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Diagnostic value of bone scintigraphy in osteomyelitis of the mandible
Diagnostic value of bone scintigraphy in osteomyelitis of the mandible
Thirty-five patients each with a tentattve diagnoses of osteomyelitrs of the mandible were examined with ggTcm-labeled phosphorus compounds. The scintigraphic findings were compared with the radiographic features and related to disease stages to evaluate the diagnostic potential of bone scintigraphy in different disease stages. The scintigraphy was valuable to exclude bone tissue involvement in some patients with clinical stgns and symptoms similar to those of osteomyelitts and with equivocal radiographic findings. In 13 patients with chronic osteomyelitis. scintigraphy revealed a larger extent of the lesion than the radiography. In lesions with permeated bone destructions with penetration of the cortex, the uptake of ggT~m was higher than in lesions with a motheaten or sclerotic appearance. This study supports the view that ggTcm-bone scintigraphy is a useful tool at various stages of osteomyelitrs, that is. In its early detection, in the treatment or biopsy plannrng. and in the evaluation of the efficacy of treatment IOK\,
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1993;75:650-71
steomyelitis localized in the mandible can often be diagnosed on the basis of clinical and radiographic evaluations. However, in some patients the clinical presentation is not specific, and the radiographic signs are vague, making the diagnosis difficult to establish in early stages. Early diagnosis is of primary concern. One of the major conclusions of Wannfors’ extensive study’ on chronic osteomyelitis of the jaws was that prompt action at the onset of initial symptoms was decisive for the prognosis. Bone scintigraphy with ““Tc”‘-labeled diphosphonates has been shown to be a sensitive method for the identification of focal bone disease. The reported sensitivity for the detection of bone infections ranges from 89?G2to 100%~.3This diagnostic technique has therefore been advocated for osteomyelitis at ditTerent skeletal sites.‘, ‘M There have. however. been few studies of the application of bone scanning of lesions in the jaws7 Bone scintigraphy for osteomyelitis 01 the mandible has. as far as I know, only been reported for a few patients. x.y 4 systematic evaluation of the diagnostic potential of bone scintigraphy in different stages of osteomyelitis in the mandible appears not to have been performed. The aim of this study was to 1993 h\, Mwby-Year Book, C opqright 0030-4220/93/$ I .OO + IO 7/ 16/43569
650
Inc
present the diagnostic merits of scintigraphy in early and chronic osteomyelitis localized in the mandible. PATIENTS The sex and age distribution of the 35 patients tire presented in Table I. The patients in this study comprise relevant cases referred for radiologic and scintigraphic ex;tmination between 1979 :tnd 1990. The bone scintigraphy wus performed either to diagnose and locate the extent and activity of osteomyelitis or to exclude osteomyelitis in patients with bone tissue changes that clinically were indicative of osteomyelitis. Eleven scintigraphic follow-up examinations were performed in eight patients. METHODS Clinical examination The written reports on the patients were collected immediately after the scintigraphic examination. Pertinent information on the patients was recorded. 11 any information was ambiguous, the clinician who treated the patient was interviewed. Radiographic
examination
Panoramic radiography was performed for al1 patients with an Orthopantomograph (Palomex Instrumentarium Corp. Helsinki. Finland). Periapical in-
OKAI SUKGERY OK\L MEDICINE, Volume 7.5, Number 5
ORRI
Rohlin
P~TtlOl.o(i\
Table I. Activity degree of uptake in scintigraphic and sex and age distribution of patients I .‘lcrwir,v degree
~
Normal
Age groups /years) 45-59
~~~
~~~ 60
~
TOtal
I
4 I 6
traoral radiographs using a parallelling technique and the mandibular occlusal projection were always also taken. Frontal or lateral tomography was performed in seven patients using a Polytome U with hypocycloidal movement (Massiot/Philips, Paris, France). After the written report was completed, the clinical and radiologic findings were considered jointly by the oral surgeon and the oral radiologist. For the patients reported in this study, bone scintigraphy was considered to be of value. Scintigraphic
using yyTc”‘-labeled methylene diphosphonate
--or-30-44
Sex F M F M F M F M
Lov” increiise Moderate increase Marked increase Tota I
examination
651
examination
Within 2 weeks of the radiographic examination, bone scintigraphy was performed after intravenous injection of about 370 M Bq “9Tc’“-labeled methylene diphosphonate (99Tc”-MDP). The scintigraphy was performed 3 hours later with a gamma camera (Nuclear Chicago, Pho Gamma IV, Chicago, Ill.). The jaws were examined in the anteroposterior and left and right lateral projections. The first scan in anteroposterior projection was performed in fixed time (4 minutes). The lateral scans were made so that the number of counts of each were identical to that of the frontal scan to obtain the same density. Report of findings The report on each patient was written on a special form under the following headings: e clinical examination (onset of symptoms, pain, swelling, tenderness, trismus) l radiographic examination (extent of the lesion, appearance of the bone structure graded in four major patterns as described in Table II, comparison with previous radiographic examinations, tentative diagnosis) l scintigraphic examination (extent of the lesion, the intensity of uptake, graded by interpretation by a nuclear medicine physician as normal uptake, low increase. moderate increase, and marked increase)
comparison between findings of the different examinations The final diagnosis was based on biopsy material (n = 19) the clinical course and follow-up radiographic examinations (n = 16), or both.
