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Oral cancer is a major public health problem, with 350 000 to 400 000 new cases identified worldwide each year. Worldwide, oral squamous cell carcinoma (OSCC) is the sixth most common cancer for both sexes (Parkin et al., 1999). Incidence varies widely between countries and geographical areas, but it is generally most common in developing countries. Even in the United States, however, it was estimated that oral and pharyngeal cancers would account for 29 800 cases and 8100 deaths in 1999 (Landis et al., 1999). These variations have traditionally been explained by differences in lifestyle exposure to specific risk factors such as tobacco, betel, and alcohol use, although environmental factors (especially infective agents) and socioeconomic factors, genetics, and ethnicity may also be involved.
Oral cancer is a term that usually includes cancers of the lip, tongue, salivary glands, and other sites in the mouth (gum, floor of mouth, and other unspecified parts of the mouth). Approximately 90% of oral cancers are squamous cell carcinomas (OSCCs). Pharyngeal cancer is a term that includes cancers of the nasopharynx, oropharynx, and hypopharynx.
In the developed world, some 42% of OSCC affects the lip, but most intraoral OSCC involve the floor of the mouth or the lateral border of the tongue (the graveyard or coffin area; 22% the tongue, 17% the floor of mouth). In the developing world, cancers of the tongue and buccal mucosa are the most common (Sankaranarayanan, 1990).
Oral cancer is especially common in disadvantaged older people with lifestyle factors of smoking tobacco and drinking alcohol. Incidence increases with age, a steep rise beginning in the age group 60–64 years (Ries et al., 1999). The overall male-to-female ratio is greater than 2:1, but for oropharyngeal cancer the ratio is 4:1 (Ferlay et al., 2001). The excess in older males has largely been attributed to the habits of males, particularly tobacco and alcohol use, and the length of exposure to carcinogens/mutagens.
Among younger individuals, the incidence of OSCC is rising, particularly for tongue cancers. Evidence that traditional risk factors may not be responsible for this trend suggests the need for more definitive and cost-effective means to detect OSCC in populations that until recently have been considered at low risk.
Two-thirds of all OSCC in males and three-quarters in females arise in the developing world (Parkin et al., 1999), where it is the third most common cancer. It is particularly common in South-Central Asia, home to one fifth of the world’s population. Probably 58% of the cases are concentrated in South and Southeast Asia (Nair et al., 2004). In most regions of India, oral cancer is the most common cancer in men and the third most common cancer in women. In Karachi, oral cancer ranks second of all malignancies among both males and females, with one of the highest reported incidences in the world (Bhurgri, 2005). Brazil also has a high incidence in males, and the area including southern Brazil, Uruguay, and Argentina has the highest rates in Latin America. The gender difference in OSCC rates has been decreasing over time, presumably as tobacco and alcohol consumption equalize (Tumino and Vicario, 2004).
The highest incidence of OSCC worldwide, at up to 55 cases per 100 000 per year, has been recorded in the Bas-Rhin de´partement of France (Blot et al., 1996; Levi et al., 1998), but incidence in Hungary and other parts of Eastern Europe is rising (La Vecchia et al., 2004). In Central and Eastern Europe, Hungary, Croatia, Slovenia, Ukraine, Russia, and Lithuania have incidence above 7 per 100 000; intermediate rates at 6–7 per 100 000 are seen in Spain, Switzerland, Germany, Poland, and Italy; and rates below 4 per 100 000 are found in Greece, the Netherlands, some Nordic countries, and England and Wales (Levi et al., 1998). In the United States, OSCC is the tenth most common cancer among males (Moore et al., 1999, 2000).
Oral squamous cell carcinomas are often diagnosed late. Five-year survival is relatively low, at approximately 50%; and this has changed very little in the past 30 years (Swango, 1996). In the United States, 5-year survival is much lower in Blacks (34%) than Whites (55%). Survival is particularly low in black males (28%), compared with 47% in females. In Europe, 5-year survival is about 44% (Berrino et al., 1999). Localized cancers have the highest 5-year relative survival (79%), those with regional disease intermediate (42%), and cancers with distant metastases the lowest (19%) (Gloeckler Ries et al., 1994). OSCC is associated with a very high risk of second primary tumors (SPTs) in the same location (Cooper et al., 1989).
The incidence of lip cancer in men has decreased in many countries, such as in Finland (Tarvainen et al., 2004) and Pakistan, but the rates in Pakistan have remained level in females (Bhurgri, 2005).
