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pyrig No Co t fo rP Focal Osteoporotic Hematopoietic Bone Marrow ub lica tio Defect Formation Around a Dental Implant:te n ss e n c e
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A Case Report
Metin S¸ençimen, DDS, PhD1/Cagri Delilbasi, DDS, PhD2/Aydin Gülses, DDS3/Kemal Murat Okçu, DDS, PhD1/Omer Gunhan, DDS, PhD4/Altan Varol, DDS, PhD5
Focal osteoporotic bone marrow defects usually appear as asymptomatic radioluencies in the edentulous posterior mandible of middle-aged women. The exact causative factor in the majority of focal osteoporotic bone marrow defects is still unknown. Because of their radiological similarity with many intraosseous lesions, accurate diagnosis is possible only with histopathological examination. A focal osteoporotic bone marrow defect that occurred 2 years postoperatively apical to an implant is presented with clinical, radiographic, and histopathologic features. According to the literature scan, this is the first case report of this phenomenon caused by a dental implant. Int J Oral Maxillofac Implants 2011;26:e1–e4
Key words: bone marrow, defect, dental implant, hematopoietic, hemoglobin h
F
ocal osteoporotic bone marrow defects (FOBMDs) of the jaws are asymptomatic radiolucent lesions that are most commonly located in the molar area of middle-aged women.1–3 These poorly demarcated lesions are usually discovered incidentally during routine radiographic examination and rarely mentioned
1 Associate
Professor, Department of Oral and Maxillofacial Surgery, Gülhane Military Medical Academy, Ankara, Turkey. 2 Associate Professor, Faculty of Dentistry, Department of Oral and Maxillofacial Surgery, Yeditepe University, I˙stanbul, Turkey. 3Senior Resident, Department of Oral and Maxillofacial Surgery, Gülhane Military Medical Academy, Ankara, Turkey. 4Professor, Department of Pathology, Gülhane Military Medical Academy, Ankara, Turkey. 5Specialist, Faculty of Dentistry, Department of Oral and Maxillofacial Surgery, Marmara University, I˙stanbul, Turkey. Correspondence to: Dr Aydın Gulses, Gülhane Military Medical Academy (GATA), Dental Sciences Center, Department of Oral and Maxillofacial Surgery, 06018 Etlik Ankara, Turkey. Fax: 903123046020. Email:
[email protected]
in differential diagnosis of radiolucent lesions of the jaws.1 Radiographically, the appearance of the lesion can vary from well-defined radioluencies with distinct sclerotic borders to ill-defined areas with irregular borders.2 Histologically, the lesion consists of haematopoietic or, less commonly, fatty marrow.1–3 The causative factor in the majority of FOBMDs is still unknown. The presence of disease that results in marrow hyperplasia from increased demands for red blood cell production, such as chronic anemia, is one of the theories proposed to explain the pathogenesis.3–5 Most lesions occur at former extraction sites.6 Although FOBMD requires no treatment,7,8 it is reasonable to obtain proper diagnosis to avoid needless surgical attempts, such as aggressive curettage in cystectomy with or without peripheral osteoctomy, which may result in the loss of a great amount of vital tissue. This is the first reported case of a FOBMD occurring secondary to dental implant placement. Since the etiology of the phenomenon is unique and specific, the case is presented in detail with clinical, radiographic, and histopathological features. The International Journal of Oral & Maxillofacial Implants e1
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Fig 2 The periapical radiograph revealed the presence of an extensive and poorly circumscribed osteoporosic area around the proximal implant. Fig 3 No pathology was found on the radiographs taken before implant placement in 2007.
CASE REPORT A 35-year-old woman was referred to the Gülhane Military Medical Academy, Department of Oral and Maxillofacial Surgery, in May 2009 for routine follow-up of her implant-supported prosthesis. In 2007, the patient underwent bilateral placement of two dental implants in the mandibular posterior regions. In 2004, the patient had extraction of the right and left mandibular second premolars and the first and second molars due to chronic periodontal disease. Her medical history revealed numerous hospital admissions because of signs and symptoms of hemoglobin H (HbH) disease, including paleness and jaundice. The preoperative blood screening revealed a low hemoglobin (Hgb) level. Relevant blood investigations at the follow-up were included: Hgb, 9.1 g/dL; PCV findings were normal. During the second-year routine follow-up, the panoramic (Fig 1) and the periapical (Fig 2) radiographs demonstrated an extensive and poorly circumscribed osteolytic area that was invading mostly the distal part e2 Volume 26, Number 1, 2011
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Fig 1 The OPTG showed an ill-defined radiolucency on the right side of the mandible.
of the posterior implant at the right side of the mandible with the coronoapical and mesiodistal dimensions of 8 ± 0.5 mm and 13 ± 0.5 mm. Comparison with previous radiographs demonstrated no such lesion (Fig 3). No extraoral abnormalities were detected during physical examination. No pathologic alterations or symptoms of infection at the affected site were apparent. There was no expansion of the buccal or lingual cortical plates in the region of the right body of the mandible. Periodontal tissues in the area were healthy with no evidence of disease. The dental implant was stable and functioning perfectly. The peri-implant sulcular depth measured 2.4 to 3.6 mm with a periodontal probe. An aspiration needle biopsy was attempted but cortical penetration was not possible. Consequently, it was decided to perform an excisional biopsy. A horizontal-semilunar incision was made 10 mm apical to the gingival margin and a mucoperiostal flap was elevated to preserve the attached gingiva. No cortical thinning or erosion was observed at the site of the lesion. A bony window was created via a 5-mm
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Fig 4 Hypercellular bone marrow in the hematoxylin-eosin stained specimen (HE; ×400)
Fig 5 Immunohistochemical stain of glycophorine A-marked groups of hyperplastic erythroid precursors among other myeloid elements (arrows). (Glycophorine, streptovidine-biotine peroxidase; ×400.)
trephine drill and an empty cavity was found in the cancellous bone. A brown-red layer of tissue was lining the cavity. Several small, fat-like pieces of tissue were removed and the cavity was totally curetted; the specimen was fixated in 10% formalin and submitted for histopathologic examination. The pathology report affirmed that the specimen consisted of hypercellular bone marrow (Fig 4). The examined specimen was particularly rich from erythroid precursors which were marked with glycophorine A (1:400, Neomarkers). Other myeloid elements were also observed with some lymphoid follicles (Fig 5). The ratio of fat cells to haematopoietic elements was greatly decreased (10/90). The diagnosis of focal osteoporotic bone marrow defect was rendered. The biopsy site healed without complications.
