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Year : 2022  |  Volume : 18  |  Issue : 3  |  Page : 617-622

Bone invasion in oral squamous cell carcinoma: Comparative analytic study in orthopantomogram and technetium 99 m bone scan

Department of Oral Medicine and Radiology, Government Dental College and Hospital, Ahmedabad, Gujarat, India

Date of Submission16-Dec-2020
Date of Acceptance12-Aug-2021
Date of Web Publication16-Feb-2022

Correspondence Address:
Jaya Dubey
Department of Oral Medicine and Radiology, Government Dental College and Hospital, Ahmedabad - 380 016, Gujarat
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jcrt.JCRT_1642_20

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 > Abstract 

Aims and Objective: To compare the bone invasion in orthopantomogram (OPG) and technetium 99 m bone scan in oral squamous cell carcinoma (OSCC).
Materials and Methods: Clinically and histopathologically proven 30 cases of OSCC were randomly selected. OPG and Tech 99m bone scan was carried out in all selected patients. The results were analyzed according to age, sex, and site of involvement. OPG findings and bone scanning uptake were also compared according to site, grade, and difference of uptake.
Results: Group of patients which showed definite bone invasion in OSCC were positive in radionuclide uptake imaging while another group of patients which showed no changes in OPG had some patients which were positive on radionuclide uptake imaging while few were negative on both OPG and bone scanning.
Conclusion: Combination of OPG and Tech 99m bone scan was more accurate in detecting bone invasion in OSCC than OPG and bone scan alone.

Keywords: Bone invasion, oral squamous cell carcinoma, orthopantomogram, technetium (Tech) 99m bone scan

How to cite this article:
Shah JS, Dubey J, Rathva YK. Bone invasion in oral squamous cell carcinoma: Comparative analytic study in orthopantomogram and technetium 99 m bone scan. J Can Res Ther 2022;18:617-22

How to cite this URL:
Shah JS, Dubey J, Rathva YK. Bone invasion in oral squamous cell carcinoma: Comparative analytic study in orthopantomogram and technetium 99 m bone scan. J Can Res Ther [serial online] 2022 [cited 2022 Aug 10];18:617-22. Available from: https://www.cancerjournal.net/text.asp?2022/18/3/617/337794

 > Introduction Top

Oral squamous cell carcinoma (OSCC) is the most common cancer of the oral cavity and constitutes 90%–95% of all oral malignancy. In India, oral cancer accounts for up to 30%–50% of all cancer.[1] Oral malignancy is responsible for considerable morbidity and mortality, therefore, an accurate staging, which include evaluation of bone involvement, is crucial for treatment planning and for improving survival rates. These tumors have tendency to invade the surrounding bone structures, and this occur in 12%–88% of the cases. An important factor in pretreatment evaluation of oral cancer patients is the assessment of the presence and extent of bone invasion. Preoperative evaluation of the bone for invasion by tumor has always been a difficult problem.[2] For a treatment perspective, it is crucial to determine the bone involvement caused by these tumors, and more importantly, the amplitude of bone involvement, since an underestimation lead to a partial resection, resulting in local recurrence and potential metastasis. Clinical evaluation is very important to assess the presence of bone involvement in oral malignancies. Several imaging modalities such as conventional radiography, ultrasonography, computed tomography (CT), bone scanning, and magnetic resonance imaging (MRI) have been used to investigate the presence of bone involvement in oral cancer. All these methods have their own advantages and limitation. Various new diagnostic methods such as combined CT and positron emission tomography scan can bring an atomic localization to the metabolic lesion activity with improved diagnostic capability.[3],[4]

Panoramic radiographs play an important role in the detection of bone invasion by oral carcinoma, especially in determining the superior–inferior extent of the tumor in the bone, which is one of the most important factors influencing the selection between rim and segmental resection of the mandible. Orthopantomograms (OPGs) are unable to detect bone invasion until 30% of the mineral content has lost and also deficient in the evaluation of symphyseal region.[5] CT in the preoperative assessment of malignant tumors seems to be most valuable technique, because it shows bone and soft tissues and has a highest sensitivity and specificity for assessment of bone destruction. MRI has the advantage of better demonstration of soft tissue and tumor interfaces.[6]

