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Year : 2022  |  Volume : 10  |  Issue : 2  |  Page : 49-56

The role of 18F-fluorodeoxyglucose positron emission tomography/computed tomography in oral squamous cell carcinoma: A systematic review

Department of Oral Medicine and Maxillofacial Radiology, Dr. G. D Pol Foundations YMT Dental College and Hospital, Navi Mumbai, Maharashtra, India

Date of Submission08-May-2022
Date of Decision30-May-2022
Date of Acceptance16-Jun-2022
Date of Web Publication22-Jul-2022

Correspondence Address:
Simran Naresh Verma
Dr. G. D. Pol Foundations YMT Dental College and Hospital, Sector- 4, Kharghar, Navi Mumbai - 410 210, Maharashtra
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jomr.jomr_12_22

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Objective: The aim of this study was to systematically review the literature to assess the role of 18F-fluorodeoxyglucose (FDG) positron emission tomography (PET)/computed tomography (CT) in oral squamous cell carcinoma (OSCC). Materials and Methods: The literature was searched using MEDLINE and ScienceDirect databases. Studies comparing fusion imaging PET/CT with other imaging modalities in the staging, identifying secondary metastasis, treatment response assessment, and follow-up of OSCC, were deemed eligible. Results: Six studies met the inclusion criteria. The average mean was found to be 85.47%, 78.80%, 78.50%, and 89.22% for sensitivity, specificity, positive predictive value (PPV), and negative predictive value, respectively. The risk of bias graph shows that there was 50% low risk of bias in selection of patients, more than 25% low risk of bias in conduct/interpretation of the index test, and > 25% risk of bias in reference standard. 18F-FDG PET/CT is a good prognostic factor for overall and progression-free survival. Conclusion: FDG PET/CT has a good diagnostic accuracy for identifying metastatic nodes, especially subcentimeter metastatic nodes that appear morphologically normal on CT images. PET/CT is promising in the diagnosis and evaluation of distant metastases and for identifying unknown and second primary malignancies. Advances in Knowledge: Fusion imaging is gaining importance with its ability to identify tumor as small as 0.5 mm and provide early diagnosis, thereby increasing quality of life of patients. PET/CT provides valuable information for therapeutic planning, therapeutic assessment, follow-up, and surveillance in the care of patients with OSCC.

Keywords: 18F-fluorodeoxyglucose, lymph nodes, metastasis, oral squamous cell carcinoma, positron emission tomography/computed tomography

How to cite this article:
Verma SN, Das DA. The role of 18F-fluorodeoxyglucose positron emission tomography/computed tomography in oral squamous cell carcinoma: A systematic review. J Oral Maxillofac Radiol 2022;10:49-56

How to cite this URL:
Verma SN, Das DA. The role of 18F-fluorodeoxyglucose positron emission tomography/computed tomography in oral squamous cell carcinoma: A systematic review. J Oral Maxillofac Radiol [serial online] 2022 [cited 2022 Dec 5];10:49-56. Available from: https://www.joomr.org/text.asp?2022/10/2/49/351667

