Oral Oncology 50 (2014) 387–403
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Oral Oncology journal homepage: www.elsevier.com/locate/oraloncology
International trends in head and neck cancer incidence rates: Differences by country, sex and anatomic site Edgar P. Simard ⇑, Lindsey A. Torre, Ahmedin Jemal Surveillance and Health Services Research Program, American Cancer Society, Atlanta, GA, USA
a r t i c l e
i n f o
Article history: Received 31 October 2013 Received in revised form 16 January 2014 Accepted 26 January 2014 Available online 13 February 2014 Keywords: Epidemiology Global Head and neck cancer Human papillomavirus Incidence Larynx Mouth Oropharynx Oral cavity Trends
s u m m a r y Objective: To describe trends in country and sex-specific incidence rates of head and neck cancer (HNC), focusing on changes across calendar periods. Materials and MethodsMaterials and Methods: Sex and country specific rates of HNC were calculated for 1998–2002 and 1983–1987 using population-based registry data assembled by the Cancer Incidence in Five Continents (CI5) data system for 83 registries representing 35 countries. HNCs were categorized into three groups: oral cavity (including tongue and mouth), oropharynx (including tonsil and oropharynx) and other HNC (including larynx and poorly-specified tumors of the lip/oral cavity/pharynx). Age-standardized rates per 100,000 persons were calculated using the 1960 world standard population. Changes in rates between 1998–2002 and 1993–1987 were assessed. Results: During these periods there was substantial global variation in HNC incidence trends by cancer site, country/registry and sex. Rates of oral cavity cancer increased among men and women in some European and Asian countries (Czech Republic, Slovak Republic, Denmark, Estonia, Finland, the United Kingdom and Japan). In France and Italy, rates declined among men but increased among women. Oral cavity incidence rates declined among men and women in many Asian registries as well as in Canada and the United States. Oropharyngeal cancer rates increased among both men and women in a number of European countries (Belarus, Czech Republic, Denmark, Finland, Iceland, Latvia, Norway and the United Kingdom) whereas they declined in some Asian countries. The largest increase in oropharyngeal rates was among Brazilian men. Rates of other HNCs varied substantially by country and sex. Conclusion: From 1983–1987 to 1998–2002, trends in HNC rates differed by subtype, country and sex. Oral cavity cancer incidence rates increased in many countries with tobacco epidemics that are currently peaking and declined in areas where tobacco use peaked some time ago. In contrast, rates of oropharyngeal cancer increased in a number of countries where tobacco use has declined, perhaps due to the emerging importance of human papillomavirus infection. Continued monitoring of trends in incidence rates is needed to inform global cancer prevention strategies. Ó 2014 Elsevier Ltd. All rights reserved.
Introduction Cancers of the head and neck comprise a heterogeneous grouping of tumors at various anatomic sites with different etiologic factors. Tobacco exposure (either via active or passive smoking as well as consumption of smokeless tobacco) is the most important risk factor for head and neck cancers (HNCs) [1]. The fraction of HNC cases due to tobacco exposure likely varies across the globe. One recent pooled analysis of data from North America, Latin America and Europe found that tobacco exposure accounted for approximately 33% of HNC cases [2]. Alcohol exposure is also important ⇑ Corresponding author. Address: American Cancer Society, 250 Williams Street NW, Atlanta, GA 30303, USA. Tel.: +1 404 417 5935; fax: +1 404 321 4669. E-mail address: [email protected] (E.P. Simard). http://dx.doi.org/10.1016/j.oraloncology.2014.01.016 1368-8375/Ó 2014 Elsevier Ltd. All rights reserved.
in HNC etiology, and in the same study it accounted for approximately 4% of cases while the interaction between tobacco and alcohol accounted for almost three-fourths of HNCs [2]. Another recent study found differences in the joint hazard of smoking and alcohol consumption in relation to HNC (mouth and oropharyngeal cancer) deaths. Specifically, 42% of HNC deaths in low-income countries versus 80% in high-income countries were due to tobacco and alcohol use, likely reflecting different exposure patterns in relation to economic development status [3]. In addition, a series of recent studies in economically-developed nations have described the role of persistent infection with human papillomavirus (HPV) as an etiologic factor in the development of HNC (mainly restricted to the oropharynx, tonsils and base of the tongue) [4,5]. In some regions (i.e., North America, Australia, and Northern
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Table 1 Age-standardized oral cavity cancer (tongue & mouth; C01-06) incidence rates and rate ratios by sex among adults P 15 years, select registries. Males
Europe Eastern Europe Belarus Czech Republic Poland Cracow Warsaw City Russia (St Petersburg) Slovak Republic Northern Europe Denmark Estonia Finland Iceland Latvia Norway Sweden United Kingdom (4 registries) UK, Scotland Western Europe France (6 registries) Germany (Saarland) Switzerland (4 registries) The Netherlands Eindhoven Maastricht Southern Europe Italy (6 registries) Slovenia Spain (5 registries) Asia Eastern Asia China Hong Kong Shanghai Japan (5 registries) Southern Asia India Mumbai (Bombay) Chennai (Madras) South-Eastern Asia Philippines (Manila) Singapore Chinese Indian Malay Thailand (Chiang Mai) Western Asia Israel Jews Non-Jews Kuwait Kuwaitis Non-Kuwaitis North America Canada (9 registries) United States SEER (9 Registries): Black SEER (9 Registries): White South America Caribbean Martinique (France) Central America Costa Rica South America Brazil (Goiania) Colombia (Cali) Ecuador (Quito) Peru (Trujillo) Oceania Australia (6 registries)
Females
1983–1987
1998–2002
Rate ratio
(95% CI)
p Value
1983–1987
1998–2002
Rate ratio
(95% CI)
p Value
6.10 5.77
8.93 7.19
1.46 1.25
1.36 1.16
1.58 1.34
0.00 0.00
0.69 0.87
0.73 1.35
1.06 1.54
0.86 1.31
1.31 1.82
0.56 0.00
6.01 5.68 10.16 12.21
5.40 4.99 9.43 14.22
0.90 0.88 0.93 1.16
0.64 0.71 0.84 1.08
1.25 1.08 1.02 1.26
0.52 0.21 0.12 0.00
1.35 1.11 0.83
1.26 1.59 1.39 1.37
1.18 1.25 1.64
0.85 1.01 1.28
1.64 1.55 2.10
0.34 0.04 0.00
4.51 6.03 2.54 4.46 4.50 3.78 4.00 5.62
7.12 8.47 4.09 3.56 6.85 4.32 3.50 5.18 8.65
1.58 1.40 1.61
1.42 1.15 1.39
1.76 1.71 1.86
0.00 0.00 0.00
1.54 0.96 0.92 1.30 1.54
1.30 0.84 0.84 1.20 1.39
1.82 1.10 1.02 1.40 1.70
0.00 0.55 0.12 0.00 0.00
2.33 0.81 1.56 2.99 0.68 2.07 1.75 1.75 2.34
3.08 1.62 2.18 2.65 0.89 2.18 2.20 2.75 3.80
1.32 2.00 1.40 0.89 1.29 1.05 1.26 1.57 1.62
1.15 1.34 1.18 0.45 0.89 0.88 1.10 1.42 1.41
1.53 3.00 1.67 1.75 1.87 1.26 1.43 1.74 1.86
0.00 0.00 0.00 0.72 0.18 0.57 0.00 0.00 0.00
21.93 13.15 10.57
15.25 13.11 10.17
0.70 1.00 0.96
0.65 0.85 0.83
0.75 1.16 1.11
0.00 0.96 0.61
2.13 1.77 2.33
3.12 3.35 3.96
1.46 1.89 1.70
1.22 1.35 1.33
1.76 2.64 2.18
0.00 0.00 0.00
3.95 4.24
4.90 6.13
1.24 1.45
0.92 1.06
1.67 1.98
0.17 0.03
2.05 1.74
3.11 2.76
1.51 1.59
1.04 0.99
2.20 2.54
0.04 0.07
6.97 13.68 7.85
6.08 11.02 8.66
0.87 0.81 1.10
0.78 0.72 0.98
0.98 0.91 1.24
0.02 0.00 0.11
1.66 1.22 0.97
2.41 1.97 2.17
1.45 1.62 2.23
1.20 1.19 1.73
1.76 2.20 2.88
0.00 0.00 0.00
6.99 1.96 3.98
4.72 1.97 4.43
0.68 1.01 1.11
0.60 0.85 1.03
0.76 1.19 1.20
0.00 0.95 0.01
3.02 1.51 1.61
2.38 1.71 1.98
0.79 1.13 1.23
0.67 0.94 1.11
0.92 1.35 1.37
0.00 0.19 0.00
19.14 16.65
15.49 15.96
0.81 0.96
0.76 0.87
0.87 1.06
0.00 0.41
9.83 14.10
8.12 9.83
0.83 0.70
0.75 0.62
0.91 0.79
0.00 0.00
7.99
5.30
0.66
0.54
0.81
0.00
9.19
3.97
0.43
0.36
0.53
0.00
5.35 14.73
4.64 6.43 2.83 5.95
0.87 0.44
0.69 0.27
1.09 0.71
0.21 0.00
1.42
1.78 6.08
1.26
0.89
1.78
0.22
0.53
0.40
0.68
0.00
5.44
3.59
0.66
0.48
0.90
0.01
2.64 2.49
1.21
0.07
1.77
1.59
0.89
0.71
1.13
0.34
11.33
2.18
0.98
1.49
2.83
2.13
0.75
0.37
1.55
0.44
7.08
5.70
0.80
0.76
0.85
0.00
3.22
2.92
0.91
0.84
0.97
0.01
14.61 8.92
9.65 7.16
0.66 0.80
0.58 0.76
0.76 0.84
0.00 0.00
4.49 4.32
3.31 3.41
0.74 0.79
0.60 0.74
0.91 0.84
0.00 0.00
14.10
9.93
0.70
0.50
0.98
0.04
1.67
3.56
2.69
0.76
0.56
1.02
0.06
1.74
1.27
0.73
0.48
1.10
0.11
0.22 0.07
2.66 2.81 1.35 2.54
1.16
0.80
1.69
0.45
1.07
0.98
1.17
0.16
9.72 3.67
7.01
12.73 2.57 1.01 3.44
1.31 0.70
6.32
0.90
0.88 0.47
1.96 1.05
2.42
0.85
0.96
0.00
Source: Cancer Incidence in Five Continents. Incidence rates per 100,000 population, age-standardized to the 1960 standard world population. Abbreviation: 95% CI, 95% confidence interval. Rate ratio comparing 1998–2002 to 1983–1987. Significant rate ratios in bold. Rates not reported if the numerator included fewer than 16 cases.