l
RESULTS Clinical examination No particularly susceptible age could be identified. Most of the patients had intermittent episodes of tenderness and pain. Six patients had diffuse pain and swelling that was poorly localized. In seven patients an intermittent loss of sensitivity occurred. Radiographic
examination
The lesions were mostly located in the molar region and the mandibular angle. The appearance of the bone structure varied between the lesions and even within the same lesion. The major bone pattern is presented in Table II. In 10 patients the appearance was unspecific and discernible as a poorly delineated area with decreased bone density. A sclerosis was poorly delineated in six patients (Fig. 1, ~1). Nine lesions, most of which had a rather limited extent, were characterized by a poorly delineated bone destruction with a motheaten appearance, sometimes surrounded by sclerotic bone tissue. In 10 patients a permeated bone destruction with penetration of the cortex was observed (Fig. 2, A and E). In most cases there was a periosteal bone reaction (Fig. 2, B). Scintigraphic
examination
In six patients the uptake was normal (Tables I and II). There was a low increase in 1 I, a moderate increase (Fig. 1, B) in 5, and a marked increase (Fig. 2, C) in 13 other patients. The distribution of activity was found to be nonuniform in the diseased area in one half of the patients (Fig. 2, C).
652
Rohlirl
Fig. 1. A, Panoramic radiograph 01‘5 I-fear-old ~onun with diH‘usc patn around parotid gland reveal, ~r~ght mandible to be sclerotic. B, Bone images (lateral and anleroposterior prelections) 3 hours after injection of ““Tc”‘-labeled MDP shon ;t moderate increase 01‘ uptake in arc;] that corresponds to sclerotic lesion.
Comparison between the findings different examinations (Table II)
of the
The six cases with normal uptake were radiographically characterized by poorly delineated areas with decreased bone density. As the bone scintigraphy showed normal activity, these six patients were screened out and were thought not to have involvement of the bone tissue. For five of these patients the diffuse pain decreased, and four of them are at present asymptomatic. The radiographic follow-up examinations did not reveal any changes of the bone structure
compared with the initial patient.
who
ascribed
examinations.
the symptoms
The sixth
to “oral
galva-
nism,” still complains of pain and swelling. Patients with low increase of the uptake had experienced symptoms from 1 month to I year. The structure of the bone tissue varied but never had the permeated appearance. The extent of the lesion was rather limited. The radiographic examination revealed the same extent of these lesions as the bone scintigraphy. The five patients with moderate increase of the up-
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Fig. 2. A, Panoramic radiograph of S4-year-old man detnonstrates permeateddestruction with multiple illdefined sclerotic and lptic areas and penetration of the cortex of right mandible from midline posteriorly to angulus. Cortical outlines of mandibular canal zre not visible. B, Occlusal projection of right mandible shows permeated destruction and periosteal new bone (avvow.~/.C, Bone images (lateral and anteroposterior proshow marked increase of uptake in area that corresponds to ,jections) 3 hours after injection of “‘Tc”‘-MDP ’ radiographic lesion in right mandible. Increased uptake in left anterior mandible where radiographs revealed unchanged bone structure. D, Panoramic radiograph 4 years later demonstrates expansion of lesion. Entire tnandible except for most superior part on left side is involved. Note configuration of in&urn. which is V-shaped on right side from extended contours of neck and coronoid process.Left side is normal and U-shaped. E, Panoramic radiograph 6 years after initial examination indicates further progression of lesion on left side.
take had experienced symptoms from 2 months to 2 years. The appearance of the bone structure varied. The radiographic and scintigraphic extent of the lesion were in accord with each other for three lesions (Fig. I) although the other two lesions appeared larger scintigraphically. In I3 patients with marked increase of the uptake, the duration of symptoms varied between I week and I year. Radiographically, the lesions were mostly seen as permeated bone destructions with periosteal bone reaction. The extent of the lesions, which was wide-
spread, was larger scintigraphically for all patients except two (compare Fig. 2, A and Fig. 2, C). Scintigraphic
follow-up
examination
Four patients had a moderate increase of the uptake initially. In three patients the follow-up examination was performed after I year and in one patient after 2 years. The uptake decreased to low uptake in three patients. Their clinical symptoms have decreased more and more during the following years. In the fourth patient the uptake remained moderate
654
Rohlitt
joints reveal erosive hone changeh 01 Fig. 2. F, Sagittal tomograms of right and left temporomandihular cond\ile. Outlines of temporal component arc well detined. G, Bone images (lateral and anteropostcrior projections) present marked increase of uptake in ramuh. condyle, and coronoid process: there is no uptake in temporal hone. Anterior region ol’ mandible shows decrease in uptake compared with Fig. 2, c‘.
