- Email: [email protected]
Oral cavity and pharynx cancer incidence rates in the United States, 1975–1998☆
Oral Oncology 38 (2002) 610–617 www.elsevier.com/locate/oraloncology
Oral cavity and pharynx cancer incidence rates in the United States, 1975–1998§ Marı´a Teresa Cantoa,*, Susan S. Devesab a National Institute of Dental and Craniofacial Research, DER, 45 Center Drive, Building 45, Room 4AN24K, Bethesda, MD 20892-6401, USA Chief, Descriptive Studies Section, Biostatistics Branch, Epidemiology and Biostatistics Program, Division of Cancer Epidemiology and Genetics, National Cancer Institute Executive Plaza South, Room 8048, Bethesda, MD 20892, USA
b
Received 18 March 2001; accepted 1 June 2001
Abstract To identify subgroups of oral cavity and pharynx (OCP) cancers that may be etiologically distinct, we evaluated age-adjusted incidence rates by histologic type, anatomical site, race, and sex using cases diagnosed during 1975–1998 in nine US Surveillance, Epidemiology, and End Results (SEER) program registries. Male/female rate ratios were about one for adenocarcinoma (AC), three or more for squamous cell carcinoma (SCC), and undetermined for Kaposi’s sarcoma (KS). Among males, black/white rate ratios exceeded two for cancers of the palate, tonsil, oropharynx, and pyriform sinus, and were less than one only for lip and salivery gland cancers. Among females, rates by race were similar for all oral sites except lip, but rates for each of the pharynx subsites were higher among blacks. Findings suggest that OCP cancers may be separated into SCC of the lip, SCC of the oral cavity, SCC of the pharynx, AC, and KS. # 2002 Elsevier Science Ltd. All rights reserved. Keywords: Oral; Pharynx; Cancer; SEER; Incidence
1. Introduction Cancers of the oral cavity and pharynx (OCP) include tumors of the lip, tongue, gingival (gums), floor of the mouth, soft and hard palate, tonsils, salivary glands, oropharynx, nasopharynx, hypopharynx, and other less frequent sites [1]. In 2001, it was estimated that OCP cancers would account for 30,100 new cases and 7800 deaths in the United States [2]. The age-adjusted (world standard) incidence rate for total OCP cancers were 8.3 per 100,000 population in 1994–1998, but varies greatly (range=4.8 to 17.7 per 100,000) according to race and sex groups [3]. These cancers represent 3% of all cancers in the United States [1]. More than 95% of all OCP cancers occur in persons 40 years of age or older, and the median age at time of diagnosis is in the sixth decade [1]. The major risk factors for OCP cancers are the use of tobacco products §
Portions of this manuscript were presented at the meeting of the American Association of Public Health Dentistry in October 1999. * Corresponding author. Tel.: +1-301-594-5497; fax: +1-301-4808319. E-mail addresses: [email protected] (M.T. Canto), devesas@ exchange.nih.gov (S.S. Devesa).
and excessive alcohol consumption, estimated to account for 75% of all OCP in the United States [4]. Patterns and risks associated with tobacco and alcohol use have been shown to account for nearly all of the observed racial differences in rates for OCP cancers [5]. Other risk factors are exposure to certain viruses (humanpapilloma, Epstein–Barr) [6] and use of marijuana [7]. Nutritional factors, particularly the consumption of fresh fruits and vegetables, appear to be associated with decreased risk for these cancers [8,9]. Differences in rate patterns and risk factors for some subsites such as nasopharynx, lip, salivary glands, and other subsites also have been recognized [10,11]. Routine Surveillance, Epidemiology and End Results (SEER) program publications present recent rates by 10 subsites within the OCP, but the subsites are often grouped together in the SEER analyses presenting more detailed rates, such as by time, geographic area, stage at diagnosis, or years of survival. During 1975–1998, total oral cavity and pharynx cancer incidence rates have been higher among men than women, higher among blacks than whites, and fairly stable among females while declining among white males since the mid-1970s and rising among black males at least until the 1980s [3].
1368-8375/02/$ - see front matter # 2002 Elsevier Science Ltd. All rights reserved. PII: S1368-8375(01)00109-9
611
M.T. Canto, S.S. Devesa / Oral Oncology 38 (2002) 610–617
Furthermore, SEER publications do not present data according to histologic cell type. It is known that carcinomas account for the overwhelming majority of all oral cancers (up to 96%), followed next by sarcomas [1]. Thus, the purpose of this paper is to present and evaluate age-adjusted incidence rates for cancers of oral cavity and pharynx subsites by histologic type and to explore temporal trends for these cancers by race and sex. This is the first time this information has been presented for oral cavity and pharynx cancers. This information is valuable because it identifies where disparities related to oral cancer exist.
2. Methods Data for this analysis come from the US Surveillance, Epidemiology and End Results (SEER) program [3,12]. Nine registries (San Francisco–Oakland, Connecticut, Detroit, Hawaii, Iowa, New Mexico, Seattle, Utah, and Atlanta) for which data are available for cases diagnosed since 1975 were included in the analysis. Although these areas are not a random sample of the US population, they account for about 10% of the population. Population estimates were derived using data provided by the US Census Bureau. Age-adjusted (world standard) incidence rates for malignant cancers of the oral cavity and pharynx were calculated by sex, race, histologic type, specific oral cavity subsites, and expressed per 100,000 person-years. For the trend analysis, three time periods were used to obtain stable rates: 1975–1982, 1983–1990 and 1991–1998. In the early years, tumors were coded according to the Manual of Tumor Nomenclature and Coding (MOTNAC) [13]. Subsequently, the International Classification of Disease for Oncology, first and second edition (ICDO, ICDO-2) [14,15] were used; no changes in the categories occurred for oral cavity and pharynx cancers. All tumors of the oral cavity and pharynx were categorized according to the ICDO-2 codes for topography and morphology (Table 1) [15]. Data were reviewed and then collapsed into the categories presented in this analysis. Figures were prepared using a log scale and uniform y:x axis ratio to allow comparisons not only within but also between figures [16]. The percent change (PC) in rates was calculated from 1975–1982 to 1991–1998.
