| Abstract|| |
Background: Chemiluminescence is the production of light as a result of a chemical reaction. Oral potentially malignant disorders (OPMDs) include both precancerous lesions and conditions that carry an increased risk of cancer. There are different etiological and risk factors for OPMDs such as smoking, alcohol consumption, infections such as viral and fungal, sun exposure and certain other genetic factors. The most common etiological factor for OPMDs is tobacco usage. Chemiluminescence is a light-based detection system and is very useful for detecting OPMDs for early intervention. Because it is a non-invasive procedure, it can be used to evaluate dysplastic changes in various OPMDs at their initial stage for timely intervention. Vital staining has also been used as a chair-side marker for delineating normal and dysplastic oral mucosal tissues. Aim: To compare the efficacy of chemiluminescence with Lugol's iodine to that with toluidine blue in diagnosing dysplastic changes in tobacco associated oral lesions. Methodology: A total of 84 patients with clinically suspicious oral mucosal lesions and OPMDs with tobacco habit history were included and randomly assigned to either of the diagnostic study groups (Group A: chemiluminescence with Lugol's iodine or Group B: chemiluminescence with toluidine blue). All these patients were subjected to a histopathological examination (reference standard). Results: The sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV), and receiver operating characteristics (ROC) were 91.7%, 66.7%, 84.6%, 80%, and 0.792 for chemiluminescence with Lugol's iodine group (P = 0.001) respectively whereas for chemiluminescence with toluidine blue, the sensitivity, specificity, PPV, NPV and ROC were 100%, 60%, 93.3%, 100% and 0.800 (P = 0.002), respectively. Conclusion: The combination of chemiluminescence with toluidine blue had a better diagnostic efficiency in detecting dysplasia in tobacco-associated oral lesions when compared to the group of chemiluminescence with Lugol's iodine.
Keywords: Chemiluminescence, dysplasia, Lugol's iodine, oral potentially malignant disorders, toluidine blue
|How to cite this article:|
Swathi K V, Maragathavalli G, Uma Maheswari T N. Comparing the efficacy of chemiluminescence with lugol's iodine versus toluidine blue in the diagnosis of dysplasia in tobacco associated oral lesions - A diagnostic study. Indian J Dent Res 2021;32:459-66
|How to cite this URL:|
Swathi K V, Maragathavalli G, Uma Maheswari T N. Comparing the efficacy of chemiluminescence with lugol's iodine versus toluidine blue in the diagnosis of dysplasia in tobacco associated oral lesions - A diagnostic study. Indian J Dent Res [serial online] 2021 [cited 2023 Feb 6];32:459-66. Available from: https://www.ijdr.in/text.asp?2021/32/4/459/337847
| Introduction|| |
According to the evidence-based literature, in India, tobacco consumption has been responsible for half of all cancers in men and one-fourth of cancers in women. It had also been estimated by the World Health Organisation (WHO) that tobacco-related deaths may exceed 1.5 million annually in 2020 in India. Around 7,000 different chemicals have been found in tobacco products, of which more than 60 chemicals have been found to have carcinogenic potential. Tobacco products are available in smoke and smokeless forms. In India, only less than one-fifth (19%) of tobacco consumed is in the form of cigarettes, over half of all tobacco consumed in India is smoked as bidi (Indian specific non-filtered cigarette), which are smoke forms of tobacco, and about one-fourth of tobacco consumption is in smokeless forms, such as chewing tobacco and mishri (prepared by roasting tobacco leaves, used as dentifrice). The WHO in 1978 had initially proposed the terms 'precancerous lesions' and 'precancerous conditions' and the precancerous lesion was defined as 'a morphologically altered tissue in which cancer is most likely to occur than its apparently normal counterpart' and precancerous condition was 'a generalised state where there was an increased risk of cancer'. A workshop in 2005 redefined all oral lesions with a potential for malignant transformation to be grouped under the title 'potentially malignant disorders.' A new term 'potentially premalignant oral epithelial lesion (PPOEL)' has recently been used as a broad term to define both histologic and clinical lesions that have the potential for malignant transformation.
Tobacco-associated oral lesions include tooth stain, tobacco-related blanching of mucosa seen in chewers (chewers mucosa), abrasions, tobacco excrescence, smoker's melanosis, periodontal conditions, burns and keratotic patches, hairy tongue, acute necrotising ulcerative gingivitis, stomatitis nicotina palati (smoker's palate), palatal erosions, leukoplakia and squamous cell carcinomas.