2.82
3.01
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Figure 1. Trends in oral cavity cancer incidence rates in select countries by sex (Cancer Incidence in Five Continents, 1983–2002). Notes: Rates are displayed on the log scale. Rates not reported if numerator included fewer than 16 cases. Registries without data for all four time periods are not displayed. Oral cavity includes tongue and mouth.
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Table 2 Age-standardized oropharynx cancer (tonsil and oropharynx; C09-10) incidence rates and rate ratios by sex among adults P 15 years, select registries. Males
Europe Eastern Europe Belarus Czech Republic Poland Cracow Warsaw City Russia (St Petersburg) Slovak Republic Northern Europe Denmark Estonia Finland Iceland Latvia Norway Sweden United Kingdom (4 registries) UK, Scotland Western Europe France (6 registries) Germany (Saarland) Switzerland (4 registries) The Netherlands Eindhoven Maastricht Southern Europe Italy (6 registries) Slovenia Spain (5 registries) Asia Eastern Asia China Hong Kong Shanghai Japan (5 registries) Southern Asia India Mumbai (Bombay) Chennai (Madras) South-Eastern Asia Philippines (Manila) Singapore Chinese Indian Malay Thailand (Chiang Mai) Western Asia Israel Jews Non-Jews Kuwait Kuwaitis Non-Kuwaitis North America Canada (9 registries) United States SEER (9 Registries): Black SEER (9 Registries): White South America Caribbean Martinique (France) Central America Costa Rica South America Brazil (Goiania) Colombia (Cali) Ecuador (Quito) Peru (Trujillo) Oceania Australia (6 registries)
Females
1983–1987
1998–2002
Rate ratio
(95% CI)
p Value
1983–1987
1998–2002
Rate ratio
(95% CI)
p Value
1.00 2.55
4.75 4.36
4.74 1.71
4.11 1.54
5.47 1.90
0.00 0.00
0.15 0.41
0.23 0.72
1.50 1.73
1.00 1.37
2.26 2.19
0.05 0.00
1.45 3.25 1.21 5.41
2.64 3.57 3.43 8.63
1.82 1.10 2.84 1.60
1.07 0.85 2.30 1.43
3.10 1.41 3.50 1.78
0.04 0.47 0.00 0.00
0.68 0.33 0.37
1.15 0.39 0.41
1.69 1.17 1.12
1.11 0.80 0.74
2.58 1.73 1.69
0.02 0.42 0.59
1.90 3.21 0.60
3.81 4.21 1.22
2.00 1.31 2.04
1.72 1.00 1.54
2.34 1.73 2.72
0.00 0.05 0.00
0.64 0.44 0.18
1.45 0.40 0.34
2.26 0.90 1.91
1.75 0.45 1.19
2.92 1.80 3.07
0.00 0.77 0.01
1.24 1.09 1.05 1.26 1.07
3.21 2.06 1.81 2.13 2.44
2.59 1.89 1.72 1.70 2.28
1.95 1.50 1.46 1.50 1.86
3.45 2.39 2.03 1.92 2.80
0.00 0.00 0.00 0.00 0.00
0.30 0.46 0.43 0.43 0.34
0.42 0.68 0.80 0.65 0.78
1.38 1.48 1.87 1.52 2.28
0.78 1.02 1.45 1.23 1.62
2.42 2.15 2.41 1.87 3.20
0.27 0.04 0.00 0.00 0.00
13.68 3.42 5.43
9.43 6.42 5.89
0.69 1.88 1.08
0.63 1.45 0.89
0.76 2.43 1.32
0.00 0.00 0.43
0.74 0.76 1.05
1.48 1.21 1.68
2.01 1.59 1.60
1.50 0.92 1.10
2.69 2.76 2.33
0.00 0.10 0.02
1.31 2.13
2.18 2.99
1.67 1.41
1.04 0.91
2.67 2.18
0.05 0.15
0.67 0.84
3.13 9.45 2.02
2.80 8.20 2.41
0.89 0.87 1.20
0.75 0.75 0.95
1.06 1.00 1.51
0.21 0.05 0.14
0.59 0.54 0.31
0.57 0.99 0.19
0.97 1.84 0.61
0.67 1.17 0.31
1.40 2.90 1.22
0.86 0.01 0.15
1.63 0.48 0.68
1.25 0.38 1.33
0.77 0.78 1.95
0.61 0.54 1.67
0.97 1.11 2.28
0.02 0.17 0.00
0.48 0.33 0.16
0.26 0.15 0.18
0.54 0.48 1.15
0.34 0.29 0.80
0.84 0.77 1.63
0.00 0.00 0.46
4.68 2.42
2.82 3.58
0.60 1.48
0.52 1.17
0.70 1.87
0.00 0.00
0.98 0.60
0.61 0.52
0.62 0.86
0.44 0.50
0.87 1.48
0.00 0.58
0.96
0.93
0.97
0.59
1.59
0.91
1.02
0.62
0.61
0.36
1.02
0.05
0.94
0.32
0.55
0.26
1.16
0.08
1.53
1.55
1.01
0.68
1.51
3.70
2.14
0.58
0.37
0.91
0.01
1.06
0.58
2.05
1.23
3.40
0.01
0.28
0.57
0.18
1.98
2.36
1.19
1.08
1.31
0.00
0.79
0.70
0.89
0.76
1.03
0.12
6.48 2.39
4.93 2.90
0.76 1.21
0.62 1.11
0.93 1.32
0.01 0.00
1.55 0.96
0.95 0.73
0.61 0.77
0.42 0.66
0.90 0.89
0.01 0.00
8.83
6.93
0.78
0.52
1.18
0.24
0.98
1.07
1.10
0.66
1.84
0.72
4.56 1.20
2.47
2.46
0.76
0.66
0.86
0.71
1.04
0.13
0.99
0.90
1.10
0.92
Source: Cancer Incidence in Five Continents. Incidence rates per 100,000 population, age-standardized to the 1960 standard world population. Abbreviation: 95% CI, 95% confidence interval. Rate ratio comparing 1998–2002 to 1983–1987. Significant rate ratios in bold. Rates not reported if the numerator included fewer than 16 cases.
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Figure 2. Trends in tonsil and oropharynx cancer incidence rates in select countries by sex (Cancer Incidence in Five Continents, 1983–2002). Notes: Rates are displayed on the log scale. Rates not reported if numerator included fewer than 16 cases. Registries without data for all four time periods are not displayed. Oropharynx includes tonsils and oropharynx.
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Europe) HPV may be responsible for more than 60% of HNC cases at these specific sub-sites [6]. While previous studies have described trends in HNC incidence rates at the country or regional level [7,8], we sought to describe trends in rates internationally with a focus on differences by anatomic sub-site and sex. As more precise estimates of the contribution of various risk factors to HNC emerge at the country-level such an evaluation of HNC incidence trends would inform both clinicians treating patients as well as cancer prevention and control programs with regards to areas that warrant focused attention and intervention.
Methods Incident HNC cases among individuals aged 15 years or greater were obtained from the International Agency for Research on Cancer’s (IARCs) Cancer Incidence in Five Continents (CI5) databases. Volumes 6 [9] (including cancers diagnosed during 1983–1987), 7 [10] (1988–1992), 8 [11] (1993–1987), and 9 [12] (1998–2002) of CI5 were used to obtain country and/or registry level data for different HNC sub-sites for males and females separately (the different years of data contributing from each registry are shown in Appendix A). Data from 85 population-based cancer registries with high-quality data representing 37 countries were used in the current analysis. In order to describe HNC rates and changes in rates over time and across countries, we focused on incidence rates reported during two combined calendar periods: 1983–1987 (from CI5 volume 6) and 1998–2002 (from CI5 volume 9). HNC cases reported from local registries were coded using combinations of International Classification of Diseases (ICD) codes (versions 7–10) and International Classification of Diseases for Oncology (ICD-O, versions 1–3) [11,12]. To allow for comparisons between registries over time, cases were converted to ICD-9 [13] (used during 1979–1988) and ICD-10 [14] (used from 1999 onwards). Invasive HNC cases (of any histology) were categorized into three broad groups using information regarding anatomic site available across CI5 volumes based on their different etiologic risk factors. Oral cavity cancers included cancers of the tongue and mouth (ICD-9 codes 141 and 143-5 and ICD-10 codes C01-02 and C03-06) and were considered in large part to be associated with tobacco and alcohol use. Oropharyngeal cancers included the tonsils and oropharynx (ICD-9 code 146 and ICD-10 codes C09-10) and were considered to be associated with HPV infection, in addition to tobacco and alcohol use. The last category was other HNCs which included poorly-defined tumors of the lip/oral cavity/pharynx (ICD-9 code 149 and ICD-10 code C14), the hypopharynx (ICD-9 code 148 and ICD-10 codes C12-13) as well as the larynx (ICD-9 code 161 and ICD-10 code C32). Consistent with prior HNC studies [15–18], tumors of the salivary gland, nasal cavity and sinuses and nasopharynx were excluded because they have different etiologic associations and incidence trends [19,20]. Five-year average annual incidence rates for the three categories of HNC were calculated during the two calendar periods (1983–1987 and 1998–2002) for each registry and sex (cancer counts and corresponding population estimates are provided in aggregate by IARC although annual data may not be available for every registry during every 5-year period). In instances where data from multiple regional registries were available for an economically developed country, registry specific data were aggregated to obtain a national estimate so as to simplify the interpretation of trends for multiple registries and countries. This was done for the United Kingdom (n = 4 registries), France (n = 6), Switzerland (n = 4), Italy (n = 6), Spain (n = 5), Canada (n = 9), Australia (n = 6), and Japan (n = 5). The United States also aggregates nine registries
by black and white race. For the other countries either a national registry was available or data from one or more registries are provided at the registry-level. HNC incidence rates were age-standardized to the 1960 world standard population using the Segi method [21] as modified by Doll [22] by 5-year age increments (15–19, 20–24, . . ., 80–84, 85+) to account for the different age structures across and within countries over the study period [22]. To assess changes in rates the rate ratio (RR) was calculated with corresponding 95% confidence intervals (95% CIs) as the ratio of rates during 1998–2002 divided by those during 1983–1987 [23]. A two-sided Z-test was calculated to evaluate the significance of the RR with a corresponding P-value and P-values less than 0.05 were considered statistically significant. Sex-specific HNC rates are also presented graphically on the log scale for selected countries/registries with noteworthy trends for the entire study period using CI5 data from volumes 6–9 (covering years 1983–1987, 1988–1992, 1993–1997, 1998–2002, respectively) [24]. For stability and reliability, rates were not reported if the numerator contained fewer than 16 cases (numerators for all rates are shown in Appendix B). All analyses were conducted SAS version 9.3 (SAS Institute, Cary, North Carolina).