3. Results During the 1978–1998 period, a total of 65,130 in-situ and malignant cancers of the OCP were diagnosed, of which 98% were microscopically confirmed and approximately 5% were carcinoma in situ; to maximize the numbers available for analysis, all cases were included (Table 2). The majority of OCP cancers (83%) were
Table 1 ICDO-2 codes for topography and morphology used in the analysis ICDO-2 code Morphology Squamous cell carcinoma Adenocarcinoma Kaposi’s sarcoma Other (excluding lymphoma) Topography Lip Total tongue Base of the tongue Other specified tongue Tongue, multiple sites not further specified (MNS) Total gum Upper gum Lower gum Gum MNS Floor of the mouth Total palate Hard palate Soft palate Uvula Palate MNS Other mouth Cheek and vestibule Retromolar Other mouth Salivary glands MNS Parotid gland Other salivary glands MNS Tonsil Oropharynx Nasopharynx Pyriform sinus Hypopharynx Other oral cavity and pharynx MNS
8050–8082 8140–8573 9140 8000–8045, 8090–8130, 8680–9581
000–009 019–029 019 020–024 028–029 030–039 030 031 039 040–049 050–059 050 051 052 058–059 060–069 060–061 062 068–069 079–089 079 080–089 090–099 100–109 110–119 129 130–139 140–149
squamous cell carcinomas (SCC). Of those, 87% were SCC, 9% keratinizing SCC, approximately 2% nonkeratining SCC, 1% lymphoepithelial carcinoma, and less than 1% papillary carcinoma, papillary SCC, small cell nonkerarinizing, spindle cell type SCC, adenoid SCC, or microinvasive. Sixty-seven percent of SCC occurred in the oral cavity and 30% in the pharyngeal region and 3% had not site specified. The most common site for this histologic type in the oral cavity was the tongue and in the pharynx, the tonsils. Adenocarcinomas (AC) accounted for 9% of all OCP; they occurred mainly in the salivary glands, especially the parotid glands. Kaposi’s sarcoma (KS) accounted for 1.2%, and they occurred in the palate, mostly in the hard palate. Approximately 4% and 10% of AC and KS, respectively, were found in the pharynx. All OCP cancers occurred more frequently among males than females (Table 2). By type, the male/female rate ratios ranged from less than 1.02 for AC to 3–4 for SCC. By site, the male/female ratios for salivary gland
612
M.T. Canto, S.S. Devesa / Oral Oncology 38 (2002) 610–617
Table 2 Incidence cases and ratesa for oral cavity and pharynx cancer by sex, race, histologic type and anatomic site, 9-SEER, 1975–1998 Rate ratios White males
White females
Black males
Black females
(Males/females)
(Blacks/whites)
Count
Rate
Count
Rate
Count
Rate
Count
Rate
Whites
Blacks
Males
Females
Total
37,095
13.9
17,782
5.4
4640
20.0
1795
6.1
2.57
3.25
1.43
1.13
Histologic type Squamous cell carcinoma Adenocarcinoma Kaposi’s sarcoma Other and NS
31,811 2460 680 2824
12.0 0.9 0.3 1.0
13,824 2731 4 1227
4.2 0.9 0.0 0.4
4035 249 88 356
17.6 1.0 0.3 1.4
1355 297 6 143
4.7 1.0 0.0 0.5
2.88 1.02 N/A 2.97
3.72 1.08 N/A 2.96
1.47 1.11 1.08 1.34
1.14 1.04 N/A 1.34
Anatomic site Lip Tongue Gum Floor of the mouth Other mouth
7086 7092 1050 3984 2248
2.5 2.7 0.4 1.6 0.8
1155 3885 1049 1920 1680
0.3 1.2 0.3 0.6 0.5
27 950 105 613 258
0.1 4.1 0.4 2.6 1.1
21 347 69 185 139
0.1 1.2 0.2 0.6 0.5
8.86 2.25 1.41 2.55 1.75
1.95 3.44 1.77 4.18 2.44
0.04 1.52 1.16 1.70 1.32
0.20 0.99 0.85 1.00 0.91
Salivary glands
2747
1.0
2213
0.7
203
0.8
201
0.6
1.55
1.46
0.84
0.88
Palate Tonsil Oropharynx Nasopharynx Pyriform sinus Hypopharynx Other NS OCP
2169 3549 989 1352 2451 1169 1209
0.8 1.4 0.4 0.5 0.9 0.4 0.5
1421 1621 430 663 675 480 590
0.5 0.5 0.1 0.2 0.2 0.2 0.2
413 690 189 231 507 217 237
1.8 3.0 0.8 0.9 2.3 0.8 1.0
182 254 46 99 107 67 78
0.6 0.9 0.2 0.3 0.5 0.2 0.3
1.84 2.48 2.76 2.34 4.17 3.02 2.48
2.73 3.39 5.21 2.85 5.80 4.06 4.23
2.15 2.20 2.18 1.74 2.49 1.82 2.18
1.41 1.60 1.11 1.44 1.67 1.53 1.35
a
Per 100,000 person-years, age-adjusted using the world standard. N/A, not applicable. NS OCP, not specified oral cavity and pharynx.
cancers were less than two in both races, and for lip cancers about two among blacks and almost nine among whites. For the remaining subsites, the male/ female rate ratios generally were higher among blacks than whites, ranging to more than five for oropharynx and pyriform sinus cancers. Incidence rates were higher among blacks than whites for most types and sites, especially among males, as shown in Table 2. By type, among males, the rate was 47% higher among blacks than whites for squamous cell carcinoma, 11% higher for AC, and 8% higher for KS. By type, rates were similar among white and black females for SCC and AC. By site, among males, black/ white rate ratios exceeded two for cancers of the palate, tonsil and all pharyngeal subsites except the nasopharynx and hypopharynx. In contrast, male rates were notably higher among whites than blacks for cancer of the lip and very similar for gingival (gum) cancer. Among females, rates among whites and blacks were similar in the oral cavity except for cancers of the lip, gingival (gum) and salivary glands, in contrast to incidence rates for all subsites in the pharynx that were higher among blacks than whites. Total, OCP incidence rates declined from 1975–1982 to 1991–1998 among all four race/sex groups (Table 3; Fig. 1). SCC incidence rates also declined among all
four groups, although less rapidly among black males than whites. AC rates increased among all groups, except black females. Virtually unknown before 1980, OCP KS rates among males rose rapidly to 0.36 per 100,000 person-years in 1983–1990, and changed slightly to 0.34 in 1991–1998 among whites; among blacks KS rates rose rapidly from 0.23 to 0.47 per 100,000 person-years (Fig. 1), although rates among black males were based on only 25 and 63 cases, respectively. Among females, the number of Kaposi’s sarcomas was less than 10 per time period, and rates were negligible. Rates for OCP cancers not classified as one of the major histologic subtypes increased among black males, rose slightly for white males, and declined among females. Fig. 2 (A,B,C) show temporal trends for specific subsites in the oral cavity and pharynx. Lip cancer rates declined among males while changing little among white females. Rates generally decreased for cancers of the floor of the mouth and other mouth. In contrast, rates increased for tongue cancers among whites but not among blacks. For palate cancers, rates decreased among females and increased among males. Gingival (gum) cancer rates decreased for all groups, and some increases in salivary gland cancers were suggested. Rates for cancers of the tonsil increased among males and
M.T. Canto, S.S. Devesa / Oral Oncology 38 (2002) 610–617 Table 3 Percent change (1975–1982 to 1992–1998) for oral cavity and pharynx cancer by race, sex, histologic type and anatomic site, 9-SEERa White males Total
White females
Black males
Black females
14.0
9.8
6.4
18.2
17.6 11.4 3300 12.8
13.3 12.9 N/A 19.5
10.8 9.6 N/A 47.4
20.0 2.0 N/A 30.2
Anatomic site Lip Tongue Gum Floor of the mouth Other mouth
45.3 10.7 10.5 30 16.9
3.3 5.2 7.4 31.0 4.4
37.5 5.5 37.5 30.4 8.9
N/A 14.7 51.5 31.1 23.5
Salivary glands
14.0
5.9
39.7
10
Palate Tonsil Oropahrynx Nasopharynx Pyriform sinus Hypopharynx Other NS OCP
8 13.0 2.7 17.2 17.3 26.5 6.4
15.2 21.7 26.7 8.7 25 23.5 15.8
0 4.8 16.5 3.3 14.7 15 5.1
4.8 26.4 50 28.2 30 3.7 13.6
Histologic type SCC Adenocarcinoma KS Other and NS
a
N/A, not applicable. NS OCP, not specified oral cavity and pharynx.
declined among females. For cancers of the pharynx, rates generally declined among whites but they increased among black males for all sites except pyriform sinuses.