The incidence of OSCC in U.S. white men stabilized in the 1980s and started to decrease, but incidence in women and especially black men began to increase. About that time, an increased incidence of tongue cancer was noted in young people (under 45 years of age) in many countries (Davis and Severson, 1987; MacFarlane et al., 1987; Moller, 1989; Hindle and Nally, 1991; MacFarlane et al., 1992; Wennerberg et al., 1994; Hindle et al., 1996; Kari et al., 1997; Mork and Glattre, 1998; Myers et al., 2000; Shiboski et al., 2000; Annertz et al., 2002; Schantz and Yu, 2002; Shiboski et al., 2005).
OSCC incidence has also changed in Pakistan and India (Gupta, 1999). Data for 1995–2004 from the Karachi Cancer Registry, Pakistan, showed an earlier onset of disease for all categories (Bhurgri, 2005). The incidence of tongue cancer increased, but a more dramatic increase in OSCC in the cheek was evident in both sexes (Bhurgri, 2005). In males in India, however, a statistically significant decreasing trend in the overall age-adjusted incidence rates of OSCC was observed during the period 1986–2000, which may be attributable to a decrease in the usage of pan and tobacco (Sunny et al., 2004). The high prevalence of smokeless tobacco use among young adult men and women may explain the stable trend in oral cancer incidence in this group.
In Europe during the period 1955–90, several countries in Central and Eastern Europe had at least a twofold increase in OSCC, principally in males under 45 years of age (La Vecchia et al., 2004), and Denmark, Finland, Norway, and Sweden showed more than fivefold increases in young males (Annertz et al., 2002; Tarvainen et al., 2004). Similar increases were also seen in young women in England and Wales (Hindle and Nally, 1991), Scotland (MacFarlane et al., 1992), and Greece (Zavras et al., 2003).
In most European countries, oral cancer mortality had been rising between the 1950s and 1980s, in both genders, and with a twofold increase in men in the Czech Republic, Poland, Romania, and Spain, and a fourfold rise in Hungary and Germany (La Vecchia et al., 1997; Levi et al., 1999). Similar increases were recorded in the United States (Schantz and Yu, 2002), Thailand (Reichart et al., 2003), India and Pakistan (Gupta, 1999), Uruguay (De Stefani et al., 1994a, b), and Brazil. Mortality continued to increase in many European countries during 1980–99, especially in Eastern Europe, although mortality levelled off in Poland and the Czech Republic, and actually fell in some Western European countries including Austria, Germany, and England and Wales (La Vecchia et al., 2004). The disparity in mortality between males and females is largely attributable to differences in incidence.
The increases at younger ages, seen in many countries, indicate cohort effects that suggest that the increase in overall incidence is likely to continue in future decades (Boyle et al., 1992; Macfarlane et al., 1994).
The incidence of tumors of the tongue and tonsil rose in young Whites in the United States over the period 1973–2001 (Shiboski et al., 2005). The incidence of OSCC of the tongue in adults under 40 years of age increased by 60% between 1973–84 and 1985–97 (Schantz and Yu, 2002). Mortality from cancers of the mouth in males increased in 19 of 24 countries between 1950–54 and 1980–85 (MacFarlane et al., 1994). Oropharyngeal cancer incidence rose rapidly in Scotland between 1950 and 1998, particularly among males and females aged 35–64 years during the period 1989–96, although age-standardized mortality appeared to have stabilized (Robinson and Macfarlane, 2003).
These increases in OSCC appear to reflect lifestyle habits that have become common in younger generations, such as the use of tobacco, alcohol, and betel. The rising trend in Central and Eastern Europe appears to reflect the rise in all tobacco-related neoplasms, but the rise in OSCC in Scotland, despite the fall in lung cancer, may reflect increased alcohol use (Levi et al., 2003). The rises in Russia may reflect increasing alcohol use (Zatonski, 1998). The rises in South Asia reflect growing betel use (Nair et al., 2004). However, the increases in other countries have often been seen in the absence of these conventional lifestyle risk factors, particularly in women, which raises questions about the cause of these cancers.
Carcinogenesis is the result of disturbed growth control arising from DNA damage (mutation) which can arise spontaneously (probably from free radical damage), but may also be precipitated by mutagens (Scully et al., 2000). Tobacco, alcohol, betel, and areca nut are the main risk factors (La Vecchia et al., 1997; Bagnardi et al., 2001; Boeing et al., 2002), but significant numbers of younger patients with OSCC deny exposure to any known risk factors (Ehlinger et al., 1993; Mackenzie et al., 2000; Llewellyn et al., 2003).
