People’s Journal of Scientific Research / Volume 16 / Issue 1 / Jan-June 2023

Research Article

Study on Biochemical Perspectives of Antioxidant and

Oxidant Indices in Oral Squamous Cell Carcinomas

(OSCCs) and Other Oral Potentially Malignant

Disorders (OPMDs)

Gaurav Arya1, Ranu Shukla2

1Department of Oral Medicine and Radiology, People’s Dental Academy, Bhopal, 2Department of

Biochemistry, L N Medical College and Research Centre, Bhopal.

ABSTRACT: Background-Oxidative stress in biological systems is a complex process that is characterized by an

inequity between the production of free radicals (FR) and the ability of the body to eliminate these

reactive species through the use of endogenous and exogenous antioxidants. The pathogenesis of oral

cancer has been linked to alterations in the antioxidant defense mechanism.

Materials & Methods- Saliva from twenty patients with OSCC, forty patients with OPMDs and

twenty healthy subjects in the age group of thirty five to seventy five years was analyzed for levels of

nitric oxide, vitamin C, total sialic acid and GSH using spectrophotometry.

Results - The levels of salivary vitamin C and glutathione were significantly reduced and those of nitric

oxide and sialic acid were raised in patients having OPMD's and oral squamous cell carcinoma. The co-

relation between the AOI and calculated ratios indicated that antioxidant potential of the saliva was

decreased and was statistically related to (p <0.001) development of OPMD, which further may

progress to oral cancer, notably OSCC.

Conclusion- The current study demonstrated that the estimation of vitamin C, nitric oxide, sialic acid

and GSH in saliva could be used as an early potential diagnostic biomarker in the screening of oral

cancer. The antioxidant-oxidant indices (AOI's) can be used as a reliable tool for predicting the oral

microenvironment and its predicted change towards development of oral cancer. This optimized

developed protocol was also found to be simple and cost effective.

KEYWORDS: oral cancer; saliva; AOI; spectrophotometry

Address for correspondence : Dr Gaurav Arya, Department of Oral Medicine and Radiology, People’s Dental Academy, Bhanpur,

Bhopal-462037 , E-mail: dr.gauravarya@gmail.com

Submitted: 14.05.2023, Accepted: 14.06.2023, Published: 26.06.2023

INTRODUCTION:

Oral cancer includes a group of neoplasms

affecting any region of the oral cavity, pharyngeal

regions and salivary glands. Head and neck cancers

(HNCs) have emerged as a leading cause of cancer-

related mortality and morbidity worldwide. It is

estimated that more of 90% of all oral neoplasms are

OSCC.[1] Saliva is one of the vital fluids secreted in

human beings. It is of importance to understand that

the use of saliva is and will be a most promising

detection method for the diagnosis of oral cancer.

Obtaining saliva samples is non-invasive; there is a

lower risk of infection, while direct contact of saliva

with oral pathologies can contribute to the earlier

detection of relevant diseases. Although the oral cavity

is frequently examined, 60% of intra oral carcinomas

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How to cite this article: Arya G, Shukla R. Study on Biochemical

Perspectives of Antioxidant and Oxidant Indices in Oral Squamous Cell

Carcinomas (OSCCs) and Other oral Potentially Malignant Disorders

(OPMDs). PJSR. 2023;16(1):1-8.

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DOI:

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People’s Journal of Scientific Research / Volume 16 / Issue 1 / Jan-June 2023

Arya G et al. Antioxidant & Oxidant in OSCC & OPMDs

are in advanced stage at the time of detection.

