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Hindawi Publishing CorporationJournal of Cancer EpidemiologyVolume 2012, Article ID 701932, 17 pagesdoi:10.1155/2012/701932

Review Article

Challenges of the Oral Cancer Burden in India

Ken Russell Coelho1, 2

1 Department of Public Health and Primary Care, University of Cambridge, Forvie Site, Robinson Way, Cambridge CB2 0SR, UK2 Pembroke College, Trumpington Street, Cambridge CB2 1RF, UK

Correspondence should be addressed to Ken Russell Coelho, [email protected]

Received 7 February 2012; Revised 8 June 2012; Accepted 21 June 2012

Academic Editor: Hermann Brenner

Copyright © 2012 Ken Russell Coelho. This is an open access article distributed under the Creative Commons Attribution License,which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Oral cancer ranks in the top three of all cancers in India, which accounts for over thirty per cent of all cancers reported in thecountry and oral cancer control is quickly becoming a global health priority. This paper provides a synopsis of the incidence oforal cancer in India by focusing on its measurement in cancer registries across the country. Based on the International Classificationof Disease case definition adopted by the World Health Organisation, and the International Agency for Research on Cancer, thisreview systematically examines primary and secondary data where the incidence or prevalence of oral cancer is known to bedirectly reported. Variability in age-adjusted incidence with crude incidence is projected to increase by 2030. Challenges focus onmeasurement of disease incidence and disease-specific risk behavior, predominantly, alcohol, and tobacco use. Future researchshould be aimed at improving quality of data for early detection and prevention of oral cancer.

1. High Burden of Oral Cancer in India

Oral cancer is a major problem in the Indian subcontinentwhere it ranks among the top three types of cancer in thecountry [1]. Age-adjusted rates of oral cancer in India ishigh, that is, 20 per 100,000 population and accounts forover 30% of all cancers in the country [2]. The variationin incidence and pattern of the disease can be attributed tothe combined effect of ageing of the population, as well asregional differences in the prevalence of disease-specific riskfactors [3].

Oral cancer is of significant public health importance toIndia. Firstly, it is diagnosed at later stages which result in lowtreatment outcomes and considerable costs to the patientswhom typically cannot afford this type of treatment [4].Secondly, rural areas in middle- and low-income countriesalso have inadequate access to trained providers and limitedhealth services. As a result, delay has also been largelyassociated with advanced stages of oral cancer [5]. Earlierdetection of oral cancer offers the best chance for longterm survival and has the potential to improve treatmentoutcomes and make healthcare affordable [6]. Thirdly, oralcancer affects those from the lower socioeconomic groups,that is, people from the lower socioeconomic strata of society

due to a higher exposure to risk factors such as the use oftobacco [7]. Lastly, even though clinical diagnosis occurs viaexamination of the oral cavity and tongue which is accessibleby current diagnostic tools, the majority of cases present to ahealthcare facility at later stages of cancer subtypes, therebyreducing chances of survival due to delays in diagnosis [8].

Public health officials, private hospitals, and academicmedical centres within India have recognised oral cancer asa grave problem. Efforts to increase the body of literatureon the knowledge of the disease aetiology and regionaldistribution of risk factors have begun gaining momentum.Oral cancer will remain a major health problem and effortstowards early detection, and prevention will reduce thisburden. In light of this, the objective of this paper is toreview and summarise existing literature on the descriptiveepidemiology of oral cancer in India, focusing on theincidence of disease in the country.

2. Case Definition of Oral Cancer

Due to the heterogeneity of pathologies presented in oral cav-ity tumour research, as well as the intraoral cavity evaluationwith respect to the subsites such as the oropharynx, the case

2 Journal of Cancer Epidemiology

Barshi population based cancer registryChennai population based cancer registryDelhi population based cancer registryDindigul Ambilikkai population based cancer registryErnakulum, Srikakulam and Bhavanagar population based cancer registryKarunagappally population based cancer registryMumbai population based cancer registryMainpuri population based cancer registry

Box 1: List of cancer registries reporting incidence of oral cancer.

definition for oral cancer has been further complicated. Dueto this failure to specify and define oral cancer in peer-reviewed literature, meaningful comparisons for descriptionand epidemiological purposes have proved to be a challenge.To minimise misclassification errors and for the purpose ofthis review, oral cancer is defined as the cancer of the lip,mouth, and tongue, to include the anatomic description ofthe oral cavity as reported in previous major population-based research reports [9]. This case definition is adopted,and conforms to the definitions of oral cavity cancer bythe International Classification of Diseases (ICD) Codingscheme, WHO case definitions and IARC. Based on thesecriteria, oral cavity cancer is the 8th most frequent cancerin the world among males and 14th among females [6], themain risk factors being tobacco and alcohol use.

3. Search Strategy

A systematic search of the literature was accomplished usingthe Pubmed Database. Medical Subject headings and free textterms included the following.

