Prosthetic Rehabilitation of a Patient Diagnosed With Sarcoidosis Using Dental Implants: A Clinical Case Report

Sarcoidosis is a granulomatous disorder of unknown etiology that can affect multiple organ systems.¹  It is characterized by the formation of noncaseating granulomata, and although 20% of sufferers are asymptomatic, there is a 4% to 10% fatality rate due to pulmonary, cardiac, or central nervous system complications.²  The incidence of sarcoidosis ranges from 15 to 53 cases/100 000 and is higher among women³  and those of Afro-Caribbean decent.¹  The peak age is 20 to 40 years, with a second peak occurring in individuals older than 50 years.^2,4 

The pathogenesis of sarcoidosis is an uncontrolled and upregulated local cell-mediated immune response against an unknown “sarcoidal antigen.” The affected tissues are infiltrated by lymphocytes, monocytes, and macrophages, which secrete biological mediators (interleukin-2, interleukin-12, interferon-c, and tumor necrosis factor–α) that in turn induce the formation of noncaseating granulomata.⁵  Several infectious agents^6–10  and environmental agents¹¹  have been implicated; however, certain genetic polymorphisms are also involved,¹²  and these complex interactions likely influence the clinical manifestation, natural course, and response to treatment.¹³ 

The disease may have an acute or chronic nature with general symptoms of dry cough, dyspnea and chest discomfort, fever, fatigue, anorexia, weight loss, polyarthritis, visual problems, and skin lesions; the latter frequently occur on the face.²  The skeletal system is affected in up to 39% of patients, with intraosseous lesions commonly involving the phalanges, metatarsals, and metacarpals.^2,14  The head and neck region is affected in 10% to 15% of all cases of sarcoidosis, with the parotid salivary glands most commonly affected (3–4%¹⁵), resulting in enlargement and xerostomia, as well as the lacrimal glands, which may result in keratoconjunctivitis sicca. Sixty percent of minor salivary glands show noncaseating granulomata on biopsy in patients affected by sarcoidosis.^2,16,17 

The diagnosis of sarcoidosis is usually established with a combination of clinical and histopathological features, but for many patients, systemic treatment is not necessary.¹⁸  Patients with symptoms are generally managed with corticosteroids,¹⁹  but alternative and adjunctive treatments for chronic or refractory disease include chloroquine, hydroxychloroquine, methotrexate, azathioprine, pentoxifylline, thalidomide, cyclophosphamide, cyclosporine, and inFLIXimab.¹ 

The aim of this article is to report on the rehabilitation of a patient, diagnosed with sarcoidosis, with a dental implant–supported prosthesis. The assessment, preprosthetic surgery, implant placement, restoration, and follow-up are described.

A 31-year-old female patient was referred to the Department of Restorative Dentistry of the Royal London Dental Hospital by her general dental practitioner for rehabilitation of the missing maxillary left central incisor (tooth 9) in March 2011 as she was unhappy with her current removable partial dental prosthesis.

She reported a history of an ectopic tooth No. 9, which was surgically exposed and bonded for orthodontic traction at the age of 10 years. The root underwent resorption, and the tooth was extracted at the age of 14. She had noticed a significant change in the alveolus around region No. 9 and was now also complaining of increased mobility in the maxillary left lateral incisor (tooth No. 10). The patient had been diagnosed with pulmonary sarcoidosis in January 2010 but was not undergoing active treatment. She was a nonsmoker and took no prescribed medications.

Clinical examination (Figure 1) revealed a minimally restored dentition, a medium smile line, and thin gingival biotype. Tooth No. 10 was diminutive, grade 2 mobile, had 4-mm labial and 8-mm mesial gingival recession, and tested positive to sensibility testing. The edentulous region of No. 9 was wider than that of the maxillary right central incisor (tooth No. 8), and there was severe vertical and horizontal alveolar ridge deficiency in No. 9 region. Tooth No. 8 was of normal proportions with 2-mm mesial gingival recession. The maxillary left canine (tooth No. 11) was missing at the time of assessment, and the patient did not recall why. An acrylic tissue-supported partial removable dental prosthesis replaced tooth No. 9; the prosthetic tooth was 2-mm shorter than that of tooth No. 8 and had a large pink acrylic flange replacing the missing hard and soft tissues.

