lacrimal Fig. 1 High-power photomicrograph of lingual mucosa demonstrating non-caseating granulomas of sarcoidosis (case 1). An individual granuloma is shown in the left corner swelling. In view of this the GMP recom (haematoxylin & eosin) menced prednisolone and referred her to a local physician. Further investigations including liver function tests and SACE were within normal limits as were a chest X-ray and CT scan. In view of the per sisting salivary gland swelling she was referred to the oral medicine department for further investigation. On further questioning she reported dryness of the mouth and eyes. She also had arthralgia, weight loss and blurred vision which had worsened recently. She had no chest symptoms. On examina tion she had no swelling of the parotid, submandibular or lacrimal glands. She had slightly reduced visual acuity in the right eye and was noted to have ‘shotty’ cervical lymphadenopathy. Intra-orally she had a well lubricated and generally healthy oral mucosa. There was a good flow of clear saliva from all major sali vary gland duct orifices. A provisional diagnosis of sarcoidosis (Heerfordt’s syndrome) was made based on the his tory of salivary gland swelling, lac rimal involvement and seventh nerve palsy whilst the differential diagnosis Fig. 2 Anteroposterior chest radiograph showing bilateral hilar lymphadenopathy with borderline nodularity in case 2 included Sjögren’s syndrome. The unstimulated whole salivary flow and stimulated parotid salivary and submandibular glands which were leakage indicating activity in the optic flow rates were within normal limits. highly vascular. Parotid sialography nerve head. The patient declined any Schirmer’s test was negative for both was essentially normal with no delay of further investigations and a diagnosis eyes. Her autoimmune profi le includ emptying or sialectasis. A chest x-ray of salivary and ocular sarcoidosis was ing Ro and La antoantibodies was nega showed bilateral hilar lymphadenopathy made. In view of her persisting symp tive. The SACE was repeated and on this with borderline nodularity (Fig. 2) and toms oral prednisolone was continued occasion found to be raised at 94 U/L she was subsequently referred to a chest for two months before being reduced and (normal level 27-82 U/L). Ultrasound physician and ophthalmologist. Formal then stopped as her symptoms resolved. examination demonstrated an enlarged pulmonary function tests were normal She has since remained symptom free for jugulo-digastric lumph node and multi whilst a fluorescein angiogram showed two years with no further active treat ple hypoechoic areas within the parotid optic disc hyperfl uorescence and some ment required.

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CASE 3: PAROTID GLAND at 69 IU/L (10-50 IU/L) and alkaline SWELLING phosphatase at 497 IU/L (30-130 IU/L). A 27-year-old gentleman of mixed eth The C-reactive protein (CRP) was raised nicity with a Caucasian mother and Afri at 98 mg/L (<5 mg/L). Blood cultures can father was admitted under the care were negative and HIV, hepatitis B of the neurologists with a three month and C and tuberculosis were excluded. history of generalised muscle aching Serology for toxoplasma, cytomegalo and weakness in his legs causing diffi virus, Epstein Barr virus and brucella culty in walking up stairs. He also had was unremarkable and an autoantibody bilateral swelling of the parotid glands screen was negative. SACE was raised at for which an oral medicine opinion 224 U/L (8-52 U/L). was requested. He had previously been Ultrasound examination demonstrated prescribed non-steroidal anti-infl am both parotid glands to be enlarged and matory drugs by his GMP which had inflamed with non-specific features of improved his symptoms over a period parotitis. Reactive lymph nodes were of six weeks. He then developed a fl u noted at the level of the carotid bifur like illness, fever, productive cough, cation bilaterally. MRI demonstrated a widespread rash and cervical lymphad normal intracranial appearance with enopathy with associated diffi culty in marked enlargement of both parotid swallowing. On this occasion his GMP glands. Chest X-ray was unremarkable Fig. 3 Bilateral parotid swelling in case 3 prescribed a course of antibiotics but his whilst a CT scan demonstrated bilat symptoms persisted and he went on to eral, enlarged axillary, peri-portal and swelling, cutaneous or genital dryness develop night sweats and reported two inguinal lymphadenopathy. A gallium or joint symptoms. She also had fatigue stone weight loss in eight weeks. He also sca n showed i nc r ea sed upta ke of t r ace r i n and a persistent, unproductive cough for reported dryness of the mouth. the liver, lacrimal glands, central