Review Oral cancer

Ethnicity and oral cancer

Crispian Scully and Raman Bedi

Oral squamous-cell carcinoma, the main type of oral

cancer, is among the ten most common cancers in the
world. The aims of this paper were first, to consider
whether there was evidence of marked ethnic
variations in the incidence, management, and survival
of oral cancer, and then, to review possible
explanations for these variations. Evidence from the
literature suggests that there is marked, inter-country
variation in both the incidence and mortality from
oral cancer. There is also growing evidence of intra-
country ethnic differences, mostly reported in the UK
and USA. These variations among ethnic groups have
been attributed mainly to specific risk factors, such as
alcohol and tobacco (smoking and smokeless), but
dietary factors and the existence of genetic
predispositions may also play a part. Variations in
access to care services are also an apparent factor. The
extent of ethnic differences in oral cancer is masked by
the scarcity of information available. Where such data
are accessible, there are clear disparities in both
incidence and mortality of oral cancer between ethnic
groups.
Lancet Oncol 2000; 1: 37–42
Most oral cancers are squamous-cell carcinomas (SCC) and
it is customary to include cancers of the lip, tongue, gum,
floor of the mouth, and unspecified parts of the mouth in
this group1 (Figure 1).
Most of our population-based information is derived
from cancer registry data, and increasing international
collaboration has helped to improve the standard and
consistency of reporting.2 However, sub-groupings of
national or regional data by variables such as ethnicity or
socio-economic status, have not been widely adopted. Never
the less, it is clear that the incidence of oral cancer varies
widely between countries and geographical areas of the
world,2 and that it is generally most common in developing
countries. These variations have traditionally been explained
by the exposure of these populations to specific risk factors,
such as tobacco and alcohol.3,4
Interest in ethnic variations in health and disease has, in
part, arisen from the need to have a better understanding of
discrepancies in three factors: first, the prevalence of illness
and health-related behaviours; second, the quality of services
provided and their accessibility; and third, the explanatory
variables of genetic predisposition, environment and socio-
economic determinants of health.
Racial differences relate to the group that a person
belongs to as a result of a mix of physical features (eg skin
colour, hair texture), ancestry, and geographical origins.
Figure 1. Oral cancer
Race is traditionally considered as being defined by others,
whereas ethnicity is self-defined.5 Thus, the concept of
ethnicity is one in which individuals themselves define the
group to which they belong, as a result of cultural habits or
beliefs, together with other factors such as language, religion,
and diet. These differentials between ethnicity and race are
gradually being eroded, and are now so intertwined that
consideration of one necessarily requires consideration of
the other. In this paper, therefore, race and ethnicity will be
used synonymously, except where there are clear differences,
which need to be explained.5
Epidemiology of oral cancer
Estimates for 1990 indicate a total of 8.1 million new cancer
cases, divided almost exactly between industrialised and non-
industrialised countries.6 This shows a 37% increase from the
figures provided for 1975,6 representing an increase of
approximately 2.1% per year; this is compared with a rate of
growth of the world's population of 1.7% per year.6 The
number of new mouth (oral) cancers in 1990 was estimated to
be 212 000 cases worldwide, amounting to 2.6% of total
cancers.2 Mouth cancer is the 12th most common cancer in
the world, but is the eighth most frequent cancer in men.2 The
CS and RB are both Co-Directors of the WHO Collaborating Centre
for Disability, Culture and Oral Health at the Eastman Dental
Institute, University College London, UK.
Correspondence: Professor Raman Bedi, National Centre for
Transcultural Oral Health, Eastman Dental Institute, University
College London, 256 Gray's Inn Road, London WC1X 8LD, UK. Tel:
+44 (0) 207 915 2314/1193. Fax: +44 (0) 20 7915 1233.
