The use of SPECT bone scans to evaluate patients with idiopathic jaw pain

Vol. 90 No. 6 December 2000

ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY ORAL AND MAXILLOFACIAL RADIOLOGY

Editor: Sharon L. Brooks

The use of SPECT bone scans to evaluate patients with idiopathic jaw pain Donald J. DeNucci, DDS, MS,a Clara C. Chen, MD,b Christine Sobiski, DDS, MSSA,c and Sean Meehan, DMD,d Bethesda, Md, and Yokosuka, Japan NATIONAL INSTITUTES OF HEALTH

Objective. The purpose of this study was to investigate the potential usefulness of single photon emission computed tomography (SPECT) bone scanning with technetium-99m methylene diphosphonate (Tc-99m MDP) in the diagnosis of idiopathic jaw pain. Unlike planar bone scanning, SPECT uses tomographic technology to provide 3-dimensional images, which are more useful in localizing small lesions. Study design. Twenty patients, each with a diagnosis of chronic idiopathic jaw pain, were compared after SPECT bone scanning with 20 age-matched and gender-matched normal controls. Uptake was identified and compared in sites with previously detected jaw pathoses and jaw pain. Results. Nineteen of 20 patients with jaw pain evaluated with SPECT had positive scans, in contrast with 12 of 20 control subjects (P < .04). Positive scans were correlated with painful sites in 15 of 20 patients, with the remaining 5 patients demonstrating no uptake in painful locations. Patients with jaw pain demonstrated 37 of 80 mouth quadrants with positive scans, in contrast with 21 of 80 mouth quadrants in the controls (P < .01). Nineteen of 24 painful mouth quadrants had uptake in the pain group. Of the 21 quadrants positive in the controls, 17 were correlated with previously detected jaw pathoses. The sensitivity and specificity for detecting painful sites were 0.79 and 0.68, respectively. The sensitivity and specificity for detecting previously identified pathoses in the jaws of normal controls were 0.80 and 0.93, respectively. Conclusion. Patients with idiopathic jaw pain had a significantly greater frequency of positive SPECT bone scans when compared with normal controls. However, the sensitivity and specificity of SPECT bone scans in detecting painful sites were low. These findings suggest that SPECT bone scanning with Tc-99m MDP is not indicated as a routine imaging procedure for the detection of jaw pathoses, but may be considered as a potential research tool in the future study of chronic idiopathic jaw pain.

(Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2000;90:750-7)

Chronic idiopathic jaw pain is a poorly understood condition that has been managed with a wide variety of unverified therapies with limited degrees of success. Patients seen with chronic idiopathic jaw pain appear to comprise a heterogenous population whose diagnoses may include aFormerly

Colonel US Army Dental Corps and Guest Researcher, National Institute of Dental and Craniofacial Research, National Institutes of Health, Bethesda, Maryland. Presently Consultant, Orofacial Pain, Walter Reed Army Medical Center, Washington, DC. bDepartment of Nuclear Medicine, Warren G. Magnuson Clinical Center, National Institutes of Health, Bethesda, Maryland. cFormerly Clinical Fellow, National Institute of Dental and Craniofacial Research, National Institutes of Health, Bethesda, Maryland. dFormerly Clinical Associate, Clinical Investigations and Patient Care Branch, NIDR, NIH. Presently Lieutenant Commander, Dental Corps, United States Naval Reserve, US Naval Hospital, Yokosuka, Japan. Received for publication Oct 12, 1999; accepted for publication Dec 19, 1999. Copyright © 2000 by Mosby, Inc. 1079-2104/2000/$12.00 + 0 7/16/105906 doi:10.1067/moe.2000.105906

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several underlying descriptive conditions, including trigeminal neuralgia, atypical facial pain, atypical odontalgia, phantom tooth pain, and psychogenic pain.1-15 Diagnosis of this condition has been difficult because of the lack of consistent clinical findings that can be correlated with patient symptomatology.2,16-27 Several authors have suggested that chronic idiopathic jaw pain may be the result of a low-grade osteomyelitis or a chronic inflammation of the jaws associated with “jaw bone cavities.”28-30 Bouquot et al30 evaluated 224 tissue samples removed from suspected bone cavities within the jaws of patients with chronic pain and reported that “all tissue samples demonstrated clear evidence of chronic intraosseous inflammation.” Based on these findings, this condition was labeled “neuralgia-inducing cavitational osteonecrosis” (NICO). Others investigators have suggested that this condition is caused by an infarctioninduced osteonecrosis of the jaw, which is secondary to a generalized hypercoagulable state.31-33 This generalized