after 1 year. He still has recurrent pain and swelling but the periods of remission have become longer. Among the patients with marked increase of the uptake, one patient had one follow-up examination. and three patients went through two folto*-ups each. One lesion showed only minimal uptake I jear after the primary examination even though the patient complained of tenderness and pain. After 3 !ears. the patient was asymptomatic. The other three patients exhibited marked increase at both follou-up examnations and their clinical symptoms relapsed even though they were given high doses of antibiotic\. One of these patients is illustrated in Fig. 2. DISCUSSION The experience from application of boric scintigraphy in osteomyelitis of the mandible in this study is summarized in Table III. In the early stage of osteomyelitis, the patient may have clinical symptoms like diffuse pain and negative or equivocal radiographic findings such ;is localized osteoporosis. The diagnosis in the mandible may therefore be dificult to confirm from the clinical and radiographic tindings. similar to early osteomyelitis in orthopedic patients.j, “I I’ An-
other factor that complicates the diagnosis of osteomyelitis ofthejaws is that inconclusive clinical symptoms ma\ raemble those of patients who ascribe their s!;mptoms to “oral @vanism.” In the present study, hone scintigrams presenting normal uptake made it possible to exclude bone tissue changes in six patients. :IS :I negnti\,c ‘lOT~“‘-s~;~n rules out boric tissue invol\ernent. >I positive one, on the other hand, indicates sctivc boric tissue but i\ nonspecific for inflamnlatorq Icsionx. .Zn increase of uptake is seen both in arca with norn\al increased bone activity. for example. cpiphyseal ccntcrs in children and healing boric tiauc, and in ;IIX:;I~ with pathologic bone reactions as ;I result of ncoptastic disease or inflammation. U9Tc”‘accumulation alter injection of ““Tc”‘-labeled phosphorus con~pou~~Cl~ reflects an increase of the apposition of hydra\!apatite in hard tissue”, Ii and in pathologic calcifications of soft tissue.” .As shown in the diagrum (Fig. 3) of diagnostic methods. boric tI\uc reaction, and latency period, the period of Iatenc) hctween ;I stimulus that might give rise to clinical ~>mptoms and the increased apatite l’ormation rcveuled by 5cintigraphy is often shorter than that of the \trucfural change revealed by radi-
OK.\I SI’KC,I K\ OK\, MI,DI(‘I~\I; Volume 75, Numhcr 5
OK\L
III. Possible findings of radiographic scintigraphy in osteomyelitis
Table
*s/aye of (Ii.\ease Initial I:,stahli\hed
Chronic After-
“flare-ups” treatment
Kohlin
P\r~woc;\
Radiographic
and scintigraphic
.jindings ~__~
1~_
examinations and diagnostic value of bone
Srintigraphic __ ~~
,jnding.~ -~~ ---T
Value of scitztigraph
Increased
uptake
To detect
Increased
uptake
Changed bone structure Changed bone structure
Normal or increased Normal or increased
To determine exact extent i,f bone lesion To identify most active are., of lesion To evaluate extent and degree 01 activity To evaluate treatment
uptake
disease
I
None or equivocal Changed bone structure
ography. The period of latency for osteomyelitis in the mandible is said to be about IO days from the onset of clinical symptoms to the radiographic changes.13 Such a delay in treatment might significantly lessen the chance of cure.“. I6 In general, the bone scan is highly sensitive after the first 3 days from the onset of symptoms but shorter times, 24 to 48 hours, have also been reported. ‘. lo Increased activity that indicates bone tissue involvement may even precede the clinical symptoms5- 6. “’ The shorter lag-time of scintigraphy is beneficial not only for the early detection of osteomyelitis but also to visualize the true extent of the lesion in the established disease stage as shown in Table III. Scintigraphy was of particular value to exclude progression beyond the mandible in two patients. In 13 other patients. the bone scans compared with the radiographs revealed a larger extent, which was manifested in later radiographic follow-up examinations. A marked increase of the uptake was found in most lesions presenting a larger extent scintigraphically than radiographically. Besides the marked increase, most of these lesions were radiographically characterized as permeated bone destruction with penetration of the cortex and periosteal reaction, reflecting an aggressive bone lesion. As also found by Jacobsson et al.,” the uptake of L)9T~“’was inhomogeneous in some lesions, indicating different degrees of activity inside the same lesion. For planning surgical interventions and obtaining representative biopsy specimens, scintigraphy can be advantageous to identify the region of interest. Chronic osteomyelitis of the mandible remains a difficult infection to treat. As suggested in Table III, bone scintigraphy might be useful as a means of evaluating the treatment of osteomyelitis. The radiographic examination is sometimes not specific enough to constitute a basis for the evaluation of the treat-
655
(screening)
uptake