Email: R.Bedi@eastman.ucl.ac.uk

THE LANCET Oncology Vol 1 September 2000 37

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Oral cancer
Figure 2. Transcultural tobacco products. (a) Traditional bidis (an unfiltered, hand rolled cigarette). (b) Gutkha – sweetened chewing
tobacco.
sex ratio is 2.0 (M:F). Mouth cancer in men mostly occurs in
western and southern Europe, south Asia, Melanesia,
southern Africa and Australia/New Zealand. In women, it is
prevalent in south-central Asia, Melanesia and Australia/New
Zealand.2
The cause has been attributed to specific risk factors:
tobacco3 and/or alcohol4 in western and southern Europe, and
southern Africa, and betel quid7 (Figure 2) in south-central
Asia and Melanesia. The high rates of oral cancer in
Australia/New Zealand are due to lip cancer, related to solar
radiation. Each year, there are 197 000 deaths, worldwide,
from cancer of the mouth and pharynx, with the highest
mortality from mouth cancer occurring in Melanesia and
south-central Asia. These mortality rates are about double
those seen in industrialised countries.2,8
Surgical resection and/or radiotherapy are the main
treatments for oral cancer. For small primary cancers (stages 1
and 2, without regional spread), wide surgical excision or
radiotherapy alone can result in local tumour control and
long-term survival. However, mortality rates for oral cancer
have substantially increased in many countries. There is no
evidence that survival rates for oral-cavity cancer have
improved, in the USA during the period 1973 – 1989.9
Although the efficacy of screening for oral cancer in increasing
survival and reducing mortality remains unproven,10,11 it is
believed that Cuba's on-going oral cancer screening
programme has resulted in a higher proportion of cancers
being localised at diagnosis, and a comparatively high survival
rate.12 A reduced incidence of oral pre-cancerous lesions has
been reported after a primary prevention trial carried out in
India.13 In addition, it has been shown that abstinence from
tobacco for a 6-week period can result in the reversal of
potentially precancerous oral lesions.14
Analysis based on individual records from the national
mortality and registration files, secular and cohort trends in
mortality from cancer in Scotland, from 1953 to 1993, and
incidence from 1960 to 1990, showed increases in both
mortality from, and incidence of, oral cancers in young adult
men.15 In Germany, Czechoslovakia and Hungary, there has
been an almost ten-fold rise in mortality from oral cancer in
38
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Review
men aged 35 – 44, within one generation.16 There is good
evidence, therefore, that Europe has a pronounced upward
trend in this disease.17,18 The only country that appears to be an
exception is Finland,17 although an increase has been recorded
in Denmark.19 The EUROCARE-2 study showed that 5-year
survival rates were highest for lip cancer, but low for cancers
of the tongue and other parts of the oral cavity.18 Marked
inter- and intra-country variations in the survival rates, by
sex, age and social class, were also seen.18
Oral cancer and ethnic variations
At present, no clear trend has been observed between the
incidence of oral cancer and socio-economic status.20 A
positive trend (ie high rates in more affluent groups), is seen
in Colombian men, but a negative trend (high rates in
deprived groups) is observed in Danish men and Swedish
women.20 However, there is growing evidence of intra-country
ethnic differences; for example, a significantly higher number
of deaths from oral cancer has been recorded in men from the
Indian subcontinent in the UK, than in the indigenous UK
population.21,22 In addition, oral cancer appears to be most
prevalent in areas with a high Asian population.23 The Chinese
have a lower risk of oral cancer than Indians in Malaysia and
also show a later age of onset.24 In Australia, migrants from the
Mediterranean littoral and the Middle East have lower rates of
mouth cancer than the Australian-born population.25 South-
east Asian migrants to France have also been found to have a
lower risk of mouth cancer,26 as have Maghrebian (Algerian,
Tunisian, and Moroccan) migrants.27 This was revealed by
examining mortality data from the period 1979 – 1985, and
population data from the 1982 French census. Ashkenazi Jews
appear to have a greater risk of developing cancer in Israel
than Sephardis, or those of eastern origin.28
The relation between oral cancer mortality and socio-
economic status is stronger than that for incidence.20 In men, a
higher mortality from oral cancer is clearly seen in socially
disadvantaged groups in most countries, with the exception of
Japan and California, USA.20 The negative trend was most