nasal which she had been referred to the chest His medical history included asthma region, parotid glands and submandibu department. She was a non-smoker. She for which he used a salbutamol inhaler lar glands as well as in the axillary and was known to have macular degenera and eczema. He had also been diagnosed inguinal lymphatic chains. tion and sickle cell trait and to be iron at the age of seven years with tempo Incisional biopsy of the parotid gland deficient for which she was taking ral lobe epilepsy which was controlled demonstrated multiple non-caseating iron supplements. with carbamazepine and vigabatrin. epithelioid granulomas surrounding the On examination she had no facial He was a non-smoker and did not drink ducts and destroying the acinar struc swelling but had dryness of the oral alcohol. He had not travelled abroad for tures. Similar granulomas were present mucosa with lack of saliva pooling several years. in a skin biopsy. A diagnosis of multi-sys and reduced quantities of saliva milk On examination he had a widespread tem sarcoidosis with cutaneous, hepatic, able from the major salivary ducts. The annular erythematous dry scaly rash neurological and salivary gland involve unstimulated whole salivary fl ow rate on his trunk and all four limbs. He was ment was made. He was reviewed by a was 0.1 ml/minute (normal value >0.2 pyrexial and was noted to have marked respiratory physician and commenced on ml/minute). She was negative for Ro non-tender bilateral parotid swelling prednisolone 60 mg daily with bisphos and La autoantibodies. The SACE was (Fig. 3). He had widespread cervical, phonate and calcium supplementation. raised at 225 U/L (normal level 27-82 U/ axillary and inguinal lymphadenopathy. His skin rash improved within a few days L). There was also derangement of liver Respiratory and abdominal examination and after three months the SACE and enzymes with alkaline phosphatase 276 was unremarkable. Neurological exami CRP had returned to normal while the IU/L (30-130 IU/L), aspartate transami nation revealed increased tone in the left liver function tests had improved consid nase 58 IU/L (10-50 IU/L), GGT 151 leg with brisk reflexes at the knees and erably. His prednisolone was reduced at IU/L (1-55 IU/L). The white cell count ankles bilaterally. Vibration sense was this stage to 20 mg daily. A further three was low at 3.89 x109 (normal value 4.0 reduced in the left toes and ankle and months later his neurological defi cits, – 11.0 x109) with a neutropenia and pinprick sensation was reduced over the parotid swelling and oral dryness are lymphopenia. Ultrasound of the parotid sole of the left foot. His gait was abnor improving and continue to be monitored. glands demonstrated small hypoechoic mal and he walked with a semi-spastic areas throughout the parenchyma but gait. Cranial nerves were intact. CASE 4: XEROSTOMIA sialography showed no abnormality in Blood tests revealed a normocytic A 35-year-old Afro-Caribbean lady was either parotid gland and did not sup anaemia with a haemoglobin of 11.6 referred to the oral medicine department port a diagnosis of Sjögren’s syndrome. g/dl (normal range 13.0 -16.5 g/dl). with a two year history of a dry mouth A labial gland biopsy reported the pres Liver function tests were abnormal with and gritty eyes. She was taking fre ence of non-caseating granulomas. A gamma-glutamyl transferase at 885 IU/ quent sips of water and was using arti chest X-ray was reported as showing L (1-55 IU/L), aspartate transaminase ficial tears daily. She denied any facial bilateral hilar lymphadenopathy and a

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reticular nodular pattern of increased lung markings seen throughout both lungs consistent with pulmonary paren chymal sarcoidosis. Pulmonary function tests demonstrated a restrictive pulmo nary defect. CT scan demonstrated par atracheal lymphadenopathy. She was referred to the liver unit where a liver biopsy was performed which conﬁ rmed a granulomatous hepatitis. Ocular assess ment excluded ocular sarcoid. A diagnosis of multi system sarcoidosis with pulmonary, bone marrow, hepatic and salivary gland involvement was made. She was advised to use sugar free gum and prescribed saliva stimulating tablets for the symptomatic control of her dry mouth. She was also commenced on prednisolone 30 mg daily by the chest Fig. 4 Intraoral photograph showing gingival swelling with mild erythema in sarcoidosis (case 5) physicians. This led to a progressive improvement in her chest symptoms and a return of the SACE level to within nor mal limits. One year later she remains on prednisolone at a reduced dose of 15 mg daily, has no chest symptoms with a normal chest X-ray and improved pul monary function tests.