ment, as the altered structure of the bone tissue remains irrespective of whether the therapy is successful or not. Successful therapy was associated with a decrease in uptake in the whole lesion in four patients and in parts of the lesion in one patient. In one patient the decrease of the uptake preceded the decrease of clinical symptoms. To increase the diagnostic potential of scintigraphy in inflammations, new compounds have recently been introduced. These compounds are based on the main characteristics of acute inflammation, that is, the exudation of fluid and plasma protein and attraction of leucocytes into the affected area and they are, for example y9Tcm-nanocolloid’7 (small human albumin I9 or 99T~mcollid ‘particles), “‘In-oxine-labeled.“. labeled white blood cells.17 Although Vorne et a1.17 found a high diagnostic accuracy for 99Tc’“-nanoco1loid in infectious bone and joint diseases, they advocated further evaluation of the method. “Blood-pool” images, that is, images taken immediately after the injection of 9yTcm-MDP, have also been suggested to improve the diagnostic value of bone scintigraphy, particularly to distinguish osteomyelitis from cellulitis.‘. lo A further refinement of this method is dynamic quantitative bone scintigraphy, comprising serial images from I minute to 240 minutes after the injection. Such a technique with high reproducibility (SD + 7%) has been developed at our hospital for the examination of skeletal metastases in patients with prostaticcarcinoma. *OCurrently, weapply themethod in patients with osteomyelitis in the mandible to investigate whether time-count rate curves can provide additional diagnostic information. I conclude that bone scintigraphy is a useful complement to clinical and radiographic examinations in the diagnosis of osteomyelitis in different stages. To interpret the scintigraphic results accurately, one
656 Rohlin DIAGNOSTIC
METHOD
BONE TISSUE
History (possible symptoms)
REACTION
LATENCY
PERIOD
stimulus subjective
Histology
osteoblast
Bone scintigraphy
Radiography
----------------Lincreased apatite formation __----_-_L----__-increased collagen formation
changed
1-2 days
bone
about
structure
10 days
Fig. 3. Diagram shows place of scintigraphy in diagnostic methods. Increased apatite formation that occurs as reactive response in osteomyelitis is observable by scintigraphy. After longer latency period, increased bone apposition and resorption result in change of bone structure so that reaction will also be observable by radiography. must, however, be familiar with the mechanisms, both biochemical and physiologic, that affect the uptake of 99Tcm-labeled MDP. Above all, the 99Tcm-MDP bone scintigram can be advocated in cases with inconclusive clinical and radiographic findings as a negative scan rules out a bone lesion, and a positive scan indicates a bone lesion. In chronic osteomyelitis, scintigraphy is valuable for the determination of the exact extent and the most active region of the lesion for the preoperative planning. Scintigraphy might also be advantageous in the evaluation of the treatment. REFERENCES I. Wannfors K. Chronic osteomyelitis of the jaws [Thesis]. Stockholm: Karolinska Insitutet, 1990:6-56. 2. Howie DW, Savage JP, Wilson TG, Paterson D. The technctium bone scan in the diagnosis of osteomyelitis in childhood. J Bone Joint Surg [Am] 1983;65:431-7. 3. Al-Scheikh W, Sfakianakis GN, Mnayamneh W. et al. Subacute and chronic bone infections: diagnosis using In-1 I I. Ga-67 and Tc-99m MDP bone scintigraphy and radiography Radiology 1985;155:501-6. 4. Duszynski DO, Kuhn JP, Afshani E, Riddlesberger MM Jr. Early radionuclide diagnosis of acute osteomyelitis. Radiology I975;l I7:337-40. 5. Stoles PV, Hilty MD, Sfakianakis GN. Bone scan patterns in acute osteomyelitis. Clin Orthop 1980;153:2 I O-7.
6. Mortensson W. Edeburn G, Fries M, Nilsson R. Chronic recurrent multifocal osteomyelitis in children: a roentgenologic and scintigraphic investigation. Acta Radio1 198X:29:56570.
7. Reiskin AB. Lurie AC;. Specialized radiographtc techniques. In: GoaL DW. White SC, eds. Oral radiology: principles and interpretation. St Louis: CV Mosby, 1987:3X)-2. 8. Graffman S, Rangne A. Scintigraphy in the diagnosis 01’ osteomyelitis of the jaws. Int J Oral Surg 1977:6:247-50. 9. Jacobsson S, Hollender L, Lindberg S, Larsson .A. Chrontc sclerosing osteomyelitis of the mandible: scintigraphic and radiographic findings. 0~4~ Sr RG ORAL MED ORN PATWI I978:45:
167-73.
IO. Gilday DL. Lng B, Paul DJ, Paterson J. Diagnosis 01 osteomyelitis in children by combined blood pool and bone imaging. Radiology 1975:l 17:331-5. I I Park H-M. Wheat LJ. Siddiqui AR. et al. Scintigraphic evaIuation of diabetic osteomyelitis: concise communication. .I Nucl Med 1982;23:569-73. I?. Rohlin M, Larsson A, Hammarstrom L. ‘)‘)“?l c-labeled phosphorus compounds. Ca-45 and Sr-85 in diphosphonate-treated rats. Acta Radio1 1977:16:5 13-24. 13. Lysell L, Rohlin M. Initial Tc-99m diphoaphonate uptake 11, mineralized and demineralized bone implants in rats. Int J Oral Surg 1985:14:371-5. 13. Lodwick GS. Reactive response to local injury in bone, Radio1 Clin North Am 1964;l 1:2OY-19. 15. Harris NH. Some problems in the diagnosis and treatment 01’ acute osteomyelitis. J Bone Joint Surg [Br] 1960:42:535-41 16. .Jacobsson S, Hollender L. Treatment and prognosis of diffuse sclerosing osteomyelitis (DSO) of the mandible. 0~41 SIIRG OK!\~
MFD OK,\I
PATIWL
1980;49:7-
14.