Bone scanning is a nuclear medicine technique, which is possibly one of the most commonly performed functional diagnostic procedures. Bone scintigraphy with 99tc-labelled bisphosphonates has been proposed as an alternative, highly sensitive method for the detection of even minimal bone involvement as it is able to reveal increased metabolic bone activity and precise localization of increased bone metabolism in patient with malignant bone lesion. It may be positive even if there is approx. 10% increase in osteoblastic activity than normal. Due to higher sensitivity it has an ability to show very early physiological changes in bone. However, it has been found to be non-specific and its resolution is not high as that of radiographs and does not show morphological alteration. Hybrid Tc scan/OPG has high sensitivity and specificity in detecting the existence and extent of malignant bone infiltration.[5],[7]

Conventional radiography including OPG is insensitive to early bone changes but provides accurate morphological information necessary for tumor localization and detection of structural abnormalities. Whereas nuclear bone scan is a highly sensitive but lack structural delineation. Hence, it is difficult to locate the focus. Therefore, the fusion of functional and static imaging may be more accurate in defining the surgical margin than individual imaging. The study had been carried out in clinically and histologically diagnosed OSCC cases to evaluate bone invasion in OPG and bone scanning by recording uptake level in affected area. Till today, many studies had been done showing various imaging methods to know the bone invasion and its extent in OSCC, but they were mostly aimed on CT and MRI. This study aimed to evaluate the same by doing OPG and bone scanning as very few reports available on the same.

 > Materials and Methods Top

This descriptive study was carried out in our institute. Ethical approval was taken for the study as well as informed consent was obtained from all subjects. Clinically and histologically diagnosed 30 cases of OSCC were selected irrespective of age, sex, and site of involvement in mandible and maxilla. Patients having inflammatory periapical or periodontal diseases and jaw bone disease such as fibrous dysplasia, osteomyelitis, osteosarcoma, osteonecrosis, Paget's disease, and osteoporosis were excluded as radiotracer uptake may increase in defective area of bone. Pregnant women were also excluded.

OPG and bone scan was carried out in all selected patients. OPG was performed on a Planmeca Proline Excess machine, with parameters 65–70 Kvp, 10 mA at 10s. Bone scintigraphy was performed by using GE-INFINIA machine in dual head gamma camera with parallel hole collimator and dose of 10–20 mci, 70–74 mbq Tc-99m methylene diphosphate (MDP) is injected intravenous and various image were taken like an anterior and both lateral projections were performed with respect to mandible and maxilla. The radionuclide imaging studies and OPG were evaluated in detail.

Thirty patients were divided into two groups based on OPG findings. OPG of Group I (15 patients) was showing bone invasion and they were categorized in three grades based on extension of bone invasion, periphery, internal structure, and effects on surrounding structures [Table 1], and the comparison of bone invasion and radiotracer uptake according to OPG grade were carried out [Table 2]. Whereas in Group II (15 patients), OPGs were not showing any bony invasion. Patients of both groups were analyzed for uptake of Tech 99m on affected and nonaffected side of jaws and difference were noted [Table 3].
Table 1: Grading criteria of bone invasion (oral squamous cell carcinoma) in orthopantomogram

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Table 2: Group I radiotracer uptake according to orthopantomogram grade (n=15)

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Table 3: Difference in uptake of Tec 99m

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The results were also analyzed to find the occurrence of OSCC according to age, sex, and site of involvement. OPG findings and bone scanning uptake were also evaluated for mandibular or maxillary OSCC at different localities.

Clinical diagnostic criteria of oral squamous cell carcinoma

It may appear in the form of ulceroproliferative growth or as nonhealing ulcer showing following characteristics[8]

  • Color-Mixed reddish to pinkish whitish
  • Surface-Papillary projections with ulcerations
  • Border-Raised, Everted and irregular
  • Edge-Rolled out
  • Base-Indurated
  • Tenderness-usually Non-tender
  • Bleeding on probing-Present
  • Floor-Fixed to underlying structures.