(1) “oral cancer” OR “mouth cancer” OR “tonguecancer.” The use of these terms generated a listof numerous MeSH entry terms which includedsubheadings of these main terms to include mouthneoplasms, oral neoplasms, cancer of the mouth, andhead and neck cancers. All these variations of theterm were added to the search, except head and neckcancers since, this did not meet the case definitioncriterion.

(2) “Epidemiology” OR “Descriptive Statistics” OR“Incidence” OR “Prevalence” OR “Longitudinal” OR“Cohort” OR “Case Control” OR “Cross sectional.”

Free text terms included

(3) India OR South Asia.

All three search terms were stringed together to perform atargeted search with the following inclusion criteria.

(1) Studies where incidence or prevalence of oral cancerwas measured.

(2) Population-based studies—Hospital-/Community-based registries.

(3) Studies with standardised criteria for diagnosis oforal cancer.

(4) Studies published in the English language.

The search strategy included all published studies referencingthe incidence and, if possible, prevalence of oral cancer invarious regions of India. Even though at first it was thoughtit would be important to limit the search to include only themost recent up-to-date studies from the past ten years, it waslater decided that it would be important to include all studiesin the initial review due to a dearth of available peer-reviewedliterature on the specified case definition. The search revealedfew frequency studies to include the associated risk factors forthe disease, such as use of alcohol and tobacco. Even thougha few of these studies were selected in the analysis, for thepurpose of this paper, it was decided not to focus solely onthese studies due to the heterogeneity in the case definitionsof oral cancer.

Only studies presenting primary research were includedas part of this review. All studies were included if theymeasured incidence of oral cavity cancer in a standard-ised manner. A number of studies generated through thesearch, presented primary data from national and regionalcancer registries in India and were included in this review.Additionally, for the purpose of representativeness, infor-mation was also retrieved from an online repository ofcancer registration data available through IARC, the cancerincidence in five continents series (CI5), volumes I–IX, thePlus data collection, and the Globocan Project; all of whichare cancer incidence and mortality projects conducted underthe auspices of the WHO.

4. Search Results

Out of the initial 416 articles generated from the first search,the abstracts were reviewed for determining inclusion basedon the established criteria. Once review was completed, 28studies were selected as relevant to the search. However, afterreviewing full texts of all articles, 11 studies were determinedto be types of studies which only measure the prevalence ofthe associated risk factors such as smoking or alcohol usewithout a direct measure of the incidence or prevalence oforal cancer. These 11 studies were excluded.

of these articles were included as studies based on pri-mary data where the incidence or prevalence of oral canceras per case definitions was known to be directly reported.

Journal of Cancer Epidemiology 3

Following an in-depth full-text review of the 17 studies,additional articles with secondary data were obtained via thereferences checks. These articles were only used as referencearticles; no data was included in the analysis. A majorityof these studies, namely 11were cross-sectional studies, 8of which described data from national and regional cancerregistries within the country (Box 1 and Table 1). In mostcases, registry data was also utilised as baseline data onpopulation characteristics. Three of the studies describeddata from population-based prospective cohort studies; oneof the studies utilised a randomized control trial conductedusing a population-based cancer registry, one of the studiesutilised a mixed methods approach to include a combinationof cross-sectional design, ten-year followup and an inter-vention study. Only one of the studies utilised a case-controlmethod nested within a population-based cancer registry.No specific review articles were identified in the search.

5. Summary of Findings

Summary of the study designs and characteristics of allthe studies included in this review is presented in Table 1.Data reported in these studies span the last thirty fiveyears across a number of regions within India. A numberof these studies utilised data from urban and rural cancerregistries established at the national or regional level. Urbanregistries included Delhi, Mumbai and Chennai, and ruralregistries included Barshi, Dindigul, Mainpuri, Karunaga-pally, Ernakulum, Srikakulam, and Bhavanagar.

Various study designs were employed to obtain a samplereflective of the Indian population. Most of these studies werepopulation-based cross-sectional studies utilising cancerregistry data, with the exception of some studies. Gupta et al.[12] conducted a case-control study; however, this study wasnested within a larger study utilising a rural based populationregistry. Sankaranarayanan et al. [22] utilised a community-based cluster-randomised controlled trial where participantswere randomised to either an intervention group or a controlgroup to test the effect of a screening programme on theoral cancer incidence and mortality. Mehta et al. [15] utiliseda mixed methods approach conducted in different phases.Malaowalla et al. [13], Gupta et al. [23], and Cancela et al.[9] conducted population-based prospective cohort studiesto examine the incidence of oral cancer tracked prospectivelyover a period of time.

Since most of the studies included national and regionalsurveys of a population, a wide range of ages were included;however, Khandekar et al. [4] selected participants in anolder age group (>51–60 years) and Maudgal et al. [17]selected participants in a younger age group (range 3–21years).

Summary of case definitions and comments on all studiesincluded in this review is presented in Table 2. In India,cancer is not a notifiable disease. Hence, most of the studiesutilised an active case finding approach to register incidentcases of oral cancer. Sources of registration data includedgovernment hospitals, private health centres, nursing homes,shelters, nongovernmental organisations (NGOs), and com-munity welfare centres. A number of survey methods were

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employed, including house-to-house recruitment, interview-ing, and data abstraction from medical records. Standardiseddiagnostic criteria for the majority of the studies includedthe coding system devised by the WHO-ICD Classificationfor the definition of oral cancer. Mehta et al. [15] reportednonstandardised approach and utilised central papillaryatrophy (CPA) of the tongue as a marker for oral lesions andprecancer, determined by clinical examination conducted bythe authors of the study.