noticeable in the UK in the period 1979 – 1983,29 and in
France, Italy and New Zealand.20 The mortality data for
THE LANCET Oncology Vol 1 September 2000
 Review
women are less clear, except in the UK, where a similar
negative trend that seen in men has been observed.29 Incidence
data on oral cavity and pharyngeal cancer, and survival rates
after diagnosis, were examined in Scotland, between 1968 and
1992. It was found that survival rates for cancers of the
tongue, mouth and pharynx, diagnosed among people less
than 65 years of age decreased between 1968 – 1972 and
1983 – 1987. Five-year relative survival rates fell from 47% to
39% over this period, whereas the equivalent rates among
people over 65 years of age, showed a modest improvement,
from 34% to 38%. When considered by degree of social
deprivation, survival is lower among people from the most
underprivileged areas, and it is among these populations that
the recent rise in incidences of cancers of the oral cavity and
pharynx have mainly occurred. These two factors may, to
some extent, explain the unfavourable trends in mortality.30
In the north-east of England, age- and sex-specific
incidence and mortality rates for both tongue and mouth
cancer rose with age, although there was little change over
time, and no improvement in crude survival was seen in either
sex. In men, for both tongue and mouth cancer, there was a
graded increase in the standardised registration and mortality
ratio from the most affluent to deprived areas, but these
differences were less marked in women. The analysis by
deprivation has shown a clear relation to material
deprivation.31
Intra-country ethnic differences in oral cancer mortality
are variable but in some countries, such as the UK, there is
growing evidence of clear differences. Migrants from East and
West Africa and the Caribbean coming to England and Wales
were studied over the period 1970 – 1985: mortality from
oropharyngeal cancer was highest in both sexes in East
Africans.32 A higher mortality from oral cancer was also
observed in people born in the Indian subcontinent, who had
migrated to England and Wales. This significantly raised the
level of risk in the Indian group who were born in India, as
compared with the white community and Indians born in the
UK, irrespective of their gender.33
The strongest evidence of intra-country ethnic differences
in oral cancer mortality comes from the USA. There, death
rates from cancer of the mouth and pharynx among blacks in
1987 (5.7 per 100 000) were higher than among whites (3.4
per 100 000). This finding has been seen in virtually all States
studied,34 and is mirrored in local studies35 and in the NCI
Surveillance, Epidemiology and End Results program (SEER),
which has monitored all major cancers within nine
geographic areas of the USA,34 since 1973. The 5-year relative
survival rate was 33% for blacks, compared with 55% for
whites.36 The peak mortality also occurred at a younger age in
blacks (55 – 64 years) than in whites (>75 years).34
In summary, it is clear that there is considerable variability
in both the oral cancer incidence and mortality data, in both
inter- and intra-country populations.37 This is primarily
attributable to variations in the prevalence of major risk
factors between populations. Moreover, from the few studies
that have explored intra-country ethnic variations, there is
growing evidence that there are such differences in both
incidence and mortality of oral cancer, especially in the UK
and USA. Understanding these differences in terms of the
standard risk factors for oral cancer may help in our
management and preventive strategies.
THE LANCET Oncology Vol 1 September 2000
For personal use only. Not to be reproduced without permission of The Lancet.
Oral cancer
Tobacco, alcohol, and dietary factors
There are a plethora of studies linking specific behaviours,
such as tobacco and alcohol use, to oral cancer.38 However,
little work has been undertaken to include psychosocial
factors (eg working environment, poor use of skills, stress,
etc).39 The evidence linking these elements to social
differentials in disease is stronger for cardiovascular
problems and mental health, than for cancer, although they
may, at least partially explain the underlying reasons for
tobacco and alcohol use and poor diet, and therefore the
variations in oral cancer.39
Consumption of tobacco products has long been
causally connected with oral cancer.7 In most industrialised
countries, prevalence of smoking is greater in the lower
social class groups.40 This pattern is often reversed in non-
industrialised countries. The key question is the extent to
which tobacco usage can explain the observed social class
differences in oral cancer risk.