Periapical radiographs (Figure 2), an orthopantomograph (Figure 3), and cone-beam computerized tomography (CBCT; Figure 4) were taken, which showed root resorption of tooth No. 10 and the maxillary left first premolar (No. 12) and evidence of an abnormal bone pattern in the anterior maxilla extending from the midline to tooth No. 12. This abnormal region had loss of definition of the cancellous bone and loss of the outline of both the buccal and palatal cortices. When reviewed by a consultant oral and maxillofacial radiologist, the appearance was considered to be consistent with previously described osteolytic areas affected by a sarcoidal process.^2,17 

A bone biopsy from region No. 9 was carried out by the Department of Oral Surgery, which, following histopathologic analysis, confirmed nonnecrotizing granulomatous inflammation indicating sarcoid changes in the maxillary bone.

The prognosis for tooth No. 10 was considered hopeless, and therefore it was extracted and the patient provided with a provisional metal-ceramic fixed resin-bonded dental prosthesis (RBP) replacing teeth Nos. 9 and 10, with teeth Nos. 8 and 12 as abutments (Figure 5).

Two months later, staged bone augmentation surgery was carried out (Figure 6). Cortico-cancellous bone allografts (RM·BB, Rocky Mountain Tissue Bank, Aurora, Colo) were used for vertical and horizontal augmentation of regions No. 9 and 10, with the 2 interproximal bone peaks at teeth Nos. 8 and 12 used as the vertical limit for the augmentation. The blocks were soaked for 10 minutes in an rhPDGF growth factor (Gem 21S, Osteohealth Company, Luitpold Pharmaceuticals, Shirley, NY) before stabilization with bone fixation screws. The overlying flap was deficient when attempting primary closure owing to the substantial increase in the horizontal and vertical dimension. Consequently, a porcine soft-tissue matrix (Geistlich Mucograft, Geistlich, Wolhusen, Switzerland) was used palatally in anticipation of possible flap dehiscence during healing. The flaps were approximated using a single horizontal mattress and multiple single interrupted sutures using 5-0 and 6-0 nylon and polytetrafluoroethylene sutures.

The patient was prescribed co-amoxiclav 3 times per day (TDS) for 7 days, ibuprofen 400 mg TDS for 7 days, chlorhexidine 0.2% mouth rinse 4 times per day (QDS), and dexamethasone 10 mg, 8 mg, 6 mg, and 4 mg as a tapering daily dose. The provisional RBP was adjusted and recemented. As anticipated, flap dehiscence was noted 2 weeks later along the palatal edge of the flap, exposing the underlying soft-tissue matrix (Figure 7). However, the matrix healed uneventfully with full epithelialization during the ensuing 10 days.

After 5 months of healing time, the CBCT scan was repeated to confirm the volume of augmented bone (Figure 8). The bone width and height allowed planning of 2 implant fixtures (Straumann, Institut Straumann AG, Basel, Switzerland) to replace teeth Nos. 9 and 10 (Figure 9).

In April 2013, implant placement was carried out 6 months after augmentation (Figure 10). Buccal and vertical graft resorption was noted; nevertheless, sufficient bone volume was maintained for implant placement in a prosthetically acceptable position despite preoperative severe ridge atrophy.

The implants were placed 3 mm more apically than usual (6 mm from the gingival zenith of the adjacent tooth No. 8) to mitigate the possible risk from resorption of the vertically augmented site; the prosthetic outcome of longer clinical crowns had already been discussed with the patient. Bone-level implants (4.1-mm diameter, 10-mm long in region No. 9, and 3.3-mm diameter, 10-mm long in region No. 10) were placed, but crestal dehiscences on both implants and a fenestration in the region 9 implant were encountered; thus, simultaneous guided bone regeneration with deproteinized bovine bone (Geistlich BioOss, Geislich, Wolhusen, Switzerland) and porcine collagen membrane was performed. Tension-free primary closure was achieved with monofilament nylon sutures (Seralon, Serag-Wiessner, Naila, Germany).

