1. Mandibular Patterns of Chronic Ischemic Bone Disease (CIBD)
Assessment of a High Risk Cadaver Cohort
American Academy of Oral Medicine, Atlanta, Georgia
April, 2016
J. E. Bouquot, DDS, MSD
Director of Research, The Maxillofacial Center for Education and Research, Morgantown, West Virginia
Wesley E. Shankland, DDS, MS
Director, Facial Pain Clinic, Columbus, Ohio
Firoozeh Samim, DDS, MS
University of British Columbia, Vancouver, British Columbia, Canada

2. CIBD: The Oldest Bone Disease
Osteonecrosis = earliest diagnosable bone disease (cavitations found in 90,000,000 year old diving dinosaurs, & a few land ones)
First paper on hip osteonecrosis:
Fothergill, 1794 (England)
First paper on jaw osteonecrosis :
Noel, 1868 (United States)
-- Called it “bone caries” or “osteitis”
Considered to be extremely rare
-- Because it was reported under 72
different names (usually the surgeon’s
name who first reported it)

3. CIBD: Like Osteomyelitis, but Not So Much
Called “aseptic osteomyelitis” – looked like infection but no micro- organisms cultured
Some called it “cardiac disease of the hip” -- thought it was a blood flow/infarction phenomenon, but couldn’t prove it
Knew that bone cavitations were unique to this particular disease
Term bone “cavitation” was coined
for this disease in 1932
Along came Arlet and Ficat

4. CIBD: Like a Brand New Disease
Ficat and Arlet (France):
-- Said it’s all one disease (a marrow disease more than a bone disease)
-- Has a wide microscopic spectrum, called Grades I – IV
-- Not seen easily with available imaging technology
-- Is a physiologic problem of ↓ blood flow in marrow
Now classified under of several microscopic dxs:
-- Ischemic osteonecrosis
-- Bone marrow edema
-- Transient/regional ischemic osteoporosis
-- Other names
Not rare: responsible for 30-40% of hip replacements
Diagnosed by MRI more than by histopathology

5. CIBD: Since Like A Brand New Disease
Up to 80% of cases were associated with hypercoagulation states
-- Small clots predominate, but marrow and brain are both susceptible to
capillary bed thrombosis
Three other very unique features:
-- Usually bilateral (up to 80% of cases)
-- In affected bone: multiple involved areas,
separated by normal marrow
-- It’s poorly visualized on
radiographs, but shows up well
on bone scans (scintigraphy)
Thrombus
Tech 99 MDP scan

6. Residual socket (filled with collagen) 14 years after extraction
Jawbone CIBD
More likely to be missed because dentists assume tooth or sinus causes of pain, don’t look further
Seem to be more painful than other locations
-- Pain diminished greatly with anticoagulants
Might be triggered by surgery/extraction, but pain doesn’t develop for decades
Low-grade inflammation/infection is often present
Same hypercoagulation
states (72-80% of cases)
Positive bone scan (97% accurate)
Positive dx anesthesia test (98%
accurate)
Positive quantitative ultrasound
(98% accurate)
Residual socket (filled with collagen) 14 years after extraction

7. BME in patient diagnosed with atypical facial neuralgia
Jawbone CIBD
My name (1989) = NICO (Neuralgia-inducing cavitational osteonecrosis)
My name (2002) = CIBD
-- Bone marrow edema
-- Regional ischemic osteoporosis
-- Ischemic cavitation
In 2010: Bouquot, McMahon
classification systems for jawbone
CIBD and osteomyelitis
-- Available in the BouquotToGo
Dropbox files
BME in patient diagnosed with atypical facial neuralgia

8. CHRONIC ISCHEMIC BONE DISEASE (CIBD) Classification
Ischemic marrow diseases:
Bone marrow edema
-- Ischemic myelofibrosis
-- Reticular fatty degeneration
-- Marrow congestion (dilated vessels)
-- Regional ischemic osteoporosis
Intramedullary fibrous scar
Ischemic marrow atrophy (honeycombed bone)
Ischemic osseous cavitation
-- Traumatic bone cyst
Ischemic bone diseases:
Partially nonviable bone
Ischemic osteonecrosis (avascular necrosis)
-- BRONJ (bisphosphonate-related osteonecrosis
of the jaws (biopsy shows acute osteomyelitis)
-- Osteoradionecrosis
Ischemic osteosclerosis
-- Bone scar
-- Condensing osteitis
Poorly forming new bone
Focal osteoporotic marrow defect
Ischemic myelofibrosis
Intramedullary fibrous scar
Bone marrow edema
Bouquot, McMahon, Annual meeting, American Academy of Oral & Maxillofacial Pathology, 2010

9. Chronic fibrosing osteomyelitis Chronic granulomatous osteomyelitis
Inflammatory Jawbone Disease Classification per Bouquot & McMahon, 2012 *
Acute osteomyelitis:
Periapical abscess
Periodontal abscess
Periapical granuloma, suppurative
Acute/subacute osteomyelitis
-- Actinomycosis
Chronic nonsuppurative osteomyelitis:
Periapical granuloma, nonsuppurative
Chronic fibrosing osteomyelitis
-- Cemental tear
-- Intramedullary fibrous scar, inflamed?
Garré's osteomyelitis
Chronic granulomatous osteomyelitis
-- Tuberculous, syphilis, fungus
-- Intramedullary foreign body reaction
-- Sarcoidosis
Chronic sclerosing osteomyelitis
-- Diffuse
-- Focal (condensing osteitis)
Chronic fibrosing osteomyelitis
Chronic granulomatous osteomyelitis
* Bouquot J, Qari H, McMahon R. Chronic fibrosing osteomyelitis (CFO) – new or long forgotten jawbone disease? OOOO 2012; 114:e39