Results Changes in HNC incidence rates from 1983–1987 to 1998–2002 varied substantially across countries for both men and women for all of the major HNC categories (oral cavity, oropharynx and other HNC). Oral cavity cancer rates increased among both men and women in 7 out of 37 countries located in Europe and Asia (Czech Republic, Slovak Republic, Denmark, Estonia, Finland, the United Kingdom and Japan) (Table 1 and Fig. 1). The largest increases were among men in Finland (RR = 1.61, 95% CI: 1.39–1.86) and women in Spain (RR = 2.23, 95% CI: 1.73–2.88). Oral cavity cancer rates decreased for men and women in 6 countries (China [Hong Kong registry], India [Mumbai registry], Philippines, Thailand, Canada and the United States). The greatest decrease among men was in the Indian registry in Singapore (RR = 0.44, 95% CI: 0.27–0.71) and among women in the Philippines (RR = 0.43, 95% CI: 0.36–0.53). Oral cavity cancer rates were stable in many South American registries (except in Martinique where rates decreased by 30% among men). In Australia, rates were stable among women but decreased by 10% among men. The first and second-highest oral cavity cancer rates in 1998–2002 among both men (15.96, 15.49) and women (9.83, 8.12) were in the two Indian registries with available data: Chennai and Mumbai, respectively. Rates were also elevated among men in France (15.25). Rates were generally more than two-times as high among men versus women, except notably in the Slovak Republic and Belarus where rates were more than 10-fold higher among men versus women. Approximately two-thirds of oropharyngeal cancers were located in the tonsil and the remaining in the oropharynx. During 1983–1987 and 1998–2002, rates of oropharyngeal cancer increased among men and women in 7 countries (Belarus, Czech Republic, Denmark, Finland, Norway, Sweden, and the United Kingdom) (Table 2 and Fig. 2). While oropharyngeal cancer rates decreased among men in France (RR = 0.69, 95% CI: 0.63–0.76), they increased among women (RR = 2.01, 95% CI: 1.50–2.69). Oropharyngeal cancer rates also decreased among men and women in China (Hong Kong) and India (Mumbai). In other global regions the trends differed by sex. For example, rates increased among men only in India (Chennai), Germany, Japan, and Canada. In the United States, the increase in oropharyngeal cancer rates was restricted to white men (RR = 1.21, 95% CI: 1.11–1.32) whereas rates significantly decreased among black men and white and
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Table 3 Age-standardized other head and neck cancer (pyriform sinus, hypopharnyx, lip/oral cavity/pharynx not otherwise specified, and larynx; C12-14, 32) incidence rates and rate ratios by sex among adults P 15 years, select registries. Males
Europe Eastern Europe Belarus Czech Republic Poland Cracow Warsaw City Russia (St Petersburg) Slovak Republic Northern Europe Denmark Estonia Finland Iceland Latvia Norway Sweden United Kingdom (4 registries) UK, Scotland Western Europe France (6 registries) Germany (Saarland) Switzerland (4 registries) The Netherlands Eindhoven Maastricht Southern Europe Italy (6 registries) Slovenia Spain (5 registries) Asia Eastern Asia China Hong Kong Shanghai Japan (5 registries) Southern Asia India Mumbai (Bombay) Chennai (Madras) South-Eastern Asia Philippines (Manila) Singapore Chinese Indian Malay Thailand (Chiang Mai) Western Asia Israel Jews Non-Jews Kuwait Kuwaitis Non-Kuwaitis North America Canada (9 registries) United States SEER (9 Registries): Black SEER (9 Registries): White South America Caribbean Martinique (France) Central America Costa Rica South America Brazil (Goiania) Colombia (Cali) Ecuador (Quito) Peru (Trujillo) Oceania Australia (6 registries)
Females
1983–1987
1998–2002
Rate ratio
(95% CI)
p Value
1983–1987
1998–2002
Rate ratio
(95% CI)
p Value
14.89 12.89
18.93 11.93
1.27 0.93
1.21 0.88
1.34 0.98
0.00 0.00
0.73 0.83
0.34 1.09
0.46 1.31
0.36 1.10
0.60 1.56
0.00 0.00
19.11 17.41 16.56 20.14
14.81 13.15 13.95 20.71
0.77 0.76 0.84 1.03
0.64 0.67 0.78 0.97
0.94 0.85 0.91 1.10
0.01 0.00 0.00 0.38
1.45 2.47 0.62 0.86
2.37 2.07 0.63 0.91
1.64 0.84 1.01 1.06
0.99 0.63 0.75 0.80
2.71 1.10 1.35 1.40
0.07 0.20 0.96 0.70
9.19 12.73 6.98 4.85 13.30 6.41 5.06 7.83 9.53
8.84 15.18 4.52 5.59 15.20 5.43 3.88 7.74 11.94
0.96 1.19 0.65 1.15 1.14 0.85 0.77 0.99 1.25
0.89 1.04 0.58 0.67 1.03 0.76 0.70 0.94 1.16
1.05 1.37 0.73 1.99 1.27 0.95 0.84 1.05 1.35
0.36 0.01 0.00 0.61 0.01 0.00 0.00 0.70 0.00
2.16 0.63 0.72
1.96 0.75 0.50
0.91 1.19 0.69
0.77 0.69 0.51
1.08 2.07 0.94
0.27 0.53 0.02
0.93 0.69 0.74 1.95 2.41
0.61 0.94 0.77 1.69 2.83
0.66 1.36 1.04 0.86 1.18
0.45 1.01 0.84 0.78 1.01
0.97 1.84 1.29 0.96 1.36
0.03 0.05 0.73 0.01 0.03
33.81 15.35 16.31
22.69 13.67 12.78
0.67 0.89 0.78
0.63 0.77 0.69
0.71 1.03 0.89
0.00 0.11 0.00
1.24 1.24 1.51
1.70 1.88 2.12
1.37 1.52 1.40
1.07 0.98 1.01
1.75 2.36 1.94
0.01 0.07 0.05
9.39 10.12
9.75 10.17
1.04 1.00
0.85 0.80
1.27 1.26
0.71 0.97
1.32 1.29
1.57 1.65
1.19 1.28
0.72 0.72
1.99 2.25
0.50 0.42
22.35 17.72 23.92
14.36 16.03 23.15
0.64 0.90 0.97
0.60 0.82 0.90
0.69 1.00 1.04
0.00 0.05 0.36
1.42 1.07 0.47
1.08 1.29 0.67
0.76 1.20 1.42
0.59 0.84 0.92
0.98 1.70 2.19
0.03 0.31 0.13
16.19 4.40 6.87
8.52 4.41 6.63
0.53 1.00 0.96
0.49 0.90 0.91
0.57 1.12 1.03
0.00 0.97 0.24
1.93 0.87 0.69
0.61 0.41 0.53
0.32 0.47 0.76
0.25 0.36 0.63
0.41 0.63 0.92
0.00 0.00 0.00
27.93 15.11
16.66 15.00
0.60 0.99
0.56 0.89
0.64 1.10
0.00 0.89
6.11 4.15
2.89 3.81
0.47 0.92
0.41 0.75
0.55 1.12
0.00 0.40
10.23
9.81
0.96
0.82
1.12
0.60
3.42
1.96
0.57
0.43
0.76
0.00
10.77 15.87
0.81 0.35
0.69 0.20
0.96 0.60
0.01 0.00
1.24
0.55
0.44
0.26
0.75
0.00
17.54
8.73 5.49 5.35 6.58
0.38
0.30
0.48
0.00
5.19
1.46
0.28
0.18
0.44
0.00
7.60 6.96
7.09 9.45
0.93 1.36
0.83 0.95
1.05 1.95
0.25 0.11
1.22
0.91
1.64
0.19
4.29 18.78
4.37 5.09
1.02 0.27
0.57 0.14
1.83 0.52
10.86
7.39
0.68
0.65
22.63 12.67
15.81 8.31
0.70 0.66
16.08
13.12
7.50 10.92 8.17 3.15
10.52
0.95
1.16
0.95 0.00
0.71
0.00
2.04
1.44
0.70
0.64
0.78
0.00
0.63 0.63
0.78 0.69
0.00 0.00
4.65 2.85
3.50 2.07
0.75 0.73
0.61 0.67
0.93 0.79
0.01 0.00
0.82
0.61
1.10
0.17
1.83
5.95
0.79
0.64
0.98
0.02
1.14
0.42
0.37
0.19
0.71
0.00
16.12 8.63 2.32 2.83
1.48 1.06 0.73
1.03 0.83 0.40
2.11 1.35 1.34
0.06 0.67 0.28
1.63
1.73 1.78
1.09
0.68
1.76
0.72
7.34
0.70
1.31
1.03
0.79
0.68
0.91
0.00
0.66
0.74
0.00
Source: Cancer Incidence in Five Continents. Incidence rates per 100,000 population, age-standardized to the 1960 standard world population. Abbreviation: 95% CI, 95% confidence interval. Rate ratio comparing 1998–2002 to 1983–1987. Significant rate ratios in bold. Rates not reported if the numerator included fewer than 16 cases.