Amoxicillin 500 mg TDS for 5 days and ibuprofen 400 mg TDS for 5 days were prescribed along with chlorhexidine 0.2% mouth rinse QDS. The provisional RBP was again adjusted and recemented.

A periapical radiograph taken 3 months after surgery and prior to implant exposure surgery confirmed the position of implants in relation to the prosthetic plan and alveolar bone above the level of implant shoulder (Figure 11).

Because of extensive coronal repositioning of the flap during the 2 surgeries and the extent of vertical augmentation necessary, sulcus deepening was carried out 3 months after implant placement (Figure 12). A split-thickness flap was raised and apically relocated, and a soft-tissue allograft (AlloDerm Regenerative Tissue Matrix, Acelity, San Antonio, Tex) was rehydrated in saline and cut to size to cover the exposed connective tissue bed. The provisional RBP was recemented.

Subsequently, the patient became pregnant and decided to defer further treatment until after the birth of her child, and so implant exposure surgery was delayed until October 2014 (Figure 13).

Provisional composite resin screw-retained implant crowns were placed and adjusted during 3 subsequent appointments to modify the soft-tissue emergence profile (Figure 14). As anticipated, the implant clinical crowns were longer than the adjacent teeth with deficient interimplant papilla. A periapical radiograph showed the provisional crowns in situ and bone remodeling at the implant-abutment junction (Figure 15).

After a 6-month provisionalization period, definitive screw-retained linked crowns made from a milled cobalt chromium framework veneered with ceramic were fabricated with pink colored ceramic used on the cervical part of the prosthesis to conceal the interimplant papillary deficiency (Figure 16). A periapical radiograph (Figure 17) taken following definitive restoration showed well-maintained peri-implant bone levels, and the bone trabeculation appeared normal.

During the most recent follow-up appointment, 4 years after staged bone augmentation and implant placement, the bone levels remain stable (Figure 18), and the patient remains satisfied with the esthetic and functional outcome.

Seventy-four cases of oral sarcoidosis have been reported in the literature,^{16,17,20–23}  with a female-to-male ratio of 1.5:1, a slight racial predilection to Caucasians, and ages ranging from 5 to 72 years (median, 37 years).²⁰  Oral soft-tissue lesions have been reported as one of the first manifestations of systemic sarcoidosis,^16,20,22,23  with the buccal mucosa being the most commonly affected site followed by the gingiva, lips, floor of the mouth, sublingual glands, tongue, palate, and submandibular gland.^16,17,20,22 

The common clinical presentation is an asymptomatic localized submucosal swelling and well-circumscribed brown-red or violaceous papule, nodule, or finely granular macule. This makes the case reported unusual in that there were no visible changes to the oral mucosa. Other presentations include ulcers (which may become secondarily infected and symptomatic), fistulae, gingival inflammation, hyperplasia, and recession.^{2,16,17,20,22,24–26} 

As in the case presented, the maxilla and mandible may be involved,^{20,21,22,23,25–29}  with a higher incidence in the anterior maxilla and posterior mandible.²⁰  Clinical manifestations of osseous involvement include loose teeth, pain radiating to the ears, and swelling. Nasal obstruction, nonhealing sockets, paresthesia, facial palsy, and a foul taste are also described.^{16,20–23,26,27,29,30}  Radiographically, these lesions appear as ill-defined radiolucencies that occasionally erode the cortex but do not cause expansion^2,17 ; however, in rare cases, they may cause extensive destruction of the midface.³¹ 

Up to 60% of orofacial lesions spontaneously resolve within 2 years. Symptomatic or progressing cases frequently respond to corticosteroid therapy, which may be administered intralesionally or systemically.^2,16  Surgical excision of granulomatous swellings may be required,¹⁶  especially for intraosseous lesions such as in this case, which respond well to excision or curettage.^22,23,28,29  Combined surgical and medical management has been described,²⁵  as has extraction,²⁶  splinting²⁷  of mobile teeth, and even radiotherapy.³⁰ 

There have been no previous published accounts of the placement of dental implants in a patient diagnosed with sarcoidosis. Moretti et al²¹  described the management of a patient treated for peri-implantitis who presented with implants already placed into an iliac crest bone graft replacing teeth lost due to sarcoidosis affecting the periodontium. After periodontal treatment and over the 6-year follow-up described, during which the patient had 2 exacerbations of sarcoidosis both systemically and intraorally requiring steroid treatment, the implants lost 30%–50% of their bone support. This was despite the patient maintaining excellent oral hygiene and having 3–4 monthly maintenance visits at a postgraduate periodontal center.

