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O R I G I N A L A R T I C L E

Impact of oral potentially malignant disorders on quality of life

Jyothi Tadakamadla

1

| Santhosh Kumar

1

| Ratilal Lalloo

2

| Dara Balaji Gandhi Babu

3

| Newell W. Johnson

1

1Menzies Health Institute Queensland and School of Dentistry and Oral Health, Griffith University, Qld, Australia

2School of Dentistry, The University of Queensland, St Lucia, Qld, Australia

3Department of Oral Medicine and Radiology, Panineeya Institute of Dental Sciences & Research Centre, Hyderabad, Telangana, India

Correspondence

Jyothi Tadakamadla, Menzies Health Institute Queensland and School of Dentistry and Oral Health, Griffith University, Queensland, Australia.

Email: jyothi.tadakamadla@griffithuni.edu.au

Background: Oral potentially malignant disorders (OPMDs) could have a significant psychological impact on patients, principally because of the unknown risk of malig- nant transformation, while the physical and functional impairments could differ. This study aimed to assess the impact of three different OPMDs and their disease stages on the quality of life (QoL) of affected patients.

Methods: Oral leukoplakia (OL), oral lichen planus (OLP) and oral submucous fibro- sis (OSF) patients who were undergoing treatment at an oral medicine clinic of a dental teaching hospital in India were the study population. All subjects completed the recently developed OPMDQoL questionnaire and a short form 12 item (version 2) health survey questionnaire (SF-12v2). OPMDQoL questionnaire consists of 20 items over four dimensions. A higher score denotes poor OHRQoL. SF-12v2 has two components, a Physical Component Summary (PCS) and Mental Component Summary (MCS).

Results: A total of 150 subjects (50 each of OL, OLP and OSF) participated. OL patients (37.7  7.9) reported significantly better OPMDQoL scores than OLP (47.3  5.8) and OSF (45.4  9.2) patients. OLP patients reported significant prob- lems in obtaining a clear diagnosis for their condition, more so than the other OPMDs. OL patients reported fewer problems for the dimension, “physical impair- ment and functional limitations ” than the OLP and OSF patients. A significant trend was observed with the overall OPMDQoL and MCS, deteriorating as the disease stage increased.

Conclusions: OLP and OSF have a significant impact on the QoL of affected individ- uals: OL less so. Increasing stage of the disease is associated with worsening QoL.

K E Y W O R D S

oral leukoplakia, oral lichen planus, oral submucous fibrosis, quality of life

1 | I N T R O D U C T I O N

Patients’ input in evaluating their oral health needs and treatment plans has been extensively promoted,1and the subjective perception of the impact of oral health status on quality of life (QoL) has become an important method of evaluating treatment outcomes.2 Studies indicate that oral diseases like periodontal diseases and tooth loss significantly impact QoL.3In particular, oral malignancies

are significantly associated with physical, psychological and func- tional problems that influence overall QoL. Hence, QoL is used as an important treatment outcome in head and neck cancer patients.4 Although oral potentially malignant disorders (OPMD) are not life threatening until they transform into malignancies they might cause pain, affect the functioning of the oral cavity, or cause psychosocial impairment due to anxiety associated with their potentially malignant nature.5

60

|

© 2017 John Wiley & Sons A/S.

Published by John Wiley & Sons Ltd

wileyonlinelibrary.com/journal/jop J Oral Pathol Med. 2018;47:60–65.