  Introduction Top

Head-and-neck squamous cell carcinomas develop from the mucosal epithelium in the oral cavity, pharynx, and larynx and are the most common malignancies that arise in the head-and-neck region. Epidemiological studies have revealed a diverse range of risk factors for oral squamous cell carcinoma (OSCC) as classified by the International Agency for Research on Cancer (IARC) of the World Health Organization. These risk factors include tobacco consumption, alcohol consumption, both of which can have a synergistic effect, exposure to environmental pollutants, and infection with viral agents such as human papillomaviruses and Epstein–Barr virus. Among some Asia-Pacific populations, oral cancer is associated with chewing of areca nut products including betel quid including variety of customized mixtures of areca nut, betel leaf, slaked lime, and/or tobacco, as well as spices according to the local custom.[1] In worldwide reports, cancers of all regions of the oral cavity are grouped and collectively represent the sixth most common cancer in the world.[2] According to the latest reports of the IARC and GLOBOCAN for OSCC, annual incidence is higher around the world, which is over 3 million diagnosed cases and the annual mortality is about 1,45,000 deaths.[1],[3] The development of squamous cell carcinoma of the oral cavity is considered a complex multistep process. Normal oral mucosal keratinocytes are chronically exposed to risk factors, which can break the homeostasis and generate genetic instability. The proliferation and uncontrolled growth, along with a battery discharge, granted adaptive advantages over the surrounding cells, which promote local invasion and orchestrate a collaboration of the surrounding stromal cells.[4] The addition of fusion imaging PET/CT scans to achieve both an anatomical aspect to the image via the CT component and a functional aspect via the PET component has shown to improve clinical staging of OSCC over PET or CT alone.[5] A major advantage of PET/CT over PET alone is the notable reduction in scanning time. In this fusion imaging, the CT data are used for attenuation correction and a whole-body scan can be performed in 2 min. An additional advantage of PET/CT is that the intrinsic hardware provides high-quality images through coregistration of both image datasets in a relatively fast acquisition time.[6] PET/CT is an imaging modality with high diagnostic performance in the assessment of head-and-neck squamous cell carcinomas and induced a significant change in the management of the study population.[5]

It has its applications in pretreatment staging of OSCC, radiotherapy (RT) planning, treatment response assessment, and posttherapy follow-up. The purpose of this article is to systematically review the role of 18F-FDG PET CT in OSCC.

  Materials and Methods Top

Protocol and registration

Analysis and inclusion criteria methods were specified in advanced and documented in the protocol for systematic review according to Preferred Reporting Items for Systematic Reviews and Meta – Analyses- Protocol.

Types of publication

The review included studies on human and published in English language.

Types of studies

The review included randomized controlled trials, clinical trials, and research and review articles, which were published between May 2005 and March 2021.

Information sources

The information source was the MEDLINE (PubMed) and ScienceDirect library.

Type of population

Patients of all sex and ages who were diagnosed with squamous cell carcinoma of the oral cavity.

Disease definition

OSCC refers to cancer occurring between the vermillion border of the lips and the junction of the hard and soft palate or the posterior one-third of the tongue starting in squamous cells, thin, flat cells lining the inside of the lips and oral cavity.

Literature search strategy

Wide search of online literature was done using databases: MEDLINE (PubMed) and ScienceDirect library to find studies that included the role of 18F-FDG PET/CT in OSCC.

Keywords used for the search

“18F FDG PET CT IN ORAL CANCER” AND “SQUAMOUS CELL CARCINOMA” AND “HUMAN TRIALS.” The search was limited to English language and matching with the title. Articles published from May 2005 to March 2021 were searched.

Inclusion criteria

All the included studies should have followed the inclusion criteria listed as follows:

  1. Studies of patients with OSCC
  2. RCT, clinical trials, and research and review articles
  3. Studies with the amount of more than 15 individuals
  4. Studies published between May 2005 and March 2021
  5. Studies in English language
  6. Studies on humans.

Exclusion criteria

The following exclusion criteria were applied to all the articles:

  1. Studies on animals, not on humans
  2. Systematic reviews and meta-analysis
  3. Studies including SCC apart from oral cavity.

Sequential search strategy

The selected articles were subjected to clear inclusion and exclusion criteria. Following the initial literature search, all articles' titles were chosen according to title relevancy, considering the exclusion criteria. The following studies were based on irrelevant data obtained from the abstracts. The final stage of screening involved reading the full texts and confirming each study's eligibility based on the inclusion and exclusion criteria.

Statistical analysis

Assessment of risk of bias in the included studies

This assessment was conducted using the recommended approach for assessing risk of bias in studies included in Cochrane Reviews using the tool RevMan 5.4.

We used the two-part tool to address the specific domains, using QUADAS tool for quality checks. Each domain includes one or more specific entries in a “risk of bias” table. Within each entry, the first part of the tool involves describing what was reported to have happened in the study. The second part of the tool involves assigning a judgment relating to the risk of bias for that entry: low risk, unclear risk, or high risk.