4. Discussion Based on these data it appears that there are several distinct forms of OCP cancers, based on histologic type and anatomic site patterns by race, sex, and over time. Data presented here suggest that OCP cancers may be separated into five subgroups: SCC of the lip, SCC of the oral cavity, SCC of the pharynx (including nasopharynx), adenocarcinoma (including salivary glands), and Kaposi’s sarcoma. The most frequent sites for OCP cancers continue to be tongue and floor of the mouth (SCC of the oral cavity), followed closely by cancer of the tonsils (SCC pharynx). For the 1975–1998 period, SCC rates declined while AC increased among all groups except black females (Percentage change= 2.02) and KS rates increased particularly among males. This analysis revealed variations according to histologic type, anatomic subsite, race, sex and temporal trends. Rates for SCC of the oral cavity were higher among black males than white males but were similar
613
among females. In general, palate, tonsil and pharynx cancer rates were higher among blacks than whites for both males and females, and could be grouped as SCC of the pharynx. Although males are affected two to three times as often as females in the USA, the incidence of tongue and other oral cavity cancers among women can be greater or equal to that of men in countries like India [17]. Black males had the highest incidence rates for OCP cancers and SCC. One exception was lip cancer, which was more frequent among whites. Lip cancer, which is associated with tobacco use and solar keratoses [10], continues to decline among males, although a slight increase was observed among white females (Fig. 2A). The decreases among males are in contrast to rising melanoma rates of another UV-radiation-related cancer [3]. Declines in cancers of the lip and other subsites of the oral cavity may be largely attributed to decreased use of cigarettes. In contrast, tongue cancer rates rose among white males and females from 1975–1982 to 1991–1998. An earlier report using SEER data for 1973–1992 found that the increases were mainly in the age group of 35–39 years [18]. Further, an increase in tongue cancer among young adults has been reported in studies from the UK and across Europe [19]. The lack of higher gingival (gum) cancer rates among blacks compared to whites may be related to less use of snuff or chewing tobacco by blacks compared to whites [20]. The smaller male/female ratio for gingival (gum) cancer compared to other sites of the mouth might relate to snuff use among women. A previous study clearly demonstrated an increased risk of OCP among older white women who used snuff [21]. Alcohol use also has declined, though not as dramatically as smoking. The alcohol relationship with oral cancer has been well established, although the specific mechanism for its carcinogenic effect is not known [22]. Interactive effects between smoking and alcohol are important, particularly among current smokers. Studies that have looked at type and amount of alcohol consumed and its relation to OCP did not look at alcohol and specific OCP subsites. Men consume more alcoholic beverages than women, and more blacks abstain from alcohol than whites [22,23]. Such differences are consistent with the higher risk for OCP in men than women but do not explain the racial disparities observed. Convincing evidence exists that diets high in fruits and vegetables decrease the risk for OCP [24]. Recent figures showed that only 34% of African Americans age 2 and older meet the Dietary Guidelines minimum average daily goal of at least five servings of vegetables and fruits in a day, in contrast to 41% of whites [25]. A diet that includes fresh fruit and vegetables rich in betacarotene, vitamin C, and vitamin E has been associated with a reduced risk of oral cavity and pharynx cancers
614
M.T. Canto, S.S. Devesa / Oral Oncology 38 (2002) 610–617
Fig. 1. 1975–1982 to 1991–1998 age-adjusted (world) incidence trends by type. Oral cavity and pharynx cancers in the nine SEER areas.
[26]. A previous study comparing diets of whites and blacks concluded that the diets were similar in fruit, vegetable and fat consumption [27]. It was suggested that blacks were more frequent consumers of preserved and processed meats that tend to be high in N-nitroso compounds. In addition, nutritional deficiencies of iron, riboflavin, and other vitamins have been implicated in PlummerVinson Syndrome, a condition seen particularly among Swedish women that predisposed them to some forms of pharyngeal cancer. Incidence of oral cancers in Sweden declined with the advent of iron and vitamin supplementation [26]. These deficiencies could contribute to higher pharyngeal cancer incidence rates observed among black females. Presently, detailed information on diet by sex and race are not available. Environmental exposures such as radiation and nitrosamines have been linked to OCP cancers [10,28– 30]. Adenocarcinomas occur predominantly in the salivary glands, and the incidence rates for salivary gland tumors increased since the 1980s, with rates higher in whites than blacks. Established risk factors for salivary gland cancers are exposure to radiation, a history of cancer and exposure to nitrosamines [28–30]. Individuals treated during childhood (1939–1962) with radiation to reduce the size of their tonsils and adenoids are
at higher risk of developing these tumors and should be monitored [31]. Also, rising rates of salivary gland tumors have been reported mainly in the elderly, particularly those age 70 and over [29]. Explanations suggested were the recent increased use of fine needle aspiration and higher utilization of health services by the elderly population [29]. Further analyses looking at age-specific patterns are needed using SEER and the combined SEER/Medicare databases. Other risk factors include exposure to viruses such as human papilloma virus (HPV) [32,33] and human immunodeficiency virus type 1 (HIV-1) [34]. HPV was detected in approximately 15% of squamous cell carcinomas of the head and neck [32,33]. Recently, it was shown that HPV has a predilection for certain anatomical sites, especially the tonsillar region [32]. The few OCP cancers occurring in individuals without a prior history of tobacco and alcohol use may be related to exposure to the virus [33–35]. Whether or not observed increases in cancer of the tonsils among white males and increases in tongue cancer among whites in the USA are related to HPV needs to be further explored. In the absence of HIV-1 infection, KS is rare [34]. Although the SEER program does not collect information on HIV seropositivity, the increase in Kaposi’s sarcoma began during the mid-1980s and continued into
M.T. Canto, S.S. Devesa / Oral Oncology 38 (2002) 610–617
615
Fig. 2. (a–c) 1975–1982 to 1991–1998 age-adjusted (world) incidence trends by site. Oral cavity and pharynx cancers in the nine SEER areas.
616
M.T. Canto, S.S. Devesa / Oral Oncology 38 (2002) 610–617
Fig. 2. (Continued).
1990s, a period of time coinciding with the HIV epidemic in the United States. Another virus related to OCP cancers is Epstein–Barr virus (EBV). EBV has been linked to nasopharynx cancers and a rare squamous cell carcinoma of the salivary glands among Inuit Canadians, Alaskans and Greenland Eskimos, but this association has not been found in other populations [29]. This analysis showed a slight increased in salivary glands among males (Fig. 2B). More information is needed in the role of viruses and the etiology of OCP cancers.
Acknowledgements The authors appreciate the sustained high quality registry operations of the SEER program participants, the dedication of the NCI SEER staff, the computer programming and figure development by John Lahey of IMS, Inc. and the comments on the manuscript by Dr. Gina Day Stephenson of the American Health Foundation, formerly of the National Cancer Institute.