CASE 5: GINGIVAL SWELLING A 41-year-old Afro-Caribbean lady was referred to the oral medicine depart ment by the department of oral surgery following the extraction of her wisdom teeth. At the time of surgery it was noted that she had generalised swell ing of her gingivae despite good oral hygiene although the patient had been unaware of this. She suffered from sickle cell trait and glucose-6-phosphate defi Fig. 5 Two distinct sarcoid nodules affecting the upper lip in case 6 ciency but was otherwise fit and well with no chest symptoms. On examina as having pulmonary sarcoidosis and intralesional steroid injections and had tion she had generalised swelling of the commenced on prednisolone with good reduced in size. She had previously been gingivae with areas of erythema (Fig. effect. At the present time she remains diagnosed with cutaneous sarcoido 4). An incisional biopsy was performed on therapy and under review. sis affecting the legs and face, whilst which reported that the corium was biopsies of the lower lip at that time had almost completely replaced by numer CASE 6: LIP AND PALATAL also been reported as sarcoid deposits. ous, non-caseating granulomas consist SWELLING Further similar deposits had also been ent with a diagnosis of sarcoidosis. She A 43-year-old African lady was referred removed from above the anterior com was referred to a chest physician who to the oral medicine department with a missure in the supraglottis. Recent lung found no evidence of chest involvement. recurrence of a swelling on the upper function tests were within normal limits In view of the absence of any symptoms lip. This was causing her considerable although CT scan had shown extensive or extra-oral involvement no treatment social embarrassment and occasional mediastinal lymphadenopathy but lit was commenced. discomfort when eating. She had had tle in the way of parenchymal changes. Five years later she developed short a nodule surgically excised from the She had at no stage been given systemic ness of breath and a chest X-ray showed same site one year earlier which had therapy for the sarcoidosis. her to have bilateral hilar lymphadenop been confirmed as sarcoidosis. A further On examination she had a scar on the athy. In view of this she was diagnosed upper lip nodule had been treated with upper lip at the site of the previous exci-

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sion. There were two distinct nodules Oral involvement may be the initial include chloroquine and hydroxychlo affecting the upper lip, swelling of the manifestation of the sarcoidosis.6-8 In one roquine,19 methotrexate,20 azathioprine,21 midline of the lower lip and a further of the cases described in this series the pentoxyfylline,22 and thalidomide.23 Inf swelling of the soft palate (Fig. 5). Due diagnosis of oral sarcoidosis preceded liximab, a monoclonal antibody targeted to the position of the upper lip swell the need for systemic treatment for pul against TNF α has been found to be help ings and the patient’s wishes to avoid monary involvement by fi ve years. ful in refractory sarcoidosis.24,25 further scarring they were treated with The diagnosis of sarcoidosis is estab Orofacial sarcoidosis may require no intralesional triamcinolone, resulting in lished by the presence of clinical features treatment but cases requiring treat a reduction of their size. No treatment combined with the supporting his ment frequently respond to corticoster was considered necessary for the swell topathological finding of non caseating oid therapy which may be administered ings of the lower lip or soft palate. At the granulomas.1 Serum ACE may be raised in intralesionally or systemically. In some present time we are awaiting her review active sarcoidosis as this enzyme is pro cases surgical excision of granuloma six months after this procedure to assess duced by