The domains of sequence generation, allocation concealment, incomplete outcome data, and selective outcome reporting were addressed in the tool by a single entry for each study. There was a good reliability between the two reviewers with a high kappa coefficient (k > 0.89).

We completed a “risk of bias” table for each included study. We also presented the results graphically.

Risk of bias assessment parameters

  1. Bias in selection of patients
  2. Bias in the conduct or interpretation of index test
  3. Concern that the index test, its conduct or interpretation differ from the review question
  4. Bias in reference standard, its conduct, or its interpretation have introduced bias
  5. Concern in target condition defined does not match the review question
  6. Bias due to patient flow.

  Results Top

The above PRISMA diagram [Figure 1] shows that the initial computerized search strategy yielded 1984 titles. In the first case, selection authors screened the articles by reading titles and abstracts of the retrieved publications and 1165 were discarded because these articles did not meet the inclusion criteria.
Figure 1: PRISMA DIAGRAM showing article selection for the role of 18F-FDG PET/CT in OSCC

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Out of 819 articles, 468 articles were eliminated as they were systematic reviews and meta-analysis. Out of 351 full-text articles, 345 were discarded as they were animal-based studies, studies in language other than English, and squamous cell carcinoma other than oral cavity. Six articles met our inclusion criteria completely. Most of these studies showed promising role of 18F-FDG PET/CT in providing valuable information for therapeutic planning, therapeutic assessment, follow-up, and surveillance in the care of patients with OSCC.

[Graph 1] shows 50% low risk of bias in selection of patients, more than 25% low risk of bias in conduct/interpretation of the index test, and >50% low risk of bias in concern that the index test, its conduct, or its interpretation differs from the review question. There is <25% risk of bias in reference standard, its conduct, or its interpretation that could have introduced bias, 50% low risk of bias in concern to target condition not matching the review question and a little more than 25% low risk of bias due to patient flow [Graph 1].

The average mean was calculated for sensitivity, specificity, PPV, and NPV, which was found to be 85.47%, 78.80%, 78.50%, and 89.22%, respectively [Table 1].
Table 1: Average mean-sensitivity, specificity, positive predictive value and negative predictive value

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This risk of bias table shows that Angelina Cistara et al. took efforts to address each risk of bias item for the study whereas the study conducted by Chun Ta Liao et al. only took care of bias in selection of patients and not of other parameters. Hidetomo Nishilawa et al. in his study only addressed the concern in the target condition defined does not match the review question. Piere Delable et al. did not address bias in selection of patients and bias due to patient flow, other parameters gave unclear results. Pasha et al.'s study also gave unclear results for the risk of bias included in his study.[11],[20],[10],[21],[7] Tzu Chen Yen et al. addressed all the parameters except the bias in reference standard, its conduct, or its interpretation that could have introduced bias [Figure 2].[17]
Figure 2: Risk of bias summary: Review authors' judgments about each risk of bias item for each included study

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  Discussion Top

18F-FDG PET/CT has entered a new phase of development since a major technologic breakthrough in past 20 years. Its application in oral cancers has become one of the standard imaging modalities in staging, restaging, treatment planning, and monitoring of therapeutic efficacy. This systematic review was an attempt to summarize the literature of the studies conducted to evaluate the role of 18F-FDG PET/CT in OSCC. Our search comprised 5 clinical trials. We found that 18F-FDG PET/CT had a plethora of roles in OSCC.

Tzu Chen et al. in their study observed an incidence of 49% cervical nodal metastases for BSCC patients, with most of these cases involving patients above 35 years of age. The presently observed incidence of nodal metastases was higher in Taiwanese population than the incidence found in Indian patients, despite similar pathology in the two populations. It is conceivable that with similar etiologies, difference in tumor biology can exist.[8],[9] Nishikawa et al. proved that 18F-FDG PET/CT has 100% sensitivity, 85.7% specificity, 90.5% accuracy, and standardized uptake value (SUV) max ≥3.5. They also stated that delayed cervical lymph node metastasis of stage I and stage II OSCC has been reported to occur at a frequency of 22%. In their study, detection of cervical lymph node metastasis was possible using only FDG PET/CT, but not by conventional diagnostic procedures, in 3 of 7 patients (42.9%). It might therefore be possible to prevent delayed metastases in OSCC using FDG PET/CT during preoperative tests. They suggested that FDG PET/CT is a useful conventional methodology for diagnosis of metastasis; the criterion for this technique is still undecided [Table 2]. Further studies are required to improve the reliability of a universal cutoff value for SUVmax.[10]
Table 2: Characteristics of studies