Others have reported a diagnosis of periodontitis as a manifestation of systemic disease with regard to sarcoidosis, which is often rapidly progressing.^14,24,29,32  Most confirmed the presence of a sarcoid process occurring in the periodontal tissues by histopathology.^14,24,29  It seems plausible that this process could just as easily affect the peri-implant tissues as the periodontal ones, and therefore, the increased risk of peri-implantitis must be considered, discussed with the patient before treatment, and factored into any maintenance program.

As sarcoidosis is considered by some to be a foreign-body reaction, there may be concerns about the safety of implantation of a foreign material. Exposure to environmental titanium has been associated with increased risk of developing sarcoidosis, although this was by inhalation rather than implantation,¹⁷  with occupational exposure to titanium increasing the risk 3-fold (odds ratio, 3.15; 95% confidence interval, 1.02–9.68), although the sample in this study was only 8 affected subjects and 5 control subjects.³³ 

Patients who require systemic therapy for the management of their disease are likely to be taking corticosteroids,¹⁹  antimalarial agents, and immunosuppressants,¹  and while there are no specific reports on the effects of medication for sarcoidosis on dental implant treatment, there is literature on the general effects of corticosteroids and immunosuppressants on dental implants. Animal studies^34–36  have shown a reduced removal torque of implants placed in the tibiae of rabbits given prednisolone, cyclosporin, and a combination of cyclosporin and nifedipine. One of these studies also placed implants in the rabbit's mandibles and found no difference in removal torque between those given prednisolone and the control animals, concluding that corticosteroids may not have such a significant effect on bone density and osseointegration in mandibular bone as they do in skeletal long bones.³⁴  These studies must be interpreted carefully.

A case series reporting on the placement of dental implants in patients taking immunosuppressive medications following organ transplant reported that patients showed excellent results at 3 years³⁷ ; however, a single patient followed up for 10 years had moderate vertical bone loss.³⁸  Moy et al³⁹  published retrospective data on the treatment of 1140 patients over a 21-year period, 78 of whom were taking corticosteroids, and no significant difference was found in the failure rate between those taking steroids and the rest of the cohort. To summarize, a review by Diz et al⁴⁰  concluded that no convincing evidence has been published to demonstrate an increased dental implant failure rate in patients taking systemic corticosteroids or immunosuppression therapy.

This case has shown another example of how sarcoidosis can affect the bones of the head and neck and the effects this can have on the periodontium. Based on assessment and radiographic and histopathologic investigations, multiple rehabilitation options may be considered; any patient's suitability for these options must take into account the current activity status of the patient's sarcoidal process and any systemic therapies being employed.

Block allograft hard-tissue augmentation followed by implant placement with simultaneous guided bone regeneration and soft-tissue augmentation were successfully undertaken in this case; our outcome and follow-up results after 4 years show that the rehabilitation was successful, at least in the short term. Longer-term follow-up and studies with greater patient numbers are required to provide stronger evidence on this treatment modality in this patient group; however, recruiting a desirable number of patients is unlikely to be possible, and in such circumstances, low-level evidence in the form of case reports is of some benefit.

Abbreviations

CBCT:

cone-beam computerized tomography

QDS:

4 times per day

RBP:

resin-bonded prosthesis

TDS:

3 times per day

The authors thank Dr Jimmy Makdissi, Senior Clinical Lecturer and Honorary Consultant in Oral and Maxillofacial Radiology.

Martin James, Jay Matani, and Shakeel Shahdad declare no competing interests relevant to this article.