6. Measurement of Disease Incidence

A majority of the studies reported the calculation ofincidence rates as a measure of disease occurrence. Incidenceis defined by the number of new cases of oral cancer, whichoccur in a defined population of disease-free individuals,over a specified period of time. The incidence rate of oralcancer is generally expressed for 100,000 population—overone year (or a range of years). IARC, in its series on the cancerIncidence in Five Continents, utilised incidence rates for adefined period [26]. Age- and sex-specific incidence rates arecalculated to provide an estimate of the risk of oral cancerin defined groups in India. Figure 1 shows the age specificincidence rates for oral cancer between 1983 and 2002; bygender and location (based on 4 cancer registries) in India.An increasing trend based on age; however, lower incidencerecorded amongst females as compared to males is indicativeof gender differences in the lifestyle and behavioural patternsassociated with incidence of oral cancer.

Additionally, incidence of oral cancer is age specific.Thus, for comparison of incidence rates in different areas orfor the same area, over a period of time, it is necessary toadjust the rates for variations in the proportion of populationin different age groups. The generally adopted procedure isthat of direct standardisation, which applies the age- and sex-specific incidence rates of the area under consideration toworld-standard population, to derive the number of cancercases expected to occur in the standard population. Suchage-standardised (or adjusted) incidence rates are useful ininternational or secular comparisons.


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orga

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atio

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and

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mu

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yce

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us

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3–21

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Reg

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Mah

aras

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ral)

1700

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ance

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sion

s

Can

cela

etal

.[9]

1996

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9

Pro

spec

tive

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ort

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dom

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m,K

eral

a;(u

rban

area

)32

,347

mal

epa

rtic

ipan

ts

Meh

taet

al.[

18]

1966

Mix

edM

eth

ods

Stu

dyw

asco

ndu

ced

in3

phas

es:fi

rst

phas

eof

the

stu

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prec

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ase

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ate

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Van

der

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etal

.[19

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992

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dom

lyse

lect

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ted

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amin

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sm

edia

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ined

inea

chca

sean

dan

exam

inat

ion

ofth

eor

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vity

was

perf

orm

ed.

>21

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asof

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icip

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Ta

ble

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onti

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ed.

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gnA

geC

ity,

stat

e(r

egio

n)

Sam

ple

size

(n)

Jaya

leks

hm

iet

al.[

20]

1990

–200

5

Cro

ss-s

ecti

onal

stu

dyof

allr

esid

ents

inth

ear

eau

sin

gca

nce

rre

gist

ry;a

llth

eh

ouse

hol

dsw

ere

visi

ted

bytr

ain

edin

terv

iew

ers.

Info

rmat

ion

colle

cted

onso

ciod

emog

raph

icfa

ctor

s,re

ligio

n,f

amily

inco

me

inru

pees

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tyle

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fact

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usi

ng

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page

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dard

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tion

nai

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asel

ine

info

rmat

ion

colle

cted

onlif

esty

le,i

ncl

udi

ng

toba

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ing,

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soci

odem

ogra

phic

fact

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Kar

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dia

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s

Wah

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]19

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dan

alyt

ical

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Indi

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3]W

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Age

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116.

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ales

and

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0,00

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Lead

ing

site

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ong

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:13.

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edby

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SR:1

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,pro

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).In

fem

ales

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ast

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mon

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5),o

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),an

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dder

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4).

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nyet

al.[

10]

WH

O-I

CD

Cla

ssifi

cati

onfo

rdi

ffer

ent

typ

esof

can

cers

incl

udi

ng

oral

can

cer

Age

-adj

ust

edra

tes,

linea

rre

gres

sion

mod

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sed

onth

elo

gari

thm

ofth

eob

serv

edin

cide

nce

rate

s.A

nn

ual

perc

enta

ge.

Th

orat

etal

.[11

]W

HO

(Nat

ion

alC

ance

rsR

egis

try

Pro

ject

)IC

DC

lass

ifica

tion

Inci

den

ceR

ates

for

toba

cco-

depe

nde

nt

can

cers

.P

reva

len

ceof

toba

cco

hab

its.

Ela

ngo

etal

.[1]

WH

O-I

CD

Cla

ssifi

cati

on

Age

-adj

ust

edra

tes

and

age

spec

ific

inci

den

cera

tes

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late

d.C

um

ula

tive

risk

and

corr

espo

ndi

ng

con

fide

nce

inte

rval

sw

ere

also

calc

ula

ted.

Am

ongs

tal

lcan

cers

,To

ngu

ean

dO

ralC

avit

yC

ance

rw

asth

epr

edom

inan

tsi

tein

allg

rou

ps,e

xcep

tin

rura

lmal

es.