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Although national health bodies in the developed world are now encouraging evaluation of the impact of disease by use of patient reported outcome measures,6the use of QoL assessments is limited in oral medicine practice.7 The literature on the QoL in OPMD patients is scanty, but from the limited literature available, a few generic QoL instruments have been used in the past.8Recently, we developed a condition-specific OPMDQoL questionnaire, which was found to be valid and reliable in assessing the QoL in oral leuko- plakia (OL), oral lichen planus (OLP) and oral submucous fibrosis (OSF) patients in a Telugu-speaking Indian population.9 Despite all three of these conditions having a similar psychological impact, prin- cipally because of the unknown risk of malignant transformation, the physical and functional impairments could differ. Here, we aimed to assess the ability of the instrument to differentiate the impact of three different OPMDs on various aspects of QoL. This assessment helps in further evaluating the discriminant validity of the OPMD- QoL questionnaire. Also, we aimed to determine the differences in QoL based on the extent of the disease. This will help to determine if the instrument has utility for studies of disease progression and response to therapy. In addition, we compared the impact of the three different OPMDs and their disease stages on general health- related QoL.

2 | M A T E R I A L A N D M E T H O D S

All OL, OLP and OSF patients, with no other mucosal conditions or systemic diseases, undergoing treatment at the oral medicine clinic of Panineeya Institute of Dental Sciences and Research Centre, Hyderabad, India, were invited to participate. The study was con- ducted during the period, October 2014 to May 2015. Written informed consent was obtained from all participants. The Ethics Committees of Griffith University and Panineeya Institute of Dental Sciences and Research Centre granted approval for the study.

Diagnosis of the OPMD was made by specialists at the oral med- icine clinic based on a clinical examination which was confirmed by histopathological assessment. Detailed disease history was recorded, and a thorough clinical examination of the head, neck and mouth was conducted by a single examiner (JT). Information obtained included age, gender, past medical and dental history, history of the present complaint and details of relevant habits.

Habit history included information on the use of cigarettes, bidi (tobacco rolled in a dried Temburni leaf), smokeless tobacco or areca nut. Those subjects who smoked or used smokeless tobacco or areca nut for at least 6 months prior to diagnosis were considered as cur- rent users.10 Those few patients who claimed to have indulged in any of these habits in the past but not now were considered as non- users. As only two subjects stated that they consumed only beedis, these were included with cigarette users. Most of the subjects used areca nut along with tobacco (gutka and pan with areca nut). Users of areca nut with or without tobacco were considered as one vari- able. Those using only smokeless tobacco were very few, and thus, the association of smokeless tobacco use with the outcome could

not be evaluated. In addition, data on duration of substance use in years (categorised as 1-5 years, 6-10 years and>10 years) and units of cigarettes smoked or areca nut/tobacco chewed per day were also recorded (categorised as 1-5 units/day, 6-10 units/day and

>10 years units/day).

Disease severity was assessed based on the extent of clinical signs and symptoms. The speed of progression could not be consid- ered due to the cross-sectional nature of the study. Disease severity was divided into stages as described by the specified authors, as fol- lows: the staging of OSF was based on the extent of mouth opening assessed by measuring interincisal distance.11 Patients were classi- fied into, stage 1 - mouth opening>35 mm, stage 2 - mouth opening of 30-35 mm, stage 3 - mouth opening of 20-29 mm and stage 4 - mouth opening of<20 mm. The scoring proposed by Escudier et al12 was used for grading OLP. Each patient was given a site, severity and pain score, the final score being the addition of the product of site and severity score and the pain score. Most OLP patients had a severity score ranging from 3 to 6 and were categorised into; stage 1 - score of 3 or less, stage 2 - score of 4, stage 3 - score of 5 and stage 4 - score≥6. Staging of OL was based on the system proposed by van der Waal et al (2000) which considers size and the presence of homogenous and/or non-homogenous lesions: Stage 1 - single or multiple homogenous lesions which are<2 cm in size; stage 2 - sin- gle or multiple homogenous lesions which are 2-4 cm in size; stage 3 - single/multiple homogenous lesions which are >4 cm in size or single/multiple non-homogenous lesions measuring up to 4 cm in size; stage 4: - single or multiple non-homogenous lesions which are