References 5. Conclusions Because the patterns and etiologies differ, routine tabulations should report rates for the oral cavity separately from those for the pharynx. Furthermore, it would be useful for the present category of gum and other oral cavity to be broken down into gingiva, cheek and vestibule, other mouth, and palate. These suggestions would be helpful in the surveillance of trends, because although these cancers are related to behavioral and environmental exposures such as use of tobacco products, consumption of alcohol, and infection with certain viruses, the mechanisms may vary according to specific site and type.
[1] Silverman S. Oral cancer. Hamilton, London: BC Decker, 1998. [2] Greenlee RT, Hill-Harmon MB, Murray T, Thun N. Cancer statistics, 2001. CA Cancer J Clin 2001;55:15–36. [3] Ries LAG, Eisner MP, Kosary CL, Hankey BF, Miller BA, Clegg L, et al. SEER cancer statistics review, 1973–1998. Bethesda, MD: National Cancer Institute, 2001. [4] Blot WJ, McLaughlin JK, Winn DM, Austin DF, Greenberg RS, Preston-Martin S, et al. Smoking and drinking in relation to oral and pharyngeal cancer. Cancer Res 1988;48:3282–7. [5] Day GL, Blot WJ, Austin DF, Bernstein L, Greenberg RS, Preston-Martin S, et al. Racial differences in risk of oral and pharyngeal cancers: alcohol, tobacco and other determinants. JNCI 1993;86(6):465–73. [6] Blot WJ, McLaughlin JK, Devesa SS, Fraumeni JF, Jr. Cancers of the oral cavity and pharynx. In: Schottenfeld D, Fraumeni JFJ, editors. Cancer epidemiology and prevention. New York: Oxford University Press, 1996.
M.T. Canto, S.S. Devesa / Oral Oncology 38 (2002) 610–617 [7] Zhang Z, Morgestern H, Spitz MR, Tahkin DP, Yu GP, Marshall JR, et al. Marijuana use and increased risk of squamous cell carcinoma of the head and neck. Cancer Epidemiology, Biomarkers & Prevention 1999;8:1071–8. [8] Mouth and Pharynx. In: Food, nutrition and the prevention of cancer: a global perspective. Menasha, WI: BANTA Group, 1997. p. 96–106. [9] McLaughlin JK, Gridley G, Block G, Winn DM, Preston-Martin S, Schoenberg JB, et al. Dietary factors in oral and pharyngeal cancer. JNCI 1988;80:1237–43. [10] Devesa SS, Grauman DG, Blot WJ, Penello G, Hoover RN, Fraumeni JF, Jr. Atlas of cancer mortality in the United States, 1950–94 (NIH Publ No. (NIH)99-4564). Washington, DC: US Govt Print Off, 1999. [11] Yu MC, Henderson BE. Nasopharyngeal cancer. In: Schettenfeld D, Fraumeni JF, Jr, editors. Cancer epidemiology and prevention. New York: Oxford Press, 1996. [12] SEER Cancer incidence public-use database, 1973–1998. Bethesda: US Department of Health and Human Services, National Cancer Institute, 2001. [13] Percy CL, Berg JW, Thomas LB. Manual of tumor nomenclature and coding. American Cancer Society, 1968. [14] Percy C, Holten VV, Muir C. International classification of diseases for oncology (ICD-O). 2nd ed. Geneva: World Health Organization, 1976. [15] Percy C, Van Holen V, Muir C. International classification of diseases for oncology. Geneva: World Health Organization, 1990. [16] Devesa SS, Donaldson J, Fears T. Graphical presentation of trends in rates. Am J Epidemiol 1995;141:300–4. [17] Johnson N. Tobacco use and oral cancer: a global perspective. Journal of Dental Education 2001;65:328–39. [18] Swango PA. Cancer of the oral cavity and pharynx in the United States: an epidemiologic overview. J Public Health Dent 1996;56: 309–18. [19] Franceschi S, Bidoli E, Herrero R, Mun˜oz N. Comparison of cancers of the oral cavity and pharynx worldwide: etiological clues. Oral Oncology 2000;36:106–15. [20] Tobacco use among US racial/ethnic minority groups—African Americans, American Indians and Alaskan Natives, Asian Americans and Pacific Islanders, and Hispanics: a report of the Surgeon General. Atlanta, Georgia: US Department of Health and Human Services, Centers for Disease Control, 1998. [21] Winn DM, Blot WJ, Shy CM, Pickle LW, Toledo A, Fraumeni JF, Jr. Snuff dipping and oral cancer among women in the southern United States. N Engl J Med 1981;304:745–9.
617
[22] Wight AJ, Ogden GR. Possible mechanisms by which alcohol may influence the development of oral cancer—a review. Oral Oncol 1998;34:441–7. [23] National Household Survey on Drug Abuse: population estimates 1993. Rockville, MD: Department of Health and Human Services, Substance Abuse and Mental Health Administration, 1994. [24] Potter JD, Chavez A, Chen J, Ferro-Luzzi A, Hirohata T, James WPT, et al. Food, nutrition and the prevention of cancer: a global perspective. Washington DC: World Cancer Research Fund/American Institute of Cancer Research, 1997. [25] Healthy People 2000: National Health Promotion and Disease Prevention Objectives. US Department of Health and Human Services, Public Health Service, 1991. [26] Gridley G, McLaughlin JK, Block G, Blot WJ, Winn DM, Greenberg RS, et al. Diet and oral and pharyngeal cancer among blacks. Nutr Cancer 1990;14:219–25. [27] Swanson CA, Gridely G, Greenberg RS, Schoenberg JB, Swanson GM, Brown LM, et al. A comparison of diets of blacks and whites in three areas of the United States. Nutr Cancer 1993;20: 153–65. [28] Modan B, Biadtz D, Mart H, Steintz R, Levins RG, et al. Radiation induced head and neck tumors. Lancet 1974;1:277–9. [29] Zheng T, Holford TR, Chen Y, Ward B, Liu W, Flannery J, et al. Are cancers of the salivary gland increasing? Experience from Connecticut, USA. Int J Epidemiol 1997;26:264–71. [30] Horn-Ross PL, Ljung BM, Morrow M. Environmental factors and the risk of salivary gland cancer. Epidemiology 1997;8:414–9. [31] Schneider AB, Lubin J, Ron E, Abrahams C, Stovall M, Goel A, et al. Salivary gland tumors after childhood radiation treatment for benign conditions of the head and neck: dose-response relationships. Radiat Res 1998;149:625–30. [32] Wilczynski SP, Lin BT, Xie Y, Paz IB. Detection of human papillomavirus DNA and oncoprotein overexpression are associated with distinct morphological patterns of tonsillar squamous cell carcinoma. Am J Pathol 1998;152:145–56. [33] Gillison ML, Koch WM, Shah KV. Human papillomavirus in head and neck squamous cell carcinoma: are some head and neck cancers a sexually transmitted disease? Curr Opin Oncol 1999;11: 191–9. [34] Reitz MSJ, Nerurkar LS, Gallo RC. Perspective on Kaposi’s sarcomas: facts, concepts, and conjectures. Journal of the National Cancer Institute 1999;91:1453–8. [35] Fouret P, Monceaux G, Teman S, Lacourrege L, St Guily JL. Human papillomavirus in head and neck squamous cell carcinomas in nonsmokers. Arch Otolaryngol Head Neck Surg 1997;123: 513–6.