San

kara

nar

ayan

anet

al.

[2]

WH

O-I

CD

Cla

ssifi

cati

on

Of3

585

subj

ects

inth

ein

terv

enti

ongr

oup

refe

rred

,52.

4%w

ere

exam

ined

byph

ysic

ian

s,36

subj

ects

wit

hor

alca

nce

rs,a

nd

1310

wit

hor

alpr

eca

nce

rsw

ere

diag

nos

ed.

Oft

he

63or

alca

nce

rsre

cord

edin

the

can

cer

regi

stry

,47

wer

ein

the

inte

rven

tion

grou

pan

d16

wer

ein

the

con

trol

grou

p,in

cide

nce

rate

sof

56.1

and

20.3

per

100,

000

pers

on-y

ears

inth

ein

terv

enti

onan

dco

ntr

olgr

oups

.Th

epr

ogra

mse

nsi

tivi

tyfo

rde

tect

ion

ofor

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nce

rw

as76

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and

the

spec

ifici

ty76

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;th

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siti

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edic

tive

valu

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as1.

0%fo

ror

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the

inte

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tion

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p,72

.3%

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ses

wer

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II,a

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12.5

%in

the

con

trol

Ou

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em

easu

res

wer

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ase

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lity,

and

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can

cer

mor

talit

y.O

ralc

ance

rm

orta

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inth

est

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grou

psw

asan

alys

edan

dco

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byth

eu

seof

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ster

anal

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.Age

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nce

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sw

ere

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ula

ted,

sen

siti

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and

spec

ifici

tyfo

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alca

nce

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soca

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late

d.D

ata

onor

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nce

,sta

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dm

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Ta

ble

2:C

onti

nu

ed.

Firs

tA

uth

orD

iagn

osti

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rite

ria

Com

men

ts

Gu

pta

etal

.[12

]In

terv

iew

,Clin

ical

Mou

thE

xam

inat

ion

and

Stan

dard

ised

met

hod

sfo

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agn

osis

ofO

rall

esio

ns;

WH

O-I

CD

Cla

ssifi

cati

onA

ge-a

dju

sted

inci

den

cera

tes

wer

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late

d.

Mal

aow

alla

etal

.[13

]St

anda

rdiz

edm

eth

odto

incl

ude

case

con

firm

atio

nof

OC

Cba

sed

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opsi

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fin

edas

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ance

rou

sor

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sion

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cer

prev

alen

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tere

cord

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er10

0,00

0an

daf

ter

follo

wu

pw

asco

ndu

cted

,25/

100,

000

per

year

—85

%of

part

icip

ants

repo

rted

oral

hab

its

ofso

me

form

—to

bacc

o,an

d/or

com

bin

atio

nw

ith

chew

ing

pan

orsu

pari

.

Swam

inat

han

etal

.[14

]St

anda

rdiz

edm

eth

odto

incl

ude

Cod

ing

usi

ng

WH

Ost

anda

rdIC

DC

lass

ifica

tion

Stu

died

inci

den

cepa

tter

n,o

fwh

ich

,104

5in

cide

nt

can

cers

regi

ster

edin

2003

wer

efo

llow

edu

pfo

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tim

atin

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year

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.Ave

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ann

ual

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dard

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rate

per

100,

000

ofal

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cers

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6)th

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1.9)

.Mos

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nce

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rm

enst

omac

h(5

.6),

mou

th(4

.2)

and

esop

hag

us

(3.7

).(2

2.1)

was

ran

ked

atth

eto

pam

ong

wom

enfo

llow

edby

brea

st(1

0.9)

and

ovar

y(3

.3).

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cer

patt

ern

was

desc

ribe

du

sin

gav

erag

ean

nu

alin

cide

nce

rate

san

dsu

rviv

alex

peri

ence

was

expr

esse

dby

com

puti

ng

obse

rved

surv

ival

byac

tuar

ial

met

hod

and

age

stan

dard

ized

rela

tive

surv

ival

(ASR

S).

Meh

taet

al.[

15]

Ora

lpre

can

cer

lesi

ons

defi

ned

asC

entr

alPa

pilla

ryA

trop

hyof

the

ton

gue,

iden

tifi

edby

clin

ical

exam

inat

ion

s.D

iagn

osis

subj

ecti

ve(p

ink

area

devo

idof

papp

illae

was

pres

ent

inth

ece

ntr

eof

the

dors

um

ofth

eto

ngu

e),B

iops

ies

not

con

duct

ed

Dis

trib

uti

onof

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PAac

cord

ing

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ssoc

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dto

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ou

se.

Cor

rela

tion

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yses

was

also

con

duct

edbe

twee

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bacc

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mpt

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bin

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nw

ith

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pala

tale

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emia

(14%

),le

uko

plak

ia(8

%),

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th(3

%).

10ye

arfo

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up

(mea

n6.