17 Vorne M. Lantho T, Paakkinen S, Salo S. Soinr I. Clinical
Rohlin
ORhl SLlRGtRY ORAI MI L>ICII\IEOR41 P4THOl.OGY Volume 75. Number 5 comparison of 99Tcm-HMPA0 labeled leucocytes and 99T~mnanocolloid in the detection of inflammation. Acta Radio1 1989:30:663-7. 18. Giitzfried HF, Paulus GW, Feistel H. Diagnostik und Verlaufkontrolle der Kieferosteomyelitis durch 4-Phasen und markierte Leukolyten-szintigraphie. Fortschr Kiefer Gesichtschir E in Jahrbuch. XXX11 1987:172-j. 19. Adatepe MH, Potiell OM, lsaacs GH, Nichols K, Cefola R. Hematogenous pyogenic vertebral osteomyelitis: diagnostic. J Nucl Med 1986;27:1680-5. 20. Sundkvist GMG. Ahlgren L, Lilja B. Mattsson S. Abraham-
BOUND
VOLUMES
AVAILABLE
657
sson P-A. Dynamic quantitive bone scintigraphy in patients with prostatic carcinoma treated by orchiectomy. Eur J Nucl Med 1990:16:671-6. Reprint requests. Madeleine Rohlin, DDS, Odont Dr Department of Oral Radiology Centre for Oral Health Sciences Carl Gustafs v$g 34 S-2 I4 2 I MalmB, Sweden
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Thirty-five patients each with a tentattve diagnoses of osteomyelitrs of the mandible were examined with ggTcm-labeled phosphorus compounds. The scintigraphic findings were compared with the radiographic features and related to disease stages to evaluate the diagnostic potential of bone scintigraphy in different disease stages. The scintigraphy was valuable to exclude bone tissue involvement in some patients with clinical stgns and symptoms similar to those of osteomyelitts and with equivocal radiographic findings. In 13 patients with chronic osteomyelitis. scintigraphy revealed a larger extent of the lesion than the radiography. In lesions with permeated bone destructions with penetration of the cortex, the uptake of ggT~m was higher than in lesions with a motheaten or sclerotic appearance. This study supports the view that ggTcm-bone scintigraphy is a useful tool at various stages of osteomyelitrs, that is. In its early detection, in the treatment or biopsy plannrng. and in the evaluation of the efficacy of treatment IOK\,
Sr RI, OH\I
Mm
OH\I
P\IIIOI
0
1993;75:650-71
steomyelitis localized in the mandible can often be diagnosed on the basis of clinical and radiographic evaluations. However, in some patients the clinical presentation is not specific, and the radiographic signs are vague, making the diagnosis difficult to establish in early stages. Early diagnosis is of primary concern. One of the major conclusions of Wannfors’ extensive study’ on chronic osteomyelitis of the jaws was that prompt action at the onset of initial symptoms was decisive for the prognosis. Bone scintigraphy with ““Tc”‘-labeled diphosphonates has been shown to be a sensitive method for the identification of focal bone disease. The reported sensitivity for the detection of bone infections ranges from 89?G2to 100%~.3This diagnostic technique has therefore been advocated for osteomyelitis at ditTerent skeletal sites.‘, ‘M There have. however. been few studies of the application of bone scanning of lesions in the jaws7 Bone scintigraphy for osteomyelitis 01 the mandible has. as far as I know, only been reported for a few patients. x.y 4 systematic evaluation of the diagnostic potential of bone scintigraphy in different stages of osteomyelitis in the mandible appears not to have been performed. The aim of this study was to 1993 h\, Mwby-Year Book, C opqright 0030-4220/93/$ I .OO + IO 7/ 16/43569
650
Inc
present the diagnostic merits of scintigraphy in early and chronic osteomyelitis localized in the mandible. PATIENTS The sex and age distribution of the 35 patients tire presented in Table I. The patients in this study comprise relevant cases referred for radiologic and scintigraphic ex;tmination between 1979 :tnd 1990. The bone scintigraphy wus performed either to diagnose and locate the extent and activity of osteomyelitis or to exclude osteomyelitis in patients with bone tissue changes that clinically were indicative of osteomyelitis. Eleven scintigraphic follow-up examinations were performed in eight patients. METHODS Clinical examination The written reports on the patients were collected immediately after the scintigraphic examination. Pertinent information on the patients was recorded. 11 any information was ambiguous, the clinician who treated the patient was interviewed. Radiographic
examination
Panoramic radiography was performed for al1 patients with an Orthopantomograph (Palomex Instrumentarium Corp. Helsinki. Finland). Periapical in-
OKAI SUKGERY OK\L MEDICINE, Volume 7.5, Number 5
ORRI
Rohlin
P~TtlOl.o(i\
Table I. Activity degree of uptake in scintigraphic and sex and age distribution of patients I .‘lcrwir,v degree
~
Normal
Age groups /years) 45-59
~~~
~~~ 60
~
TOtal
I
4 I 6
traoral radiographs using a parallelling technique and the mandibular occlusal projection were always also taken. Frontal or lateral tomography was performed in seven patients using a Polytome U with hypocycloidal movement (Massiot/Philips, Paris, France). After the written report was completed, the clinical and radiologic findings were considered jointly by the oral surgeon and the oral radiologist. For the patients reported in this study, bone scintigraphy was considered to be of value. Scintigraphic
using yyTc”‘-labeled methylene diphosphonate
--or-30-44
Sex F M F M F M F M
Lov” increiise Moderate increase Marked increase Tota I
examination
651
examination
Within 2 weeks of the radiographic examination, bone scintigraphy was performed after intravenous injection of about 370 M Bq “9Tc’“-labeled methylene diphosphonate (99Tc”-MDP). The scintigraphy was performed 3 hours later with a gamma camera (Nuclear Chicago, Pho Gamma IV, Chicago, Ill.). The jaws were examined in the anteroposterior and left and right lateral projections. The first scan in anteroposterior projection was performed in fixed time (4 minutes). The lateral scans were made so that the number of counts of each were identical to that of the frontal scan to obtain the same density. Report of findings The report on each patient was written on a special form under the following headings: e clinical examination (onset of symptoms, pain, swelling, tenderness, trismus) l radiographic examination (extent of the lesion, appearance of the bone structure graded in four major patterns as described in Table II, comparison with previous radiographic examinations, tentative diagnosis) l scintigraphic examination (extent of the lesion, the intensity of uptake, graded by interpretation by a nuclear medicine physician as normal uptake, low increase. moderate increase, and marked increase)
comparison between findings of the different examinations The final diagnosis was based on biopsy material (n = 19) the clinical course and follow-up radiographic examinations (n = 16), or both.
