Dr. Bouquot, Oral Injuries Fall, 2011 Residual (ghost) Sockets Radiographic features & histopathology of poor healing in 76 cases J.E. Bouquot,* W.P. Glaros,** S. Zarghouni * * University of Texas, Houston ** Private Practice, Houston, Texas Dr. J. E. Bouquot, Professor & Chair Department of Diagnostic Sciences. Room 3.094b University of Texas School of Dentistry 6516 M.D. Anderson Blvd., Houston, TX 77030 713-500-4420; Jerry.Bouquot@uth.tmc.edu; bouquot@aol.com

Residual sockets Background © Photo(s): Dr. J.E. Bouquot, University of Texas, Houston,: presented at AAOM annual meeting, 2012 Residual sockets Background When a tooth is extracted a great deal happens: PDL necrosis Lamina dura disappears New crestal cortex forms Mucosa covers defect Inflammation/granulation tissue Blood vessels heal Fibroplasia Nerves regenerate/heal Socket fills with new bone -- Starts from periphery New bone remodels But does it?

Residual sockets Background © Photo(s): Dr. J.E. Bouquot, University of Texas, Houston,: presented at AAOM annual meeting, 2012 Residual sockets Background Alveolar bone remodels after extraction to accommodate altered physiologic stresses Result: loss of socket outline in 3-9 months However: outlines of poorly remodeled or residual (ghost) sockets are not uncommon in patients, even decades after extraction Very few have explanatory disease or meds Remain indefinitely? Probably Laminar rain

Residual sockets Background © Photo(s): Dr. J.E. Bouquot, University of Texas, Houston,: presented at AAOM annual meeting, 2012 Residual sockets Background 1850s: Poor healing of sockets in phosphorus toxicity (“phossy jaw”) 1860s; chronic osteitis (ischemic bone disease) 1952: Box: 1,120 hollow 3rd molar sockets 2003: BRONJ in metastatic cancer -- Bisphosphonates (Zometa, Aredia) -- Poor healing of sockets -- Chronically exposed bone, pain -- Micro = acute osteomyelitis -- Considerable interest in bone physiology, healing, bone turnover, etc. Phossy jaw, circa 1860 BRONJ (above photos = same patient)

Residual sockets Background © Photo(s): Dr. J.E. Bouquot, University of Texas, Houston,: presented at AAOM annual meeting, 2012 Residual sockets Background 2006: BRONJ in osteoporosis (Fosamax, etc.) 2007: First report of BRONJ-like exposed alveolar bone * 2009: 1st report of BRONJ (Zometa Rx for breast cancer) with numerous residual sockets remaining after 18 months ** No characterization yet of residual sockets BRONJ-like osteonecrosis, unknown etiology BRONJ with sockets remaining after 18months Same patient as above * Bouquot J, Moore E. Osteonecrosis of the jaws – exposed bone without the bisphosphonates. Proceedings, annual meeting, American Academy of Oral Medicine. 2007. ** Shetty K, Bouquot J. Residual (ghost) sockets in bisphosphonate use. Gen Dent 2009; 57:130-135.

Residual sockets Objective & methods © Photo(s): Dr. J.E. Bouquot, University of Texas, Houston,: presented at AAOM annual meeting, 2012 Residual sockets Objective & methods Objective: To report the surgical and microscopic appearance of a series of radiographically visible residual sockets biopsied years and decades after extraction Methods: 76 cases identified from 3 biopsy services over a 22 year period Information from biopsy request form: -- Demographic information -- Lesion location -- Historical information -- Clinical signs & symptoms -- Surgical description This is a convenience sample; no frequency rates can be suggested IRB approval from the University of Texas Health Sciences Center at Houston