Oral cavity and pharynx cancer incidence rates in the United States, 1975–1998§ Marı´a Teresa Cantoa,*, Susan S. Devesab a National Institute of Dental and Craniofacial Research, DER, 45 Center Drive, Building 45, Room 4AN24K, Bethesda, MD 20892-6401, USA Chief, Descriptive Studies Section, Biostatistics Branch, Epidemiology and Biostatistics Program, Division of Cancer Epidemiology and Genetics, National Cancer Institute Executive Plaza South, Room 8048, Bethesda, MD 20892, USA
b
Received 18 March 2001; accepted 1 June 2001
Abstract To identify subgroups of oral cavity and pharynx (OCP) cancers that may be etiologically distinct, we evaluated age-adjusted incidence rates by histologic type, anatomical site, race, and sex using cases diagnosed during 1975–1998 in nine US Surveillance, Epidemiology, and End Results (SEER) program registries. Male/female rate ratios were about one for adenocarcinoma (AC), three or more for squamous cell carcinoma (SCC), and undetermined for Kaposi’s sarcoma (KS). Among males, black/white rate ratios exceeded two for cancers of the palate, tonsil, oropharynx, and pyriform sinus, and were less than one only for lip and salivery gland cancers. Among females, rates by race were similar for all oral sites except lip, but rates for each of the pharynx subsites were higher among blacks. Findings suggest that OCP cancers may be separated into SCC of the lip, SCC of the oral cavity, SCC of the pharynx, AC, and KS. # 2002 Elsevier Science Ltd. All rights reserved. Keywords: Oral; Pharynx; Cancer; SEER; Incidence
1. Introduction Cancers of the oral cavity and pharynx (OCP) include tumors of the lip, tongue, gingival (gums), floor of the mouth, soft and hard palate, tonsils, salivary glands, oropharynx, nasopharynx, hypopharynx, and other less frequent sites [1]. In 2001, it was estimated that OCP cancers would account for 30,100 new cases and 7800 deaths in the United States [2]. The age-adjusted (world standard) incidence rate for total OCP cancers were 8.3 per 100,000 population in 1994–1998, but varies greatly (range=4.8 to 17.7 per 100,000) according to race and sex groups [3]. These cancers represent 3% of all cancers in the United States [1]. More than 95% of all OCP cancers occur in persons 40 years of age or older, and the median age at time of diagnosis is in the sixth decade [1]. The major risk factors for OCP cancers are the use of tobacco products §
Portions of this manuscript were presented at the meeting of the American Association of Public Health Dentistry in October 1999. * Corresponding author. Tel.: +1-301-594-5497; fax: +1-301-4808319. E-mail addresses: [email protected] (M.T. Canto), devesas@ exchange.nih.gov (S.S. Devesa).
and excessive alcohol consumption, estimated to account for 75% of all OCP in the United States [4]. Patterns and risks associated with tobacco and alcohol use have been shown to account for nearly all of the observed racial differences in rates for OCP cancers [5]. Other risk factors are exposure to certain viruses (humanpapilloma, Epstein–Barr) [6] and use of marijuana [7]. Nutritional factors, particularly the consumption of fresh fruits and vegetables, appear to be associated with decreased risk for these cancers [8,9]. Differences in rate patterns and risk factors for some subsites such as nasopharynx, lip, salivary glands, and other subsites also have been recognized [10,11]. Routine Surveillance, Epidemiology and End Results (SEER) program publications present recent rates by 10 subsites within the OCP, but the subsites are often grouped together in the SEER analyses presenting more detailed rates, such as by time, geographic area, stage at diagnosis, or years of survival. During 1975–1998, total oral cavity and pharynx cancer incidence rates have been higher among men than women, higher among blacks than whites, and fairly stable among females while declining among white males since the mid-1970s and rising among black males at least until the 1980s [3].
1368-8375/02/$ - see front matter # 2002 Elsevier Science Ltd. All rights reserved. PII: S1368-8375(01)00109-9
611
M.T. Canto, S.S. Devesa / Oral Oncology 38 (2002) 610–617
Furthermore, SEER publications do not present data according to histologic cell type. It is known that carcinomas account for the overwhelming majority of all oral cancers (up to 96%), followed next by sarcomas [1]. Thus, the purpose of this paper is to present and evaluate age-adjusted incidence rates for cancers of oral cavity and pharynx subsites by histologic type and to explore temporal trends for these cancers by race and sex. This is the first time this information has been presented for oral cavity and pharynx cancers. This information is valuable because it identifies where disparities related to oral cancer exist.
2. Methods Data for this analysis come from the US Surveillance, Epidemiology and End Results (SEER) program [3,12]. Nine registries (San Francisco–Oakland, Connecticut, Detroit, Hawaii, Iowa, New Mexico, Seattle, Utah, and Atlanta) for which data are available for cases diagnosed since 1975 were included in the analysis. Although these areas are not a random sample of the US population, they account for about 10% of the population. Population estimates were derived using data provided by the US Census Bureau. Age-adjusted (world standard) incidence rates for malignant cancers of the oral cavity and pharynx were calculated by sex, race, histologic type, specific oral cavity subsites, and expressed per 100,000 person-years. For the trend analysis, three time periods were used to obtain stable rates: 1975–1982, 1983–1990 and 1991–1998. In the early years, tumors were coded according to the Manual of Tumor Nomenclature and Coding (MOTNAC) [13]. Subsequently, the International Classification of Disease for Oncology, first and second edition (ICDO, ICDO-2) [14,15] were used; no changes in the categories occurred for oral cavity and pharynx cancers. All tumors of the oral cavity and pharynx were categorized according to the ICDO-2 codes for topography and morphology (Table 1) [15]. Data were reviewed and then collapsed into the categories presented in this analysis. Figures were prepared using a log scale and uniform y:x axis ratio to allow comparisons not only within but also between figures [16]. The percent change (PC) in rates was calculated from 1975–1982 to 1991–1998.