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hypercoagulable state has also been linked to avascular necrosis of the femoral head and other cardiovascular conditions. Based on these diverse etiologic hypotheses, treatment has included antibiotic therapy, anticoagulants, hyperbaric oxygen, psychotherapy, antidepressants, topically applied pharmaceuticals, and aggressive surgical procedures aimed at eradicating the suspected disease process.8,16,18,27,28,34-36 Varying degrees of success have been ascribed to these management strategies.16,36,37 However, there exist no verified clinically predictable procedures that consistently eliminate or markedly reduce chronic idiopathic jaw pain in the long term. The purpose of this study was to investigate the potential usefulness of single photon emission computed tomography (SPECT) bone scanning in the diagnosis of chronic idiopathic jaw pain thought to be related to a chronic inflammatory or infective process within the alveolus. Because conventional imaging procedures, such as planar film radiography, computerized tomography, and magnetic resonance imaging, have proven to be unreliable and have provided little useful diagnostic information in these patients,38-40 a newer imaging modality, designated SPECT bone scanning with technetium-99m methylene diphosphonate (Tc-99m MDP) was chosen for evaluation. Unlike planar bone scanning, SPECT uses tomographic technology to provide 3dimensional images, which are more useful in localizing small lesions. The study was designed to compare the SPECT images of the jaws of 20 patients with a diagnosis of chronic idiopathic jaw pain with those of 20 agematched and gender-matched healthy controls. It was hypothesized that if chronic idiopathic jaw pain is caused by a chronic inflammatory or infective process within the jaws, then patients with pain would consistently demonstrate an increased uptake of radioisotope in their jaws when compared with healthy subjects.

confirm the presence of chronic idiopathic jaw pain and to assure that the controls were free of chronic jaw pain. For the purposes of the study, chronic idiopathic jaw pain was defined as pain confined to the maxilla or mandible for a duration of more than 3 months and for which no organic cause could be detected. Patients with intermittent, lancinating pain suggestive of trigeminal neuralgia were excluded, as were those with temporomandibular disorders, an identifiable neuropathy, an infection, or myofascial pain. Patients with a history of surgery to the jaws within the past 6 months, a severe psychiatric disorder, or those involved in litigation related to their pain were also excluded.

METHODS AND MATERIALS Patients This study was approved by the Clinical Center Institutional Review Board, National Institutes of Health. Twenty patients, aged 31 to 62 years (mean age, 50.1 years) with a presumptive diagnosis of idiopathic jaw pain who met the inclusionary criteria for the study were selected from a population of patients referred to the National Institutes of Health Pain Research Clinic for assessment of chronic orofacial pain. Nineteen of the 20 patients were women. In addition, 20 gendermatched and age-matched (to the nearest year) individuals without jaw pain were recruited from the general population to serve as normal controls. Each patient or control subject signed a detailed informed consent form. All candidates for the study were initially interviewed and clinically evaluated by the primary investigator to

Patient evaluation All patients underwent a clinical evaluation by a dentist and a dentist/social worker, which included a psychosocial interview and assessment, radiographs of the jaw, and an examination of the hard and soft tissues of the head, neck, and oral cavity. Patients were asked to report the intensity and discomfort associated with their pain with a reliable and validated pain scale.41,42 Consultative referral to other medical specialists was accomplished when it was necessary to more clearly define the diagnosis and to rule out conditions thought to be contributing to the patient’s pain. All patients then underwent a second evaluation by a general dentist who acquired a comprehensive dental history and then identified and recorded any clinical or radiographically detectable pathoses in the jaws. Pathoses included periodontal disease, periapical pathoses, active dental caries, cracked teeth, neoplastic processes, and surgical scars. If a clinically or radiographically identifiable cause for a patient’s pain was found, the patient was referred for appropriate treatment and eliminated from the study. Normal control subjects were interviewed and provided with a comprehensive oral examination with panoramic radiographic imaging and additional radiographs as appropriate to define existing dental pathoses. All findings in the controls were recorded for subsequent correlation with scintigraphic findings. Bone scanning Three-phase bone scanning was performed with 25 mCi of Tc 99m MDP. A single-headed gamma camera equipped with a low energy, high resolution collimator was used for the blood flow and blood pool phases of the study. Images were acquired over the head and neck with a magnification factor of 1.5. These images were then repeated 2 to 3 hours later in the delayed phase of the study. In addition, SPECT of the skull and a whole body scan were performed during the delayed phase of the study. SPECT images were acquired with either a dual-headed or triple-headed camera.