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In the literature, there have been reports of studies which have introduced open-mouth scan that leads to increased space between the oral structures. This method allowed a much better evaluation of the palate, tongue, and alveolar ridge structures. For each true-positive result, the site was effectively identified and extent of the primary lesion was determined more easily using the open mouth scan, whereas tumor localization failed in 38% of the patients evaluated using closed-mouth technique. The better results of the open-mouth scan are even more evident when considering tumor extent and involvement of the adjacent structures.

These data suggest that the open-mouth scan could be a great aid in detecting tumors of unknown origin in patients affected by laterocervical lymph node metastases.[11]

A study was conducted by Chun Ta Liao et al. to focus on the implications of pre-RT/concurrent chemo RT (CCRT) FDG PET for RT/CCRT planning in patients with OSCC disease. The pre-RT/CCRT FDG PET/CT scan led to a modification of treatment strategy in 7 of the 29 OSCC patients with extracapsular spread (ECS). ECS to the cervical lymph nodes is the most significant adverse prognostic indicator in OSCC patients.[20] The presence of extra nodal invasion of the cervical lymph nodes reflects a significant adverse shift in tumor behavior.[16],[17] The authors have listed five important findings in the study: first, pre-RT/CCRT PET results may prompt treatment modification in as many as 24% of high risk OSCC patients. Second, subjects in their study underwent a pre-RT/CCRT PET scan and had a higher rate in the early event detection. Among these patients, two remained diseases free at 7 and 23 months after surgery. Third, they proved that a pre-RT/CCRT PET scan may be particularly beneficial in OSCC patients with both ECS and SUV nodal values > 5.2 in the first PET scan. Fourth, the 29 patients who underwent a second PET scan showed an encouraging trend toward an improved survival compared with the cohort of 154 patients who did not undergo a second PET scan. Fifth, among the 29 high-risk OSCC patients who received a second PET scan, in three of the patients, the treatment plan was changed from curative to palliative treatment, and in four, either the radiation dose or the field of their adjuvant treatment plan was changed. Hence, they hypothesized that high-risk OSCC patients with ECS and patients with SUV nodal values ≥5.2 at the primary staging FDG PET scan could benefit from a second 18F-FDG PET/CT scan.[18]

Lee et al.[19] studied the prognostic role of FDG PET/CT in the care of 57 patients with N0 squamous cell carcinoma of the oral portion of the tongue and said that MTV is an independent prognostic factor. The presence of occult metastases in N0 OSCC can be correlated with MTV volumes, as confirmed by Chung et al.[20] Matsubara et al. conducted a study to evaluate the nodal staging of oral cavity cancers using FDG PET/CT and compared it with other treatment modalities, which showed that PET/CT had 77% sensitivity, 97% specificity, 76% positive predictive value (PPV), 98% negative predictive value (NPV), and 95% accuracy, whereas ultrasound-CT showed 73% sensitivity, 99% specificity, 88% PPV, 98% NPV, and 96% accuracy.