3. Results During the 1978–1998 period, a total of 65,130 in-situ and malignant cancers of the OCP were diagnosed, of which 98% were microscopically confirmed and approximately 5% were carcinoma in situ; to maximize the numbers available for analysis, all cases were included (Table 2). The majority of OCP cancers (83%) were
Table 1 ICDO-2 codes for topography and morphology used in the analysis ICDO-2 code Morphology Squamous cell carcinoma Adenocarcinoma Kaposi’s sarcoma Other (excluding lymphoma) Topography Lip Total tongue Base of the tongue Other specified tongue Tongue, multiple sites not further specified (MNS) Total gum Upper gum Lower gum Gum MNS Floor of the mouth Total palate Hard palate Soft palate Uvula Palate MNS Other mouth Cheek and vestibule Retromolar Other mouth Salivary glands MNS Parotid gland Other salivary glands MNS Tonsil Oropharynx Nasopharynx Pyriform sinus Hypopharynx Other oral cavity and pharynx MNS
8050–8082 8140–8573 9140 8000–8045, 8090–8130, 8680–9581
000–009 019–029 019 020–024 028–029 030–039 030 031 039 040–049 050–059 050 051 052 058–059 060–069 060–061 062 068–069 079–089 079 080–089 090–099 100–109 110–119 129 130–139 140–149
squamous cell carcinomas (SCC). Of those, 87% were SCC, 9% keratinizing SCC, approximately 2% nonkeratining SCC, 1% lymphoepithelial carcinoma, and less than 1% papillary carcinoma, papillary SCC, small cell nonkerarinizing, spindle cell type SCC, adenoid SCC, or microinvasive. Sixty-seven percent of SCC occurred in the oral cavity and 30% in the pharyngeal region and 3% had not site specified. The most common site for this histologic type in the oral cavity was the tongue and in the pharynx, the tonsils. Adenocarcinomas (AC) accounted for 9% of all OCP; they occurred mainly in the salivary glands, especially the parotid glands. Kaposi’s sarcoma (KS) accounted for 1.2%, and they occurred in the palate, mostly in the hard palate. Approximately 4% and 10% of AC and KS, respectively, were found in the pharynx. All OCP cancers occurred more frequently among males than females (Table 2). By type, the male/female rate ratios ranged from less than 1.02 for AC to 3–4 for SCC. By site, the male/female ratios for salivary gland
612
M.T. Canto, S.S. Devesa / Oral Oncology 38 (2002) 610–617
Table 2 Incidence cases and ratesa for oral cavity and pharynx cancer by sex, race, histologic type and anatomic site, 9-SEER, 1975–1998 Rate ratios White males
White females
Black males
Black females
(Males/females)
(Blacks/whites)
Count
Rate
Count
Rate
Count
Rate
Count
Rate
Whites
Blacks
Males
Females
Total
37,095
13.9
17,782
5.4
4640
20.0
1795
6.1
2.57
3.25
1.43
1.13
Histologic type Squamous cell carcinoma Adenocarcinoma Kaposi’s sarcoma Other and NS
31,811 2460 680 2824
12.0 0.9 0.3 1.0
13,824 2731 4 1227
4.2 0.9 0.0 0.4
4035 249 88 356
17.6 1.0 0.3 1.4
1355 297 6 143
4.7 1.0 0.0 0.5
2.88 1.02 N/A 2.97
3.72 1.08 N/A 2.96
1.47 1.11 1.08 1.34
1.14 1.04 N/A 1.34
Anatomic site Lip Tongue Gum Floor of the mouth Other mouth
7086 7092 1050 3984 2248
2.5 2.7 0.4 1.6 0.8
1155 3885 1049 1920 1680
0.3 1.2 0.3 0.6 0.5
27 950 105 613 258
0.1 4.1 0.4 2.6 1.1
21 347 69 185 139
0.1 1.2 0.2 0.6 0.5
8.86 2.25 1.41 2.55 1.75
1.95 3.44 1.77 4.18 2.44
0.04 1.52 1.16 1.70 1.32
0.20 0.99 0.85 1.00 0.91
Salivary glands
2747
1.0
2213
0.7
203
0.8
201
0.6
1.55
1.46
0.84
0.88
Palate Tonsil Oropharynx Nasopharynx Pyriform sinus Hypopharynx Other NS OCP
2169 3549 989 1352 2451 1169 1209
0.8 1.4 0.4 0.5 0.9 0.4 0.5
1421 1621 430 663 675 480 590
0.5 0.5 0.1 0.2 0.2 0.2 0.2
413 690 189 231 507 217 237
1.8 3.0 0.8 0.9 2.3 0.8 1.0
182 254 46 99 107 67 78
0.6 0.9 0.2 0.3 0.5 0.2 0.3
1.84 2.48 2.76 2.34 4.17 3.02 2.48
2.73 3.39 5.21 2.85 5.80 4.06 4.23
2.15 2.20 2.18 1.74 2.49 1.82 2.18
1.41 1.60 1.11 1.44 1.67 1.53 1.35
a
Per 100,000 person-years, age-adjusted using the world standard. N/A, not applicable. NS OCP, not specified oral cavity and pharynx.
cancers were less than two in both races, and for lip cancers about two among blacks and almost nine among whites. For the remaining subsites, the male/ female rate ratios generally were higher among blacks than whites, ranging to more than five for oropharynx and pyriform sinus cancers. Incidence rates were higher among blacks than whites for most types and sites, especially among males, as shown in Table 2. By type, among males, the rate was 47% higher among blacks than whites for squamous cell carcinoma, 11% higher for AC, and 8% higher for KS. By type, rates were similar among white and black females for SCC and AC. By site, among males, black/ white rate ratios exceeded two for cancers of the palate, tonsil and all pharyngeal subsites except the nasopharynx and hypopharynx. In contrast, male rates were notably higher among whites than blacks for cancer of the lip and very similar for gingival (gum) cancer. Among females, rates among whites and blacks were similar in the oral cavity except for cancers of the lip, gingival (gum) and salivary glands, in contrast to incidence rates for all subsites in the pharynx that were higher among blacks than whites. Total, OCP incidence rates declined from 1975–1982 to 1991–1998 among all four race/sex groups (Table 3; Fig. 1). SCC incidence rates also declined among all
four groups, although less rapidly among black males than whites. AC rates increased among all groups, except black females. Virtually unknown before 1980, OCP KS rates among males rose rapidly to 0.36 per 100,000 person-years in 1983–1990, and changed slightly to 0.34 in 1991–1998 among whites; among blacks KS rates rose rapidly from 0.23 to 0.47 per 100,000 person-years (Fig. 1), although rates among black males were based on only 25 and 63 cases, respectively. Among females, the number of Kaposi’s sarcomas was less than 10 per time period, and rates were negligible. Rates for OCP cancers not classified as one of the major histologic subtypes increased among black males, rose slightly for white males, and declined among females. Fig. 2 (A,B,C) show temporal trends for specific subsites in the oral cavity and pharynx. Lip cancer rates declined among males while changing little among white females. Rates generally decreased for cancers of the floor of the mouth and other mouth. In contrast, rates increased for tongue cancers among whites but not among blacks. For palate cancers, rates decreased among females and increased among males. Gingival (gum) cancer rates decreased for all groups, and some increases in salivary gland cancers were suggested. Rates for cancers of the tonsil increased among males and
M.T. Canto, S.S. Devesa / Oral Oncology 38 (2002) 610–617 Table 3 Percent change (1975–1982 to 1992–1998) for oral cavity and pharynx cancer by race, sex, histologic type and anatomic site, 9-SEERa White males Total
White females
Black males
Black females
14.0
9.8
6.4
18.2
17.6 11.4 3300 12.8
13.3 12.9 N/A 19.5
10.8 9.6 N/A 47.4
20.0 2.0 N/A 30.2
Anatomic site Lip Tongue Gum Floor of the mouth Other mouth
45.3 10.7 10.5 30 16.9
3.3 5.2 7.4 31.0 4.4
37.5 5.5 37.5 30.4 8.9
N/A 14.7 51.5 31.1 23.5
Salivary glands
14.0
5.9
39.7
10
Palate Tonsil Oropahrynx Nasopharynx Pyriform sinus Hypopharynx Other NS OCP
8 13.0 2.7 17.2 17.3 26.5 6.4
15.2 21.7 26.7 8.7 25 23.5 15.8
0 4.8 16.5 3.3 14.7 15 5.1
4.8 26.4 50 28.2 30 3.7 13.6
Histologic type SCC Adenocarcinoma KS Other and NS
a
N/A, not applicable. NS OCP, not specified oral cavity and pharynx.
declined among females. For cancers of the pharynx, rates generally declined among whites but they increased among black males for all sites except pyriform sinuses.
