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Honeycombed Bone in a Jaw – New Variant of a Disease as Old as the Dinosaurs (Ischemic Osteonecrosis)

Jerry E Bouquot, DDS, MSD, DABOMP, DABOM(Hon), FAAOMP, FACD, FICD1*, Steven B. Whitaker, DDS, DABOMP, FAAOMP, FACD2*and Jacques Imbeau, DMD, FACNEM3

1Clinical Professor & Past Chair of Oral Pathology, Department of Oral & Maxillofacial Surgery, School of Dentistry, West Virginia University, Morgantown, West Virginia
2Associate Professor & Past Chair of Diagnostic Sciences, Department of Endodontics, School of Dentistry, West Virginia University, Morgantown, West Virginia
3Director, Integrative Dental Medicine and Natural Medicine, Auckland, New Zealand

*Corresponding author

*JE Bouquot, Clinical Professor & Past Chair of Oral Pathology, Department of Oral & Maxillofacial Surgery, School of Dentistry, West Virginia University, Morgantown, West Virginia 212 Tibbs Road, Morgantown, WV 26508, USA

Abstract

Introduction: Ischemic osteonecrosis (ION) has a very unique clinical feature: ischemic osteocavitations (cavitations), large bony voids or hollow spaces, so specific to ION that their presence in 200,000,000-year-old dinosaur fossils has allowed scientists to diagnose osteonecrosis from our current time. ION has been reported recently, and often, in the jaws and therein, a unique variant has been seen: cavitations with the marrow missing while trabeculae remain. We refer to this variant as ischemic marrow atrophy (honeycombed bone) and present a case here.

Case report: A 47-year-old female presented with a 6-year history of atypical facial pain, diagnosed and treated (unsuccessfully) as a neuralgia. In the area of the pain, an area of low bone density was seen in the mandibular left third molar region, decades after the molar was extracted. The area became much more painful with firm palpation and had complete pain relief with diagnostic anesthesia testing. Surgical curettage showed a void in the bone, with numerous semitransparent, thin bony trabeculae traversing the void. Thorough curettage affected complete disappearance of the pain, which had not returned at the last follow-up visit, two years later.

Conclusion: We present the first detailed case of a pain-producing osteocavitation containing residual bony trabeculae with no surrounding marrow. Diagnosed as ischemic marrow atrophy (honeycombed bone), it was curetted with complete elimination of the pain.

Keywords:Osteonecrosis, ischemic osteonecrosis, cavitation, osteocavitation, ischemic osteocavitation, bone marrow edema.

Introduction

Ischemic osteocavitations (osteocavitations, cavitations) are bony voids or “air-filled spaces” resulting from a slowly diminishing blood supply to cancellous bone [1-3]. They occur throughout the skeleton but are usually seen in the femoral head as part of ischemic osteonecrosis (ION), a major cause of hip replacement today [4]. They are so specific to that disease that ION can be definitively diagnosed by their presence [4,5]. In fact, paleontologists have diagnosed ION from the existence of osteocavitations in fossilized femoral heads of deep-diving dinosaurs and reptiles from the Jurassic Period (201-145 million years ago), making it one of the oldest diagnosable diseases on the planet [6,7].

ION can produce severe pain and when occurring in the jawbones can mimicking symptoms of toothache, periapical infection or facial neuralgia [2,8]. This is a special problem for those with neuralgic symptoms, since the ION disease frequently provides only very subtle or completely negative changes on dental radiographs, even cone beam CT images. It is easily overlooked in a simplified diagnostic workup.We have encountered, amongst more than 16,000 jawbone marrow biopsy samples, numerous ION lesions with osteocavitations which were not entirely empty: the bony void contained numerous bare or denuded trabeculae traversing from one wall of the cavitation to the opposing cortical wall. Microscopically, these trabeculae appear mostly viable and most often appear to have no soft tissue whatsoever on their surfaces, or at most, a thin fibrous encasement. When the surgeon touches these trabeculae with a curette, they seem to disappear or instantly shatter into very small fragments.

We present herein an example of this variant, which we are calling “honeycombed bone,” in a patient previously diagnosed with facial neuralgia pain. This appears to be the first published case of this special form of ION, other than its inclusion in a jawbone osteonecrosis classification system some years ago [9].

Case report

Clinical presentation

A 46-year-old woman had suffered from severe, nonlancinating, intermittent pain of her lower left face for more than 6 years. The pain had been diagnosed as atypical facial pain (atypical facial neuralgia, Persistent Idiopathic Facial Pain, PIFP) and had proven unresponsive to several medications. While visiting with a new dentist for routine dental care she mentioned the pain and its location, so the dentist palpated her left mandibular alveolus, finding that the greatest pain increase was elicited with firm finger pressure on the facial and crestal surfaces of her left third molar region (her third molars had all been extracted when she was 19 years old). When the dentist gave her a left mandibular block to anesthetize her for replacement of a small restoration on her second molar, the facial pain disappeared entirely, within seconds. This led to a pantographic radiograph being taken for better evaluation.