394
E.P. Simard et al. / Oral Oncology 50 (2014) 387–403
Figure 3. Trends in other head and neck cancer incidence rates in select countries by sex (Cancer Incidence in Five Continents, 1983–2002). Notes: Rates are displayed on the log scale. Rates not reported if numerator included fewer than 16 cases. Registries without data for all four time periods are not displayed. Other head and neck includes hypopharnyx, lip/oral cavity/pharnyx not otherwise specified, and larynx.
395
E.P. Simard et al. / Oral Oncology 50 (2014) 387–403 Table A1 Years of data by volume and registry, Cancer Incidence in Five Continents.
Europe Eastern Europe Belarus Czech Republic Poland Cracow Warsaw City Russia (St Petersburg) Slovak Republic Northern Europe Denmark Estonia Finland Iceland Latvia Norway Sweden United Kingdom (4 registries) Merseyside and Cheshire North Western Oxford Region West Midlands UK, Scotland Western Europe France (6 registries) Bas-Rhin Calvados Doubs Isere Somme Tarn Germany (Saarland) Switzerland (4 registries) Geneva Neuchatel St Gall-Appenzell Vaud The Netherlands Eindhoven Maastricht Southern Europe Italy (6 registries) Genoa Province Florence and Prato Parma Province Ragusa Province Torino Varese Province Slovenia Spain (5 registries) Granada Murcia Navarra Tarragona Zaragoza Asia Eastern Asia China Hong Kong Shanghai Japan (5 registries) Hiroshima Miyagi Prefecture Nagasaki Prefecture Osaka Prefecture Yamagata Prefecture Southern Asia India Mumbai (Bombay) Chennai (Madras) South-Eastern Asia Philippines (Manila) Singapore Chinese
Vol. 6
Vol. 7
Vol. 8
Vol. 9
1983–1987 1983–1987
1988–1992 1988–1992
1993–1997 1993–1997
1998–2002 1998–2002
1983–1986 1983–1987 1983–1987 1983–1987
1988–1992 1989–1992 – 1988–1992
1993–1997 1993–1997 1994–1997 1993–1997
1998–2002 1998–2002 1998–2002 1998–2002
1983–1987 1983–1987 1982–1986 1983–1987 1983–1987 1983–1987 1983–1987
1988–1992 1988–1992 1987–1992 1988–1992 1988–1992 1988–1992 1988–1992
1993–1997 1993–1997 1993–1997 1993–1997 1993–1997 1993–1997 1993–1997
1998–2002 1998–2002 1998–2002 1998–2002 1998–2002 1998–2002 1998–2002
1983–1987 1983–1987 1983–1987 1983–1986 1983–1987
1988–1992 1988–1992 1988–1992 1988–1992 1988–1992
1993–1997 1993–1997 1993–1997 1993–1997 1993–1997
1998–2002 1998–2002 1998–2002 1998–2002 1998–2002
1983–1987 1983–1987 1983–1987 1983–1987 1983–1984 1983–1987 1983–1987
1988–1992 1988–1992 1988–1992 1988–1992 1988–1992 1988–1992 1988–1992
1993–1997 1993–1997 1993–1997 1993–1997 1993–1997 1993–1997 1993–1997
1998–2002 1998–2002 1998–2002 1998–2002 1998–2002 1998–2002 1998–2002
1983–1987 1983–1987 1983–1987 1983–1987
1988–1992 1988–1992 1988–1992 1988–1992
1993–1997 1993–1996 1993–1997 1993–1996
1998–2002 1998–2002 1998–2002 1998–2002
1983–1987 1986–1988
1988–1992 1988–1992
1993–1997 1993–1997
1998–2002 1998–2002
1986–1987 1985–1987 1983–1987 1983–1987 1985–1987 1983–1987 1982–1987
1988–1992 1988–1991 1988–1992 1988–1992 1988–1991 1988–1992 1988–1992
1993–1996 1993–1997 1993–1997 1993–1997 1993–1997 1993–1997 1993–1997
1998–2000 1998–2002 1998–2002 1998–2002 1998–2002 1998–2000 1998–2002
1985–1987 1984–1987 1983–1986 1984–1987 1983–1985
1988–1992 1988–1992 1987–1991 1988–1992 1986–1990
1993–1997 1993–1996 1993–1997 1993–1997 1991–1995
1998–2002 1997–2001 1998–2002 1998–2001 1996–2000
1983–1987 1983–1987
1988–1992 1988–1992
1993–1997 1993–1997
1998–2002 1998–2002
1981–1985 1983–1987 1983–1987 1983–1987 1983–1986
1986–1990 1988–1992 1988–1992 1988–1992 1988–1992
1991–1995 1993–1997 1993–1997 1993–1997 1993–1997
1996–2000 1998–2002 1998–2002 1998–2002 1998–2002
1983–1987 1983–1987
1988–1992 1988–1992
1993–1997 1993–1997
1998–2002 1998–2002
1983–1987
1988–1992
1993–1997
1998–2002
1983–1987
1988–1992
1993–1997
1998–2002 (continued on next page)
396
E.P. Simard et al. / Oral Oncology 50 (2014) 387–403
Table A1 (continued)
Indian Malay Thailand (Chiang Mai) Western Asia Israel Jews Non-Jews North America Canada (9 registries) Alberta British Columbia Manitoba New Brunswick Newfoundland and Labrador Nova Scotia Ontario Prince Edward Island Saskatchewan United States SEER (9 Registries): Black SEER (9 Registries): White South America Caribbean Martinique (France) Central America Costa Rica South America Brazil (Goiania) Colombia (Cali) Ecuador (Quito) Peru (Trujillo) Oceania Australia (6 registries) New South Wales South Tasmania Victoria Western Capital Territory
Vol. 6
Vol. 7
Vol. 8
Vol. 9
1983–1987 1983–1987 1983–1987
1988–1992 1988–1992 1988–1992
1993–1997 1993–1997 1993–1997
1998–2002 1998–2002 1998–2002
1982–1986 1982–1986
1988–1992 1988–1992
1993–1997 1993–1997
1998–2002 1998–2002
1983–1987 1983–1987 1983–1987 1983–1986 1983–1987 1983–1987 1983–1987 1983–1987 1983–1987
1988–1992 1988–1992 1988–1992 1988–1992 1988–1992 1988–1992 1988–1992 1988–1992 1988–1992
1993–1997 1993–1997 1993–1997 1993–1997 1993–1997 1993–1997 1993–1997 1993–1997 1993–1997
1998–2002 1998–2002 1998–2002 1998–2002 1998–2002 1998–2002 1998–2002 1998–2002 1998–2002
1983–1987 1983–1987
1988–1992 1988–1992
1993–1997 1993–1997
1998–2002 1998–2002
1983–1987
–
1993–1997
1998–2002
1984–1987
1988–1992
1995–1996
1998–2002
1988–1989 1982–1986 1985–1987 1984–1987
1990–1993 1987–1991 1988–1992 1988–1990
1995–1998 1992–1996 1993–1997 –
1999–2002 1998–2002 1998–2002 1998–2002
1983–1987 1983–1987 1983–1987 1983–1987 1983–1987 1983–1987
1988–1992 1988–1992 1988–1992 1988–1992 1988–1992 1988–1992
1993–1997 1993–1997 1993–1997 1993–1997 1993–1997 1993–1997
1998–2002 1998–2002 1998–2002 1998–2002 1998–2002 1998–2002
black women. During 1998–2002 oropharyngeal cancer rates were highest among men in France (9.43) and among women in Switzerland (1.68). Generally, oropharyngeal cancer rates were 2–5 times as high among men compared to women, except in Belarus and the Slovak Republic where the sex disparity was more than 20-fold. With respect to rates and trends of other HNC (which included poorly-defined tumors of the lip/oral cavity/pharynx as well as the hypopharynx and larynx), they reflect patterns of laryngeal cancer which accounted for more than two-thirds of the cases during 1983–1987 and 1998–2002. Trends in other HNC incidence rates varied during 1983–1987 and 1998–2002 by country/registry and sex (Table 3 and Fig. 3). Incidence rates increased for both men and women in the United Kingdom (Scotland registry only) whereas they decreased for both sexes in 10 countries (Finland, Italy, China [Hong Kong], India [Mumbai], Singapore [Chinese], Thailand [Chang Mai], Canada, United States, Costa Rica, and Australia). The largest increase in rates between 1983–1987 and 1998–2008 among men occurred in Belarus (RR = 1.27, 95% CI: 1.21–1.34) and among women occurred in Switzerland (RR = 1.40, 95% CI: 1.01–1.94). Whereas the largest decreases were among non-Kuwaiti men in Kuwait (RR = 0.27, 95% CI: 0.14–0.52) and among women in Thailand (RR = 0.28, 95% CI: 0.18–0.44). Rates of other HNCs during 1998–2002 were highest among men in Spain (23.15) and France (22.69) and among women in the Indian registry of Chennai (3.81) and among black women in the United States (3.50). Rates of other HNC were generally at least
five-fold higher among men compared to women, with notable exceptions in Belarus and Spain where they were more than 50- and 30-times as high in men versus women, respectively. Discussion This analysis of international variations in HNC incidence rates documents significant heterogeneity in trends by sub-site, country and sex. Rates of oral cavity cancer increased among both men and women in a number of European countries but were stable or decreased in a number of Asian countries and rates decreased for men and women in Canada and the United States. Rates of oropharyngeal cancer also increased among both men and women in a number of European nations. These trends were concentrated mainly among eastern (Belarus, Czech Republic) and some northern European nations (the United Kingdom, Denmark, Estonia, Finland, Latvia, Norway, Sweden) as well as some Asian countries (Japan and India [Chennai]). In contrast, oropharyngeal cancer rates declined among men and women in China (Hong Kong) and India (Mumbai). For other HNCs (mainly of the larynx), incidence rates declined for men and women in nine countries and trends varied by sex in other areas. The different trends in incidence rates across countries by HNC sub-site and sex likely reflect differences in the prevalence of known HNC risk factors. Tobacco use is the strongest HNC risk factor, especially for oral cavity and other HNCs. Exposure to this carcinogen via active or