4. Discussion Based on these data it appears that there are several distinct forms of OCP cancers, based on histologic type and anatomic site patterns by race, sex, and over time. Data presented here suggest that OCP cancers may be separated into five subgroups: SCC of the lip, SCC of the oral cavity, SCC of the pharynx (including nasopharynx), adenocarcinoma (including salivary glands), and Kaposi’s sarcoma. The most frequent sites for OCP cancers continue to be tongue and floor of the mouth (SCC of the oral cavity), followed closely by cancer of the tonsils (SCC pharynx). For the 1975–1998 period, SCC rates declined while AC increased among all groups except black females (Percentage change= 2.02) and KS rates increased particularly among males. This analysis revealed variations according to histologic type, anatomic subsite, race, sex and temporal trends. Rates for SCC of the oral cavity were higher among black males than white males but were similar
613
among females. In general, palate, tonsil and pharynx cancer rates were higher among blacks than whites for both males and females, and could be grouped as SCC of the pharynx. Although males are affected two to three times as often as females in the USA, the incidence of tongue and other oral cavity cancers among women can be greater or equal to that of men in countries like India [17]. Black males had the highest incidence rates for OCP cancers and SCC. One exception was lip cancer, which was more frequent among whites. Lip cancer, which is associated with tobacco use and solar keratoses [10], continues to decline among males, although a slight increase was observed among white females (Fig. 2A). The decreases among males are in contrast to rising melanoma rates of another UV-radiation-related cancer [3]. Declines in cancers of the lip and other subsites of the oral cavity may be largely attributed to decreased use of cigarettes. In contrast, tongue cancer rates rose among white males and females from 1975–1982 to 1991–1998. An earlier report using SEER data for 1973–1992 found that the increases were mainly in the age group of 35–39 years [18]. Further, an increase in tongue cancer among young adults has been reported in studies from the UK and across Europe [19]. The lack of higher gingival (gum) cancer rates among blacks compared to whites may be related to less use of snuff or chewing tobacco by blacks compared to whites [20]. The smaller male/female ratio for gingival (gum) cancer compared to other sites of the mouth might relate to snuff use among women. A previous study clearly demonstrated an increased risk of OCP among older white women who used snuff [21]. Alcohol use also has declined, though not as dramatically as smoking. The alcohol relationship with oral cancer has been well established, although the specific mechanism for its carcinogenic effect is not known [22]. Interactive effects between smoking and alcohol are important, particularly among current smokers. Studies that have looked at type and amount of alcohol consumed and its relation to OCP did not look at alcohol and specific OCP subsites. Men consume more alcoholic beverages than women, and more blacks abstain from alcohol than whites [22,23]. Such differences are consistent with the higher risk for OCP in men than women but do not explain the racial disparities observed. Convincing evidence exists that diets high in fruits and vegetables decrease the risk for OCP [24]. Recent figures showed that only 34% of African Americans age 2 and older meet the Dietary Guidelines minimum average daily goal of at least five servings of vegetables and fruits in a day, in contrast to 41% of whites [25]. A diet that includes fresh fruit and vegetables rich in betacarotene, vitamin C, and vitamin E has been associated with a reduced risk of oral cavity and pharynx cancers
614
M.T. Canto, S.S. Devesa / Oral Oncology 38 (2002) 610–617
Fig. 1. 1975–1982 to 1991–1998 age-adjusted (world) incidence trends by type. Oral cavity and pharynx cancers in the nine SEER areas.
[26]. A previous study comparing diets of whites and blacks concluded that the diets were similar in fruit, vegetable and fat consumption [27]. It was suggested that blacks were more frequent consumers of preserved and processed meats that tend to be high in N-nitroso compounds. In addition, nutritional deficiencies of iron, riboflavin, and other vitamins have been implicated in PlummerVinson Syndrome, a condition seen particularly among Swedish women that predisposed them to some forms of pharyngeal cancer. Incidence of oral cancers in Sweden declined with the advent of iron and vitamin supplementation [26]. These deficiencies could contribute to higher pharyngeal cancer incidence rates observed among black females. Presently, detailed information on diet by sex and race are not available. Environmental exposures such as radiation and nitrosamines have been linked to OCP cancers [10,28– 30]. Adenocarcinomas occur predominantly in the salivary glands, and the incidence rates for salivary gland tumors increased since the 1980s, with rates higher in whites than blacks. Established risk factors for salivary gland cancers are exposure to radiation, a history of cancer and exposure to nitrosamines [28–30]. Individuals treated during childhood (1939–1962) with radiation to reduce the size of their tonsils and adenoids are
at higher risk of developing these tumors and should be monitored [31]. Also, rising rates of salivary gland tumors have been reported mainly in the elderly, particularly those age 70 and over [29]. Explanations suggested were the recent increased use of fine needle aspiration and higher utilization of health services by the elderly population [29]. Further analyses looking at age-specific patterns are needed using SEER and the combined SEER/Medicare databases. Other risk factors include exposure to viruses such as human papilloma virus (HPV) [32,33] and human immunodeficiency virus type 1 (HIV-1) [34]. HPV was detected in approximately 15% of squamous cell carcinomas of the head and neck [32,33]. Recently, it was shown that HPV has a predilection for certain anatomical sites, especially the tonsillar region [32]. The few OCP cancers occurring in individuals without a prior history of tobacco and alcohol use may be related to exposure to the virus [33–35]. Whether or not observed increases in cancer of the tonsils among white males and increases in tongue cancer among whites in the USA are related to HPV needs to be further explored. In the absence of HIV-1 infection, KS is rare [34]. Although the SEER program does not collect information on HIV seropositivity, the increase in Kaposi’s sarcoma began during the mid-1980s and continued into
M.T. Canto, S.S. Devesa / Oral Oncology 38 (2002) 610–617
615
Fig. 2. (a–c) 1975–1982 to 1991–1998 age-adjusted (world) incidence trends by site. Oral cavity and pharynx cancers in the nine SEER areas.
616
M.T. Canto, S.S. Devesa / Oral Oncology 38 (2002) 610–617
Fig. 2. (Continued).
1990s, a period of time coinciding with the HIV epidemic in the United States. Another virus related to OCP cancers is Epstein–Barr virus (EBV). EBV has been linked to nasopharynx cancers and a rare squamous cell carcinoma of the salivary glands among Inuit Canadians, Alaskans and Greenland Eskimos, but this association has not been found in other populations [29]. This analysis showed a slight increased in salivary glands among males (Fig. 2B). More information is needed in the role of viruses and the etiology of OCP cancers.
Acknowledgements The authors appreciate the sustained high quality registry operations of the SEER program participants, the dedication of the NCI SEER staff, the computer programming and figure development by John Lahey of IMS, Inc. and the comments on the manuscript by Dr. Gina Day Stephenson of the American Health Foundation, formerly of the National Cancer Institute.