>4 cm in size.13

The newly developed OPMDQoL questionnaire was used to evaluate the condition-specific QoL.9OPMDQoL has been found to be valid and reliable in this study population.9This instrument con- sists of 20 items categorised under four subscales; Difficulties with diagnosis, Physical impairment and functional limitations, Psychologi- cal and social well-being and Effect of treatment on daily life. The response for each item is scored on a five-point Likert scale, the total score ranging from 0 to 80 with a greater score representing poorer QoL.9 Also, we used the short form 12 item (version 2) health survey questionnaire (SF-12 v2) to measure the self- perception of general health and well-being of the study subjects.14 SF-12v2 was also used as several researchers recommend using both generic and specific instruments because generic questionnaires reflect the impact of the condition on general well-being while the disease-specific questionnaires evaluate the activities and physical functioning directly affected by the disease.15The Telugu translation of SF-12v2, software to score the completed questionnaires“Health Outcomes scoring Software” and the manual were sourced from the developers, QualityMetrics (Licence #: QMO22969). All the deriva- tives of health survey forms including the Telugu translation used in this study are translated using standardised“International Quality of Life Assessment” Project translation methodology.16 The scoring software uses a scoring algorithm derived from the United States (US) general population. The developers of SF-12v2 have proposed using US norm-based scoring as it helps in international

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comparability.17The twelve items of SF-12v2 are categorised under eight subscales: four of these (physical functioning, mental health, role physical and role emotional) consist of two items each, while the other four (bodily pain, general health, vitality and social func- tioning) comprise one item each. Subscale scores are used to calcu- late summary scores on two components; Physical Component Summary (PCS) and Mental Component Summary (MCS). The scores on the PCS and MCS could range from 0 to 100 with a greater score indicating better health status.14,18

2.1 | Statistical analysis

SPPS (Version 23.0. Armonk, NY: IBM Corp) was used for statistical analysis. As the overall OPMDQoL score and subscale scores were normally distributed, parametric tests were used. One-way analysis of variance (ANOVA) was used to compare the overall QoL and sub- scale scores between the three OPMDs and their disease stages.

Post hoc analysis using Tukey HSD was executed for multiple com- parisons between the three OPMDs and stages of the disease. Also, a multivariate linear regression analysis with the generalised linear model (GLM) was performed to assess the adjusted effect of inde- pendent variables (OPMD condition, staging of disease, age, gender, occupation, education, treatment duration, tobacco and areca nut habits) on OPMDQoL. For regression analysis, age and treatment duration were used as covariates (continuous variables). G-power was used to calculate the sample size, a sample size of 131 is adequate for 13 predictors in a linear regression analysis with a power of 80% and an alpha error of 5% to detect an effect size of 0.15. A P value of<.05 was considered statistically significant.

3 | R E S U L T S

A total of 150 (50 each of OL, OLP and OSF) patients participated in this study. The response rate was 100% as none of the cases approached declined to participate. More than half (63.3%) the sub- jects were male, and the mean age was 39.8 years. The most com- monly reported complaints among the study population were burning sensation, difficulty in opening mouth, roughness on the cheek mucosa and pain in the mouth. Only a fifth of the patients have reported of being to the dentist in the past for issues other than the OPMD (not presented in tables).

There were significant differences for overall QoL, and subscale scores of“Difficulties with diagnosis” and “Physical impairment and functional limitations” between the three OPMDs (Table 1). On the post hoc analysis, OL patients (Mean Standard deviation:

37.7 7.9) reported significantly better QoL than OLP (Mean Standard deviation: 47.3  5.8) and OSF (Mean  Standard deviation: 45.4 9.2) patients. OLP patients reported significant problems in obtaining a clear diagnosis for their condition compared to the other OPMDs. OL patients also reported signifi- cantly fewer problems for the dimension,“physical impairment and functional limitations” than the OLP and OSF patients. There were

no differences between the OPMDs for the dimensions, “effect of treatment on daily life” and “psychological and social well-being.”