Residual sockets demographics, location, ETC. (N =76 cases) © Photo(s): Dr. J.E. Bouquot, University of Texas, Houston,: presented at AAOM annual meeting, 2012 Residual sockets demographics, location, ETC. (N =76 cases) Average age at biopsy was 54 years -- Age range: 28-86 years Onset of socket: decades since extractions (none < 5 years) No known etiologic factor 81.6% (n = 62): in females 84.2% (n = 64): in mandible 97.4% (n = 74): molar/premolar area 35.5% (n = 27): ghost marrow of nearby bone * * Ghost marrow (see photos): faint ground glass appearance; evidence of ischemic damage; term is derived from orthopedic/radiology literature

Residual sockets clinical features (N =76 cases) © Photo(s): Dr. J.E. Bouquot, University of Texas, Houston,: presented at AAOM annual meeting, 2012 Residual sockets clinical features (N =76 cases) 38.2% (n =29): pain/tenderness No mention of clinical saucerization No mention of decreased alveolar height or width 5.3% n = 4): sharp socket rim 18.4% (n = 14): multiple sockets 7.9% (n = 6): bilateral Sharp (unremodeled?) socket rim Bilateral residual sockets (above 2 photos = same patient)

Residual sockets radiology (N =76 cases) © Photo(s): Dr. J.E. Bouquot, University of Texas, Houston,: presented at AAOM annual meeting, 2012 Residual sockets radiology (N =76 cases) 77.6% (n = 57): socket-shaped outline -- 61.0% (n = 34) = complete outline -- 39.0% (n = 23) = partial outline (usually <50%) 22.4% (n = 17): rounded radiolucencies -- 12 = poorly demarcated -- 3 = well demarcated -- 2 = Eagle’s nest -- 8 = small lamina dura at edge 1.3% (n =1): osteosclerosis nearby 17.1% (n = 13): radiolucencies nearby 35.5% (n = 27): ghost marrow nearby Complete socket Round radiolucency Eagle’s nest Eagle’s nest Partial sclerotic rim

Residual sockets radiology (N =76 cases) © Photo(s): Dr. J.E. Bouquot, University of Texas, Houston,: presented at AAOM annual meeting, 2012 Residual sockets radiology (N =76 cases) Fiber filled socket Ghost marrow Ghost marrow

Residual sockets Surgical appearance (N =76 cases) © Photo(s): Dr. J.E. Bouquot, University of Texas, Houston,: presented at AAOM annual meeting, 2012 Residual sockets Surgical appearance (N =76 cases) 32.9% (n = 25): covered by crestal bone 67.1% (n = 51): covered by fibrous scar 67.1% (n = 51): hollow, “air-filled” 13.2% (n = 10): filled with fatty marrow 10.5% (n = 8): filled with fibrous scar -- 4 = chronic inflammatory cells in socket 9.2% (n = 7): unremodeled bone Cortex so thin perio probe can perforate it Fibrous scar; fibrous “cortex” Hollow socket Hollow socket Hollow sockets Hollow socket with exposed nerve Necropsy example: Adams WR, Spolnik KJ, Bouquot JE. J Oral Pathol Med 1999.

Residual sockets Hollow socket (n = 51) © Photo(s): Dr. J.E. Bouquot, University of Texas, Houston,: presented at AAOM annual meeting, 2012 Residual sockets Hollow socket (n = 51) 67.1% = Cavitated Debris & fibrosed marrow Cavitation Edges: Bare bone Thin fibrous layer Thin layer of new bone Thin layer of fatty marrow Partially nonviable (n = 18 of 51) Ischemic myelofibrosis Case 17 Cavitation Cavitation Inactive new bone Partially nonviable lamina dura Case 17 Case 17

Residual sockets marrow-filled socket (n = 10) © Photo(s): Dr. J.E. Bouquot, University of Texas, Houston,: presented at AAOM annual meeting, 2012 Residual sockets marrow-filled socket (n = 10) 13.2% = Fatty Marrow Marrow fibrosis Features: Bare bone Thin fibrous layer Thin layer of new bone Thin layer of fatty marrow Partially nonviable (n = 18 of 61) Marrow fibrosis Inactive new bone Does this represent many of the focal osteoporotic marrow defects?