l
RESULTS Clinical examination No particularly susceptible age could be identified. Most of the patients had intermittent episodes of tenderness and pain. Six patients had diffuse pain and swelling that was poorly localized. In seven patients an intermittent loss of sensitivity occurred. Radiographic
examination
The lesions were mostly located in the molar region and the mandibular angle. The appearance of the bone structure varied between the lesions and even within the same lesion. The major bone pattern is presented in Table II. In 10 patients the appearance was unspecific and discernible as a poorly delineated area with decreased bone density. A sclerosis was poorly delineated in six patients (Fig. 1, ~1). Nine lesions, most of which had a rather limited extent, were characterized by a poorly delineated bone destruction with a motheaten appearance, sometimes surrounded by sclerotic bone tissue. In 10 patients a permeated bone destruction with penetration of the cortex was observed (Fig. 2, A and E). In most cases there was a periosteal bone reaction (Fig. 2, B). Scintigraphic
examination
In six patients the uptake was normal (Tables I and II). There was a low increase in 1 I, a moderate increase (Fig. 1, B) in 5, and a marked increase (Fig. 2, C) in 13 other patients. The distribution of activity was found to be nonuniform in the diseased area in one half of the patients (Fig. 2, C).
652
Rohlirl
Fig. 1. A, Panoramic radiograph 01‘5 I-fear-old ~onun with diH‘usc patn around parotid gland reveal, ~r~ght mandible to be sclerotic. B, Bone images (lateral and anleroposterior prelections) 3 hours after injection of ““Tc”‘-labeled MDP shon ;t moderate increase 01‘ uptake in arc;] that corresponds to sclerotic lesion.
Comparison between the findings different examinations (Table II)
of the
The six cases with normal uptake were radiographically characterized by poorly delineated areas with decreased bone density. As the bone scintigraphy showed normal activity, these six patients were screened out and were thought not to have involvement of the bone tissue. For five of these patients the diffuse pain decreased, and four of them are at present asymptomatic. The radiographic follow-up examinations did not reveal any changes of the bone structure
compared with the initial patient.
who
ascribed
examinations.
the symptoms
The sixth
to “oral
galva-
nism,” still complains of pain and swelling. Patients with low increase of the uptake had experienced symptoms from 1 month to I year. The structure of the bone tissue varied but never had the permeated appearance. The extent of the lesion was rather limited. The radiographic examination revealed the same extent of these lesions as the bone scintigraphy. The five patients with moderate increase of the up-
OR.\1
Volume
SliKCit
RY OR\1
7.5. Number
b~l~L)ICIP\L.
OR,\l.
hl
Rohlin
1101 O(;l
653
5
Fig. 2. A, Panoramic radiograph of S4-year-old man detnonstrates permeateddestruction with multiple illdefined sclerotic and lptic areas and penetration of the cortex of right mandible from midline posteriorly to angulus. Cortical outlines of mandibular canal zre not visible. B, Occlusal projection of right mandible shows permeated destruction and periosteal new bone (avvow.~/.C, Bone images (lateral and anteroposterior proshow marked increase of uptake in area that corresponds to ,jections) 3 hours after injection of “‘Tc”‘-MDP ’ radiographic lesion in right mandible. Increased uptake in left anterior mandible where radiographs revealed unchanged bone structure. D, Panoramic radiograph 4 years later demonstrates expansion of lesion. Entire tnandible except for most superior part on left side is involved. Note configuration of in&urn. which is V-shaped on right side from extended contours of neck and coronoid process.Left side is normal and U-shaped. E, Panoramic radiograph 6 years after initial examination indicates further progression of lesion on left side.
take had experienced symptoms from 2 months to 2 years. The appearance of the bone structure varied. The radiographic and scintigraphic extent of the lesion were in accord with each other for three lesions (Fig. I) although the other two lesions appeared larger scintigraphically. In I3 patients with marked increase of the uptake, the duration of symptoms varied between I week and I year. Radiographically, the lesions were mostly seen as permeated bone destructions with periosteal bone reaction. The extent of the lesions, which was wide-
spread, was larger scintigraphically for all patients except two (compare Fig. 2, A and Fig. 2, C). Scintigraphic
follow-up
examination
Four patients had a moderate increase of the uptake initially. In three patients the follow-up examination was performed after I year and in one patient after 2 years. The uptake decreased to low uptake in three patients. Their clinical symptoms have decreased more and more during the following years. In the fourth patient the uptake remained moderate
654
Rohlitt
joints reveal erosive hone changeh 01 Fig. 2. F, Sagittal tomograms of right and left temporomandihular cond\ile. Outlines of temporal component arc well detined. G, Bone images (lateral and anteropostcrior projections) present marked increase of uptake in ramuh. condyle, and coronoid process: there is no uptake in temporal hone. Anterior region ol’ mandible shows decrease in uptake compared with Fig. 2, c‘.