Table 2 demonstrates that there was a significant trend with the overall QoL scores increasing as the stage of the disease increased.

Moreover, the scores of most of the individual dimensions of OPMD- QoL also increased with the increase in the stage of the disease. In particular, subjects with stage 4 disease had significantly greater scores for the dimension“physical impairment and functional limita- tions” than those with stages 1, 2 and 3. Table 3 shows that OLP patients had better PCS scores than OSF patients, while there were no differences between the three OPMDs for MCS scores. Subjects with stage 4 disease had significantly lower MCS scores, indicating poor QoL than those belonging to other disease stages (Table 4).

Table S1 presents the results from the multiple linear regression analysis. Females had poorer QoL than males. Age, education status, occupation and the“treatment duration” did not have any influence on overall OPMDQoL. As observed in univariate analysis, OPMD condition and disease stages were significantly associated with OPMDQoL. OL patients had an estimated 4.87 units less OPMDQoL score than OSF patients. Also, subjects with mild disease had signifi- cantly lower OPMDQoL scores than those who had more severe dis- ease, with subjects in stage 1 presenting 7.87 units less OPMDQoL score (better QoL) than those in stage 4. Subjects who smoked 6-10 cigarettes per day had better QoL (b = 4.15) than those who were smoking more than ten cigarettes per day. Also, those patients who were using areca nut with or without tobacco for 1-5 years and 1-5 times per day reported better QoL than those who used for more than ten years and greater than ten units per day, respectively.

4 | D I S C U S S I O N

In this study, we assessed the effect of three different OPMDs and the disease stages on QoL. To our knowledge, this is the first study to use a condition-specific instrument to compare the QoL between the three most common OPMDs (OL, OLP and OSF) in South Asia.

It was observed that there were significant differences between the three OPMDs and their disease stages for overall OPMDQoL scores and few subscale scores.

The response rate in this study was excellent with all patients agreeing to participate. As hypothesised, there were differences in OPMDQoL dimension scores between the three OPMDs. When the subscale scores were compared, OLP patients reported significant problems in being given a clear diagnosis of their condition com- pared to those with either of the other disorders. This difference might be because, OSF is clearly associated with areca nut chewing while the aetiopathogenesis of OLP is both unclear and multifacto- rial, involving anxiety, stress, genetics and associations with several systemic diseases.19 The multifactorial nature of OLP makes the diagnosis difficult for general dental practitioners. Reports from sev- eral parts of India indicate that general dentists have poor knowl- edge of OPMDs and oral cancers. For example, a survey among dentists of one district in Karnataka state found that approximately

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half of the dentists were not aware that some innocuous looking oral mucosal lesions could transform into oral cancer.20 Another study reported that only just above a third of the dentists of Banga- lore city in the state of Karnataka routinely examined the oral mucosa.21

OSF patients reported greater levels of physical impairment and functional limitations than OL and also OLP. This can be attributed to the multiple signs and symptoms associated with OSF, which includes limited mouth opening due to the fibrosis—a matter not of major concern in OLP patients.22 On the other hand, OL patients reported low scores in this dimension which might be because some of them were diagnosed incidentally during regular dental screening.

It is known that OL which is homogenous (white in colour with a flat, thin and smooth surface) is usually asymptomatic.23One of the striking findings in this study was that all three OPMDs had similar scores for impaired psychological and social well-being, scores which demonstrate that the potentially malignant nature of the disease had its impact on this aspect of their life, irrespective of differences in the functioning of the oral cavity. Prolonged treatment regimes with no definitive cure are in itself distressing for OPMD patients.24,25 However, no differences were observed between the three OPMDs for the dimension“Effect of treatment on daily life.”