The detection of these OPMDs or oral cancers initially requires a proper clinical visual examination and palpation of the affected site and neck region. There have been various chairside diagnostic tools, which serve as adjuncts for the detection of dysplasia in these lesions, which could aid in timely intervention. These optical devices detect changes in the optical properties of the surface epithelium and submucosa. These changes are based on light absorption, scattering or fluorescence of the tissue. In vivo microscopy uses specific probes for real-time imaging of morphometric features at a gross level for an impression of nuclear and cellular features of the lining mucosa. Vital staining is also one of the most efficient chairside diagnostic tools for detecting dysplasia in various OPMDs. It can be done as supravital or intravital staining. Various stains have been used for vital staining, which include toluidine blue, methylene blue, Lugol's iodine, rose Bengal, acetic acid. Toluidine blue is a basic thiazine metachromatic stain, and Lugol's iodine is potassium iodide in water. According to the literature, these two stains have proven to be very useful in the early detection of dysplastic changes with less number of false-positives or false-negatives; hence, this study aims to compare the diagnostic efficacy of these two stains along with a light-based detection system (chemiluminescence). The gold standard for detection of dysplasia in OPMDs is histopathological examination as it is generally accepted that the histopathological features of a given lesion, especially the presence and degree of epithelial dysplasia, are currently the most useful indicators of the risk of malignant transformation. For an overall accurate assessment of the malignant transformation risk of these OPMDs, all clinical, molecular, and histopathological features must be evaluated properly. These adjunctive diagnostic aids can be used in the timely intervention of oral cancer as they are useful in the early detection of dysplastic changes. They can also be routinely used as a screening tool in patients with suspicious oral mucosal lesions. According to the literature, most studies have explored the diagnostic efficacies of adjuncts such as vital staining, light-based optical devices separately; however, the overall diagnostic accuracy was less compared to that of histopathology; hence, this study was carried out to determine the combined diagnostic efficacy of light-based (chemiluminescence) with vital staining dyes (Lugol's iodine/toluidine blue) with histopathology as the gold standard in the identification of dysplastic lesions in a spectrum of tobacco-associated oral mucosal lesions.
| Aim|| |
To compare the efficacy of chemiluminescence with Lugol's iodine versus toluidine blue in diagnosing dysplastic changes in tobacco-associated oral lesions.
| Objectives|| |
- To test the diagnostic efficacy of chemiluminescence with Lugol's iodine in diagnosing dysplasia in tobacco-associated oral lesions.
- To test the diagnostic efficacy of chemiluminescence with toluidine blue in diagnosing dysplasia in tobacco-associated oral lesions.
- To evaluate which combination of the above is more sensitive and specific in detecting dysplastic changes in tobacco-associated oral lesions.
| Methodology|| |
Diagnostic accuracy study (institutional study).
Patients with a history of tobacco consumption and clinically diagnosed with oral mucosal lesions were selected for the study.
- Patients who were clinically diagnosed with oral mucosal lesions associated with tobacco consumption (smoke/smokeless type of tobacco).
- Oral submucous fibrosis (patients with areca nut chewing were also included in the study if their habit history revealed different types of tobacco chewing/smoking habits at different time frames), leukoplakia, tobacco pouch keratosis, quid-induced, lichenoid reaction, erythroplakia, erythroleukoplakia, proliferative verrucous leukoplakia and other suspicious oral mucosal lesions.
- Patients above 18 years of age.
- Oral mucosal lesions not associated with a tobacco history such as oral lichen planus and certain other autoimmune vesiculobullous lesions.
- Patients who have an allergy to dyes or with known hypersensitivity reactions.
Prior to the start of the study, ethical clearance was obtained from the Institutional Ethical Committee, Saveetha University (SRB/SDMDS11/17OMR/15). Written informed consent was obtained from the study participants prior to the start of the study. The patient information sheet was handed over to each of the patients that explained the study in detail.
Study centre and duration
The study was conducted in Saveetha Dental College, Chennai, from June 2018 to December 2019.
Sample size estimation was done based on the key article (Jain N, Nagarajappa A.K, Bhasin M, Pandya D, and Tripathi K.P. Role of chemiluminescence examination as a non-invasive diagnostic tool in early detection of leukoplakia. Journal of Oral Biology and Craniofacial Research 2018; 8:177–18, original article) using nMaster Software version 2.
Eighty-four patients (with 85 lesions) were enrolled in this study and were randomly assigned to either of the diagnostic study groups (Group A: chemiluminescence with Lugol's iodine, Group B: chemiluminescence with toluidine blue) who were clinically diagnosed with OPMDs or suspicious oral mucosal lesions associated with tobacco consumption habit (smoke/smokeless forms/combinations).