Persistent difficulties arising in oral cancer are late

diagnosis, poor response of tumor to chemotherapy,

lack of reliable biomarkers for early diagnosis and

post-therapeutic monitoring.[2]

Biomarkers of oxidative stress have been a

major source of debate related to monitoring oxidative

stress and the possible resulting damage. Biomarkers

of oxidative stress have been measured in plasma,

whole blood, urine, respired gases, muscle, and other

skeletal tissues. Saliva is an attractive bio-specimen for

a number of reasons including the ease of its collection

and the copious amount the human body is capable of

producing for examination. Saliva is increasingly used

and well validated in diagnosing. Moreover, saliva is

reported to be suitable to detect the body's oxidative

stress level.[3]

The present study was done as a part of

biochemical evaluation using standardized materials

and methods to assess the antioxidant–oxidant indices

(AOI) in patients having oral potentially malignant

disorders and oral cancer. This was a research-based

study with non-invasive laboratory experimentation

on patients suffering with OSCC and OPMD with

those of normal controls. The study was aimed to

evaluate and compare the salivary levels of nitric

oxide, vitamin C, total Sialic acid and GSH in patients

with oral potentially malignant disorders (OPMDs)

and oral squamous cell carcinoma (OSCC) with

healthy controls. We determined the antioxidant to

oxidant indices (AOI) of above mentioned biomarkers

in saliva of OPMD and those of OSCC patients. Lastly,

we correlated changes in AOI of vitamin C, nitric

oxide, Glutathione (GSH) and sialic acid in saliva of

patients with OPMD with OSCC and control patients.

MATERIALS & METHODS:

The data was collected non-invasively

from patients visiting the Jawaharlal Nehru cancer

center, Bhopal and Dept. of Oral Medicine and

analyzed for levels of nitric oxide, vitamin C, total

sialic acid and GSH using spectrophotometry.

a. Study group 1: Patients who were histopatho-

logically diagnosed with OSCC (n = 20)

b. Study group 2: Patients who were histopatho-

logically diagnosed with OPMD (n = 40)

c. Control group: Normal healthy individuals with

clinically normal oral mucosa (n = 20).

All the patients were examined using the

mouth mirrors and probes under the artificial light.

Their history and clinical findings were recorded using

the standard proforma after informed consents.

Inclusion criteria-

1. Histopathologically diagnosed new cases of

OSCC & OPMD were included in the study group.

Exclusion criteria-

1. Patients undergoing treatment such as

chemotherapy and radiotherapy;

2. Past history of any major illness such as liver

disease, tuberculosis, diabetes and

hypertension;

3. Any history of malignancy other than oral

cancer;

4. Recurrent or secondary lesions;

5. Subjects on antioxidants/multivitamin

preparations;

6. The healthy controls had no habit of tobacco,

alcohol, were devoid of any chronic illness

and were not on any long-term medication.

Armamentarium-

 Dental oral mirror (odontoscope)

 Straight dental probe

 Plain test tubes

 Normal Saline

 Sterile container for saliva

 Cooling centrifuge

 Micropipettes with plastic disposable

Radiology, RKDF Dental College and Research

Centre, Bhopal. Informed consent was obtained

from all the patients before collection of samples.

The study was performed in the Department of

Biochemistry, RKDF Dental College and

pipette tips

 Cuvettes

 Water bath

 Distilled water

 Beaker

 Stirrer

Research Centre, Bhopal after obtaining approval

from the university ethical committee.

Method Of Collection of Data - Saliva from twenty

patients with OSCC, forty patients with OPMDs

and twenty healthy subjects in the age group of

thirty five to seventy five years was

 Measuring cylinder

 Test tube stand

 Reagents for vitamin C, NO, GSH &

Sialic acid.

 Spectrophotometer

 Auto analyzer

Arya G et al. Antioxidant & Oxidant in OSCC & OPMDs

People’s Journal of Scientific Research / Volume 16 / Issue 1 / Jan-June 2023

Sample collection and processing of saliva:

5ml of unstimulated salivary sample was

collected from each patient after rinsing and spitting

with normal saline (0.9% v/v) for a period of one

minute between 10 am to 12 pm to avoid circadian

variations. Two milliliters of saliva was collected and

transferred for biochemical analysis.

Patients were given detailed information about

the collection protocol:

(a) Refrain from eating or drinking at least 90

minutes prior to salivary collection.

(b) To sit in a comfortable position with eyes open

and head tilted slightly forward.

collection.