Radiographic appearance

The pantogram showed a large, irregular, somewhat oval area of low bone density in the left mandibular third molar site (Figure 1). This extended from a thin crestal bone down to the superior wall of the inferior alveolar canal. There was an irregular pattern of thin trabeculae seen throughout the radiolucency, with some areas showing the trabeculae to be somewhat parallel to each other. The central region showed an inverted triangular area of faintly increased radiopacity.

At surgery.

The third molar site was covered widely by a thick, dense fibrous scar tissue rather than cortical bone. Once removed, an underlying space or void was seen, with several areas showing semitransparent, glistening trabeculae crossing from one side to the other, and interconnecting with other trabeculae (Figure 2). When a curette lightly touched these trabeculae, they seemed to “dissolve” into small slivers and rounded calcified fragments. The walls of the cavitation were thoroughly curetted, and a small amount of tissue was able to be retrieved intact for microscopic interpretation.

 Histopathology

Microscopically, the tissue consisted almost entirely of small, thin shards of bony trabeculae, with only occasional missing osteocytes and with no attached marrow (Figure 3). Some shards had undergone delamination. Small amounts of fibrous tissue were attached to some bone fragments, and similar fibrous fragments were seen to be independent of bone. No granulation tissue or inflammatory cells or bacterial colonies were present, nor were there areas of soft tissue or bone necrosis.

The two largest tissue fragments, representing the central triangular region, were comprised entirely of intertwining, immature bony strands with a background stroma of degenerated fatty and loosely fibrous tissue (Figure 4). No mature or lamellar bone was seen in this region, nor were inflammatory tissues or cells.

 Diagnosis and follow-up

The final diagnosis for this lesion was ischemic marrow atrophy, a variant of ischemic osteonecrosis and a special form of ischemic osteocavitation, detailed here for the first time, and referred to also as “honeycombed bone” because of its appearance at surgery. This diagnosis assumes that the marrow, which has a somewhat separate blood supply than the bone itself, had previously atrophied or necrosed, leaving relatively viable, but partially compromised, bony trabeculae behind. The central triangular sclerosis was given the name of another variant of ischemic osteonecrosis: stagnant immature bone (newly formed but inactive bone, with no apparent ability to mature into lamellar bone). Immediately after the anesthesia wore off the patient indicated that she felt no remnant of her previous pain, although the surgical site was somewhat tender and “sore.” Within two weeks there was no pain or tenderness in the region, and the pain had not returned at the last follow-up visit two years later.

Figure 1: Radiographic appearance of posterior left mandible. A) Moderately well demarcated radiolucency (arrows) in third molar site, extending down to the inferior alveolar canal, with a central faintly radiopaque inverted triangle. B) Close up of lesion shows a pattern of thin bony trabeculae surrounding the more opaque central region (arrow).

Figure 2: Appearance at surgery. A) After removing a crestal covering of thick fibrous scar tissue, an underlying hollow space was seen with trabeculae crossing the space and connecting with other trabeculae; B) Close-up shows the trabeculae to be glistening on their surfaces and to be semitransparent.

Figure 3: Microscopic appearance. A) Entire specimen consisted of surgically fragmented, often very thin bony trabeculae with few missing osteocytes (a sign that the bone is minimally necrotic), and with almost no attached soft tissue; B) Higher power shows almost no soft tissue, with few missing osteocysts but occasional microcracks (arrow), a sign of bone desiccation.

Figure 4: Microscopic appearance of central triangular opacity. A) Stagnant immature bone (new bone but with no residual osteoblastic activity) is seen, with occasional missing osteocytes and no mature bone formation; B) Higher power shows degenerated fatty/fibrous stroma.

Discussion

While this is the first detailed report of honeycombed bone (ischemic marrow atrophy), we have been seeing it clinically and microscopically for some time, and it was included in the osteonecrosis classification system we proposed in 2010 (Table 1) [9].

Table 1: The Bouquot-McMahon osteonecrosis classification system for jawbone ischemic lesions.9

  • Marrow congestion (dilated vessels): Normal marrow except that capillaries or veins

are dilated more than 6 RBC diameters; may be cause of pain.

  • Ischemic myelofibrosis: Fat cells slowly are replaced by a loose, wispy fibrous tissue

which seems to be streaming between the fat cells; a few mast cells, perhaps a few

chronic inflammatory cells; often multifocal.