granulomas. However the level tous swellings may be required.26 Sim if repeat injection or further interven of this enzyme is only raised in 50-80% ple symptomatic treatment to stimulate tion is required. of patients with sarcoidosis.16,17 In the or replace saliva may help in cases second case presented in this paper the of xerostomia. DISCUSSION serum ACE was initially within normal Orofacial presentations of sarcoido Oral involvement in sarcoidosis is rare. limits but later became raised with the sis are rare. It is, however, important A recent review of the English literature progression of the condition. The meas that the wide range of presentations of found only 68 well-documented cases urement of this enzyme may be useful sarcoidosis in the orofacial region are of oral sarcoidosis.9 Of these 39 cases in monitoring the response to treatment. recognised as they may indicate the were female and 25 were male with the A biopsy of affected tissue should be presence or future development of sys data being incomplete in the other four performed as the demonstration of non temic involvement and the need for sys cases. The jaws were affected in 21 cases caseating granulomas strongly supports temic therapy. (maxilla nine, mandible eight, maxilla the diagnosis of sarcoidosis, although The authors would like to thank Professor S. J. and mandible four). Presenting features other granulomatous conditions such as Challacombe and Dr P. J. Shirlaw for permission in these cases were loosening of the tuberculosis, orofacial granulomatosis, to present their cases. teeth, pain, nasal obstruction, swelling foreign body reactions and deep seated 1. Baughman R, Lower E E, Du Bois R M. Sarcoidosis. of the mandible, maxillary bone loss and fungal infections need to be excluded. Lancet 2003; 61: 1111-1118. non-healing socket. The soft tissues of In cases of orofacial sarcoidosis refer 2. Thomas K W, Hinninghake G W. Sarcoidosis. JAMA 2003; 289: 3300-3303. the oral cavity were affected in 47 cases, ral for chest and ophthalmological 3. Gribbin J, Hubbard R, Le Jeune I, Smith C J P et al. Incidence and mortality of idiopathic pulmonary with the buccal mucosa being the most assessment is important. A chest X-ray fibrosis and sarcoidosis in the UK. Thorax Epub commonly affected soft tissue site. The should also be performed to investigate 2006 July 14. 4. Rybicki B A, Major M, Popovich J Jr, Maliarik M common clinical presentations were for the presence of hilar lymphadenopa J, Iannuzzi M C. Racial differences in sarcoidosis localised swellings or nodules, ulcers, thy. The involvement of other speciali incidence: a 5-year study in a health maintenance organization. Am J Epidemiol 1997; 145: 234-241. gingivitis, gingival hyperplasia and ties may be indicated by clinical features 5. Du Bois R M, Goh N, McGrath P, Cullivan P. Is there gingival recession. Soft tissue involve and investigation results. Other imaging a role for microorganisms in the pathogenesis of sarcoidosis? J Int Med 2003; 253: 4-17. ment of the oral cavity presented as a techniques may be useful in the diag 6. Blinder D, Yahatom R, Taicher S, Hashomer T. Oral firm swelling affecting the lips, gingi nosis of sarcoidosis. CT may demon manifestations of sarcoidosis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1997; 83: 458-461. vae, fl oor of mouth, tongue, hard or soft strate the presence of mediastinal and 7. Fatahzadeh M, Rinaggio J. Diagnosis of systemic palate, buccal mucosa and vestibule. hilar lymphadenopathy and pulmonary sarcoidosis prompted by orofacial manifestations. J Am Dent Assoc 2006; 137: 54-60. Salivary gland involvement has also or neurological involvement. Magnetic 8. Jackowski J, Dragistic D, Arnold G, Dirschka T. been reported with sarcoidosis present resonance imaging (MRI) may show Primary oral sarcoidosis preceding Lofgren’s syn 10,11 drome. Oral