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A

B Fig 1. A, Color and digitally enhanced SPECT image of patient with idiopathic jaw pain. Areas of maximal uptake are red with lesser or minimal uptake as yellow. Blue color indicates absence of isotope uptake. When compared with control subject, increased uptake is evident in both jaws with focal area of intense uptake in right posterior maxilla in location of patient’s pain. Right maxillary tuberosity was explored surgically. Biopsy specimen taken from area confirmed osteomyelitis. B, Panographic radiograph of patient in A. Arrows point to areas patient described as painful. Radiograph did not appear to suggest any pathologic changes in these areas.

Images were reviewed by a medical radiologist specializing in nuclear medicine. The first 12 patients comprised a pilot study and were known by the nuclear medicine evaluator to have jaw pain, but the location of the pain was not disclosed until after the SPECT images were evaluated. Correlative findings during the pilot study demonstrating isotope uptake in areas of jaw pain in the first 12 patients prompted the addition of 8 more patients with jaw pain and 20 control subjects to the study. With the addition of healthy controls, the nuclear medicine evaluator was completely blinded as to the status of the subject presenting for the bone scan. For purposes of analysis, the subjects’ mouths were

divided into conventional dental quadrants (right maxilla, left maxilla, right mandible, and left mandible), yielding a total of 80 quadrants in each group. In both groups, each quadrant was scored positive or negative, depending on whether the nuclear medicine report indicated isotope uptake. Then these findings were correlated with the results of the earlier clinical and radiographic examination. The data were analyzed with the chi-square test and an analysis of sensitivity and specificity with appropriate arithmetic calculations.

Results The results of the blood flow and blood pool phases

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A

B Fig 2. A, Color and digitally enhanced SPECT image of control subject demonstrating minimal isotope uptake. Areas of maximal uptake are red with lesser or minimal uptake as yellow. Blue indicates absence of isotope uptake. Uptake in this subject appears to be in temporomandibular joint region, although patient reported no associated symptoms. All subjects in both groups demonstrated uptake associated with cervical spine. Precise reason for this is unknown. B, Panographic radiograph of control subject in A. No evidence of clinical or radiographic pathosis.

of the bone scan were normal in all patients and control subjects. Delayed images, including SPECT in the jaw pain group, yielded 19 of 20 subjects with positive bone scans in 1 or more quadrants (Fig 1). In contrast, only 12 of 20 of the control subjects had positive bone scans (P < .04). In the jaw pain group, positive scans were correlated with painful sites in 15 subjects. Of the remaining 5 patients with a negative scan in a painful quadrant, 4 had positive scans in other quadrants, which could not be correlated with previously identified pathoses or pain, and 1 patient had a completely

negative scan. Three of the patients with a positive scan in a painful quadrant had concomitant mild to moderate periodontitis (probing depths of less than 6 mm), which were adjudged not to be the cause of the patient’s reported pain based on the patient’s lack of reported pain when these areas were probed. In the control group in which patients reported no painful areas, 10 of the 12 positive scans showed clinical correlation with an identifiable pathoses such as periodontal disease or a periapical lesion, whereas the remaining 2 positive scans did not (Fig 2).

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Fig 3. This graph depicts results of SPECT bone scanning of 80 quadrants in each group of 20 subjects. Note increased cumulative uptake in pain group when compared with controls (P < .01). Note also greater number of false positive scans in pain group when compared with controls. False positive scans are those that demonstrated no apparent correlation with either pain or an existing identifiable pathosis.