A case–control study in Brazil showed the risk for cancer in the head and neck to be raised for those who reported cancer at any site in a first-degree relative, with a greater risk if the relative had cancer in the head and neck (Foulkes et al., 1995). In a UK study, most young OSCC patients had had a relative with cancer (Llewellyn et al., 2003). Some have suggested that familial clustering of cancer points to a genetic component, but so far no study has provided clear-cut evidence to support this view.
There is an excess mortality from OSCC in minority ethnic and in socially disadvantaged groups (Scully and Bedi, 2000) (Table 1).
Examination of mortality trends from 1973–87 suggests that the disparity in mortality between Blacks and Whites in the United States was most probably attributable to differences in survival, rather than differences in incidence (Goldberg et al., 1994). In Europe, there is an increased mortality in immigrants from the Indian subcontinent (Swerdlow et al., 1995).
The results of many studies have been summarized by the International Agency for Research on Cancer (IARC) showing the importance of specific risk factors, i.e., tobacco, betel, and alcohol use (IARC 1986a, b, 1988), which contain known carcinogens.
Tobacco use in all forms appears to carry a risk. Oral cancer risks show a clear decline after stopping tobacco use (La Vecchia et al., 1999). Oral leukoplakia, the most common premalignant oral lesion, is related to tobacco use (Gupta, 1984). Smokers have a sevenfold risk of an oral dysplastic lesion ( Jaber et al., 1999).
Cigarette smokers appear to be about five times more likely to develop OSCC than nonsmokers. Those who abstain (e.g., Mormons and Seventh Day Adventists) have a lower incidence. In one study, the odds ratio for consumption of more than 20 cigarettes a day was double that of smokers consuming fewer cigarettes (Lopez et al., 2000). In one European study, the risk of oral cancer in smokers of low/medium-tar cigarettes was 8.5-fold higher than in nonsmokers, and more than 16-fold for high-tar cigarette smokers (La Vecchia et al., 1990).
Smoking bidi, the unfiltered cigarettes with a small amount of flaked tobacco, which is widely practised in South Asia, increases the risk of OSCC (Rahman et al., 2005). Cigars may predispose to leukoplakia (Baric et al., 1982) and oral and pharyngeal cancers (Shanks and Burns, 1998). Pipe smoking carries a risk of leukoplakia and OSCC (Baric et al., 1982). Reverse smoking (holding the burning end of a cigarette or cigar within the mouth) – seen in India, South America, Taiwan, and the Philippines – is strongly associated with OSCC (Gupta et al., 1980).
Smokeless tobacco (ST) products include paan (or pan), chaalia, gutka, and naswar and are used in all sections of South Asian society. Use of these products increases the risk of OSCC (Gupta et al., 1980).
In India, different forms of chewing tobacco are used such as betel, khaini, pattiwala tobacco, maiwpuri tobacco, zarda, kiwam, and gadakhu. Risks appear to depend on the processing of the particular product, which can markedly affect the level of the carcinogen nitrosamine (Warnakulasuriya, 2004). A wide range of smokeless tobacco products is used worldwide (Table 2). Many migrants to the West continue to use them even several decades after migration. Bangladeshis, in particular, are likely to retain the habit of betel use (Bedi, 1996; Croucher and Islam, 2002). Indian migrants to the UK have a significantly higher incidence of OSCC than native UK populations (Warnakulasuriya et al., 1999), presumably related to the use of smokeless tobacco.
Betel quid is probably used by 20% of the world’s population. In some areas (e.g., Pakistan), up to 70% of primary school children use it on a daily basis (Shah et al., 2002). The way that the quid of betel is prepared and used varies widely. It may contain tobacco, areca (betel) nut, and lime or other products. The quid may be left in the mouth for long periods, even overnight, in close contact with the oral mucosa. The habit can cause premalignant lesions ( Jacob et al., 2004), submucous fibrosis, and invasive squamous cell carcinoma (Seedat et al., 1988; Nandakumar et al., 1990; Sankaranarayanan et al., 1990; Van Wyk et al., 1993).
Snuff is finely powdered plant material, principally tobacco. It is used orally or nasally, and is a risk factor for OSCC (Axell et al., 1978; Winn et al., 1991; Hirsch, 2002). The risks are mainly in snuff users who also use tobacco (Accortt et al., 2005).