Diagnostic criteria to detect bone invasion in oral squamous cell carcinoma in orthopantomogram

  1. Periphery:

    1. Ill-defined/well-defined
    2. Rounded regular/irregular in shape
    3. Localized to that area or extended border due to osseous destruction and when very extensive leads to pathologic fracture.

  2. Internal structure of lesion-complete radiolucent/presence of little residual bone (radiopaque foci)/septa within radiolucent lesion
  3. Surrounding structures

  1. Destruction of antral/nasal floor in maxillary lesion and Destruction of cortical outline of mandibular canal in mandibular lesion
  2. Root resorption
  3. Floating tooth appearance as surrounding bone and lamina dura both are affected.

Interpretation of bone scanning

  • Ideally there should be a uniform and symmetrical distribution of tracer in the skeletal system
  • Since the skeletal system is symmetrical along the longitudinal axis, images of the two halves of the body serves as an internal control for comparison and any differential uptake on two sides will be picked up
  • Bone scintigraphy is subjective assessment and consider positive when there is increase in the intensity of radiotracer uptake on affected side. It may be positive if there is only approximately 10% increase in osteoblastic activity above normal.[9],[10]

 > Results Top

Comparative analytic evaluation of the efficacy of clinical examination, site of involvement, OPG grading, and radiotracer uptake difference is shown in [Table 3]. In this study, OSCC was found to occur between the age group of 24–76 years with a mean age of 46.26 years and was more reported in male (73.33%) than females (26.66%), as shown in [Table 4]. The study reported maximum cases of OSCC in mandible than maxilla and only 1 case was reported on tongue. In mandible, 14 cases (56%) were present on alveolus [Figure 1] and 11 cases (44%) on gingivabuccal sulcus [Figure 2]. In maxilla, three cases (75%) were reported over palate [Figure 3] and 1 case (25%) on posterior alveolus, as shown in [Table 5]a. The uptake at bone scanning was also analyzed according to the site of involvement in OSCC cases. Out of 15 cases of OSCC of alveolus of mandible and maxilla, 13 (86.66%) cases showed increase in uptake in bone scan, whereas two (13.33%) cases did not show any increase in uptake on affected side as compared to that of nonaffected side. Out of 11 cases of gingival buccal sulcus OSCC, nine (81.81%) cases showed increase in uptake while 2 (18.18%) cases did not show any changes in uptake on affected side in bone scan. Out of three cases of palatal OSCC 2 (66.66%) cases showed increase in uptake and 1 (33.33%) case did not show any increase in uptake. Only 1 case of tongue carcinoma was reported and it did not show any increase in uptake in bone scanning on affected side, as shown in [Table 5]b. The result of bone scintigraphy on affected and nonaffected side was evaluated in all 30 cases of OSCC of both groups, as shown in [Table 3]. Group I had 15 patients showing bone invasion in OPG findings and increase in radiotracer uptake was noticed in all 15 cases (100%) on affected side of OSCC, whereas in group II (not showing bone invasion on OPG) out of 15 patients, 9 (60%) patients exhibited increase in radiotracer uptake and 6 (40%) patients were not showing any increase in radiotracer uptake on affected side, as shown in [Table 6]. An attempt has been made to compare results of radiotracer uptake and its difference with grading criteria of bone invasion in OPG findings. In Group I, out of 15 patients, two patients (13.33%) showed Grade I type [Figure 2]b of bone invasion and had 20907–31070 range at Tec 99m uptake [Figure 2]c, 11 patients (73.33%) showed Grade II type [Figure 3]b of bone invasion and had 10081–24970 range [Figure 3]c at uptake in bone scanning and Grade III type [Figure 1]b of bone invasion was noted in two patients (13.33%) and had 15788–17076 range [Figure 1]c at uptake in bone scanning, as shown in [Table 2].
Table 4: Age and sex-wise distribution of patient (n=30)