Saliva samples were immediately centrifuged (1000g

for 10 minutes) at 4°C to remove cell debris. The

resulting supernatants were immediately transferred to

4 separate aliquots. The sample was ﬁnally centrifuged

for about 15 minutes at 16,000 rpm for 5 minutes to

remove the cellular components

i. First group of aliquots were used for

estimating vitamin C

ii. Second group of aliquots were used for

estimating nitric oxide

iii. Third group of aliquots were used for

estimating sialic acid

iv. Fourth group of aliquots were used for

estimating glutathione peroxidase.

Antioxidant-Oxidant Index (AOI) was

calculated using the ratio between the levels of nitric

oxide (NO), vitamin C, total sialic acid and GSH

peroxidation levels. Post hoc Bonferroni's test analysis

was used for the comparison of the two study groups to

the control group. The data is expressed as mean ± SD.

The statistical signiﬁcance of the results was analyzed

using post hoc Bonferroni's test. Correlation between

the groups was done using Pearson's correlation

coefﬁcient test.

RESULTS:

The study comprised of 80 subjects, there were

27 females (34%) and 53 males (66%) in the study

group. There were ﬁfty-three males (controls-10;

OPMD-30; OSCC-13) and twenty-seven females

(controls-10; OPMD-10; OSCC - 07). The mean age

was 36.4±1.58 years in control group, 39.30±10.57

years in OPMDs and 49.25±15.58 years in OSCC.

Out of 40 OPMD patients, 5 (12.5%) were

without any habit, 18 (45%) with tobacco chewing, 10

(25%) with smoking and 7 (17.5%) with both tobacco

chewing and smoking habits.

Among 20 OSCC patients, 1 (5%) was without

any habit, 6 (30%) with habit of tobacco chewing, 4

(20%) with smoking and 9 (45%) with both smoking

and tobacco chewing.

Our results showed that, among 40 OPMD

patients, leaukoplakia was seen in 25 (62.5%) cases,

followed by oral submucous ﬁbrosis in 9 cases

(22.5%) and lichen planus in 6 (15%) cases.

7 (35%) cases revealed buccal mucosal

lesions, 6 (30%) patients showed tongue lesions, 3

(15%) cases showed lesions on tonsil, 2 (10%) showed

lesions involving alveolus. Palatal and retromolar

trigone had 1 (5%) case each.

Descriptive Statistics of Variables-

The data was recorded and analyzed

statistically using SPSS software version 20.0 using

one way ANOVA and post hoc Bonferroni's tests.

Mean of controls and patients were compared using

Student's t-test. The difference was considered

statistically signiﬁcant when p-value were 0.001 or

less. The mean salivary vitamin C level was

30.32±4.34 μmol/l in OSCC group whereas; it was

38 . 20 ± 8 . 45 μmol/ l in OPMDs group and

48.76±2.60μmol/l in control group.

The mean nitric oxide level was 27.34±5.51 μmol/l in

OSCC group, 22.5±2.33 μmol/l in OPMD group and

10.11±0.88 μmol/lin control group.

The glutathione reductase activity in control

patients was found to be 0.0915 U/ml under optimal

pH, temperature and Km. In OPMD group the GR

activity was found to be 0.0515 U/ml. Similarly, the

activity in the OSCC group was found to be 0.0292

U/ml. The total sialic acid (TSA) in the saliva of

control patients was found to be 41.241±5.3312

μg/mL. In the case of OPMD patients it was 64.25 ±

4.33 μg/mLand in the OSCC patients it was, 79.60 ± 6.93

μg/mL. As seen from the graphs above, the levels of

salivary vitamin C and glutathione were signiﬁcantly

reduced [Graph 1 & Graph 2] and those of nitric oxide

and sialic acid were raised [Graph 3 & Graph 4] in

patients having OPMD's and oral squamous cell

carcinoma. The antioxidant to oxidant index (AOI)

was measured between NO and vitamin C; NO and

GSH; total sialic acid and vitamin C and lastly, total

sialic acid and GSH. The following indices are

tabulated below with the corresponding values.

(Tables 1,2,3,4).