397
E.P. Simard et al. / Oral Oncology 50 (2014) 387–403
Table B1 Number of cases by sex, registry, and volume of Cancer Incidence in Five Continents. Males
Oral cavity (C01-06) Europe Eastern Europe Belarus Czech Republic Poland Cracow Warsaw City Russia (St Petersburg) Slovak Republic Northern Europe Denmark Estonia Finland Iceland Latvia Norway Sweden United Kingdom (4 registries) Merseyside and Cheshire North Western Oxford Region Trent West Midlands UK, Scotland Western Europe France (6 registries) Bas-Rhin Calvados Doubs Isere Somme Tarn Germany (Saarland) Switzerland (4 registries) Geneva Neuchatel St Gall-Appenzell Vaud The Netherlands Eindhoven Maastricht Southern Europe Italy (6 registries) Genoa Province Florence and Prato Parma Province Ragusa Province Romagna Region Torino Varese Province Slovenia Spain (5 registries) Basque Country Granada Murcia Navarra Tarragona Zaragoza Asia Eastern Asia China Hong Kong Shanghai Japan (5 registries) Hiroshima Miyagi Prefecture Nagasaki Prefecture Osaka Prefecture Yamagata Prefecture
Females
Vol. 6
Vol. 7
Vol. 8
Vol. 9
Vol. 6
Vol. 7
Vol. 8
Vol. 9
1019 1196
1620 1318
1803 1553
1742 1722
191 270
275 323
215 374
225 420
64 190 845 1095
61 143
82 196 817 1554
88 193 901 1506
11 73 167 103
17 57
30 87 202 168
31 85 226 188
961 250 535 22 350 480 883 1871 360 678 261 601 572 1089
391 36 249 18 55 299 537 707 145 227 117 224 218 385
422 58 359 17 61 300 626 800 148 231 125 296 468
484 60 408 27 82 337 669 968 167 303 155 294 343 557
535 82 393 24 78 333 690 1226 211 384 205 393 426 614
1383
121
537 165 252 13 214 457 856 1196 294 424 136 426 342 658
683 285 367 21 352 461 826 1559 308 503 187 561 789
828 272 416 18 355 526 899 1611 315 547 215 520 534 939
1506 582 281 168 306 84 85 310 357 110 31 71 145
1650 548 286 176 280 273 87 342 399 110 49 74 166
1592 458 293 161 313 284 83 337 319 95 27 59 138
1458 389 267 158 274 271 99 367 414 110 41 79 184
197 60 30 25 45 12 25 55 114 29 12 23 50
279 71 45 41 64 40 18 79 156 47 15 29 65
285 79 45 30 56 52 23 110 131 43 14 22 52
370 85 67 50 76 55 37 118 199 57 29 36 77
65 47
89 92
126 143
121 142
41 22
56 51
67 63
85 66
546 58 109 84 21 21 122 152 593 430 241 82 131 85 61 71
705 142 124 78 22
791 187 150 73 12 133 198 171 479 792
691 115 169 91 22
184 29 46 18 7
342 71 102 35 5
376 67 113 40 14
42 42 74 72 45 9 26 8 6 23
87 42 84 209
153 182 121 127 209
193 101 516 798 577 153 258 97 128 162
283 77 73 24 11 69 58 40 69 179 76 46 59 22 28 24
40 55 33 30 51
104 38 111 261 161 54 91 40 25 51
662 270 1018 64 159 54 701 40
619 374 1351 107 186 189 804 65
747 282 1716 122 229 267 999 99
694 321 1915 155 279 251 1070 160
309 223 510 50 72 20 350 18
326 327 737 54 115 96 426 46
326 264 900 76 119 154 494 57
383 316 1128 71 187 151 629 90
142 197 486 759 515 164 216 103 117 159
(continued on next page)
398
E.P. Simard et al. / Oral Oncology 50 (2014) 387–403
Table B1 (continued) Males
Southern Asia India Mumbai (Bombay) Chennai (Madras) South-Eastern Asia Philippines (Manila) Singapore Chinese Indian Malay Thailand (Chiang Mai) Western Asia Israel Jews Non-Jews Kuwait Kuwaitis Non-Kuwaitis North America Canada (9 registries) Canada (Excluding Quebec, Yukon and Nunavut) Alberta British Columbia Manitoba New Brunswick Newfoundland and Labrador Nova Scotia Ontario Prince Edward Island Saskatchewan United States SEER (9 Registries): Black SEER (9 Registries): White
Females
Vol. 6
Vol. 7
Vol. 8
Vol. 9
Vol. 6
Vol. 7
Vol. 8
Vol. 9
1864 679
1972 835
2188 924
2506 1020
770 551
869 610
1006 518
1132 585
231
273
289
246
294
285
289
218
133 50 8 129
130 37 11 136
153 41 8 142
207 32 20 160
45 15 10 79
71 13 5 102
73 22 9 86
101 22 11 104
145 9
164 6
206 13
256 27
141 7
159 11
208 4
216 8
8 35
4 19
11 27
15 40
6 13
6 6
6 9
14 13
2578 3648 197 404 138 75 45 122 1470 17 110
2862 3910 225 537 145 93 53 144 1552 24 89
2859 3966 275 496 151 92 58 129 1555 18 85
3046 3047 346 504 151 87 63 137 1646 22 90
1433 1788 125 282 84 40 19 43 762 4 74
1583 1960 146 297 102 40 24 60 839 12 63
1744 2192 191 302 108 48 16 75 925 8 71
1890 1892 224 377 111 45 17 75 938 16 87
460 3239
496 3097
469 3167
448 3277
175 2035
191 1953
198 2038
205 2037
72
7
33
133
42
59
76 74 13
128 61 21 21
8 43 13 8
64 10 4
South America Caribbean Martinique (France) Central America Costa Rica South America Brazil (Goiania) Colombia (Cali) Ecuador (Quito) Peru (Trujillo)
76
87
27 50 5 12
78 18 9
Oceania Australia (6 registries) New South Wales South Tasmania Victoria Western Capital Territory
1795 821 166 57 544 192 15
1960 881 194 50 578 235 22
2164 1021 177 56 603 277 30
2245 992 198 88 656 274 37
878 371 91 29 305 69 13
174 518
420 647
817 827
927 1037
16 115 100 484
41 108 673
40 156 225 824
226 89 58 5 57 105 235 368 78
294 133 81 3 114 110 274 458 97
411 130 94 3 122 164 333 549 121
Tonsil and oropharynx (C09-10) Europe Eastern Europe Belarus Czech Republic Poland Cracow Warsaw City Russia (St Petersburg) Slovak Republic Northern Europe Denmark Estonia Finland Iceland Latvia Norway Sweden United Kingdom (4 registries) Merseyside and Cheshire
74
17 26
73
33 86 28
33 90 31 20
1053 473 112 32 326 96 14
1166 485 101 33 393 138 16
1302 584 128 42 411 117 20
40 126
62 113
79 164
70 211
45 142 327 927
10 35 50 45
11 27 44
17 40 46 82
9 65 64 54
511 122 156 5 165 216 416 729 139
90 17 31 1 25 53 99 163 31
125 10 30 2 10 31 121 166 31
136 21 35 1 37 59 138 198 44
203 19 51 2 34 83 191 247 54
399
E.P. Simard et al. / Oral Oncology 50 (2014) 387–403 North Western Oxford Region Trent West Midlands UK, Scotland Western Europe France (6 registries) Bas-Rhin Calvados Doubs Isere Somme Tarn Germany (Saarland) Switzerland (4 registries) Geneva Neuchatel St Gall-Appenzell Vaud The Netherlands Eindhoven Maastricht Southern Europe Italy (6 registries) Genoa Province Florence and Prato Parma Province Ragusa Province Romagna Region Torino Varese Province Slovenia Spain (5 registries) Basque Country Granada Murcia Navarra Tarragona Zaragoza Asia Eastern Asia China Hong Kong Shanghai Japan (5 registries) Hiroshima Miyagi Prefecture Nagasaki Prefecture Osaka Prefecture Yamagata Prefecture Southern Asia India Mumbai (Bombay) Chennai (Madras) South-Eastern Asia Philippines (Manila) Singapore Chinese Indian Malay Thailand (Chiang Mai) Western Asia Israel Jews Non-Jews Kuwait Kuwaitis Non-Kuwaitis North America Canada (9 registries) Canada (Excluding Quebec, Yukon and Nunavut) Alberta British Columbia Manitoba New Brunswick Newfoundland and Labrador Nova Scotia
154 41 74 95 124
172 40
259 95 166 236 299
63 16 42 53 50
69 22
149 178
177 72 119 179 231
44 70
70 28 56 56 104
69 34 47 90 118
944 310 187 160 170 62 55 78 183 66 16 24 77
1095 317 199 131 175 211 62 112 234 70 24 35 105
1068 297 233 122 200 173 43 139 212 75 13 49 75
899 212 177 112 203 145 50 179 237 84 19 45 89
61 17 9 6 17 8 4 25 46 14 3 7 22
112 28 16 16 34 14 4 27 53 22 6 5 20
113 24 22 16 26 18 7 43 73 35 8 6 24
155 42 28 15 28 31 11 37 79 30 8 9 32
22 24
32 32
36 67
55 71
8 5
8 21
18 16
17 21
244 15 29 23 6 6 58 113 409 110 90 17 24 21 21 27
299 68 45 28 1
355 55 71 41 4
61 7 18 4 0 1 18 14 32 22 11 5 3 0 6 8
72 17 17 5 1
78 14 15 3 0
20 12 27 15 12 0 4 3 2 6
29 17 36 9
37 48 39 52 28
307 47 59 32 7 61 109 53 383 212 211 44 57 41 35 35
1 1 2 3 2
75 16 20 7 3 13 23 6 55 19 15 4 4 1 4 6
58 99 382 195 190 30 64 29 35 37
86 98 445 204
147 70 175 15 31 9 114 6
145 61 261 21 29 26 177 8
116 61 428 23 72 52 263 18
183 57 580 44 119 52 321 44
50 48 51 8 9 2 30 2
33 35 64 3 2 9 45 5
33 40 60 3 10 7 37 3
43 31 94 8 13 8 54 11
454 98
482 162
461 174
423 223
75 24
57 31
56 32
83 32
28
52
39
50
36
40
45
33
40 2 2 41
39 7 6 50
41 6 4 44
67 8 5 56
8 0 0 16
13 3 1 29
10 2 2 18
17 1 1 18
17 1
26 1
29 2
54 3
11 1
10 0
18 1
21 2
1 9
2 4
3 1
1 0
0 2
3 0
0 1
0 1
706 1022 46 128 36 17 7 18
834 1175 66 165 63 31 20 42
922 1290 76 187 42 30 22 41
1214 1215 125 232 66 55 23 85
317 396 20 57 13 11 2 8
324 434 20 63 18 9 7 15
370 483 27 82 17 8 5 16
423 423 41 73 27 14 9 22
(continued on next page)
400
E.P. Simard et al. / Oral Oncology 50 (2014) 387–403
Table B1 (continued) Males
Ontario Prince Edward Island Saskatchewan United States SEER (9 Registries): Black SEER (9 Registries): White
Females
Vol. 6
Vol. 7
Vol. 8
Vol. 9
Vol. 6
Vol. 7
Vol. 8
Vol. 9
430 3 21
420 3 24
489 4 31
583 5 40
191 3 12
182 1 9
197 0 18
218 2 17
200 865
178 903
207 1045
228 1299
59 412
62 429
57 380
58 386
50
4
16
51
12
20
25 20 11
47 30 8 3
1 15 3 0
10 2 0
610 246 57 17 221 59 10
855 359 97 28 249 111 11