In relation to disease stages, there was a significant trend of patients in advanced stages of disease reporting poorer overall T A B L E 1 Effect of different OPMD conditions on overall and subscale scores of OPMDQoL

Oral Leukoplakia (A) N= 50

Oral Lichen Planus (B) N= 50

Oral Submucous Fibrosis (C)

N= 50 F value, significance Post hoc Difficulties with diagnosis 4.1 1.2 7.0 1.6 3.9 1.0 90.049, P< .001 A< B B > C Physical impairment and functional

limitations

10.5 4.0 16.8 2.1 17.4 4.2 57.805, P< .001 A< B A< C Psychological and social well-being 17.8 4.3 18.3 3.0 18.6 4.9 0.392, P= .677

Effect of treatment on daily life 5.3 1.8 5.7 1.7 5.6 2.0 0.438 P= .646

Overall OPMDQoL 37.8 8.0 47.8 5.2 45.4 9.2 23.445, P< .001 A< B A < C

OPMDQoL, Oral potentially malignant disorders quality of life.

T A B L E 2 OPMDQoL and subscale scores in relation to the disease severity Stage 1 (A)

N= 39

Stage 2 (B) N= 35

Stage 3 (C) N= 40

Stage 4 (D) N= 36

F value,

significance Post hoc

Difficulties with diagnosis 4.0 1.4 4.8 1.8 4.8 1.6 6.4 2.1 12.15, P< .001 A< D B < D C < D Physical impairment and

functional limitations

11.5 4.7 14.6 3.9 15.1 4.3 18.7 2.7 20.68, P< .001 A< B A < C A < D B < D C < D

Psychological and social well-being 16.0 3.5 17.8 3.0 18.7 4.2 20.6 4.3 9.499, P< .001 A< C A < D B < D Effect of treatment on daily life 4.8 2.1 6.5 1.6 5.7 1.8 5.3 1.5 5.731, P< .001 A< B B > D

Overall OPMDQoL 36.2 8.1 43.7 5.5 44.3 7.3 51.0 6.8 27.401, P< .001 A< B A < C A < D B < D C < D OPMDQoL, Oral potentially malignant disorders quality of life.

T A B L E 3 PCS and MCS scores in patients with different Oral Potentially Malignant Disorders

Oral Leukoplakia (A) N= 50

Oral Lichen Planus (B) N= 50

Oral Submucous Fibrosis (C)

N= 50 F value, significance Post hoc

Physical Component Summary 54.2 5.6 55.1 5.4 51.5 7.0 4.785, P= .01 C< B

Mental Component Summary 45.6 8.6 43.6 5.1 46.9 7.0 2.794, P= .064

T A B L E 4 SF-12 v2 component scores in relation to the disease severity Stage 1(A)

N= 50

Stage 2(B) N= 50

Stage 3(C) N= 50

Stage 4(D)

N= 50 F value, significance Post hoc Physical Component Summary 53.6 6.2 51.0 7.3 53.4 6.1 56.4 3.4 4.947, P< .05 D> B

Mental Component Summary 50.7 8.5 45.0 5.6 44.2 6.3 41.2 3.5 15.162, P< .001 A< B, A < C, A < D

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OPMDQoL and worse subscale scores than those in the initial stages. This finding might serve as a proxy measure of instru- ment’s responsiveness to treatment. Further research is recom- mended to evaluate the utility of the questionnaire in recording response to treatment over time through changes in the effects sizes.26

In this study, SF-12v2 was used as it is simple, and less time- consuming than the longer forms. It has also been found to be valid and reliable in a diverse range of populations in several coun- tries.17 It was observed that OLP patients had better physical health (PCS) than OSF patients. This could be attributed to the dif- ferences in social status among the three OPMDs. OSF is associ- ated with areca nut chewing, and those subjects with OSF usually belong to manual occupations that need physical labour and there- fore might have reported difficulties with regular physical activities.