10. The Problem
Medical pathologists get the entire femoral head to study, oral pathologists get bits and pieces (curettage is the Rx)
Medicine has proven the multifocal nature
of CIBD, dentistry has not
Medicine has correlated histopathology with
various gross appearances, dentistry has not
Dentistry has found ischemic/inflammatory
bone disease in the majority of implant sites
CIBD, mandible
Normal mandible

11. Investigative Objective
Chronic ischemic bone disease (CIBD) has very unique histopathologic, imaging and gross anatomic characteristics, including multi-site involvement and bone cavitations. While the gross appearances are well established in long bones, they remain largely unknown for the jaws, despite the fact that jaws are among the most commonly affected bones. The purpose of this investigation was to characterize CIBD in mandibles from a cadaver cohort representing patients with high risk of chronic systemic ischemia.

12. Investigative Protocol
Hemi-mandibles were obtained from cadaver material in the Department of Anatomy, WV School of Osteopathic Medicine, Lewisburg, WV
Gender, age at death, cause of death and additional health records as available were reviewed
Only cadavers from persons with chronic illnesses likely to be associated with systemic ischemia were accepted
-- Cardiovascular disease, stroke, cancer/chemotherapy, chronic lung disease,
kidney failure, liver failure, etc.
Only well preserved cadavers were selected, but no special embalming procedures were performed
Lateral jaw radiographs were obtained and then samples were slowly decalcified in a 1:1 solution of formalin and formic acid
Once decalcified, each mandible was incised by scalpel blade along its long axis. Cut surfaces were examined grossly and via magnification, spatula-tested for firmness and texture, and photographed

13. Investigative Protocol
Representative transverse and cross-sectional samples were taken from all abnormal regions for microscopic evaluation
Similar samples were also taken routinely from the #32, #29, #26 areas
Tissue samples were processed via research-grade procedures for bone evaluation, cut at 7 μ, and stained with hematoxylin and eosin
Microscopic features searched for were those in the orthopedic literature for ischemic osteonecrosis (IO), bone marrow edema (BME) and osteomyelitis
Ischemic and inflammatory diagnoses were taken from the classification systems described by Bouquot & McMahon (2010, 2012)
Abnormal
marrow
Normal
fatty marrow
Normal
fatty marrow

14. Investigative Results
66 hemi-mandibles were processed
62.2% (n = 46) from females
Average age at death = 69.0 years
(66.2 for males; 71.3 for females)
Range, age at death = years
24 were edentulous; 11 of the others had no posterior teeth
Overall, 24 (33.4%) mandibles showed 34 grossly abnormal areas of medullary bone
Terminal Disease Type
Number
% (N) with Gross Abnormality
Autoimmune disease 6
50.0 (3)
Cancer 22
45.5 (10)
Heart disease 18
22.2 (4)
Stroke 19
36.8 (7)
Total: 66
33.4 (24)

15. Investigative Results N = 34 Lesions
Average lesional size = 1.4 x 0.4 cm.
-- Range: 0.5 x 0.3 mm –- 8.1 x 2.7 cm.
8 mandibles had multiple lesions:
-- 2 had 3 separate sites
-- 6 had 2 separate sites
Brown discoloration =79.3% (n = 23),
Typically very soft or “mushy” (n = 20)

16. Investigative Results N = 34 Lesions in 24 Mandibles
Bone cavitations in 26.5% (N = 9)
-- 2 with surrounding discoloration
Dense focal sclerosis in 11.8% (n = 4)
Cavitation in vivo

17. Investigative Results N = 34 Lesions in 24 Mandibles
79.5% (n =27) of lesions were touching or surrounding the inferior mandibular nerve
Normal
Remember:
no other bones have sensory nerves inside

18. Investigative Results N = 34 Lesions in 24 Mandibles
40.7% (n = 14) of positive gross sites showed CIBD microscopically
Proteinaceous & calcific necrotic marrow detritus
Ischemic marrow atrophy

19. Investigative Results N = 34 Lesions in 24 Mandibles
40.7% (n = 14) of positive gross sites showed CIBD microscopically
Oil Cyst
Bone marrow edema

20. Investigative Results N = 34 Lesions in 24 Mandibles
17.6% showed chronic fibrosing osteomyelitis

21. Investigative Results N = 34 Lesions in 24 Mandibles
11.2% (n = 4) of lesions were easily localized via radiographs

22. Investigative Results N = 34 Lesions in 24 Mandibles
11.2% (n = 4) of lesions were easily localized via radiographs

23. Investigative Results N = 34 Lesions in 24 Mandibles
11.2% (n = 4) of lesions were easily localized via radiographs

24. Investigative Results N = 34 Lesions in 24 Mandibles
Conclusions: CIBD is seen in 1/3 of cadaver mandibles from individuals who have died in presumably ischemic states. The lesions are typically in the molar/premolar region and 1/3 of affected persons had multiple sites of involvement. Radiographs are not helpful in localizing most lesions.