It can be seen from the analysis that there was

a statistically signiﬁcant difference between the

reduced levels of vitamin C and GSH to those that of

raised nitric oxide and sialic acid levels in patients

People’s Journal of Scientific Research / Volume 16 / Issue 1 / Jan-June 2023

Arya G et al. Antioxidant & Oxidant in OSCC & OPMDs

Deviation

Difference (i-J)

Table 1: AOI in controls and study groups. *ANOVA, p-value <0.001 considered statistically signiﬁcant

variable group n mean Std.

Control 20 0.207 0.023

p-value

Table 2: AOI in controls and study groups. *ANOVA, p-value <0.001 considered statistically signiﬁcant.

variable group n mean Std. p-value

AOI

NO / GSH

Control

OPMD

0.11

0.436

0.012

0.122

<0.001

Cancer

0.936

0.289

Table 3: AOI in controls and study groups. *ANOVA, p-value <0.001 considered statistically signiﬁcant.

variable group n mean Std. Deviation p-value

Control 20 0.845 0.093

Table 4: AOI in controls and study groups. *ANOVA, p-value <0.001 considered statistically signiﬁcant

variable group n mean Std. Deviation p-value

Control 20 0.45 0.052

AOI

TSA / GSH

OPMD

1.247

0.351

<0.001

Cancer

2.72

0.842

Table 5: Pairwise comparison of AOI index in control and study groups. *Post-hoc Bonferroni's analysis with ANOVA, p-

value <0.001 considered statistically signiﬁcant.

Dependent variable (i) group (J) group mean Difference (i-J) p-value

Control OPMD

-0.382*

0.001

Cancer

-0.694*

0.001

AOI NO / VIT.C OPMD Control

0.382*

0.001

Cancer

-0.312*

0.001

Cancer Control

0.694*

0.001

Table 6: Pairwise comparison of AOI index in control and study groups. *Post-hoc Bonferroni's analysis with ANOVA, p-

value <0.001 considered statistically signiﬁcant.

Dependent

variable (i) group (J) group mean p-value

Control OPMD

AOI Cancer

-0.326*

-0.826*

0.001

NO / GSH OPMD Control

0.326*

0.001

Cancer

-0.500*

0.001

Cancer Control

0.826*

0.001

having or suffering from OPMD's and those having

histopathologically proven cancer of oral cavity. The

data where p-value <0.001 is statistically signiﬁcant.

Post – hoc Bonferroni's analysis was performed for

pairwise comparison between the controls, OPMD and

OSCC patients. The analysis clearly indicates

AOI NO / VIT.C

OPMD

0.589

0.166

<0.001

Cancer

0.901

0.279

AOI

TSA / VIT.C

OPMD

1.687

0.466

<0.001

Cancer

2.625

0.812

Arya G et al. Antioxidant & Oxidant in OSCC & OPMDs

People’s Journal of Scientific Research / Volume 16 / Issue 1 / Jan-June 2023

(i-J)

Table 7: Pairwise comparison of AOI index in control and study groups. *Post-hoc Bonferroni's analysis with ANOVA, p-

value <0.001 considered statistically signiﬁcant.

Dependent variable (i) group (J) group mean Difference p-value

AOI

TSA / VIT.C

Cancer

Cancer Control 1.420* 0.001

Table 8: Pairwise comparison of AOI index in control and study groups. *Post-hoc Bonferroni's analysis with ANOVA,

p-value <0.001 considered statistically signiﬁcant.

Dependent variable (i) group (J) group mean Difference p-value

AOI

TSA / GSH

Cancer

Cancer Control 2.270* 0.001

Table 9: p –value signiﬁcance chart between OPMD and OSCC group

( A) (B) Mean Difference Standard

statistical difference between the co-relation between

the values of raised NO levels to those of vitamin C.

This signiﬁcant statistical relationship where p-value is

less than 0.001 indicates changes in the biochemical

nature of saliva with patients having mucosal

potentially malignant disorders as well as oral cancer.

(Tables 5,6,7,8).