213 119 12 8 55 14 5
South America Caribbean Martinique (France) Central America Costa Rica South America Brazil (Goiania) Colombia (Cali) Ecuador (Quito) Peru (Trujillo)
20
37
4 13 0 2
20 3 4
Oceania Australia (6 registries) New South Wales South Tasmania Victoria Western Capital Territory
632 284 64 19 202 59 4
702 275 78 21 242 83 3
47
Other head and neck (pyriform sinus, lip/oral cavity/pharynx not otherwise specified, Europe Eastern Europe Belarus 2459 3433 Czech Republic 2717 2661 Poland Cracow 198 212 Warsaw City 573 495 Russia (St Petersburg) 1323 Slovak Republic 1840 2065 Northern Europe Denmark 1152 1160 Estonia 357 481 Finland 698 741 Iceland 23 30 Latvia 638 828 Norway 670 647 Sweden 1226 1198 United Kingdom (4 registries) 2453 3035 Merseyside and Cheshire 491 555 North Western 863 995 Oxford Region 303 347 Trent 883 West Midlands 796 1138 UK, Scotland 1138 1310 Western Europe France (6 registries) 2369 2727 Bas-Rhin 758 765 Calvados 448 491 Doubs 299 341 Isere 515 511 Somme 187 463 Tarn 162 156 Germany (Saarland) 368 452 Switzerland (4 registries) 561 584 Geneva 152 171 Neuchatel 66 57 St Gall-Appenzell 121 94 Vaud 222 262 The Netherlands Eindhoven 153 251 Maastricht 112 232 Southern Europe Italy (6 registries) 1759 2046 Genoa Province 186 433 Florence and Prato 437 532 Parma Province 256 236 Ragusa Province 74 57
8 5
10
11 8 2
5 15 1 3
193 84 20 5 63 20 1
215 97 22 3 65 24 4
253 108 29 6 82 24 4
and larynx; C12-14,32)
3732 2844
3733 2902
179 233
135 212
97 240
93 333
253 616 1063 2212
247 535 1336 2177
20 111 100 92
37 78
35 110 83 115
51 106 102 117
1272 462 618 25 787 668 1075 3036 582 1001 391 901 1062 1477
1244 447 621 34 787 663 1032 2983 549 995 372 907 1067 1573
287 25 104 9 69 87 206 753 193 265 100 268 195 361
279 30 117 2 61 95 189 844 171 291 93 289 386
276 33 86 4 44 132 193 819 159 267 111 278 282 452
305 32 94 11 50 128 221 785 160 268 97 227 260 447
2556 717 440 313 494 450 142 459 492 153 51 96 192
2225 542 414 254 471 404 140 404 523 133 75 104 211
110 28 16 15 27 8 16 36 65 24 3 12 26
158 49 19 16 30 29 15 51 84 27 10 5 42
166 48 19 20 43 21 15 64 69 23 4 17 25
184 43 32 23 53 18 15 58 103 21 15 18 49
244 262
245 244
23 17
21 27
39 40
41 41
2244 479 636 197 54
1759 360 516 204 56
143 22 48 23 8
199 45 59 21 4
213 47 70 16 4
170 36 59 13 3
91
401
E.P. Simard et al. / Oral Oncology 50 (2014) 387–403 Romagna Region Torino Varese Province Slovenia Spain (5 registries) Basque Country Granada Murcia Navarra Tarragona Zaragoza Asia Eastern Asia China Hong Kong Shanghai Japan (5 registries) Hiroshima Miyagi Prefecture Nagasaki Prefecture Osaka Prefecture Yamagata Prefecture Southern Asia India Mumbai (Bombay) Chennai (Madras) South-Eastern Asia Philippines (Manila) Singapore Chinese Indian Malay Thailand (Chiang Mai) Western Asia Israel Jews Non-Jews Kuwait Kuwaitis Non-Kuwaitis North America Canada (9 registries) Canada (Excluding Quebec, Yukon and Nunavut) Alberta British Columbia Manitoba New Brunswick Newfoundland and Labrador Nova Scotia Ontario Prince Edward Island Saskatchewan United States SEER (9 Registries): Black SEER (9 Registries): White South America Caribbean Martinique (France) Central America Costa Rica South America Brazil (Goiania) Colombia (Cali) Ecuador (Quito) Peru (Trujillo) Oceania Australia (6 registries) New South Wales South Tasmania Victoria Western Capital Territory
85 355 451 772 1336 659 234 388 263 166 285
370 418 731 2092 1302 412 559 321 254 546
1484 608 1709 124 270 86 1106 123
430 468 410 728 2118 413 455 314 320 616
413 210 751 2203 1404 378 627 349 287 562
21 21 62 32 20 5 10 6 4 7
53 36 34 54 37 33 7 12 7 5 6
6 19 11 13 16
49 10 74 69 80 7 28 11 7 16
1446 808 2194 160 344 262 1245 183
1367 664 2697 196 483 383 1442 193
1277 729 3029 273 506 422 1552 276
207 133 218 12 26 15 146 19
154 113 272 16 39 27 174 16
126 99 233 15 38 24 129 27
109 90 287 30 52 30 141 34
2443 612
2483 780
2336 807
2373 937
480 179
503 217
503 191
408 242
298
337
438
420
118
111
153
108
264 47 10 199
312 35 16 241
395 42 23 208
365 29 33 176
38 2 6 71
40 6 7 76
32 6 2 61
31 6 5 42
494 41
521 40
656 68
695 95
71 2
95 2
98 6
139 14
20 84
20 39
22 41
27 59
7 7
11 1
6 5
6 5
3991 6287 321 625 226 126 82 212 2206 21 172
4251 6538 353 680 216 179 114 253 2235 34 187
4131 6353 332 691 218 187 118 205 2164 33 183
4012 4016 394 629 184 173 126 210 2076 44 176
838 1314 65 117 40 21 14 37 499 9 36
916 1444 74 145 45 26 13 49 529 4 31
933 1472 90 164 51 40 16 48 489 5 30
866 867 97 126 37 40 18 43 457 7 41
708 4700
742 4589
745 4252
714 3833
176 1215
202 1278
200 1179
203 1094
104
7
92
291
27
47
107 153 32
157 207 43 17
10 26 3 0
32 7 3
2869 1290 240 82 915 310 32
2719 1251 223 86 814 312 33
385 159 40 11 134 39 2
399 173 37 9 136 42 2
84 152
225
31 99 18 9
127 27 12
2713 1208 277 99 866 236 27
2905 1307 291 90 879 307 31
41 35 60 65
16 8
24
31 40 4
21 53 9 6
429 184 26 23 147 44 5
439 184 38 21 145 47 4
402
E.P. Simard et al. / Oral Oncology 50 (2014) 387–403
passive smoking has substantially declined over the past few decades in many economically developed countries, where the health hazards of smoking are well-recognized and tobacco prevention programs have long been established [25,26]. For example, in the United States, smoking prevalence peaked in the 1960s and has since declined [25]. These patterns may have contributed, at least in part, to the declines in incidence rates for oral cavity and other HNCs noted in the current study. Consistent with previous findings [7,8,16,27–29], rates of oral cavity cancer increased among men and women in some eastern and northern European countries where tobacco use remained common such as the Czech and Slovak Republics, Denmark, Estonia, and Finland. In addition, rates of oral cavity cancer increased among women only in a number of European nations, perhaps reflecting the delayed peak in smoking prevalence among women compared to men, as has been seen in other countries [25]. Rates of oral cavity and oropharyngeal cancer also increased in the United Kingdom and it has been suggested that these trends are largely driven by increases among individuals with low socioeconomic status (among whom smoking prevalence is elevated) [30]. In addition, the high rates of oral cavity cancer among men and women in India and other Asian countries are largely due to the consumption of betel quid which can result in exposure to carcinogenic tobacco-specific nitrosamines [31,32]. The important role of alcohol consumption with regards to HNC (oral cavity cancer) also deserves mention, specifically in Hungary and other central and eastern European countries where alcohol consumption has increased or stabilized at high levels [26,33]. In these regions, the type of alcohol consumed is important. For example, in some eastern European nations alcohol is derived from fruits (e.g., plums, peaches, and apricots) which are believed to contain acetaldehyde, a compound considered possibly carcinogenic to humans [28,32,34–37]. We also documented extremely high rates of all HNCs among men in France, underscoring the importance of understanding area-specific tobacco (and alcohol) consumption practices for HNC prevention and control. A previous study [38] found the overall increase in HNC rates in France was driven by increases in pharyngeal cancer (versus oral cavity alone) but our analysis using updated data showed broad increases across all three categories of HNC. Increasing HNC rates in these regions underscore the need for prevention programs that address not only tobacco, but also alcohol consumption. With regards to oropharyngeal cancers, the role of persistent HPV infection is rising in prominence in many economically developed countries where tobacco use has declined [1]. Globally, approximately 25% of oropharyngeal cancers are due to HPV infection [39] although this attribution is higher in some economically developed countries such as the United States where the figure exceeds 60% [6]. Similar to previous studies [4,40–45], the current analysis found increases in oropharyngeal sub-sites most often associated with HPV infection in the United States and Canada, as well as a number of other economically developed European countries such as Denmark and Sweden. In other countries where data is absent regarding the role of HPV in oropharyngeal cancer and where tobacco use remains common, the cases are likely due to tobacco. Additional, representative studies from other economically developed regions with data on the prevalence of HPV DNA in tumor blocks (or other markers) is needed to quantify the contribution of HPV infection to oropharyngeal cancers in these settings. Rates of HNC stratified by subtype warrant continued monitoring in countries undergoing economic transitions because of associated increases in the prevalence of cancer risk factors (e.g., tobacco use, energy imbalance, and HPV exposure) [26]. In terms of prevention, one recent study found a reduced prevalence of oral HPV infection after bivalent HPV vaccination, suggesting the