When we analyzed the results by jaw quadrant, we found that 20 subjects with jaw pain reported 24 painful quadrants with 1 patient reporting 4 quadrants, another reporting 2 painful quadrants, and the remaining 18 subjects each reporting 1 painful quadrant. When radioisotope uptake was analyzed by quadrant, 37 of 80 quadrants were positive in the pain group. This was significantly more than in the control group where positive scans were seen in only 21 of 80 quadrants (P < .01). Of the 37 quadrants positive in the jaw pain group, 13 quadrants correlated with pain alone, 6 quadrants correlated with pain and a coexisting identifiable pathosis adjudged not to be the cause of the pain (periodontal disease), 1 quadrant correlated with an identifiable pathosis and no pain, and 17 quadrants had uptake that could not be correlated with either pain or an identifiable pathosis. Five quadrants that patients reported as painful had negative scans. Of the 21 quadrants with positive scans in the control group, 17 were correlated with identifiable pathoses, whereas the remaining 4 quadrants were not (Fig 3). The sensitivity of SPECT bone scans for detecting painful quadrants was determined to be 0.79 with 19 of 24 painful quadrants detected. However, the specificity of SPECT bone scans in detecting painful quadrants was only 0.68 with 18 false-positive quadrants. The sensitivity and specificity for SPECT bone scanning in detecting previously identified pathoses in the control group was 0.81 and 0.93, respectively. In the pain group, the sensitivity for detecting previously identified

pathoses was similar to the controls at 0.88 but the specificity was markedly reduced at 0.58. However, when painful quadrants were combined with quadrants with an identifiable pathosis, the sensitivity decreased slightly to 0.80, but specificity rose to 0.69. When data were combined for both groups, the sensitivity and specificity of SPECT bone scanning for detecting previously identified pathoses were 0.83 and 0.74, respectively.

DISCUSSION The exact mechanism by which Tc99m MDP localizes in bone is unknown, but it is thought to adsorb to hydroxyapatite crystals during new bone formation, as occurs in bone that is undergoing remodeling. Bone scanning is generally considered to be a highly sensitive but nonspecific imaging procedure used in a wide range of medical situations to detect and monitor a variety of osseous lesions.43-46 The findings of this study suggest that bone scanning with Tc99m MDP lacks sensitivity in detecting jaw pathoses in normal subjects (0.81) but has remarkably good specificity (0.93). In contrast with the controls, the patients with pain had significantly more quadrants of uptake (P < .01). However, in the pain group, although sensitivity in detecting identifiable pathosis and pain were comparable (0.80), the specificity was much lower (0.69). One explanation for this lowered specificity is that patients with jaw pain may have some unexplained metabolic activity in their jaws that accounts for a generalized increase in isotope uptake without an overt

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clinically or radiographically detectable manifestation, other than localized pain. Several investigators have suggested that chronic idiopathic jaw pain might be caused by occult osteomyelitis, osteonecrosis, or other chronic inflammatory condition, but the underlying etiologic process is not clear.28-30 One group of investigators has speculated that this osteonecrosis may be the result of an infarction within the jaw, similar to that observed with avascular necrosis in other bones.31-33 They have postulated that this condition may be the manifestation of a generalized hypercoagulable state with significant implications for the cardiovascular system as well.32 Unlike Bouquot’s reports, in which most subjects reported pain in the mandible,30 the majority of the subjects in this study reported pain in the maxilla. The maxilla is a well-vascularized structure housing the maxillary sinuses. Because of its vascularity, the maxilla would seem an unlikely location for a chronic osteomyelitis unless the vascular supply were significantly altered or compromised. The proximity of the maxillary alveolus to the maxillary sinuses might increase susceptibility to infection with pathogens normally resident to the upper respiratory tract. If an infarction were to produce osteonecrosis, perhaps some of the nearby flora (oral or respiratory) could produce a low-grade occult infection. One could postulate that an antecedent neurovascular event might be responsible for osteonecrosis. Aberrant autonomic activity is known to exacerbate certain painful conditions through vasoconstriction. Perhaps in susceptible patients, this could result in a transient or chronic ischemia that ultimately results in necrosis of bone and secondary infection. In these patients, autonomic dysfunction might be precipitated by certain systemic and local factors that might lead to impaired perfusion and subsequent osseous necrosis. Exposure to therapeutic radiation and the administration of corticosteroids are both known to have an adverse impact on bone. None of the patients reported being subjected to therapeutic radiation. However, several reported the use of oral and topical corticosteroids in the past, including intranasal preparations. The impact on the maxillary bone and sinus from the chronic use of intranasally administered steroid preparations is unknown. Emshoff et al47 speculated that chronic maxillary sinusitis may be involved in chronic idiopathic maxillary jaw pain, but they failed to demonstrate a strong relationship between the 2 conditions. In a transoral endoscopic evaluation of 50 patients with chronic idiopathic maxillary jaw pain, they determined that 62% of these patients had what they termed a “chronic maxillary sinus-related diagnosis.”