A traumatic bone cyst (TBC) was considered as a differential diagnosis in the current case. The characteristics of a TBC include occasional trauma history as a predisposing factor, irregularly shaped but welldefined and rarely symptomatic radiolucent appearance, and location at the posterior mandible. However, the biopsy discarded the possibility of a TBC. Barker et al1 reviewed a series of 197 cases of FOBMD in jaws, documenting only two cases of FOBMD with anemia. The series of Barker demonstrated similarity in etiology. Additionally, in the same study, history of teeth extractions at the affected site was detected in 46 cases. In patients with HbH disease, a thalassemia of intermediate severity may be symptomatic and may have secondary complications of hemolytic anemia. Patients with the HbH disease can generally have moderate to severe anemia, with low hemoglobin levels of 7 to 10 g/dL. In HbH disease, three of the four α-globin genes are affected, characterized by microcytic, hypochromic, and hemolytic anemia that is frequently associated with hepatosplenomegaly and mild jaundice.11 Folic acid deficiency may also occur. After placement of an endosseous implant into jaw bone, a cascade of healing reactions inhabits the soft and hard tissues. The process may cause lowgrade inflammation that could be affected by the hyperactivity of the bone marrow. The proliferation of hematopoietic marrow elements around the dental implant may be a response of the healing spongious bone to surgically initiated trauma which may occur due to overheating of bone or peri-implant bone compression at the implant osteotomy site by drilling a narrower osteotomy.
DISCUSSION Based on clinical and radiographic symptoms, it is difficult to diagnose a FOBMD.9 In the case presented, there are characteristics similar to previous studies and reports regarding sex, age, and location.1–3,10 The radiographic observations of the patient were also consistent with the previous reports.1 The differential diagnosis of these lesions includes osteomyelitis, fibrous dysplasia, and traumatic bone cyst.10 Additionally, characteristics of multilocular appearances are similar to ameloblastoma or calcifying, epithelial odontogenic tumors.2 Indistinct margins and ill-defined trabeculation characteristics of these lesions can also cause confusion in many FOBMD cases with aggressive tumors.7
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6. 7.
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10. 11.
defect of the jaws: A report of sixteen cases. J Oral Pathol 1982;11:411–416. Gordy FM, Crews KM, O’Carroll MK. Focal osteoporotic bone marrow defect in the anterior maxilla. Oral Surg Oral Med Oral Pathol 1993;76:537–542. Wilson DF, D’Rozario R, Bosanquet A. Focal osteoporotic bone marrow defect. Aust Dent J 1985;30:77–80. Sanner JR, Ramin JE. Osteoporotic, hematopoietic mandibular marrow defect: An osseous manifestation of sickle cell anemia. J Oral Surg 1977;35:986–988. Neville BW, Dam DD, Allen CM, Bouquot JE. Oral and maxillofacial pathology, ed 2. Philadelphia: Saunders, 2002:539–540. Schneider LC, Mesa ML, Fraenkel D. Osteoporotic bone marrow defect: Radiographic features and pathogenic factors. Oral Surg Oral Med Oral Pathol 1988;65:127–129. Sa’do B, Ozeki S, Higuchi Y, Nakayama E. Osteoporotic bone marrow defect of the mandible: Report of a case diagnosed by computed tomography scanning. J Oral Maxillofac Surg 1992;50:80–82. Marmulla R, Mühling J. Verification of extensive bone marrow hyperplasia using magnetic resonance imaging. J Oral Maxillofac Surg 2007;65:1590–1594. Crawford BE, Weathers DR. Osteoporotic marrow defects of the jaws. J Oral Surg 1970; 28:600–603. Laosombat V, Viprakasit V, Chotsampancharoen T, et al. Clinical features and molecular analysis in Thai patients with HbH disease. Ann Hematol 2009;88:1185–1192.
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The periapical radiograph (Fig 1) clearly showed that the placement of the anterior implant at the right side of the mandible caused minimal apical resection of the adjacent tooth. This complication should not be considered as an etiologic factor. If any pathology occurred after resection of the adjacent tooth, the microscopic examination would disclose a population of inflammatory cells or granulation tissue instead of bone marrow cells. Furthermore, the location of the lesion would not be distal to the posterior implant but would be located at the periapical site of the first premolar. In conclusion, asymptomatic radiolucency, with either distinct or ill-defined borders, located in the edentulous posterior mandible of middle-aged women should suggest the existence of FOBMD. Implant candidates with chronic anemia should be approached cautiously with complete blood screening preoperatively, and long-term follow-ups should be assessed.
pyrig No Co t fo REFERENCES rP ub lica 1. Barker BF, Jensen JL, Howell FV. Focal osteoporotic bone tio marrow defects of the jaws. An analysis of 197 new cases. n t e Oral Surg Oral Med Oral Pathol 1974;38:404–413. ss e n c e 2. Lipani CS, Natiella JR, Greene GW Jr. The hematopoietic