  • Reticular fatty degeneration: Mild version of ischemic myelofibrosis; fibers look ragged.
  • Intramedullary fibrous scar: Dense collagen fibers aggregated into scar tissue with very

little vascularity or inflammation; sharp outer borders; may be myxoid in areas.

  • Bone marrow edema: Classic CIBD, with dilated vessels, myelofibrosis, plasmostasis,

focal hemorrhage, focal fat necrosis (all types), a few mast cells, a few chronic

inflammatory cells: involved bones are almost always viable.

  • Regional ischemic osteoporosis: Low bone density with thin, widely spaced trabeculae,

a thin cortex, and diffuse or multifocal signs of ischemic marrow damage.

  • Focal osteoporotic marrow defect: Low bone density with thin, widely spaced, inactive

trabecula, a thin cortex, and minimal, if any, signs of ischemic marrow damage.

  • Ischemic marrow atrophy (honeycombed bone): Inactive, almost always viable bony

trabeculae with no or almost no attached fatty marrow or hematopoietic marrow; may have

small amounts of attached fibrous tissue; only a valid feature if no rotary instrument

touched the cancellous bone sample.

  • Ischemic osteocavitation: Intramedullary void, greater than 5 mm. diameter, with little or

no soft tissue lining; scraping walls may yield: fibrous tissue, viable trabeculae, scattered chronic inflammatory cells, plasmostasis, focal hemorrhage, ischemic myelofibrosis; surgeon must indicated the presence of the void.

Ischemic microcavitation: Bony voids or air spaces less than 5 mm, in diameter; an aging phenomenon.

  • Traumatic bone cyst (unicameral bone cyst): Variant of ischemic cavitation (see above), found primarily in young persons, usually asymptomatic, easily treated with curettage (inducing new hemorrhage).

White osteocavitations are unique to ION, the exact mechanism of bony void creation is unclear. It is even less clear how some cavitations can retain trabeculae while surrounding marrow disappears. We assume that a slow atrophy occurs, but we cannot rule out long ago episodes of medullary necrosis. While the cavitation-producing mechanism is unclear, there is no doubt that it is related to compromised vascularity, most likely secondary to an increased tendency toward hypercoagulation (usually inherited) [10,11]. It is important to emphasize that this is not a classic inflammatory process, it is a process of compromised blood flow. There are many microscopic features similar to both processes and it is important for the pathologist to be aware of the more subtle histopathologic differences [2].

Regardless of the lack of a proven pathoetiology, it is important to appreciate the significance of a thorough but conservative curettage, continuing until fresh, nondiscolored, nonbrittle bony walls are seen, with fresh red hemorrhage flowing freely instead of the usual thick, dark , slow-moving blood seen when cavitational walls are more lightly curetted [12]. Our patient was cured of her pain. Should this have been expected? Yes. Previous follow-up investigations of large numbers of jawbone ischemia patients in pain have determined that thorough curettage effectively relieves the associated pain 72-80% of times, with an average follow-up time of more than 5 years [2,13,14].

This success, however, is very much dependent on properly localizing the area of bone involvement. Our patient was fortunate in presenting with an identifiable if not diagnostic radiographic change, but most patients are less fortunate, they have normal appearing dental radiographs. Much more proficient imaging techniques are, fortunately, available for such bone lesions: 1) Technetium-99m Methylene Diphosphonate (99mTc-MDP) scintigraphy (bone scan) can accurately localized a jaw lesion about 98% of the time, although caution should be taken for negative tests (no hot spots in area) because this test has a high rate of false negatives; 2) Quantitative ultrasound, also known as through-transmission ultrasound, is equally successful without the use of radioactive materials [15-18]. In the pain-associated ION jawbone lesions, diagnostic anesthesia testing is as good as these two imaging technologies, in our opinion. This test is simple: place a small amount of local anesthesia above the periosteum in the area of pain, if the pain goes away, the test is positive; the diseased marrow will be found at that site in about 97% of positive tests.

Our patient suffered through years with often intolerable pain, even though she had a radiographic abnormality in the region of the pain. We don’t know why surgical exploration of the third molar site was not undertaken, but it makes one wonder how many other individuals with atypical facial pain have suffered equally, simply because their dentist or physician did not use a more appropriate diagnostic tool?

Conclusion

We report a variant of ischemic osteocavitation, which in turn is a variant of ION and is, in our example, associated with severe local pain. ION in all its variants is notorious for being poorly visualized on radiographs and so we suggest a more appropriate technology, such as scintigraphy, quantitative ultrasound or diagnostic anesthesia testing, before assuming a painful jawbone region is associated with neural rather than medullary dysfunction. This is especially important considering the level of pain often associated with ION.

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