The diagnostic kit [Figure 1] consisted of:
|Figure 1: Diagnostic kit: a) 1% acetic acid solution. b) 1% Lugol's iodine solution, 1% toluidine blue solution. c) Microlux DL transilluminator. d) Parts of the Microlux DL transilluminator|
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- 1% Acetic acid solution
- 1% Lugol's iodine solution
- 1% Toluidine blue solution
- Microlux transilluminator (chemiluminescent light source).
After the initial clinical examination with incandescent light, the patients with oral mucosal lesions were first asked to rinse their mouth twice with water for 20 seconds to remove any debris. This was followed by rinsing the mouth with 1% acetic acid solution for 20 s. Acetic acid acts as a cytoplasmic dehydrant, it also removes any ropey saliva. This was followed by the administration of 1% Lugol's iodine /1% Toluidine blue to the site of the lesion for 20 seconds with a cotton swab in case of localised lesion or given as a rinse in case of diffuse or widespread lesions such as oral submucous fibrosis, multifocal leukoplakia, or when no obvious lesion can be detected. Again the mouth was rinsed twice with 1% acetic acid for 20 seconds to remove any excessive mechanically retained stain. Finally, the mouth was rinsed well with water. Then, the lesions were visualised under a chemiluminescent light source. The chemiluminescent light source was Microlux DL, which is a battery-powered diffused blue-white LED light source to be used for the examination of the oral mucosa. Cells in the normal mucosa absorb the blue–white light, whereas cells with abnormal nuclei in dysplastic mucosa reflect back the light as an acetowhite hue. The presence or absence of adverse reactions such as burning sensation, pain, dysgeusia or dysphagia was noted for all the patients. If there were no adverse reactions, then they were sent for biopsy from the same site of application of the diagnostic test and further histopathological examination.
| Results|| |
The study participants included 84 patients (with 85 lesions), of which 79 were males and 5 were females in the age range from 20 to 80 years. The mean age was 44 years. The gender distribution among Group A and Group B were 94.1% males and 5.9% females, respectively. Exact sig. p = 1.000 (2-sided), 0.556 (1-sided). The true positive and true negative rates of the diagnostic test were 81.2% and 18.8 % respectively (p=0.013) and correlating with the reference test which was histopathology, the true positive rate was 75.4% and true negative rate was 24.6% (p=0.099). The majority of the disease state was true positive. There was statistical significance with regards to the index test. In this study, after the initial clinical examination under chairside light, the patients were subjected to either of the diagnostic tests (Group A or Group B), followed by reference standard (histopathological examination). The degree of uptake of the vital staining (Lugol's iodine/toluidine blue) followed by visualisation under chemiluminescent light source (Microlux DL) correlated with the degree of dysplasia in histopathological examination [Figure 2] and [Figure 3]. In Group A, increased uptake of the stain and no acetowhiteness from chemiluminescence examination revealed no dysplasia. A moderate, mild and no uptake of the stain with increase in the intensity of the acetowhiteness correlated to mild, moderate and severe dysplasia. In Group B, when there was no uptake of the stain and no acetowhiteness from chemiluminescent examination, no dysplasia was seen. Similarly a mild, moderate or severe uptake of stain and increased acetowhiteness correlated with mild, moderate and severe dysplasia, respectively. The cross-tabulation and statistical analysis of the diagnostic test of group A (Lugol's iodine and chemiluminescence) with the histopathological examination (reference standard) revealed a sensitivity of 91.7%, specificity of 66.7%, PPV of 84.6%, NPV of 80%, which were highly statistically significant (p = 0.001) [Table 1]. The area under the receiver operating characteristics (ROC) curve was 0.792 (p = 0.005, lower bound = 0.616, upper bound = 0.968) [Figure 4]. The cross-tabulation and statistical analysis of the diagnostic test of group B (toluidine blue and chemiluminescence) with the histopathological examination (reference standard) revealed a sensitivity of 100%, specificity of 60%, PPV of 93.3% and NPV of 100%, which were highly statistically significant results (p = 0.002) [Table 2]. The area under the ROC curve was 0.800 (p = 0.035, lower bound = 0.526, upper bound = 1.074) [Figure 5].