The results of this study suggest that certain patients with jaw pain may be experiencing subtle metabolic perturbations, which are detectable with SPECT. Detection may be dependent on the extent and level of activity of this process. More extensive areas of activity within the jaws may eventually begin to manifest as overt pain in some patients. For example, one 23-year-old woman who was scanned after completion of this study and not included in these data demonstrated dramatic uptake involving the entire mandibular ramus. Her chief complaint for the preceding 18 months had been persistent pain of the posterior mandible precipitated by a tooth cleaning and scaling distal to a mandibular third molar. Periapical and panoramic radiographs appeared normal. Earlier extensive dental and medical workup had failed to provide a diagnosis for the patient. The etiologic basis for this large area of uptake remains unclear. Adult periodontitis and radiographically evident periapical lesions were frequently correlated with positive SPECT scans in other subjects. Perhaps in these cases, the level of metabolic activity had reached a critical threshold resulting in significant isotope adsorption and a positive scan. This assumption suggests that there would also exist metabolically “cold” or inactive areas not detectable with SPECT that could remain symptomatic to the patient and could account for negative scans in painful quadrants. Osteomyelitis was confirmed histologically in 1 of the study patients. A 47-year-old woman insisted that her right maxillary tuberosity be surgically explored, based on the location of her pain and the results of the SPECT scan. Tissue removed from her right maxillary tuberosity was submitted to the Armed Forces Institute of Pathology and was reported as consistent with osteomyelitis. The patient reported significant sustained pain relief for several months after the procedure but continued to report pain in the bicuspid region of the same quadrant. The bicuspid was not operated on because of its proximity to the maxillary sinus and the potential for perforation. The patient’s dental history showed extraction of the right maxillary third molar at age 23 and endodontic treatment of the bicuspids and first maxillary molar several years before participation in the study. No other patients in the study underwent surgical exploration of painful sites. Based on the findings of this study, it is clear that SPECT bone scanning with Tc-99 MDP is not indicated for the routine detection or diagnosis of common dental pathoses. Aside from the fact that patients are exposed to significant levels of radiation, SPECT bone scanning appears to lack sensitivity. Moreover, other imaging modalities offer significant advantages over SPECT in detecting common dental pathoses. In patients with jaw pain, SPECT bone scanning appears to lack both the

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sensitivity and the specificity needed to make accurate therapeutic decisions. The remarkably low specificity in patients with jaw pain could result in erroneous diagnoses and inappropriate surgical interventions. SPECT bone scanning with Tc-99m and other isotopes may continue to have a role in elucidating the pathophysiology of chronic idiopathic jaw pain. The fact that the patients in this study had a significantly higher frequency of uptake on their bone scans when compared with normal controls suggests that these patients may have abnormalities that require further investigation and research. However, these data do not support the routine use of SPECT bone scanning in the diagnosis of chronic orofacial pain for which no apparent etiologic basis has been determined.

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11. 12. 13. 14. 15. 16.

17. 18.

CONCLUSION The results of this study indicate that when SPECT bone scanning was performed on 20 patients with idiopathic jaw pain and compared with 20 age-matched and gender-matched healthy controls, patients with jaw pain were significantly more likely to have radioisotope uptake in their jaws. However, the sensitivity and specificity of SPECT bone scanning in detecting painful areas of the jaw were low. Furthermore, SPECT bone scanning demonstrates only moderate sensitivity in detecting other identifiable jaw pathoses. These findings suggest that SPECT bone scanning with Tc-99m MDP is not indicated as a routine imaging procedure for the detection of dental pathoses, but may be considered as a potential research tool in the future study of chronic idiopathic jaw pain. We thank James Reynolds, MD and Ronald Dubner, DDS, PhD, for their assistance with study design. In addition, Robert Coghill, PhD, provided invaluable assistance in the preparation of the SPECT images used in the manuscript.

19. 20. 21. 22. 23. 24. 25. 26. 27.

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Reprint requests: Donald J. DeNucci, DDS, MS 10925 Citreon Ct North Potomac, MD 20878