Residual sockets marrow-filled socket, with nerve 1 case: apical nerve remains Nerve

Residual sockets intramedullary fibrous scar (n = 8) 10.5% = Fibrous Scar Intramedullary fibrous scar: Dense, avascular collagen Focal regions with lymphocytes Viable bone on edges Normal PDL

Residual sockets chronic fibrosing osteomyelitis (n = 4) Moderately loose fibrosis of marrow Few remaining adipocytes Chronic inflammatory cells Viable bone Often: osteoblastic activity

Residual sockets chronic fibrosing osteomyelitis (n = 4) Moderately loose fibrosis of marrow Few remaining adipocytes Chronic inflammatory cells Viable bone Often: osteoblastic activity

Residual sockets unremodeled bone (n = 7) © Photo(s): Dr. J.E. Bouquot, University of Texas, Houston,: presented at AAOM annual meeting, 2012 Residual sockets unremodeled bone (n = 7) 9.2% = Unremodeled Bone Case 42 Case 8 Lamina dura Socket: New bone No active osteoblasts Fatty marrow in background Medullary congestion Microcracks Lamina dura Lamina dura Case 42 Case 8 Medullary congestion Case 8 Microcrack Lamina dura Case 42

Residual sockets unremodeled bone (n = 7) Microcrack Case 26 Case 26 Case 26 Case 26

Bone& marrow outside the sockets

Residual sockets Cone beam CT may show adjacent pathology © Photo(s): Dr. J.E. Bouquot, University of Texas, Houston,: presented at AAOM annual meeting, 2012 Residual sockets Cone beam CT may show adjacent pathology Residual socket Residual socket Regional ischemic osteoporosis (variant of bone marrow edema) RIO Ghost marrow

Residual sockets fibrosis outside socket © Photo(s): Dr. J.E. Bouquot, University of Texas, Houston,: presented at AAOM annual meeting, 2012 Residual sockets fibrosis outside socket Intramedullary fibrous scar, outside socket: Dense, avascular collagen Focal regions with lymphocytes Viable bone on edges

Residual sockets abnormal bone/marrow outside socket Bone marrow edema outside sockets: Ischemic myelofibrosis Medullary congestion Focal hemorrhage (microinfarction) Oil cysts Granular adipocytes Viable bone 59.2% (n = 45) = ischemia or inflammation of surrounding bone marrow Ghost marrow; cavitation

Residual sockets in situ case: unremodeled bone inside socket Ghost marrow outside sockets = bone marrow edema Ischemic myelofibrosis Viable bone Medullary congestion Plasmostasis Microinfarction Oil cysts, mast cells Few inflammatory cells Case 8 Case 8 Case 8 Outside sockets: bone marrow edema Case 8 Case 8 Inside sockets: unremodeled bone

Residual sockets bone marrow edema inside/outside socket Case 21 Case 21 Ischemic myelofibrosis Viable bone Medullary congestion Plasmostasis Microinfarction Oil cysts, mast cells Few inflammatory cells Case 21

Residual sockets in situ case: chronic fibrosing osteomyelitis Why is this socket inflamed 14 years after extraction? How can this happen? New infection? Fibrosis keeping out the immune system? A sign of the devil?

Residual sockets conclusions © Photo(s): Dr. J.E. Bouquot, University of Texas, Houston,: presented at AAOM annual meeting, 2012 Residual sockets conclusions Residual sockets represent poor bone healing or remodeling, probably from chronic ischemia, low grade inflammation or an unidentified systemic disorder that affects bone growth and repair Most examples are asymptomatic and may not need surgical treatment May act as “red flag” to alert the surgeon or dentist to potential healing problems in subsequent surgery, implant placement or trauma of alveolar bone

Residual sockets Surgical appearance: Hollow space © Photo(s): Dr. J.E. Bouquot, University of Texas, Houston,: presented at AAOM annual meeting, 2012 Residual sockets Surgical appearance: Hollow space Case 65 Case 65 Ghost marrow 67% = cavitated How can this be? Variant of traumatic bone cyst? Variant of ischemic cavitation? Poor circulation from early life? Sockets in dried mandible