after 1 year. He still has recurrent pain and swelling but the periods of remission have become longer. Among the patients with marked increase of the uptake, one patient had one follow-up examination. and three patients went through two folto*-ups each. One lesion showed only minimal uptake I jear after the primary examination even though the patient complained of tenderness and pain. After 3 !ears. the patient was asymptomatic. The other three patients exhibited marked increase at both follou-up examnations and their clinical symptoms relapsed even though they were given high doses of antibiotic\. One of these patients is illustrated in Fig. 2. DISCUSSION The experience from application of boric scintigraphy in osteomyelitis of the mandible in this study is summarized in Table III. In the early stage of osteomyelitis, the patient may have clinical symptoms like diffuse pain and negative or equivocal radiographic findings such ;is localized osteoporosis. The diagnosis in the mandible may therefore be dificult to confirm from the clinical and radiographic tindings. similar to early osteomyelitis in orthopedic patients.j, “I I’ An-
other factor that complicates the diagnosis of osteomyelitis ofthejaws is that inconclusive clinical symptoms ma\ raemble those of patients who ascribe their s!;mptoms to “oral @vanism.” In the present study, hone scintigrams presenting normal uptake made it possible to exclude bone tissue changes in six patients. :IS :I negnti\,c ‘lOT~“‘-s~;~n rules out boric tissue invol\ernent. >I positive one, on the other hand, indicates sctivc boric tissue but i\ nonspecific for inflamnlatorq Icsionx. .Zn increase of uptake is seen both in arca with norn\al increased bone activity. for example. cpiphyseal ccntcrs in children and healing boric tiauc, and in ;IIX:;I~ with pathologic bone reactions as ;I result of ncoptastic disease or inflammation. U9Tc”‘accumulation alter injection of ““Tc”‘-labeled phosphorus con~pou~~Cl~ reflects an increase of the apposition of hydra\!apatite in hard tissue”, Ii and in pathologic calcifications of soft tissue.” .As shown in the diagrum (Fig. 3) of diagnostic methods. boric tI\uc reaction, and latency period, the period of Iatenc) hctween ;I stimulus that might give rise to clinical ~>mptoms and the increased apatite l’ormation rcveuled by 5cintigraphy is often shorter than that of the \trucfural change revealed by radi-
OK.\I SI’KC,I K\ OK\, MI,DI(‘I~\I; Volume 75, Numhcr 5
OK\L
III. Possible findings of radiographic scintigraphy in osteomyelitis
Table
*s/aye of (Ii.\ease Initial I:,stahli\hed
Chronic After-
“flare-ups” treatment
Kohlin
P\r~woc;\
Radiographic
and scintigraphic
.jindings ~__~
1~_
examinations and diagnostic value of bone
Srintigraphic __ ~~
,jnding.~ -~~ ---T
Value of scitztigraph
Increased
uptake
To detect
Increased
uptake
Changed bone structure Changed bone structure
Normal or increased Normal or increased
To determine exact extent i,f bone lesion To identify most active are., of lesion To evaluate extent and degree 01 activity To evaluate treatment
uptake
disease
I
None or equivocal Changed bone structure
ography. The period of latency for osteomyelitis in the mandible is said to be about IO days from the onset of clinical symptoms to the radiographic changes.13 Such a delay in treatment might significantly lessen the chance of cure.“. I6 In general, the bone scan is highly sensitive after the first 3 days from the onset of symptoms but shorter times, 24 to 48 hours, have also been reported. ‘. lo Increased activity that indicates bone tissue involvement may even precede the clinical symptoms5- 6. “’ The shorter lag-time of scintigraphy is beneficial not only for the early detection of osteomyelitis but also to visualize the true extent of the lesion in the established disease stage as shown in Table III. Scintigraphy was of particular value to exclude progression beyond the mandible in two patients. In 13 other patients. the bone scans compared with the radiographs revealed a larger extent, which was manifested in later radiographic follow-up examinations. A marked increase of the uptake was found in most lesions presenting a larger extent scintigraphically than radiographically. Besides the marked increase, most of these lesions were radiographically characterized as permeated bone destruction with penetration of the cortex and periosteal reaction, reflecting an aggressive bone lesion. As also found by Jacobsson et al.,” the uptake of L)9T~“’was inhomogeneous in some lesions, indicating different degrees of activity inside the same lesion. For planning surgical interventions and obtaining representative biopsy specimens, scintigraphy can be advantageous to identify the region of interest. Chronic osteomyelitis of the mandible remains a difficult infection to treat. As suggested in Table III, bone scintigraphy might be useful as a means of evaluating the treatment of osteomyelitis. The radiographic examination is sometimes not specific enough to constitute a basis for the evaluation of the treat-
655
(screening)
uptake