7ye

ar)

ofth

e18

2le

sion

ssh

owed

that

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regr

essi

onw

ash

igh

est

(87%

)am

ong

thos

ew

ho

stop

ped

thei

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okin

gh

abit

and

pers

iste

nce

amon

gth

ose

wh

odi

dn

otre

duce

thei

rsm

okin

gh

abit

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Gu

pta

etal

.[16

]O

ralm

uco

us

lesi

ons

asde

fin

edby

pres

ence

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ralL

ich

enpl

anu

sor

Ora

lLeu

kopl

akia

,WH

Ost

anda

rdiz

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iter

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iagn

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Age

-adj

ust

edin

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nce

rate

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0,00

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ere

calc

ula

ted

usi

ng

pers

onye

ars

met

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amon

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thos

ew

ho

stop

ped

toba

cco

use

.In

cide

nce

rati

oof

oral

lich

enpl

anu

sto

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cco

cess

atio

nh

abit

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vers

us

Ora

lleu

kopl

akia

toto

bacc

oce

ssat

ion

(0.3

1).

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ande

kar

etal

.[4]

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MC

lass

ifica

tion

ofth

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mer

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isto

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Stat

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seof

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cen

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dpr

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s.

10 Journal of Cancer EpidemiologyT

abl

e2:

Con

tin

ued

.

Firs

tA

uth

orD

iagn

osti

cC

rite

ria

Com

men

ts

Mau

dgal

etal

.[17

]

Clin

ical

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was

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ied

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and

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cero

us

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into

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ou

sin

gch

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ralc

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bucc

alm

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nd

furt

her

biop

syat

can

cer

spec

ialt

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ospi

tal;

WH

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ssifi

cati

on

Add

ress

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sof

sam

ple

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argi

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and

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Indi

aan

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port

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ctor

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Ver

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ith

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ance

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sor

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Table 3: Age standardized incidence rates per 100,000 population comparison—By location, time period and gender.

Author Location Year M F

CI5 Data, IARC Mumbai 1973–1975 16.3 10.3

ICMR Mumbai, Madras, Bangalore 1982–1984 11 10.5

ICMR Trivandrum (Kerala) 1982–1984 24.2 11.5

Sunny et al. Mumbai (Maharashtra) 1986–2000 12.6 7.3

Manoharan et al. Delhi 2001–2005 11.4 3.7

Table 3 summarizes the age-standardised (or adjusted)incidence rates per 100,000 population for oral cancerreported in reviewed literature by location in India andtime period under study. Different studies reported a rangeof age-adjusted incidence rates (per 100,000 population)for oral cancer. A 4-fold variation in these rates suggestsmethodological differences in the regional registration oforal cancer. The extent to which multiple sources of caseascertainment resulted in measurement bias is unclear;however, data suggests the occurrence of under reporting orover reporting at different sites.

Manoharan et al. [3] reported variable age-standardisedincidence rates across various geographical regions withinIndia for a defined period of time (2004-2005). Data forKolkata only includes 2005. Variations in case registrationtechnique such as medical record abstraction by trainedmedical social workers may have contributed to sampleselection bias. Additionally, patient interviews were utilizedto obtain information highly prone to recall bias, explainingsome variation.

As can be seen in Table 3, age-standardised incidencerates when stratified by sex were lower in females thanmales in the reported articles and data repositories acrossthe different time frames. This is consistent with our earliercomparison in Figure 1. In Figures 2 and 3, variation inage-standardised incidence rates per 100,000 populationby location and time period in males is reported in theliterature.

As can be seen Figure 4, age-standardised incidence rateswere compared across the rural males in selected studies.These rates were identified through the rural population-based cancer registries. Variation in the data calls intoquestion the robustness of cancer registration informationutilized in the methodology of these studies especially inagrarian based rural parts of India where lack of transporta-tion inhibits patients from seeking care.

7. Cancer Registry Data—Comparisons fromIARC Sources

These IARC projects provide estimates of the incidence of,and mortality from major type of cancers for all countries ofthe world. GLOBOCAN only includes data for 2008. Data onIndia was extracted from population-based cancer registries.Figure 5 shows the age-standardised incidence and mortalityrates for all types of cancer. Note that oral cancer ranks thirdamongst all types of cancer.

As can be seen in Figure 6 and consistent with earlierestimates, when stratified by sex, males have a higher age-standardised incidence and mortality rate than females.

The CI5 series compares age-standardised incidencerates in India by time, location and gender and registriessummarised in Table 4. Tables 5, 6, 7 describe a comparisonofincidence and trends consistent with earlier findings.

8. Incidence and Trends of Oral Cancer in India

Oral cancer is a heterogeneous group of cancers arising fromdifferent parts of the oral cavity, with different predisposingfactors, prevalence, and treatment outcomes. It is the sixthmost common cancer reported globally with an annualincidence of over 300,000 cases, of which 62% arise indeveloping countries.

There is a significant difference in the incidence of oralcancer in different regions of the world, with the age-adjustedrates varying from over 20 per 100,000 population in India,to 10 per 100,000 in the U.S.A, and less than 2 per 100,000 inthe Middle East [27].