Increased consumption of any alcohol-containing beverages is associated with a risk of OSCC (WRCF, 1997; WHO, 2002; Ogden, 2005). The risk decreases after stopping alcohol use, but the effects appear to persist for several years (Franceschi et al., 2000). The risk is highest among the heaviest drinkers of alcohol (Barra et al., 1990; Petti and Scully, 2005). The type of alcoholic beverage appears to influence the risk: Hard liquors confer higher risks (Barra et al., 1990; Day et al., 1994; De Stefani et al., 1998; Gronbaek et al., 1998; La Vecchia et al., 1999; Huang et al., 2003; Lissowska et al., 2003). Ecological studies suggest that the impact of alcohol on OSCC mortality has increased in recent years (Hindle et al., 2000; Petti and Scully, 2005).
The use of mouthwash with a high alcohol content (25% or higher) increases the risk of OSCC by 40% in men and by 60% in women (Winn et al., 1991). However, it appears as if the effect of alcohol from mouthwash could be similar to that of alcohol used for drinking, although in terms of attributable risk, the contribution of mouthwash use to OSCC must be very small (Elmore and Horwitz, 1995; Morse et al., 1997).
The combined effect of alcohol and tobacco on the risk of OSCC is multiplicative, not simply additive (Blot et al., 1988; Franceschi et al., 1990; Rodriguez et al., 2004) (Tables 3 and 4).
There have been a number of case reports of oral cancer in marijuana smokers but any relationship has yet to be supported by full epidemiological studies (Firth et al., 1997; Fung et al., 1999). A review of two cohort studies and 14 case–control studies showed a possible association between marijuana use and cancer risk (Hashibe et al., 2005), but regular users of marijuana are often heavy cigarette smokers (Firth, 1997; Fung et al., 1999).
Charcoal-grilled red meat (Franco et al., 1989) and fried foods (Galeone et al., 2005) have been implicated as risk factors. Increased consumption of fruits and vegetables is associated with a lower risk of OSCC (Potter et al., 1997).
Socioeconomic status plays an important role, even if it is indirect. Most premalignant lesions (Hashibe et al., 2003) and most squamous cell carcinomas of the oral cavity occur in people of low socioeconomic status (Edwards and Jones, 1999; Greenwood et al., 2003; Bhurgri, 2005).
Raised risks of oral cancer have been found in a number of occupations (Table 5). Candida albicans and viruses such as herpesviruses and human papillomaviruses may be implicated in at least some cases (Gillison et al., 1999; Scully, 2005).
Lip cancer is seen mainly in males with chronic sun exposure and in smokers (Luna-Ortiz et al., 2004). Ionizing radiation exposure is a possible risk factor for second primary cancers of the oral cavity (Hashibe et al., 2005).
Persons with poor oral hygiene appear to have increased risk of OSCC, independent of any effect of tobacco, alcohol, or other proven risk factors, but not all workers agree, so further studies are required.
Potentially Malignant (Precancerous) Clinical Lesions
Some potentially malignant (precancerous) clinical lesions that can progress to OSCC include especially:
- Erythroplasia (erythroplakia): The most likely lesion to progress to severe dysplasia or carcinoma. Erythroplastic lesions are velvety red plaques, which in at least 85% of cases show frank malignancy or severe dysplasia. Carcinomas are seen 17 times more frequently in erythroplakia than in leukoplakia (but leukoplakias are far more common).
- Leukoplakia, particularly where admixed with red lesions, as in speckled leukoplakia, and proliferative verrucous leukoplakia, sublingual leukoplakia, candidal leukoplakia, syphilitic leukoplakia (now exceptionally rare).
- Lichen planus.
- Oral submucous fibrosis ( Jeng et al., 2001).
Apart from these lesions, most other potentially malignant lesions or conditions have only a very low incidence of dysplasia or malignant change (Table 6).
There is a highly significant increase in the incidence of OSCC of the tongue in systemic sclerosis (Derk et al., 2005) and an increase of OSCC in transplant recipients (Scheifele et al., 2005).
Prevention Of Oral Cancer
There is remarkably little good-quality evidence on the prevention of OSCC. However, OSCC shares several risk factors with other diseases, and is thus potentially amenable to prevention using the principles of the Common Risk Factor Approach (Sheiham and Watt, 2000). Health promotion campaigns centered on cessation of tobacco use in particular have been advocated and directed either at primary prevention or at preventing the malignant transformation of potentially malignant lesions and conditions. Most notably, Warnakulasuriya et al. (1991) used primary health-care workers in Sri Lanka not only to screen for oral cancer and precancer, but also to deliver tobacco cessation advice to high-risk subjects.