ment, as the altered structure of the bone tissue remains irrespective of whether the therapy is successful or not. Successful therapy was associated with a decrease in uptake in the whole lesion in four patients and in parts of the lesion in one patient. In one patient the decrease of the uptake preceded the decrease of clinical symptoms. To increase the diagnostic potential of scintigraphy in inflammations, new compounds have recently been introduced. These compounds are based on the main characteristics of acute inflammation, that is, the exudation of fluid and plasma protein and attraction of leucocytes into the affected area and they are, for example y9Tcm-nanocolloid’7 (small human albumin I9 or 99T~mcollid ‘particles), “‘In-oxine-labeled.“. labeled white blood cells.17 Although Vorne et a1.17 found a high diagnostic accuracy for 99Tc’“-nanoco1loid in infectious bone and joint diseases, they advocated further evaluation of the method. “Blood-pool” images, that is, images taken immediately after the injection of 9yTcm-MDP, have also been suggested to improve the diagnostic value of bone scintigraphy, particularly to distinguish osteomyelitis from cellulitis.‘. lo A further refinement of this method is dynamic quantitative bone scintigraphy, comprising serial images from I minute to 240 minutes after the injection. Such a technique with high reproducibility (SD + 7%) has been developed at our hospital for the examination of skeletal metastases in patients with prostaticcarcinoma. *OCurrently, weapply themethod in patients with osteomyelitis in the mandible to investigate whether time-count rate curves can provide additional diagnostic information. I conclude that bone scintigraphy is a useful complement to clinical and radiographic examinations in the diagnosis of osteomyelitis in different stages. To interpret the scintigraphic results accurately, one
656 Rohlin DIAGNOSTIC
METHOD
BONE TISSUE
History (possible symptoms)
REACTION
LATENCY
PERIOD
stimulus subjective
Histology
osteoblast
Bone scintigraphy
Radiography
----------------Lincreased apatite formation __----_-_L----__-increased collagen formation
changed
1-2 days
bone
about
structure
10 days
Fig. 3. Diagram shows place of scintigraphy in diagnostic methods. Increased apatite formation that occurs as reactive response in osteomyelitis is observable by scintigraphy. After longer latency period, increased bone apposition and resorption result in change of bone structure so that reaction will also be observable by radiography. must, however, be familiar with the mechanisms, both biochemical and physiologic, that affect the uptake of 99Tcm-labeled MDP. Above all, the 99Tcm-MDP bone scintigram can be advocated in cases with inconclusive clinical and radiographic findings as a negative scan rules out a bone lesion, and a positive scan indicates a bone lesion. In chronic osteomyelitis, scintigraphy is valuable for the determination of the exact extent and the most active region of the lesion for the preoperative planning. Scintigraphy might also be advantageous in the evaluation of the treatment. REFERENCES I. Wannfors K. Chronic osteomyelitis of the jaws [Thesis]. Stockholm: Karolinska Insitutet, 1990:6-56. 2. Howie DW, Savage JP, Wilson TG, Paterson D. The technctium bone scan in the diagnosis of osteomyelitis in childhood. J Bone Joint Surg [Am] 1983;65:431-7. 3. Al-Scheikh W, Sfakianakis GN, Mnayamneh W. et al. Subacute and chronic bone infections: diagnosis using In-1 I I. Ga-67 and Tc-99m MDP bone scintigraphy and radiography Radiology 1985;155:501-6. 4. Duszynski DO, Kuhn JP, Afshani E, Riddlesberger MM Jr. Early radionuclide diagnosis of acute osteomyelitis. Radiology I975;l I7:337-40. 5. Stoles PV, Hilty MD, Sfakianakis GN. Bone scan patterns in acute osteomyelitis. Clin Orthop 1980;153:2 I O-7.
6. Mortensson W. Edeburn G, Fries M, Nilsson R. Chronic recurrent multifocal osteomyelitis in children: a roentgenologic and scintigraphic investigation. Acta Radio1 198X:29:56570.
7. Reiskin AB. Lurie AC;. Specialized radiographtc techniques. In: GoaL DW. White SC, eds. Oral radiology: principles and interpretation. St Louis: CV Mosby, 1987:3X)-2. 8. Graffman S, Rangne A. Scintigraphy in the diagnosis 01’ osteomyelitis of the jaws. Int J Oral Surg 1977:6:247-50. 9. Jacobsson S, Hollender L, Lindberg S, Larsson .A. Chrontc sclerosing osteomyelitis of the mandible: scintigraphic and radiographic findings. 0~4~ Sr RG ORAL MED ORN PATWI I978:45:
167-73.
IO. Gilday DL. Lng B, Paul DJ, Paterson J. Diagnosis 01 osteomyelitis in children by combined blood pool and bone imaging. Radiology 1975:l 17:331-5. I I Park H-M. Wheat LJ. Siddiqui AR. et al. Scintigraphic evaIuation of diabetic osteomyelitis: concise communication. .I Nucl Med 1982;23:569-73. I?. Rohlin M, Larsson A, Hammarstrom L. ‘)‘)“?l c-labeled phosphorus compounds. Ca-45 and Sr-85 in diphosphonate-treated rats. Acta Radio1 1977:16:5 13-24. 13. Lysell L, Rohlin M. Initial Tc-99m diphoaphonate uptake 11, mineralized and demineralized bone implants in rats. Int J Oral Surg 1985:14:371-5. 13. Lodwick GS. Reactive response to local injury in bone, Radio1 Clin North Am 1964;l 1:2OY-19. 15. Harris NH. Some problems in the diagnosis and treatment 01’ acute osteomyelitis. J Bone Joint Surg [Br] 1960:42:535-41 16. .Jacobsson S, Hollender L. Treatment and prognosis of diffuse sclerosing osteomyelitis (DSO) of the mandible. 0~41 SIIRG OK!\~
MFD OK,\I
PATIWL
1980;49:7-
14.
17 Vorne M. Lantho T, Paakkinen S, Salo S. Soinr I. Clinical
Rohlin
ORhl SLlRGtRY ORAI MI L>ICII\IEOR41 P4THOl.OGY Volume 75. Number 5 comparison of 99Tcm-HMPA0 labeled leucocytes and 99T~mnanocolloid in the detection of inflammation. Acta Radio1 1989:30:663-7. 18. Giitzfried HF, Paulus GW, Feistel H. Diagnostik und Verlaufkontrolle der Kieferosteomyelitis durch 4-Phasen und markierte Leukolyten-szintigraphie. Fortschr Kiefer Gesichtschir E in Jahrbuch. XXX11 1987:172-j. 19. Adatepe MH, Potiell OM, lsaacs GH, Nichols K, Cefola R. Hematogenous pyogenic vertebral osteomyelitis: diagnostic. J Nucl Med 1986;27:1680-5. 20. Sundkvist GMG. Ahlgren L, Lilja B. Mattsson S. Abraham-
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sson P-A. Dynamic quantitive bone scintigraphy in patients with prostatic carcinoma treated by orchiectomy. Eur J Nucl Med 1990:16:671-6. Reprint requests. Madeleine Rohlin, DDS, Odont Dr Department of Oral Radiology Centre for Oral Health Sciences Carl Gustafs v$g 34 S-2 I4 2 I MalmB, Sweden
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