References 5. Conclusions Because the patterns and etiologies differ, routine tabulations should report rates for the oral cavity separately from those for the pharynx. Furthermore, it would be useful for the present category of gum and other oral cavity to be broken down into gingiva, cheek and vestibule, other mouth, and palate. These suggestions would be helpful in the surveillance of trends, because although these cancers are related to behavioral and environmental exposures such as use of tobacco products, consumption of alcohol, and infection with certain viruses, the mechanisms may vary according to specific site and type.
[1] Silverman S. Oral cancer. Hamilton, London: BC Decker, 1998. [2] Greenlee RT, Hill-Harmon MB, Murray T, Thun N. Cancer statistics, 2001. CA Cancer J Clin 2001;55:15–36. [3] Ries LAG, Eisner MP, Kosary CL, Hankey BF, Miller BA, Clegg L, et al. SEER cancer statistics review, 1973–1998. Bethesda, MD: National Cancer Institute, 2001. [4] Blot WJ, McLaughlin JK, Winn DM, Austin DF, Greenberg RS, Preston-Martin S, et al. Smoking and drinking in relation to oral and pharyngeal cancer. Cancer Res 1988;48:3282–7. [5] Day GL, Blot WJ, Austin DF, Bernstein L, Greenberg RS, Preston-Martin S, et al. Racial differences in risk of oral and pharyngeal cancers: alcohol, tobacco and other determinants. JNCI 1993;86(6):465–73. [6] Blot WJ, McLaughlin JK, Devesa SS, Fraumeni JF, Jr. Cancers of the oral cavity and pharynx. In: Schottenfeld D, Fraumeni JFJ, editors. Cancer epidemiology and prevention. New York: Oxford University Press, 1996.
M.T. Canto, S.S. Devesa / Oral Oncology 38 (2002) 610–617 [7] Zhang Z, Morgestern H, Spitz MR, Tahkin DP, Yu GP, Marshall JR, et al. Marijuana use and increased risk of squamous cell carcinoma of the head and neck. Cancer Epidemiology, Biomarkers & Prevention 1999;8:1071–8. [8] Mouth and Pharynx. In: Food, nutrition and the prevention of cancer: a global perspective. Menasha, WI: BANTA Group, 1997. p. 96–106. [9] McLaughlin JK, Gridley G, Block G, Winn DM, Preston-Martin S, Schoenberg JB, et al. Dietary factors in oral and pharyngeal cancer. JNCI 1988;80:1237–43. [10] Devesa SS, Grauman DG, Blot WJ, Penello G, Hoover RN, Fraumeni JF, Jr. Atlas of cancer mortality in the United States, 1950–94 (NIH Publ No. (NIH)99-4564). Washington, DC: US Govt Print Off, 1999. [11] Yu MC, Henderson BE. Nasopharyngeal cancer. In: Schettenfeld D, Fraumeni JF, Jr, editors. Cancer epidemiology and prevention. New York: Oxford Press, 1996. [12] SEER Cancer incidence public-use database, 1973–1998. Bethesda: US Department of Health and Human Services, National Cancer Institute, 2001. [13] Percy CL, Berg JW, Thomas LB. Manual of tumor nomenclature and coding. American Cancer Society, 1968. [14] Percy C, Holten VV, Muir C. International classification of diseases for oncology (ICD-O). 2nd ed. Geneva: World Health Organization, 1976. [15] Percy C, Van Holen V, Muir C. International classification of diseases for oncology. Geneva: World Health Organization, 1990. [16] Devesa SS, Donaldson J, Fears T. Graphical presentation of trends in rates. Am J Epidemiol 1995;141:300–4. [17] Johnson N. Tobacco use and oral cancer: a global perspective. Journal of Dental Education 2001;65:328–39. [18] Swango PA. Cancer of the oral cavity and pharynx in the United States: an epidemiologic overview. J Public Health Dent 1996;56: 309–18. [19] Franceschi S, Bidoli E, Herrero R, Mun˜oz N. Comparison of cancers of the oral cavity and pharynx worldwide: etiological clues. Oral Oncology 2000;36:106–15. [20] Tobacco use among US racial/ethnic minority groups—African Americans, American Indians and Alaskan Natives, Asian Americans and Pacific Islanders, and Hispanics: a report of the Surgeon General. Atlanta, Georgia: US Department of Health and Human Services, Centers for Disease Control, 1998. [21] Winn DM, Blot WJ, Shy CM, Pickle LW, Toledo A, Fraumeni JF, Jr. Snuff dipping and oral cancer among women in the southern United States. N Engl J Med 1981;304:745–9.
617
[22] Wight AJ, Ogden GR. Possible mechanisms by which alcohol may influence the development of oral cancer—a review. Oral Oncol 1998;34:441–7. [23] National Household Survey on Drug Abuse: population estimates 1993. Rockville, MD: Department of Health and Human Services, Substance Abuse and Mental Health Administration, 1994. [24] Potter JD, Chavez A, Chen J, Ferro-Luzzi A, Hirohata T, James WPT, et al. Food, nutrition and the prevention of cancer: a global perspective. Washington DC: World Cancer Research Fund/American Institute of Cancer Research, 1997. [25] Healthy People 2000: National Health Promotion and Disease Prevention Objectives. US Department of Health and Human Services, Public Health Service, 1991. [26] Gridley G, McLaughlin JK, Block G, Blot WJ, Winn DM, Greenberg RS, et al. Diet and oral and pharyngeal cancer among blacks. Nutr Cancer 1990;14:219–25. [27] Swanson CA, Gridely G, Greenberg RS, Schoenberg JB, Swanson GM, Brown LM, et al. A comparison of diets of blacks and whites in three areas of the United States. Nutr Cancer 1993;20: 153–65. [28] Modan B, Biadtz D, Mart H, Steintz R, Levins RG, et al. Radiation induced head and neck tumors. Lancet 1974;1:277–9. [29] Zheng T, Holford TR, Chen Y, Ward B, Liu W, Flannery J, et al. Are cancers of the salivary gland increasing? Experience from Connecticut, USA. Int J Epidemiol 1997;26:264–71. [30] Horn-Ross PL, Ljung BM, Morrow M. Environmental factors and the risk of salivary gland cancer. Epidemiology 1997;8:414–9. [31] Schneider AB, Lubin J, Ron E, Abrahams C, Stovall M, Goel A, et al. Salivary gland tumors after childhood radiation treatment for benign conditions of the head and neck: dose-response relationships. Radiat Res 1998;149:625–30. [32] Wilczynski SP, Lin BT, Xie Y, Paz IB. Detection of human papillomavirus DNA and oncoprotein overexpression are associated with distinct morphological patterns of tonsillar squamous cell carcinoma. Am J Pathol 1998;152:145–56. [33] Gillison ML, Koch WM, Shah KV. Human papillomavirus in head and neck squamous cell carcinoma: are some head and neck cancers a sexually transmitted disease? Curr Opin Oncol 1999;11: 191–9. [34] Reitz MSJ, Nerurkar LS, Gallo RC. Perspective on Kaposi’s sarcomas: facts, concepts, and conjectures. Journal of the National Cancer Institute 1999;91:1453–8. [35] Fouret P, Monceaux G, Teman S, Lacourrege L, St Guily JL. Human papillomavirus in head and neck squamous cell carcinomas in nonsmokers. Arch Otolaryngol Head Neck Surg 1997;123: 513–6.