However, despite a reduction in tobacco product consumption in many developed countries, oral cancer incidence and mortality has not always fallen in these countries, leading some researchers to hypothesize that alcohol consumption (Hindle et al., 2000), genetic factors, and environmental factors such as infective agents (Scully et al., 2005) are increasing in relative importance.
Chemopreventive clinical trials aim to prevent the potentially malignant lesions or attempt to prevent malignant transformation or aim to cause regression of lesions in high-risk patient groups (Zaridze et al., 1993; Mathew et al., 1995).
Oral Cancer Awareness By The General Public And Health Professionals
Many studies have reported variable, and frequently suboptimal, levels of knowledge of oral cancer, risk factors, and diagnosis among both the public and health-care professionals. Although it is among the ten most common cancers worldwide, OSCC is rarely mentioned in the popular press, and public awareness is dismal (Canto et al., 1998). Significant numbers of the public are unaware of risk factors or even that OSCC exists, sometimes even after high-profile public education campaigns (Papas et al., 2004; Stahl et al., 2004). The reported trend among healthcare professionals is, unsurprisingly, that the knowledge and confidence of appropriate practice is related to education and experience, being greater in specialists than general dental practitioners, who in turn tend to be better informed than general medical practitioners and other health-care professionals (Reed et al., 2005; Sohn et al., 2005; Kujan et al., 2006).
From the perspective of improving the prognosis, there are two major stumbling blocks for a preventive approach. First, although many groups have attempted to educate both public and professionals about the signs and symptoms of OSCC, there is no robust evidence that these campaigns have produced a significant long-term change in the knowledge, attitudes, or behaviors of all the targeted groups or shortened delays in diagnosis (McLeod et al., 2005). Second, the probability of being diagnosed with advanced disease does not relate well to recorded delays, since variations in disease stage at presentation may also reflect underlying differences in the speed of progression of the lesion, and symptomatology does not always correlate with tumor stage (Scott et al., 2005).
Delays in diagnosis may occur as a result of patient delay in presentation or professional delay in referral to an appropriate specialist center, or both (Onizawa et al., 2003; Llewellyn et al., 2004).
Oral Cancer Screening Programs
Oral cancer fulfills many of the criteria proposed by Wilson and Junger (1968) for a disease to be suitable for screening (Speight et al., 1993), but there are many logistical hurdles and costs to be overcome in order to assess the feasibility of screening and to implement a program. As a consequence, most of the research has reported on process measures such as diagnostic test performance (Moles et al., 2002; Downer et al., 2004) or uptake or compliance with the screening (Speight et al., 2006). Where outcomes have been reported, they have mainly been proxy outcomes such as absolute survival. Survival is an unreliable outcome for this purpose because it is subject to the effects of both lead-time bias and length bias.
A Cochrane systematic review (Kujan et al., 2003) found only one cluster-randomized controlled clinical trial using population-based mortality as the primary outcome measure (Sankaranarayanan et al., 2005). This trial, based in Kerala, India, randomized nearly 200 000 people to 13 clusters to either receive periodic screening (seven clusters) in the form of a visual examination at 3-year intervals or no screening (six clusters). The results indicate no appreciable difference in OSCC mortality between the screened (21.2/100 000 person-years) and nonscreened groups (21.3/100 000 person-years).
In the absence of reliable data on effectiveness, it is difficult to justify the expense of setting up large-scale randomized controlled trials in either developed or developing countries. In an attempt to provide such data, Speight et al. (2006) undertook a computer simulation modeling exercise of the cost-effectiveness of oral cancer screening in primary care in the UK, based on data from primary research, systematic reviews, published health service costs, and – for model parameters where no robust data were available – expert opinion. The model indicated that opportunistic screening of high-risk individuals might be cost-effective in either general dental practice (because dentists performed relatively well in screening) or general medical practice (because of a greater throughput of at-risk patients). However, there was considerable uncertainty in some of the model parameters used.
Opportunities And Barriers To Progress
The randomized controlled trial in Kerala is still in progress. Since it is the only trial to examine the impact of population-based screening for OSCC with mortality as the primary outcome, the long-term results are eagerly awaited. The transferability of the results to other countries or health-care settings will be a source of debate.
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