Our results were consistent with the grouped

analysis between various salivary biomarkers as can be

from the tabulated data above. There was signiﬁcant

increase in AOI [NO/Vit.C] from control group

(0.023), OPMDs (0.167) and OSCC group (0.279)

(Table 1)

And AOI [NO/GSH] from control group

(0.012), OPMDs (0.122) and OSCC group (0.289)

(Table 2)

Similarly the increase was seen in AOI

[TSA/Vit.C] from control group (0.093), OPMDs

Control OPMD

-0.842*

-1.420*

0.001

OPMD Control

0.842*

0.001

Cancer

-0.938*

0.001

Control OPMD

-0.797*

-2.270*

0.001

OPMD Control

0.797*

0.001

Cancer

-1.473*

0.001

Variables

Group

(A-B)

error

p-value

VITAMIN C

Control

OPMD

10.56

2.489

0.003

Control

OSCC

18.44

2.489

0.003

OPMD

OSCC

7.88

1.889

0.001

NITRIC OXIDE (NO)

Control

OPMD

-12.39

1.81

0.001

Control

OSCC

-17.23

1.81

0.001

OPMD

OSCC

-4.44

1.344

0.001

GLUTATHIONE

Control

OPMD

0.04

0.0177

0.003

Control

OSCC

0.0623

0.0177

0.003

OPMD

OSCC

0.0223

0.0177

0.003

TOTAL SIALIC ACID

Control

OPMD

-23.009

2.389

0.001

Control

OSCC

-38.359

2.389

0.001

OPMD

OSCC

-15.349

1.891

0.001

People’s Journal of Scientific Research / Volume 16 / Issue 1 / Jan-June 2023

Arya G et al. Antioxidant & Oxidant in OSCC & OPMDs

GRAPH 1: Mean concentration of Vitamin C (μmol /L).

GRAPH 2: Mean concentration of salivary glutathione (U/ml).

GRAPH 3: Mean concentration of nitric oxide - NO (μmol /L).

(0.467) and OSCC group (0.812)(Table 3). The AOI

[TSA/GSH] showed increase from control group

(0.052), OPDs (0.351) and OSCC group (0.842)(Table

4). On comparing salivary vitamin C levels and GSH

levels with those of the nitric oxide and sialic acid, the

difference was highly signiﬁcant (p<0.003). Though

the levels were not signiﬁcant between OPMD and

OSCC group (p>0.001) (Table 9).

GRAPH 4: Mean concentration of salivary TSA (μg/mL)

The levels of salivary vitamin C and glutathione were signiﬁcantly reduced

and those of nitric oxide and sialic acid were raised in patients having

OPMD's and oral squamous cell carcinoma.

DISCUSSION:

A biomarker is deﬁned as a pharmacological

or physiological measurement that is used to predict a

toxic event; a speciﬁc molecule in the body, which has

a particular feature that makes it instrumental for

measuring disease progression or the effects of

treatment. Biomarkers are by deﬁnition suitable to

develop new diagnostic tools, alone or in combination

with traditional methods (Brinkman and Wong, 2006).

[4]

The immune system of an individual works in

a very well-organized manner for the sustenance of the

normal equilibrium, thus helping in achieving a

disease-free state. Free radicals are generated as a by-

product of normal cellular metabolism and the increase

in the levels of ROS may be caused either due to

increased production or decreased destruction of these

formed free radicals by the enzymatic and

nonenzymatic antioxidants. To control the inﬂux of

ROS, aerobic cells have developed their own defense

system – the antioxidant protection system, which

includes enzymatic and nonenzymatic components

that function interactively and synergistically to

neutralize free radicals.[5]

Nitric oxide (NO) is a highly reactive oxygen

radical found in normal and malignant tissues,

however its levels are much higher in malignant tissue.