vaccine may have a protective effect against infections associated with oropharyngeal cancer risk [46]. The trends presented for the heterogeneous grouping of other HNCs also deserve brief comment. This category included mainly laryngeal cancers, for which the strongest risk factor is also tobacco use [47]. The country-specific incidence trends were generally similar to those of oral cavity cancers with rates increasing in some European countries such as Belarus, Estonia and Latvia and decreasing in countries where the tobacco epidemic was established first such as the United States and Canada [29]. It should be noted that alcohol consumption is also a risk factor for laryngeal cancer (as well as some other HNCs), although the effect is much smaller than that of tobacco use [47]. Nonetheless, the synergistic role of dual use (joint tobacco and alcohol consumption) results in higher laryngeal cancer risks than either alone. The role of diet and nutrition and body mass index (BMI) may also be important to consider in light of the current HNC trends. Diets rich in fruits and vegetables are generally associated with a decreased risk of HNCs [1,47]. It is possible that fruit and vegetable consumption may decrease in economically transitioning countries possibly attenuating declines in tobacco-associated HNCs. However, the precise role of diet and obesity in HNC etiology is unclear. Large pooled studies are needed to evaluate the contribution of various dietary practices to HNC while controlling for tobacco and alcohol consumption, as smokers tend to be leaner but also drink more than non-smokers [17]. With regards to BMI, one recent prospective study found no association between BMI and HNC incidence but additional studies in other countries are needed to clarify the complex relationship between smoking, alcohol, diet, BMI, and HNC incidence [18]. Strengths of this descriptive study include the use of high-quality population-based cancer registry data from a number of countries included in the IARC CI5 databases. By grouping HNCs into broad categories, we were able to describe incidence rates and trends in relation to underlying trends in causal risk factors such as tobacco and alcohol consumption and HPV infection. In addition, we present 5-year average annual rates and compare changes over time across broad calendar periods, avoiding the instability associated with comparing annual rates based on small sample sizes. Nonetheless, the study also has limitations. IARC incidence data are limited in their global coverage, and data from Africa, where the cancer burden is substantial, are notably scarce [48]. In addition, estimates of rates and trends within countries should also be interpreted with caution as they are usually based upon a small number of registries that may not accurately represent national-level data. Also, consistent histologic classification data for the majority of CI5 registries with regards to the other HNC category precluded a more detailed evaluation of trends for this site. While the most up-to-date data were used for this analysis, incident cases are only available through 2002. When new volumes of CI5 data are released an updated analysis will be necessary for more contemporary estimates of both rates and trends. We documented trends in HNC incidence rates by country, sex, and anatomic site. For many tobacco-related HNCs, incidence rates increased in countries where tobacco use remains common (e.g., in some European and Asian countries). In contrast, in areas where tobacco use has declined, rates of HPV-associated oropharyngeal cancer increased. Continued monitoring of HNC incidence trends is warranted as many countries undergo economic transition that may be associated with the acquisition of risk factor for HNC including tobacco and alcohol use as well as HPV exposure. Establishing tobacco control programs in many regions may aid in reversing the increasing HNC incidence trends noted in the current study.
E.P. Simard et al. / Oral Oncology 50 (2014) 387–403
Conflict of interest statement None declared. Appendix A See Table A1. Appendix B See Table B1. References [1] Mayne S, Morse D, Winn D. Cancers of the oral cavity and pharynx. In: Schottenfeld D, Fraumeni J, editors. Cancer epidemiology and prevention. New York: Oxford; 2006. p. 674–96. [2] Hashibe M, Brennan P, Chuang SC, et al. Interaction between tobacco and alcohol use and the risk of head and neck cancer: pooled analysis in the International Head and Neck Cancer Epidemiology Consortium. Cancer Epidemiol Biomarkers Prevent 2009;18(2):541–50. [3] Danaei G, Vander Hoorn S, Lopez AD, Murray CJ, Ezzati M, Comparative Risk Assessment collaborating g. Causes of cancer in the world: comparative risk assessment of nine behavioural and environmental risk factors. Lancet 2005;366(9499):1784–93. [4] Chaturvedi AK, Engels EA, Anderson WF, Gillison ML. Incidence trends for human papillomavirus-related and -unrelated oral squamous cell carcinomas in the United States. J Clin Oncol: Off J Am Soc Clin Oncol 2008;26(4):612–9. [5] Gillison ML, Alemany L, Snijders PJ, et al. Human papillomavirus and diseases of the upper airway: head and neck cancer and respiratory papillomatosis. Vaccine 2012;30(Suppl. 5):F34–54. [6] Gillison ML, Chaturvedi AK, Lowy DR. HPV prophylactic vaccines and the potential prevention of noncervical cancers in both men and women. Cancer 2008;113(10 Suppl):3036–46. [7] de Camargo Cancela M, de Souza DL, Curado MP. International incidence of oropharyngeal cancer: a population-based study. Oral Oncol 2012;48(6):484–90. [8] Warnakulasuriya S. Global epidemiology of oral and oropharyngeal cancer. Oral Oncol 2009;45(4–5):309–16. [9] International Agency for Research on Cancer. Cancer incidence in five continents, Vol. VI. Lyon, France: IARC Scientific Publications, No. 120; 1992. [10] International Agency for Research on Cancer. Cancer incidence in five continents, vol. VII. Lyon, France: IARC Scientific Publications, No. 143; 1997. [11] International Agency for Research on Cancer. Cancer incidence in five continents, vol. VIII. Lyon, France: IARC Scientific Publications, No. 155; 2002. [12] International Agency for Research on Cancer. Cancer incidence in five continents, vol. IX. Lyon, France: IARC Scientific Publications, No. 160; 2007. [13] World Health Organization. Manual of the international statistical classification of diseases, injuries, and causes of death. Geneva, Switzerland: World Health Organization; 1977 [9th Rev]. [14] World Health Organization. Manual of the international statistical classification of diseases, injuries, and causes of death. 2nd ed. Geneva, Switzerland: World Health, Organization; 2004 [10th Rev]. [15] Hashibe M, Brennan P, Benhamou S, et al. Alcohol drinking in never users of tobacco, cigarette smoking in never drinkers, and the risk of head and neck cancer: pooled analysis in the International Head and Neck Cancer Epidemiology Consortium. J Natl Cancer Inst 2007;99(10):777–89. [16] Curado MP, Hashibe M. Recent changes in the epidemiology of head and neck cancer. Curr Opin Oncol May 2009;21(3):194–200. [17] Gaudet MM, Olshan AF, Chuang SC, et al. Body mass index and risk of head and neck cancer in a pooled analysis of case-control studies in the International Head and Neck Cancer Epidemiology (INHANCE) Consortium. Int J Epidemiol Aug 2010;39(4):1091–102. [18] Gaudet MM, Patel AV, Sun J, et al. Prospective studies of body mass index with head and neck cancer incidence and mortality. Cancer Epidemiol Biomarkers Prevent 2012;21(3):497–503. [19] Sun EC, Curtis R, Melbye M, Goedert JJ. Salivary gland cancer in the United States. Cancer epidemiology, biomarkers & prevention: a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology 1999;8(12):1095–100. [20] Sun X, Tong LP, Wang YT, et al. Can global variation of nasopharynx cancer be retrieved from the combined analyses of IARC Cancer Information (CIN) databases? PloS one 2011;6(7):e22039.