As was observed with the “psychological and social well-being”

domain of the OPMDQoL questionnaire, MCS scores did not differ significantly between the three disorders. Patients with severe disease had significantly greater MCS scores than those with milder forms, perhaps because of greater anxiety regarding the risk of malignant transformation: apart from the inevitable pain and disfig- urement of oral cancer, there is a considerable stigma attached to cancer in Indian communities.27

Findings from the multivariate analysis confirmed that clinical diagnosis and disease stages are associated with OPMDQoL scores.

Also, females were found to report poorer QoL than males. Gender- based differences in QoL are evident from the literature.28Smoking was associated with poor QoL, and similar findings were observed in previous research on head and neck cancer patients.29QoL is used as a clinical measure in smokers, and a systematic review has con- cluded that a negative association exists between the number of cigarettes smoked and QoL which is in accordance with our find- ings.30Areca nut usage with or without tobacco was also found to be negatively associated with QoL. Although we could not trace any literature evaluating this association, this is likely to reflect the severity of Areca nut-induced diseases.

Our study helps in understanding patient perceptions and experi- ences in different OPMDs, and we believe this helps in clinical deci- sion making. For instance, OLP and OSF patients reported greater physical impairment and functional limitations while all three condi- tions reported similar levels of psychological and social impact.

Although we have not found any published studies which have formally compared QoL in different OPMDs, a few have observed differences in perceived QoL among patients with different oral mucosal diseases.31

The present work is thus original but is not free of limitations.

This is a cross-sectional study and the findings, specifically those indicating an association between disease stages and QoL, cannot be assumed as causal. The study sample constituted subjects attending only one teaching hospital in India, and the results might not be gen- eralisable to all OPMD patients of India, nor to other populations or ethnic groups. The sample size was, nevertheless, adequate to draw

valid conclusions and inferences representative of the target popula- tion under study.

In conclusion, OLP patients reported higher scores for the sub- scale“Difficulties with diagnosis” than OL and OSF patients. OLP and OSF have a significant impact on the QoL of affected individu- als: OL less so. OL patients also had better scores for “Physical impairment and functional limitations” than those with OLP and OSF. There were no differences between the three OPMDs for the dimensions,“effect of treatment on daily life” and “psychological and social well-being.” Increasing stage of the disease is associated with worsening QoL. Therefore, OPMDQoL instrument might have utility in monitoring response to treatment. In particular, this instrument helps clinicians to understand the psychological and social impact of OPMD on the life of their patients. Clinicians might also be able to use this information to motivate patients for habit cessation and treatment adherence

A C K N O W L E D G E M E N T S

We would like to thank the patients and the other staff of the Department of Oral Medicine at Panineeya Institute of Dental Sciences & Research Centre, Hyderabad, for their willing participa- tion. We thank the developers of SF-12v2 survey for providing the questionnaire and the scoring software free of cost.

C O N F L I C T O F I N T E R E S T

All authors declare that they do not have any conflict of interests.

O R C I D

Jyothi Tadakamadla http://orcid.org/0000-0002-2518-6476

R E F E R E N C E S

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S U P P O R T I N G I N F O R M A T I O N

Additional Supporting Information may be found online in the supporting information tab for this article.

How to cite this article: Tadakamadla J, Kumar S, Lalloo R, Babu G, Johnson NW. Impact of oral potentially malignant disorders on quality of life. J Oral Pathol Med. 2018;47:60-65.

https://doi.org/10.1111/jop.12620

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exegetes, retrospectively known as the Shan-chia and the Shan-wai. In this essay I argue that one especially useful way of coming to understand what was truly at stake in

For the data sets used in this thesis we find that F-score performs well when the number of features is large, and for small data the two methods using the gradient of the

This study intends to bridge this gap by developing models that can demonstrate and describe the mechanism of knowledge creation activities from the perspective of

This study proposed the ellipse-space probabilistic neural network (EPNN), which includes three kinds of network parameters that can be adjusted through training: the variable

The results of this study found that the experimental group had higher scores than the control group, demonstrated the curricula of the global warming, energy-saving and