In comparison with the U.S. population, where oralcavity cancer represents only about 3% of malignancies, itaccounts for over 30% of all cancers in India. The variationin incidence and pattern of oral cancer is due to regionaldifferences in the prevalence of risk factors.

9. Variability in Incidence

Age-adjusted incidence of oral cancer is highly variable inIndia. The population-based cancer registry data, as wellas the literature reviewed in our search demonstrate thenationwide incidence can be as high as 20 per 100,000 pop-ulation, which varied considerably based on study designs,sampling methodology and case ascertainment, as well as byage, gender and location. Variations in age-specific incidencerates also increased with age, which drops at the age ofseventy, a trend which is consistent in multiple studies.

Studies reporting active case finding as a mode ofascertainment may only include those individuals registeredin different parts of the country. Underregistration may havebeen magnified in rural areas. As a result, registration ratemay not reflect the true incidence in these areas. This mayvery well be the case in other parts of India.

Although the definition of oral cancer in most studiesreviewed was standardised as per the WHO-ICD Classifi-cation system, the diagnosis of oral cancer is dependenton the clinical examination conducted by staff or in some


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Figure 2: Age standardized incidence rates per 100,000 population for oral cancer reported in reviewed literature—by location and timeperiod (in males only).

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Figure 4: Age standardized incidence rates per 100,000 populationcomparison—rural males only.

studies the authors themselves. Such examinations are proneto numerous variations based on practice in different partsof the country, resulting in inaccurate coding of data, andunreliable registration information.

In a majority of the studies, data were collected throughone-time community or hospital-based cross-sectional sur-veys; however, no studies refer to continuous available data.Such data would assist in understanding the trends in canceroccurrence and variation according to demographic or lifestyle characteristics of the population to determine furtheraetiological factors influencing oral cancer.

10. Aetiological Factors

High incidence of oral cancer in India can be attributed toa number of aetiological factors. Although not a focus ofthis paper, the limited studies reported the use of tobacco(smoking or chewing) or alcohol intake associated with oralcancer. Seven studies discussed the associations between useof tobacco and oral cancer incidence. Mehta et al. [15]reported the regression rate of leukoplakia as significantlyhigher among those who had stopped or reduced tobaccoconsumption in rural populations in Kerala, Andhra Pradeshand Gujarat. Gupta et al. [12] reported an associationbetween the cessation of tobacco habits and a drop inthe incidence of leukoplakia implying reduced risk for oralcancer after cessation of tobacco use. Khandekar et al. [4]reported tobacco consumption habits among subjects thatincluded chewing (in the form of betel quid, or khaini) andsmoking (bidis and cigarettes) as the common cause of oralcancer. Based on the TNM classification, 48% of these oralcancer cases presented in later stages, that is, III and IV.Mehta et al. [15] reported occurrence of CPA of the tongueas a marker for oral precancerous lesions among users ofbidis in rural parts of India with 98% lesions occurring inthis group. A ten-year followup showed that regression wasthe highest amongst those who stopped the smoking habit.Jayalekshmi et al. [20] reported a significant associationbetween oral cancer incidence and daily frequency of tobaccochewing (P < 0.001, which increased 9.2 fold among womenchewing tobacco 10 times or more a day, with the highest riskduring the first twenty years of chewing).

One study discussed the association between alcohol useand oral cancer. Cancela et al. [9] reported a significant


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Figure 6: Incidence and mortality rates (age standardized) lip andoral cancer in India—by sex extracted from Globocan, 2008 data.

association between risk between alcohol intake and devel-opment of oral cancer in Kerala males among current- andpast-drinkers. They quoted an increased hazard ratio (HR) of49% (95% CI = 1–121%) among current drinkers and 90%(95% CI = 13–218%) among past drinkers. A significant doseresponse relationship between intake frequencies, duration,and risk was observed.

11. Tobacco Use

Tobacco use and alcohol are known risk factors for cancersof the oral cavity. Estimates indicate 57% of all men and11% of women between 15–49 years of age use some formof tobacco. Besides smoking, use of smokeless tobacco is alsowidely prevalent as noted in Box 2, the use of Betel quid, alsoreferred to as pan consist of pieces of areca nut, processedor unprocessed tobacco, aqueous calcium hydroxide (slakedlime), and some spices wrapped in the leaf of piper betelvine leaf. This is very common and is accepted sociallyand culturally in many parts of India. Additionally, gutka,zarda, kharra, mawa, and khainni are all dry mixtures oflime, areca nut flakes, and powdered tobacco custom mixedby vendors. In recent years, commercially available sachetsof premixed areca nut, lime, condiments with or withoutpowdered tobacco have become very popular, particularlyamong younger Indians. Typically, the pan or gutka is keptin the cheek and chewed or sucked for 10–15 minutes, withsome users keeping it in overnight.

Acquisition of the tobacco habit typically occurs early inlife through imitation of a family member or peers. Variousstudies carried out across the country report that at least athird of school students less than 15 years of age have usedone form or another of tobacco. However, with improvedpublic health education, the prevalence of these risk factorsis decreasing around the globe, including in India [1].