Pirre Delabie et al. observed a pericardial involvement in 29% of patients, a left atrial involvement in one case, and a myocardial involvement in most cases. Metastases were located in the right and left ventricles, respectively, in about 60% and 40% of cases. Myocardial involvement is almost exclusively the result of retrograde lymphatic spread through tracheal or bronchomediastinal channels. The mean duration between diagnosis of tongue cancer and cardiac metastasis was relatively short at 20 ± 14 months. Although cardiac metastasis usually occurred in patients with advanced stages of the disease, this location was isolated in almost a third of them. 18F-FDG PET/CT was the initial imaging modality in 24% of the patients revealing cardiac metastasis from a tongue cancer. 18F-FDG PET/CT can be proposed as an option in the monitoring of SCC of the oral cavity for the detection of occult recurrence.[21]

Andrade et al. also gave similar findings that diagnostic accuracy by 18F-FDG PET/CT in detecting microscopic disease as well as small tumor residuals in anatomic areas such as the tongue or lymphatic tissue improved, which could potentially replace currently used single modality CT imaging for the assessment of treatment response in head-and-neck cancer.[22] They have also mentioned that FDG PET/CT was a better predictor for the presence of residual disease, after 4 months compared with 4 weeks.[23] Stephen Harre et al. showed the prevalence of DM in their study, which achieved 10% at the time of diagnosis. This rate is in the range of the current literature, though many authors found higher numbers. Teknos et al. found 25% of DM in 12 patients,[24] Brouwer et al. 12% of DM 34 patients[25] and Gourin et al. 19% of DM in 27 patients.[26]

It is well known that 18F-FDG is not a specific radiopharmaceutical marker of malignancy, since 18F-FDG uptake in normal or active inflammatory tissues may occur, thus limiting image interpretation. To overcome these drawbacks, more specific PET tracers reflecting specific biologic tumor characteristics may be useful to differentiate tumors by inflammation, these tracers which are under clinical investigation include 18F– fluorothymidine for DNA synthesis (18F-FLT), 18F-fluoroethyl-L-thyrosine (18F-FET), and L-methyl-11C-methionine (11C-MET) for amino acid uptake and protein synthesis.[27],[28],[29] Among these tracers, 18F-FLT seems to be the most promising because of its specificity. The most important clinically relevant finding given by Helsen et al. was the high NPV.

A negative PET/CT scan is, therefore, highly indicative for the absence of disease obviating further therapeutic interventions.[30] The use of FDG PET/CT surveillance also resulted in less serious adverse events and was cost-effective compared to routine neck dissection.[31] Fakhry et al. reported a higher accuracy for FDG PET/CT than stand-alone FDG-PET, attributable to a higher specificity because of improved anatomical localization, which decreased the number of false positive and equifocal findings.[32] The magnitude and dynamics of this effect have recently been elaborated in the study of Helsen et al.,[33] which confirmed that the diagnostic performance increases until 11 weeks after treatment and reaches a plateau thereafter.

FDG PET/CT is a diagnostic modality in OSCC is not without its share of limitations. 18F-FDG uptake reflects glucose metabolism and can be observed in several normal tissues with wide variability of the normal pattern, including salivary glands, lymphoid tissue, and brown fat as well as in various benign tumors such as common Warthin's tumor.[34] Moreover, the inflammatory processes that occur in patients submitted to surgery or RT are a frequent cause of false positive PET results, since the activated inflammatory cells show increased 18F-FDG uptake.[35],[36] There are a variety of malignant tumors which might be FDG-negative and consequently missed by FDG PET/CT such as low-grade sarcomas or signet ring cell adenocarcinomas.[37],[38],[39] FDG PET has technical resolution limitations of about 5 mm and thus is unlikely to be able to detect small volume disease, contributing to false negative results.[40],[41],[42],[43],[44] In addition for cervical lymph nodes containing micrometastases (size 0.2–2 mm), SUVmax would not indicate any abnormal accumulation. In view of this, FDG PET/CT should be used in combination with sentinel lymph node biopsy.[10]

  Conclusion Top

In the care of patients with OSCC, FDG PET/CT has a good diagnostic accuracy for identifying metastatic nodes, especially subcentimeter metastatic nodes that appear morphologically normal on CT images. PET/CT is promising in the diagnosis and evaluation of distant metastases and for identifying unknown and second primary malignancies. It provides valuable information for therapeutic planning, therapeutic assessment, follow-up, and surveillance in the care of patients with OSCC. FDG PET/CT parameters are predictive of patient survival.

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Conflicts of interest

There are no conflicts of interest.

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