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Figure 1: (a) Carcinoma of right lower mandibular alveolus. (b) Orthopantomogram Grade III bone invasion. (c) Positive radiotracer uptake on affected side

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Figure 2: (a) Shows carcinoma of right lower gingival-buccal sulcus. (b) Orthopantomogram Grade I bone invasion. (c) Positive radiotracer uptake

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Figure 3: (a) Carcinoma of left hard palate. (b) Orthopantomogram Grade II bone invasion. (c) Positive radiotracer uptake on affected side

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Table 5:

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Table 6: Radiotracer uptake (n=30)

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 > Discussions Top

OSCC can be detected at an early stage, but successful treatment depends on total eradication of the primary tumor and any cervical lymph node metastases.[11] The correct extension of cancer in the bone usually remains undetected on static imaging which may lead to inadequate or overexcision. The conventional radiography as well as other anatomical imaging modalities such as CT, MRI often fails to detect functional changes in the bone. However, bone scintigraphy is highly sensitive in detecting earlier changes in the bone but lack anatomical definitions.[12]

Ninety-five percent of OSCC occur in individuals in over 40 years of age. Our study result was similar to other studies as Rao et al. and Luyk et al. Worldwide, the incidence of head and neck OSCC is higher in male than female similar results was present in our study, this sex difference in oral cancer may largely reflect more indulgence of men in risk factors and also different cultural behavior and lifestyle factors among population.[1],[9],[13],[14]

Similar to available literature, our study also showed mandible was the most commonly involved (86.66%) than maxilla (13.33%), It is because of placement of tobacco is more common in lower gingivobuccal sulcus and also duration of chemical exposure near mandible.[13] The higher incidence of bone invasion in lower alveolus is similar to that of other studies by Rao et al. and Albuquerque et al. due to proximity of bone to the tumor and also to that of thin layer of soft tissue layer which allows a rapid bone invasion by tumor.[3],[5] Ca of tongue is most common OSCC of oral cavity, but on the basis of only 1 case, it is difficult to conclude bone invasion; therefore, more cases will require to show sensitivity on bone scan.

The radiotracer uptake was negative in two cases of alveolus, 2 cases of gingivobuccal sulcus, 1 case of palate and 1 case of tongue, all these negative radionuclide imaging is from group II in which there were no bone invasion in OPG. These finding shows that negative radionuclide uptake indicates no bone invasion and that suspicion of bone invasion on clinical grounds and conventional findings are likely to result in unnecessary mandibular resection. In Group II which was not showing bone invasion in OPG, 9 cases showed positive findings on bone scan. This results shows that there is an early bone involvement in bone scan due to its sensitivity. Radionuclide bone imaging detects bone invasion through increased osteoblastic activity at site of microscopic bone invasion and can therefore, detect bone invasion in early stage.[11]

The radiotracer uptake and OPG grading was also compared in Group I which suggest that as bone invasion is more in OPG, no. of uptake is decreased in bone scanning. As we know the hydroxyapatite crystal is most accessible to MDP in exposed bone, such as area of increased osteogenic or bone remodeling (i.e., altered metabolism). Old compact bone does not bind MPD as efficiently. Therefore, any focal increase in the osteogenic activity is visualized as hot spot so that in early grades there is enough bone present to uptake radiotracer. However, replacement of bone by destructive lesion results in an area of reduced radioactivity (cold spot). Therefore, radiotracer uptake decreases as bone destruction increases.[9]

 > Conclusion Top

OSCC being the most common malignancy of the oral cavity mostly occur in male and involved mandible more than maxilla. Panoramic radiographs being static imaging helpful in localization of lesion and detection of bone involvement in the later stage of OSCC.[10] While bone scintigraphy which is valuable and versatile medicine tool provides a “functional map” of bone remodeling is very sensitive technique to detect early invasion.[9],[15] This study has shown that clinical judgement in bone invasion by the lesion is only accurate in gross disease and even OPG are only reliable when there is extensive disease. If the panoramic radiograph is negative or equivocal, the bone scan can definitely be useful in showing the earliest stage of tumors invasion, that is, periosteal reaction.[14] Therefore, hybrid of panoramic and bone scan has high sensitivity and specificity in detecting the existence and extent of bone infiltration in OSCC.