Oral cancer incidence from 1990 to 2005 reveals thebenefit of public health interventions such as screeningdemonstrating potential significant reductions in oral cancerincidence. A comparison of oral cancer incidence in Indiaand USA has shown a similar downward trend in bothcountries. However, the reduction is much more dramatic inIndia, where there is a much higher prevalence of oral cancer.

Recently, the trend has also been observed towardsincreased incidence of oral cancer among young adults. Thisincrease in incidence is observed in patients with tonguecancer. In an analysis of 482 consecutive patients presentingwith head and neck cancer to a tertiary care cancer center inIndia, 135 out of the 286 (47%) oral cavity cancer patientsdid not have any known risk habits (tobacco or alcohol use,unpublished data from a blog).

12. Global Burden of Disease

Approximately 12% of deaths worldwide occur due to cancer,and in about twenty years, it is projected to increase fromabout 6 to 10 million [26].

In the USA, cancer incidence and associated mortalityhave declined due to improved infrastructure of the healthsystems that include improved health education and aware-ness translating to improved prevention, earlier detectionand availability of treatment options [28].

However, even though cancer has been previouslythought to be a disease of the western world, more thanhalf of all cancers occur in developing and under-developedcountries becoming one of the leading causes of deathand disability [29]. Consequently, cancer control is quicklybecoming a global health priority. In 2009, global healthand cancer care community leaders formed a global taskforce focused on the expansion of access to cancer careand control in developing countries and with a charter topropose, implement, and evaluate strategies to reduce theglobal burden of disease attributed to cancer [30].


Table 4: Summary of Indian cancer registries reported by IARC, CI5 Series.

CI5 I-IX registries

Registry/population Volume Time period

India, Mumbai (Bombay) 2 1964 1966



India, Poona 4 1973 1977

India, Bangalore 5 1982 1982

India, Chennai (Madras) 5 1982 1982


India, Nagpur 5 1980 1982


India, Ahmedabad 6 1983 1987





India, Barshi 7 1988 1992


India, Karunagappally 7 1991 1992


India, Trivandrum 7 1991 1992

India, Ahmedabad 8 1993 1997



India, Delhi 8 1993 1996







India, Delhi 9 1998 2002






13. Limitations

This review does not come without limitations. Firstly, anumber of studies may not have been found using theidentified search strategy. Secondly, mortality and survivalfrom oral cancer in India have not been described and criteriaused to identify studies may have resulted in publishedstudies only where results are known to be significant orwhere incidence rates are high. As a result, bias from notincluding mortality and survival and publication bias maylead to overestimating the true incidence. Finally, the searchstrategy was also limited to studies published in English,leaving out local language-based Indian journals.

14. Projections

Cancer is not uncommon in India, where the number ofpeople living with the disease is estimated to be around2.5 million, with over 0.8 million new cases and 0.55million deaths occurring each year [31]. According tothe International Agency for Research on cancer (IARC),a group chartered by the World Health Organization toconduct research and develop scientific strategies for cancerprevention and control; cancers of the oral cavity, lungs,oesophagus, stomach, cervix, and breast are some of the mostcommonly occurring forms in both the male and femalepopulation of India.


Table 5: Age standardized incidence rate—1993 to 1997.

Oral cavity and pharynx cancer Age groups 0–85+

Location in India Male Female

India, Ahmedabad 29.6 7.5

India, Bangalore 15.2 11.2

India, Chennai (Madras) 21.9 10.4

India, Delhi 18∗ 6.4∗

India, Karunagappally 16.4 6.4

India, Mumbai (Bombay) 22.5 10

India, Nagpur 23.4 8.2

India, Poona 19.3 9.4

India, Trivandrum 21.4 9.1∗

Includes data only upto 1996.See [24].

Table 6: Age standardized incidence rates—1998 to 2002.

Oral cavity and pharynx cancer Age Groups 0–85+

Location in India Male Female

India, Chennai (Madras) 20.8 10

India, Delhi 17 5.6

India, Karunagappally 20.4 8.9

India, Mumbai (Bombay) 19 8

India, Nagpur 19 7.5

India, Poona 15.6 9.5

India, Trivandrum 21.6 7.9

See [25].

Oral cancer in particular will continue to be a majorproblem. In Figure 7, crude incidence projections by Globo-can demonstrate that oral cancer crude incidence willincrease in India by 2020 and 2030 in both sexes.

Variability in the age-adjusted incidence rates of oralcancer in different regions of India has increased over theyears. Although this review does not provide substantialevidence or information on aetiological factors such assmoking or chewing tobacco and the use of alcohol whichincreases ones risk of developing oral cancer, the specificfocus on these factors will provide opportunities for futureresearch aimed at prevention and control of the disease.

15. Screening and Early Detection

Despite the fact that the oral cavity is accessible for visualexamination, and that oral cancers and premalignant lesionshave well-defined clinical diagnostic features, oral cancersare typically detected in their advanced stages. In fact, inIndia, 60–80% of patients present with advanced disease ascompared to 40% in developed countries. Consistent withpatients presenting for medical care with more advanceddisease in India compared with developed countries, overallsurvival is also reduced. Early detection would not onlyimprove the cure rate, but it would also lower the cost andmorbidity associated with treatment.