Its generation is thought to be by a family of enzymes

called nitric oxide synthase (NOS). NOS are available

in three isoforms NOS1 or type 1 or nNOS (neuronal),

NOS2 or type 2 or iNOS (inducible), NOS3 or type 3 or

eNOS (endothelial). Out of these, iNOS produces

continuous NO and is shown to be expressed in many

malignant tumors.[6]

Vitamin C is a major water- soluble

antioxidant. Generally, vitamin C is a six carbon

Arya G et al. Antioxidant & Oxidant in OSCC & OPMDs

People’s Journal of Scientific Research / Volume 16 / Issue 1 / Jan-June 2023

organic acid with structural similarity to glucose. It

acts as a potent reducing agent and its laevo (l-) form is

generally more active. Vitamin C has been shown,

together with some other antioxidant agents, to be an

endogenous modulator of the metabolism of nitric

oxide (NO) and subsequent endothelium-dependent

vasodilation. The difference in NO production at the

periodontal level is probably different from NO in the

bloodstream: In the mouth, it is an antibacterial

defense, whereas systemically, it impacts endothelial

function. [7,8]

Glutathione occurs in high concentrations (0.5

to 10mmol/L) in virtually all cells. Cellular GSH

concentrations are reduced markedly in response to

protein malnutrition, oxidative stress and many

pathological conditions. Salivary glutathione levels

may be an index of oxidative stress at the level of the

upper airways and in particular of oral cavity and

pharynx. Therefore, high salivary glutathione may be

an epidemiological marker to identify subjects with an

increased risk of developing HNSCC, to submit to

strict follow-up and chemoprevention. Metabolic

alterations of saliva could be both an epidemiological

marker and a target for chemoprevention of oral and

oropharyngeal carcinogenesis.[9,10] Sialic acid plays a

signiﬁcant role in cancer due to increased sialylation

and sialyltransferase activity.[11]

In our study, levels of nitric oxide were lowest

in control group but increased signiﬁcantly in OPMDs

and OSCC groups. The levels of nitric oxide in

OPMDs and OSCC were comparable. This is in

accordance with the study done by Juneja S et al[12],

who also reported increased level of nitric oxide in

OPMD and OSCC patients.

Serum levels of vitamin C were highest in

control group and reduced signiﬁcantly in OPMDs and

OSCC group in the present study. There was

statistically signiﬁcant difference in the levels of

vitamin C in OPMDs and OSCC also. Vitamin C

reduces the degradation of Vitamin E thus enhancing

chemotaxis, phagocytosis and collagen synthesis. It

inhibits the formation of nitrosamines and causes

reduction in oncogene expression. Vitamin E

maintains the integrity of membranes thus inhibiting

the growth of cancer cell and differentiation. It also

inhibits mutagenicity and formation of nitrosamines.

Synergistic action between Vitamin E, selenium and

ascorbate hinders DNA and RNA protein synthesis in

the cells. [13]

Glutathione participates in detoxiﬁcation at

several different levels, and may scavenge free

radicals, reduce peroxides or be conjugated with

electrophilic compounds. Thus, glutathione provides

the cell with multiple defences not only against ROS

but also against their toxic products. In the study done

by us, the levels of salivary glutathione reductase were

lower in OSCC when compared to OPMD and the

difference was statistically signiﬁcant (p<0.003)

In our study, the total sialic acid (TSA) in the

saliva of control patients was found to be

41.241±5.3312 μg/mL. In the case of OPMD patients

it was 64.25 ± 4.33 μg/mLand in the OSCC patients it

was, 79.60 ± 6.93 μg/mL.We also found signiﬁcantly

higher levels of free sialic acid in well-differentiated

OSCC patients compared to those of moderately

differentiated cases. This suggests correlation of

elevated salivary sialic acid levels to the progression

of OSCC. There is elevated salivary sialic acid level in

moderately /poorly-differentiated squamous cell

carcinoma without any signiﬁcant change in

well-differentiated squamous cell carcinoma. This

ﬁnding was consistent with the study by Rajaram S et

al.[14]

CONCLUSION:

The ﬁndings of the present study indicate that

estimation of Vitamin C, nitric oxide, GSH and sialic

acid can be suitably used and could assist in the early

diagnosis of potentially malignant disorders and oral

cancer using saliva. OSCC increases oxidative stress

and may trigger mutations, suggesting that it may play

a role in the initiation and development of multistage

carcinogenesis. Understanding the function of

reactive oxygen species (ROS) as key mediators in

signaling pathways may open up new avenues for

pharmacological intervention.

Financial Support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

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