In the USA, 40 years ago, smoking prevalence in whites
and blacks was about equal but, more recently blacks appear
more likely to use tobacco.41 In the UK, this same pattern of
high rates of smoking in minority ethnic groups has also
been observed.42,43
Smokeless (chewing) tobacco use is also an important
factor for South Asian populations in Asia, and in countries
such as the UK and the USA.38,44 The habit of chewing areca
(betel) nut, either with or without tobacco, can cause
cytogenetic changes in the oral epithelium, and is important
in the development of oral submucous fibrosis and mouth
cancer.45 Some indiviuals chew the nut only, while others
prefer paan (Figure 3), which may include tobacco, and
sometimes lime and catechu. Studies from India have
confirmed the association between paan tobacco chewing
and oral cancer, particularly cancer of the buccal and labial
mucosa.8,46 In South Asian communities in the UK, most
adults (82%) use tobacco and many (42%) in the 50 – 80-
year age group, chew betel (areca nut); this is compared with
only 5% in the 16 – 29-year age group.44,47 Among Asian
communities in the UK, Bangladeshis are particularly likely
to retain the habit of betel use. Paan was chewed by 78% of
Bangladeshi adults, with significantly more women than
men chewing, and adding tobacco to their quid.44 There is
extensive misinformation and lack of awareness among this
population about the risk factors and the signs of oral
cancer, irrespective of age, sex, South Asian subgroup, and
social class.48
There is growing evidence of an association between
increased alcohol consumption and risk of oral cancer, with
higher consumption in lower social class groups;4,36 for many
countries, this follows a similar pattern to tobacco use.38,49 In
‘alcohol-related’ cancers, this negative gradient is mostly
seen in men living in France, Italy, and New Zealand. The
evidence is less strong in relation to men in Brazil,
Switzerland, the UK, and Denmark.50 The differences in oral
cancer incidence in US ethnic groups have been attributed
mainly to heavy alcohol consumption by blacks, particularly
among current smokers.49
There is considerable evidence that diets rich in fresh
fruits and vegetables, and particularly in vitamin A, have a
protective effect against oral cancer and precancer.38 In some
studies of US blacks, a lower consumption of fruits and
39
Oral cancer
Figure 3. Typical contents of a betel quid (paan).
vegetables has also been found to be related to mouth
cancer,51 but not in all cases.
The problems of evaluating past dietary patterns,
assessing the intake of individuals, and controlling
confounding factors make valid studies in this area difficult
to undertake.38 The role of diet in the ethnic predisposition
to oral cancer, therefore, requires further study.
Access and use of services
Analysis of the NCI’s SEER data from 1988 to 1993, showed
that most of the increased risk of death from mouth cancer
in blacks was due to lower socio-economic status, more
advanced stage of disease, and differences in the type of
treatment they received.52 Interestingly, studies among
school employees53 showed decreased rates of oral cancer in
blacks, as compared with the general population.
Furthermore, in Veterans Administration (VA) patients,
who have equality of access to care, there were no ethnic
differences in incidence of oral cancer.54 The charts of male
patients with a diagnosis of squamous-cell carcinoma of the
head and neck at one VA Hospital were reviewed, in order to
identify prognostic indicators. No differences were observed
between Anglo-American and Hispanic patients, with
respect to site of the primary tumour, age at diagnosis,
performance status, or the frequency of surgery, radiation
therapy, or chemotherapy; although there was a tendency for
Hispanic patients to have a more advanced stage of cancer
and to have received more treatment.55
Differences have also been found in other ethnic groups.