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Conflicts of interest

There are no conflicts of interest.

 > References Top

Shah P, Venkatesh R, More C, Vassandacoumara V. A retrospective radiographic analysis of osseous changes in oral malignancy. jiaomr 2016;28:236-41.  Back to cited text no. 1
Kushraj T, Chatra L, Shenai P, Rao PK. Bone invasion in oral cancer patients: A comparison between orthopantamograph, conventional computed tomography, and single positron emission computed tomography. J Cancer Res Ther 2011;7:438-41.  Back to cited text no. 2
Albuquerque MA, Kuruoshi ME, Oliveira IR, Cavalcanti MG. CT assessment of the correlation between clinical examination and bone involvement in oral malignant tumors. Braz Oral Res 2009;23:196-202.  Back to cited text no. 3
Ahuja RB, Soutar DS, Moule B, Bessent RG, Gray H. Comparative study of technetium-99M bone scans and orthopantomography in determining mandible invasion in intraoral squamous cell carcinoma. Head Neck 1990;12:237-43.  Back to cited text no. 4
Rao LP, Das SR, Mathews A, Naik BR, Chacko E, Pandey M. Mandibular invasion in oral squamous cell carcinoma: Investigation by clinical examination and orthopantomogram. Int J Oral Maxillofac Surg 2004;33:454-7.  Back to cited text no. 5
Momin MA, Hashimoto K, Honda K, Yosue T. Validity of computed tomograpghy (CT) for the assessment of mandibular bone invasion by squamous cell carcinoma in oral cavity. JSM Dent 2013;2:1021.  Back to cited text no. 6
Jamdade AS, John A. Technetium-99m bone scan and panoramic radiography in detection of bone invasion by oral carcinoma. J Clin Diagn Res 2014;8:C49-53.  Back to cited text no. 7
Das S. A Manual on Clinical Surgery: Including Special Investigations and Differential Diagnosis. Published by Dr. S. Das, Kolkata. 2011.  Back to cited text no. 8
Gupta V. Bone scintigraphy in the evaluation of cancer. Kathmandu Univ Med J 2005;3:243-8.  Back to cited text no. 9
Jamdade A, John A. Bone scintigraphy and panoramic radiography in deciding the extent of bone resection in benign jaw lesions. J Clin Diagn Res 2013;7:2351-5.  Back to cited text no. 10
Lewis-Jones HG, Rogers SN, Beirne JC, Brown JS, Woolgar JA. Radionuclide bone imaging for detection of mandibular invasion by squamous cell carcinoma. Br J Radiol 2000;73:488-93.  Back to cited text no. 11
Suzuki A, Togawa T, Kuyama J, Nakahara T, Kinoshita F, Takenouchi T, et al. Evaluation of mandibular invasion by head and neck cancers using 99m Tc-methylene diphosphonate or 99m Tc-hydroxymethylene diphosphonate and 201 Tl chloride dual isotope single photon emission computed tomography. Ann Nucl Med 2004;18:399-408.  Back to cited text no. 12
Tandon A, Bordoloi B, Jaiswal R, Srivastava A, Singh RB, Shafique U. Demographic and clinicopathological profile of oral squamous cell carcinoma patients of North India: A retrospective institutional study. SRM J Res Dent Sci 2018;9:114.  Back to cited text no. 13
  [Full text]  
Luyk NH, Laird EE, Ward-Booth P, Rankin D, Williams ED. The use of radionuclide bone scintigraphy to determine local spread of oral squamous cell carcinoma to mandible. J Maxillofac Surg 1986;14:93-8.  Back to cited text no. 14
Adams C, Banks KP. Bone Scan. Treasure Island: StatPearls Publishing; 2020.  Back to cited text no. 15


  [Figure 1], [Figure 2], [Figure 3]

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]


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