|Table 1: Cross tabulation and statistical analysis of Diagnostic test (Group A) with reference standard (Histopathological examination)|
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|Table 2: Cross tabulation and statistical analysis of Diagnostic test (Group B) with reference standard (Histopathological examination)|
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|Figure 2: A study subject from Group A subjected to diagnostic test (Lugol's iodine + chemiluminescence) and reference standard (histopathology), The clinical diagnosis of the lesion was speckled leukoplakia in relation to left buccal mucosa. The decreased uptake of Lugol's iodine stain with enhanced acetowhite hue is seen using chemiluminescence. Histopathology is suggestive of hyperparakeratosis with moderate epithelial dysplasia|
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|Figure 3: A study subject from Group B subjected to diagnostic test (toluidine blue + chemiluminescence) and reference standard (histopathology). The clinical diagnosis of the lesion was erythroleukoplakia in relation to left buccal mucosa. An increased uptake of toluidine blue enhanced by acetowhite hue is seen using chemiluminescence. Histopathology is suggestive of moderate epithelial dysplasia|
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| Discussion|| |
This study aimed to assess the efficacy of chemiluminescence along with the combination of vital stains such as Lugol's iodine and toluidine blue in comparison to histopathology as the reference standard for diagnosis of dysplastic changes. The sensitivity, specificity, PPV, NPV and ROC were 91.7%, 66.7%, 84.6%, 80% and 0.792, respectively, for chemiluminescence with Lugol's iodine (p = 0.001), whereas these were 100%, 60%, 93.3%, 100% and 0.800 (p = 0.002), respectively, for chemiluminescence with toluidine blue.
There is a lacuna in the literature that discusses the malignant potential of dysplasia in all tobacco-associated oral lesions, such as smoker's melanosis, palatal changes in reverse smoking, tobacco pouch keratosis and quid-induced lichenoid reactions; however, in our study, a wide spectrum of all tobacco-associated oral mucosal lesions was considered without restricting to OPMDs alone. We included cases such as smoker's melanosis, tobacco pouch keratosis and quid-induced lichenoid reactions as well, which are considered to have the least potential for malignant transformation. These lesions accounted for 7% of the total mucosal lesions of the included patients in our study with a significant likelihood ratio (p = 0.01).
We had a low specificity (60%) in our study as we encountered various confounding factors due to the disease nature such as the presence of inflammatory lesions and benign keratosis that gave false-positive results and affected the outcome of our study, similar to a study done by Awan et al. in 2011 who evaluated the utility of chemiluminescence in the detection of OPMDs and benign keratosis. They found that the chemiluminescent examination had a sensitivity of 77.3%; however, the specificity was only 27.8% because they observed that non-dysplastic lesions (confirmed on histopathological examination) also showed acetowhitening, leading to an increase in the number of false-positive results in their study. In our study, the sensitivity was 100% and the specificity was 60%, as we had included all tobacco-associated oral lesions. The actual disease state was due to the majority of true-positive cases that could reflect a higher sensitivity rate and a lower specificity rate, whereas a study by Chaudhry in 2014, who evaluated the efficacy of chemiluminescence for the diagnosis of leukoplakia, found that chemiluminescence had 93.75% sensitivity and 55.56% specificity in detecting dysplastic changes in leukoplakia in comparison to histopathological examination. The sensitivity and specificity were increased when non-homogeneous leukoplakias were screened with a chemiluminescent examination. Kämmerer et al. in 2015 used a chemiluminescent light system in combination with toluidine blue to assess suspicious oral lesions. They found that sensitivity was 100% and the specificity was 30% when only chemiluminescence was used to dysplastic lesions. When a combination of chemiluminescent examination and toluidine blue stain was used, the sensitivity was 80%, whereas the specificity was 97.5%. They also did a systematic review to validate their results, and it was reported in the literature that chemiluminescent illumination (ViziLite) had a mean sensitivity of 82% and specificity of 25.8%, and when a combination of ViziLite illumination and toluidine blue stain was used as the ViziLite Plus system, the mean sensitivity and specificity were 74% and 69%, respectively. This implies that specificity (the number of false positives) can be increased when toluidine blue stain was used with chemiluminescent illumination, and this was in accordance with our study. Jain et al. in 2018 evaluated the role of chemiluminescence examination as a non-invasive diagnostic tool in the early detection of leukoplakia. They found that a combination of chemiluminescent examination (ViziLite) and toluidine blue demonstrated that the sensitivity was 100% and specificity was 97.3% in detecting dysplastic changes in leukoplakia lesions. The specificity was high in their study as they had seen only in cases of oral leukoplakia, of which most were homogenous types with a high affinity for toluidine blue. However, it was 60% in our study as the disease state was an actual true-positive state and we had also incorporated Lugol's iodine stain along, which is more efficacious in non-keratinised lesions. A study on the comparative morphological analysis of precancerous lesions and