Both sexes

MaleFemale

2030

2020

2008

0 50000 100000 150000

Population incidence

Figure 7: Crude incidence projections for lip/oral cavity cancer(2008 to 2030). Data extracted from Globocan, 2008 data. Pop-ulation forecasts were extracted from the United Nations, WorldPopulation prospects, the 2008 revision. Numbers are computedusing age-specific rates and corresponding populations for 10 age-groups.

It is imperative that cost-effective oral cancer screeningand awareness initiatives be introduced in high-risk popula-tions such as those found in India. Several large population-based oral cancer screening programs have been carried out,either as opportunistic screenings or as population-widescreenings. Although these studies have confirmed the effec-tiveness of screening to detect oral cancer and precancerouslesions, only recently has a study from India demonstratedthat oral cancer screening by trained health workers canlower mortality of the disease—especially in individuals witha history of tobacco use [32]. In this randomised, controlledtrial of almost 192,000 people, carried out over an eight-yearperiod, there was a significant reduction in mortality in theintervention arm (29.9 cases per 100,000) versus the controlarm (45.4 cases per 100,000), due to detection of oral cancerat an early stage.

A cost-effectiveness analysis revealed that an oral cancervisual inspection by trained health workers can be carriedout for under U.S. $6 per person. The incremental cost perlife-year saved was U.S. $835 for the all-screened populationand U.S. $156 in the high-risk population (individuals witha tobacco habit) [33].

Mouth self-examination could further reduce the cost ofthe screening and increase awareness in high-risk communi-ties in India. Such a simple and cost-effective strategy has thepotential to have a significant impact on the awareness of oralcancer in the broader community.

16. Future Challenges

Despite the fact that oral cancer and consequences can beprevented, treated, and controlled, there exists a signifi-cant gap in the Indian public’s knowledge, attitudes, andbehaviours. Efforts must be made to introduce a suite ofpreventive measures that has the potential to significantlyreduce the burden and to help bridge the gap betweenresearch, development and public awareness. Knowledge


Table 7: Comparison of age standardized incidence rates per 100,000 by time, location and gender.

Males Females

1998–2002 1993–1997 1998–2002 1993–1997

Chennai (Madras) 20.8 21.9 10 10.4

Delhi 17 18 5.6 6.4

Karunagappally 20.4 16.4 8.9 6.4

Mumbai (Bombay) 19 22.5 8 10

Nagpur 19 23.4 7.5 8.2

Poona 15.6 19.3 9.5 9.4

Trivandrum 21.6 21.4 7.9 9.1

Bold data only include rates upto 1996.See [25].

betel quid (or pan quid)—prepared by wrapping cured, dried tobacco leaves or stems andslices of dried or fresh areca nut in a fresh green betel leaf, smeared with a paste calciumhydroxide. In some parts of India, condiments or flavouring agents or sweeteners are added to itbidi (also referred to as chutta) is a form of Indian cigarette used in rural areas and preparedby rolling small quantity of tobacco in a dried leaf.

Box 2: Definition of tobacco products as reported in peer-reviewed literature.

dissemination to help people adopt behaviour patterns toimprove their health and decisions making process and toprovide required public health education and training topromote lifestyle modifications are key to confronting thechallenge.

The greatest threat of the oral cancer burden existsamong the lower socioeconomic strata. This segment ofthe population is the most vulnerable because of higherexposure to the risk factor—tobacco—which complicatesthe situation further. They have the most limited accessto education, prevention and treatment. These disparitiesshould be addressed to push for provision of easy, accessible,detection, and treatment services. Prevention through actionagainst risk factors, especially tobacco will be key to reducingthe burden amongst these groups.

Abbreviations

AP: Andhra PradeshASRS: Age-standardised relative survivalASR: Age-standardised rateCI5: Cancer incidence in 5 continentsCPA: Central papillary atrophyDACR: Dindigul Ambilikkai cancer registryGLOBOCAN: IARC Global Cancer ProjectHW: Health workersHR: Hazard ratioIARC: International Agency for Research on

CancerICMR: Indian Council of Medical ResearchICD: International Classification of DiseasesMeSH: Medical subject headingsNGO: Nongovernmental organisation

OCC: Oral cavity cancerTNM: Tumour node metastasisUP: Uttar PradeshUSA: United States of AmericaWHO: World Health Organisation.

Acknowledgments

Author would like to acknowledge Professor Martin Roland,Professor of Health Services Research and Dr. John Powlesfrom the Department of Public Health and Primary Care atthe University of Cambridge for mentorship and support, Dr.Rohan D’Souza, Specialist Registrar at Epsom and St. HelierHospitals NHS Trust, London, United Kingdom, and Dr.Hermann Brenner, German Cancer Research Center, Hei-delberg, Germany for comments during the review process.The author also declares that there are no potential conflictof interests, including financial interests, relationships, andaffiliation relevant to the subject of the manuscript in anyway. No funding was sought in the creation of this work.

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