Surg Oral Med Oral Pathol Oral Radiol ing as swelling of the parotid glands, organ involvement including neurologi Endod 2005; 100: 183-185. submandibular glands11 and xerostomia.12 cal, muscle and bone disease. Contrast 9. Suresh L, Radfar L. Oral sarcoidosis: a review of literature. Oral Dis 2005; 11: 138-145. A recent case report describes a case of enhancement with gadolinium improves 10. Nitzan D W, Shteyer A. Sarcoidosis of the parotid sarcoidosis presenting with xerostomia, the sensitivity of the technique. Positron salivary glands. J Oral Maxillofac Surg 1982; 40: 443-446. dysgeusia, oral burning, xerophthalmia emission tomography (PET) scanning 11. Vairaktaris E, Vassiliou S, Yapijakis C, Papakosta V and bilateral swelling.7 Heerfordt’s syn with markers has also been used.1,18 et al. Salivary gland manifestations of sarcoidosis: report of three cases. J Oral Maxillofac Surg 2005; drome is a form of systemic sarcoidosis Treatment of sarcoidosis may range 63: 1016-1021. characterised by swelling of the parotid from observation in asymptomatic or 12. Chisholm D M, Lyell A, Haroon T S, Mason D K, 13 Beeley J A. Salivary gland function in Sarcoidosis. glands, uveitis and facial nerve palsy. mild disease to systemic corticosteroid Report of a case. Oral Surg Oral Med Oral Pathol Involvement of the minor salivary therapy in more severe cases. Systemic 1971; 31: 766-771. 13. Bopp F P, Cheney M L, Donzis P B, White J A, Reed glands in patients with sarcoidosis has therapy is particularly needed for patients H T. Heerfordt syndrome: a cause of facial paraly been reported to range from 19-58%14 with neurological or ocular involvement sis. J La State Med Soc 1990; 142: 13-15. 14. Nessan V J, Jacoway J R. Biopsy of minor salivary and may help differentiate sarcoidosis or progressive respiratory disease. Ster glands in the diagnosis of sarcoidosis. N Engl J Med from Sjögren’s syndrome.15 oid sparing agents used for sarcoidosis 1979; 301: 922-924.

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15. Giotaki H, Constantopoulus S H, Papadimimitriou statin receptor scintigraphy and gallium scintigra- 22. Zabel P, Entzian P, Dalhoff K, Schlaak M. Pentoxi- C S, Moutsopoulos H M. Labial minor salivary phy in patients with sarcoidosis. J Nucl Med 2001; fylline in treatment of sarcoidosis. Am J Respir Crit gland biopsy: a highly discriminatory diagnostic 42: 21-26. Care Med 1997; 155: 1665-1669. method between sarcoidosis and Sjögren’s syn- 19. Sharma O P. Effectiveness of chloroquine and 23. Baughman R P, Judson M A, Teirstein A S, Moller D drome. Respiration 1986; 50: 102-107. hydroxychloroquine in treating selected patients R, Lower E E. Thalidomide for chronic sarcoidosis. 16. Turton C W, Grundy E, Firth G, Rigden B G, Smyth with sarcoidosis with neurologic involvement. Arch Chest 2002; 122: 227-232. J T, Turner-Warwick M. Value of measuring angi Neurol 1998; 55: 1248-1254. 24. Baughman R P, Lower E E. Inﬂiximab for refractory otensin I converting enzyme and serum lysozyme 20. Lower E E, Baughman R P. Prolonged use of meth sarcoidosis. Sarcoidosis Vasc Diffuse Lung Dis in the management of sarcoidosis. Thorax 1979; otrexate for sarcoidosis. Arch Intern Med 1995; 2001; 18: 70-74. 34: 57-62. 155: 846-851. 25. Doty J D, Mazur J E, Judson M A. Treatment of 17. Khan A H, Ghani F, Khan A, Khan M A, Khurshid M. 21. Muller-Quernheim J, Kienast K, Held M, Pfeifer S, sarcoidoisis with inﬂ iximab. Chest 2005; Role of serum angiotensin converting enzyme in Costabel U. Treatment of chronic sarcoidosis with 127: 1064-1071. sarcoidosis. J Pak Med Assoc 1998; 48: 131-133. an azathioprine/prednisolone regimen. Eur Respir J 26. Steinberg M J, Mueller D P. Treating oral sarcoido 18. Lebtahi R, Crestani B, Belmatoug N et al. Somato 1999; 14: 1117-1122. sis. J Am Dent Assoc 1994; 125: 76-79.

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