conditions by clinical examination, chemiluminescence and toluidine blue by Bagga et al. in 2017 found that the sensitivity, specificity and accuracy of chemiluminescence were 75%, 54.7% and 68%, respectively, in comparison to 57.4%, 44.1% and 44%, respectively, of toluidine blue. However, they had concluded that chemiluminescence and toluidine blue can only serve as adjunctive aids for early diagnosis of oral precancer and cancer, and cannot be compared to histopathological examination. This shows that these chairside adjunctive tools are of great importance to be used as a diagnostic adjunct and for mass screening of oral cancer; however, they require more standardisation in their grading parameters for more conclusive evidence. Regarding the comparison of autofluorescence with vital staining for detection of dysplasia in OPMDs to assess the efficacy of VELscope Vx versus toluidine blue in detecting dysplasia in oral keratotic lesions. It was found that VELscope Vx was able to identify four out of seven cases with mild dysplasia and a case of oral squamous cell carcinoma, whereas toluidine blue (TB) was able to identify five cases and the oral squamous cell carcinoma case as true-positive cases. Thus, sensitivity was 62.5% and 75% for VELscope Vx and TB, respectively. Regarding the specificity of VELscope Vx, it was 71.4%, whereas TB had a specificity of 85.7%; this again differs from our study as the mechanism of VELscope is based on tissue autofluorescence, whereas in our study, we used a chemiluminescent light source. A similar comparative study was done by Adil et al. in 2017 on the efficacy of VELscope and toluidine blue as a screening method in oral potentially malignant and malignant lesions. It was found that VELscope showed 85.36% sensitivity and 75% specificity as compared to toluidine blue that showed 83.13% sensitivity and 87.5% specificity. These findings almost suggest that VELscope has a sensitivity range of 71 to 84% and a specificity range of 85 to 87%, indicating an acceptable diagnostic accuracy in comparison to histopathology.
Until now, there is no standard grading system for visualisation by chemiluminescence that can just detect the possible presence or absence of dysplasia based on the degree of acetowhitening, which was again a potential source for observer bias and also a limitation in our study. However, a study by Epstein et al. in 2008 on the analysis of oral lesion biopsies by visual examination, chemiluminescence and toluidine blue and by evaluating four characteristics of lesions under chemiluminescent examination, namely brightness, sharpness, texture and size, found that in 97 clinically suspicious lesions, the chemiluminescent examination improved the brightness and/or sharpness of the margin in 61.8% of the identified lesions. These observations indicate that for almost a decade, there has been no standard scoring system for chemiluminescence for dysplasia and emphasises the need for the development of the same.
Future scope holds for more research in narrow emission tissue fluorescence, confocal in-vivo microscopy, tissue fluorescence spectroscopy, colposcopy, salivary biomarkers, cell and tissue markers, elastography, surface-enhanced Raman spectroscopy, optical coherence tomography, positron emission tomography, rose Bengal staining, bio-nano chip, and DNA ploidy analysis. The recommendations would be to implement these diagnostic adjuncts as a routine screening tool during routine oral cavity examination as these are non-invasive tools and can aid in the timely diagnosis of these dysplastic lesions. There is also a need for a standardised grading (scoring) system for chemiluminescent and vital staining methods for more conclusive evidence and also to eliminate potential sources of observer bias.
| Conclusion|| |
The detection of oral mucosal lesions, most of the time, is an incidental finding during a routine clinical examination. Chairside diagnostic tools such as chemiluminescence and vital staining are efficient adjuncts in the detection of dysplasia in these oral mucosal lesions. In the literature, various studies have reported the efficacy of these adjuncts for dysplasia detection; however, in this present study, a combination of chemical-based (vital staining) and optical-based (light-based) detection systems have been used to assess whether the efficacy can be improved in terms of sensitivity, specificity, PPV and NPV in the detection of dysplasia in all types of tobacco-associated oral lesions without restricting to the spectrum of OPMDs. Because it is a non-invasive, less time-consuming, efficient chairside diagnostic tool, it can be useful in mass screening for oral mucosal lesions. It can also guide histopathological diagnosis for timely and earlier intervention.
To conclude, a combination of chemiluminescence and vital stains offers a significant diagnostic value for detection of dysplastic changes in the oral mucosal lesions. This can be efficiently implemented as a routine diagnostic screening tool during initial clinical evaluation for identification of various mucosal pathologies for earlier intervention.
Declaration of patient consent
The authors certify that they have obtained all appropriate patient consent forms. In the form, the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.
We would like to acknowledge the Department of Oral Medicine and Radiology, Saveetha Dental College.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
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Dr. K V Swathi
Department of Oral Medicine and Radiology, SRM Dental College, Ramapuram, Chennai-89, Tamil Nadu
Source of Support: None, Conflict of Interest: None
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
[Table 1], [Table 2]