Cancer deaths among white, foreign-born residents of New
York State (exclusive of New York City) during the years
1969 – 1971, analysed according to country of birth, showed
Irish immigrants to have an increased risk of dying from
oropharyngeal cancers.56 Non-whites in Brazil are at twice
the risk of dying from oral (lip) cancer than the white
population.57
Genetic predisposition
The molecular changes found to be associated with oral
carcinomas in western countries (UK, USA, Australia),
particularly P53 mutations, are infrequent in the east (India,
40
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Review
south-east Asia), where the
involvement of RAS oncogenes,
including mutation, loss of hetero-
zygosity (H-RAS) and amplification (K-
and N-RAS) are common. This
observation suggests that there are
genetic differences between populations
from these geographical areas.58 There
could also be genetic differences in the
ability to metabolise pro-carcinogens
and carcinogens, by means of xeno-
metabolising enzymes, or in the ability
to repair DNA damage, between
different ethnic groups.59
For example, alcohol dehydro-
genase (ADH) oxidises ethanol to
acetaldehyde; this is cytotoxic and
results in the production of free radicals
and DNA-hydroxylated bases. ADH
type 3 genotypes appear to be
predisposed to oral cancer.60 Ethanol is also metabolised to
some extent by cytochrome P450 (CYP) IIEI (CYP2E1) to
acetaldehyde. Cytochrome P450 can activate many
environmental pro-carcinogens by exposing or adding
functional groups. Polycyclic aromatic hydrocarbons (PAH)
such as benzo(a)pyrene, a procarcinogen, are activated by
cytochrome P450 and peroxidases to toxic electrophilic and
free-radical reactive intermediates. CYP1A1 is a major
metaboliser of benzpyrene and CYP2E1 is inducible by
ethanol and can activate N-nitrosamines. Mutations in some
tumour suppressor genes may be related to cytochrome
P450 genotypes,61 and may predispose individuals to oral
cancer, although not all studies support this idea.62
Glutathione S-transferase (GST) detoxifies hydrocarbon
epoxides and DNA hydroperoxides. Benzpyrene and other
PAH products can be metabolised by GST – specifically
GSTM1 and GSTP1 genotypes. Some genotypes have
impaired activity; for example, the null genotype of GSTM1
has a decreased capacity to detoxify tobacco carcinogens.
GSTM1 and GSTP1 polymorphic genotypes and GSTM1
and GSTT1 null genotypes have been shown to predispose to
oral cancer in some61,63 but, again not all, studies.62,64
N-acetyl transferases NAT1 and NAT2 acetylate pro-
carcinogens. N-acetyl transferase NAT1*10 genotypes might
be a genetic determinant of oral cancer – at least in the
Japanese.65
Cytogenetic and molecular analyses in oral cancer have
shown changes in several chromosomes, including those
involved in the repair of DNA damaged by carcinogens,
radiation, and other mutagens.66 Patients with oral cancer
show increased sensitivity to various mutagens,67,68 a trait that
correlates with a positive family history of cancer,69 and with
tissue P53 tumour suppressor gene changes. Evidence of
defective DNA repair has also been found to underlie some
head-and-neck cancers.70
Conclusions
It is unfortunate that so little detailed information is
available about the extent of ethnic differences in oral
cancer. There is also insufficient information to address the
question of ethnic differences in the natural history of oral
THE LANCET Oncology Vol 1 September 2000
 Review
Search strategy and selection criteria
Through a comprehensive search, an attempt was made to
identify all relevant studies irrespective of language. Papers
that were not in English were considered, if they could be
translated. Relevant studies were identified by searching
several electronic databases from the date of inception.
MEDLINE was searched, highlighting the period 1966 to
April 2000, EMBASE from 1980 to 2000, DISSERTATION
ABSTRACTS from 1861 to November 1999, ERIC from
1992 to September 1998, SCISEARCH from 1982 to 2000,
and ISTP from 1981 to 2000. The subject headings or key
components used included oral cancer, head and neck
cancer, race, and ethnicity.
Conference proceedings were also searched by use of the
citation index SCISEARCH. The references of eligible
papers were checked for further relevant studies, and those
identified were sought as a citation on the SCISEARCH
database. The Cochrane Library databases were also
scanned.
cancer, although it is clear that there are intra-country
variations in the occurrence of precancerous lesions, such as
oral submucous fibrosis.71 However, with regard to
squamous-cell carcinoma, where such information is
available, there are clear ethnic differences in both incidence
and mortality rates of oral cancer.
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THE LANCET Oncology Vol 1 September 2000