403
[21] Segi M. Cancer mortality for selected sites in 24 countries (1950–57) Sendai. Japan: Department of Public Health, Tohoku University of Medicine; 1960. [22] Doll R, Cook P. Summarizing indices for comparison of cancer incidence data. Int J Cancer 1967;2(3):269–79. [23] International Agency for Research on Cancer. Cancer registration principles and methods. Lyon, France: IARC Scientific Publications, No. 95; 1991. [24] Devesa SS, Donaldson J, Fears T. Graphical presentation of trends in rates. Am J Epidemiol 1995;141(4):300–4. [25] Thun M, Peto R, Boreham J, Lopez AD. Stages of the cigarette epidemic on entering its second century. Tobacco Control Mar 2012;21(2):96–101. [26] Ezzati M, Riboli E. Behavioral and dietary risk factors for noncommunicable diseases. New Engl J Med 2013;369(10):954–64. [27] Boyle P, Ferlay J. Cancer incidence and mortality in Europe, 2004. Ann Oncol: Off J Eur Soc Med Oncol/ESMO 2005;16(3):481–8. [28] Garavello W, Bertuccio P, Levi F, et al. The oral cancer epidemic in central and eastern Europe. Int J Cancer 2010;127(1):160–71. [29] Sturgis EM, Cinciripini PM. Trends in head and neck cancer incidence in relation to smoking prevalence: an emerging epidemic of human papillomavirus-associated cancers? Cancer 2007;110(7):1429–35. [30] Conway DI, Stockton DL, Warnakulasuriya KA, Ogden G, Macpherson LM. Incidence of oral and oropharyngeal cancer in United Kingdom (1990–1999) – recent trends and regional variation. Oral Oncol 2006;42(6):586–92. [31] Nair U, Bartsch H, Nair J. Alert for an epidemic of oral cancer due to use of the betel quid substitutes gutkha and pan masala: a review of agents and causative mechanisms. Mutagenesis 2004;19(4):251–62. [32] International Agency for Research on Cancer. IARC monographs on carcinogenic risks to humans, Part E, vol. 100. Review of human carcinogens: personal habits and indoor combustions. Lyon, France: IARC Scientific Publications; 2009. [33] Bosetti C, Levi F, Lucchini F, Zatonski WA, Negri E, La Vecchia C. Worldwide mortality from cirrhosis: an update to 2002. J Hepatol May 2007;46(5):827–39. [34] Boffetta P, Hashibe M, La Vecchia C, Zatonski W, Rehm J. The burden of cancer attributable to alcohol drinking. Int J Cancer 2006;119(4):884–7. [35] Popova S, Rehm J, Patra J, Zatonski W. Comparing alcohol consumption in central and eastern Europe to other European countries. Alcohol Alcoholism 2007;42(5):465–73. [36] International Agency for Research on Cancer. IARC monograps on carcinogenic risks to humans, vol. 71. Re-evalution of some organic chemicals, hydrazine and hydrogen peroxide. Lyon, France: IARC Scientific Publications; 1999. [37] International Agency for Research on Cancer. IARC monographs on the evaluation of carcinogenic risks to humans, vol. 96. Alcohol consumption and ethyl carbamate. Lyon, France: IARC Scientific Publications; 2010. [38] Franceschi S, Bidoli E, Herrero R, Munoz N. Comparison of cancers of the oral cavity and pharynx worldwide: etiological clues. Oral Oncol Jan 2000;36(1):106–15. [39] de Martel C, Ferlay J, Franceschi S, et al. Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol Jun 2012;13(6):607–15. [40] Chaturvedi AK, Engels EA, Pfeiffer RM, et al. Human papillomavirus and rising oropharyngeal cancer incidence in the United States. J Clin Oncol: Off J Am Soc Clin Oncol 2011;29(32):4294–301. [41] Jemal A, Simard EP, Dorell C, et al. Annual Report to the Nation on the Status of Cancer, 1975–2009, featuring the burden and trends in human papillomavirus (HPV)-associated cancers and HPV vaccination coverage levels. J Natl Cancer Inst 2013;105(3):175–201. [42] Simard EP, Ward EM, Siegel R, Jemal A. Cancers with increasing incidence trends in the United States: 1999 through 2008. CA: Cancer J Clin 2012;January 4. [43] Johnson-Obaseki S, McDonald JT, Corsten M, Rourke R. Head and neck cancer in Canada: Trends 1992 to 2007. Otolaryngol – Head Neck Surg: Off J Am Acad Otolaryngol – Head Neck Surg 2012;February 10. [44] Blomberg M, Nielsen A, Munk C, Kjaer SK. Trends in head and neck cancer incidence in Denmark, 1978–2007: focus on human papillomavirus associated sites. Int J Cancer 2011;129(3):733–41. [45] Ramqvist T, Dalianis T. An epidemic of oropharyngeal squamous cell carcinoma (OSCC) due to human papillomavirus (HPV) infection and aspects of treatment and prevention. Anticancer Res May 2011;31(5):1515–9. [46] Herrero R, Quint W, Hildesheim A, et al. Reduced prevalence of oral human papillomavirus (HPV) 4 years after bivalent HPV vaccination in a randomized clinical trial in Costa Rica. PloS one 2013;8(7):e68329. [47] Olshan AF. Cancer of the larynx. In: Schottenfeld D, Fraumeni J, editors. Cancer epidemiology and prevention. New York: Oxford; 2006. p. 627–37. [48] Jemal A, Bray F, Forman D, et al. Cancer burden in Africa and opportunities for prevention. Cancer 2012;118(18):4372–84.
Contents lists available at ScienceDirect
Oral Oncology journal homepage: www.elsevier.com/locate/oraloncology
International trends in head and neck cancer incidence rates: Differences by country, sex and anatomic site Edgar P. Simard ⇑, Lindsey A. Torre, Ahmedin Jemal Surveillance and Health Services Research Program, American Cancer Society, Atlanta, GA, USA
a r t i c l e
i n f o
Article history: Received 31 October 2013 Received in revised form 16 January 2014 Accepted 26 January 2014 Available online 13 February 2014 Keywords: Epidemiology Global Head and neck cancer Human papillomavirus Incidence Larynx Mouth Oropharynx Oral cavity Trends
s u m m a r y Objective: To describe trends in country and sex-specific incidence rates of head and neck cancer (HNC), focusing on changes across calendar periods. Materials and MethodsMaterials and Methods: Sex and country specific rates of HNC were calculated for 1998–2002 and 1983–1987 using population-based registry data assembled by the Cancer Incidence in Five Continents (CI5) data system for 83 registries representing 35 countries. HNCs were categorized into three groups: oral cavity (including tongue and mouth), oropharynx (including tonsil and oropharynx) and other HNC (including larynx and poorly-specified tumors of the lip/oral cavity/pharynx). Age-standardized rates per 100,000 persons were calculated using the 1960 world standard population. Changes in rates between 1998–2002 and 1993–1987 were assessed. Results: During these periods there was substantial global variation in HNC incidence trends by cancer site, country/registry and sex. Rates of oral cavity cancer increased among men and women in some European and Asian countries (Czech Republic, Slovak Republic, Denmark, Estonia, Finland, the United Kingdom and Japan). In France and Italy, rates declined among men but increased among women. Oral cavity incidence rates declined among men and women in many Asian registries as well as in Canada and the United States. Oropharyngeal cancer rates increased among both men and women in a number of European countries (Belarus, Czech Republic, Denmark, Finland, Iceland, Latvia, Norway and the United Kingdom) whereas they declined in some Asian countries. The largest increase in oropharyngeal rates was among Brazilian men. Rates of other HNCs varied substantially by country and sex. Conclusion: From 1983–1987 to 1998–2002, trends in HNC rates differed by subtype, country and sex. Oral cavity cancer incidence rates increased in many countries with tobacco epidemics that are currently peaking and declined in areas where tobacco use peaked some time ago. In contrast, rates of oropharyngeal cancer increased in a number of countries where tobacco use has declined, perhaps due to the emerging importance of human papillomavirus infection. Continued monitoring of trends in incidence rates is needed to inform global cancer prevention strategies. Ó 2014 Elsevier Ltd. All rights reserved.
Introduction Cancers of the head and neck comprise a heterogeneous grouping of tumors at various anatomic sites with different etiologic factors. Tobacco exposure (either via active or passive smoking as well as consumption of smokeless tobacco) is the most important risk factor for head and neck cancers (HNCs) [1]. The fraction of HNC cases due to tobacco exposure likely varies across the globe. One recent pooled analysis of data from North America, Latin America and Europe found that tobacco exposure accounted for approximately 33% of HNC cases [2]. Alcohol exposure is also important ⇑ Corresponding author. Address: American Cancer Society, 250 Williams Street NW, Atlanta, GA 30303, USA. Tel.: +1 404 417 5935; fax: +1 404 321 4669. E-mail address: [email protected] (E.P. Simard). http://dx.doi.org/10.1016/j.oraloncology.2014.01.016 1368-8375/Ó 2014 Elsevier Ltd. All rights reserved.
in HNC etiology, and in the same study it accounted for approximately 4% of cases while the interaction between tobacco and alcohol accounted for almost three-fourths of HNCs [2]. Another recent study found differences in the joint hazard of smoking and alcohol consumption in relation to HNC (mouth and oropharyngeal cancer) deaths. Specifically, 42% of HNC deaths in low-income countries versus 80% in high-income countries were due to tobacco and alcohol use, likely reflecting different exposure patterns in relation to economic development status [3]. In addition, a series of recent studies in economically-developed nations have described the role of persistent infection with human papillomavirus (HPV) as an etiologic factor in the development of HNC (mainly restricted to the oropharynx, tonsils and base of the tongue) [4,5]. In some regions (i.e., North America, Australia, and Northern
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E.P. Simard et al. / Oral Oncology 50 (2014) 387–403
Table 1 Age-standardized oral cavity cancer (tongue & mouth; C01-06) incidence rates and rate ratios by sex among adults P 15 years, select registries. Males
Europe Eastern Europe Belarus Czech Republic Poland Cracow Warsaw City Russia (St Petersburg) Slovak Republic Northern Europe Denmark Estonia Finland Iceland Latvia Norway Sweden United Kingdom (4 registries) UK, Scotland Western Europe France (6 registries) Germany (Saarland) Switzerland (4 registries) The Netherlands Eindhoven Maastricht Southern Europe Italy (6 registries) Slovenia Spain (5 registries) Asia Eastern Asia China Hong Kong Shanghai Japan (5 registries) Southern Asia India Mumbai (Bombay) Chennai (Madras) South-Eastern Asia Philippines (Manila) Singapore Chinese Indian Malay Thailand (Chiang Mai) Western Asia Israel Jews Non-Jews Kuwait Kuwaitis Non-Kuwaitis North America Canada (9 registries) United States SEER (9 Registries): Black SEER (9 Registries): White South America Caribbean Martinique (France) Central America Costa Rica South America Brazil (Goiania) Colombia (Cali) Ecuador (Quito) Peru (Trujillo) Oceania Australia (6 registries)
Females
1983–1987
1998–2002
Rate ratio
(95% CI)
p Value
1983–1987
1998–2002
Rate ratio
(95% CI)
p Value
6.10 5.77
8.93 7.19
1.46 1.25
1.36 1.16
1.58 1.34
0.00 0.00
0.69 0.87
0.73 1.35
1.06 1.54
0.86 1.31
1.31 1.82
0.56 0.00
6.01 5.68 10.16 12.21
5.40 4.99 9.43 14.22
0.90 0.88 0.93 1.16
0.64 0.71 0.84 1.08
1.25 1.08 1.02 1.26
0.52 0.21 0.12 0.00
1.35 1.11 0.83
1.26 1.59 1.39 1.37
1.18 1.25 1.64
0.85 1.01 1.28
1.64 1.55 2.10
0.34 0.04 0.00
4.51 6.03 2.54 4.46 4.50 3.78 4.00 5.62
7.12 8.47 4.09 3.56 6.85 4.32 3.50 5.18 8.65
1.58 1.40 1.61
1.42 1.15 1.39
1.76 1.71 1.86
0.00 0.00 0.00
1.54 0.96 0.92 1.30 1.54
1.30 0.84 0.84 1.20 1.39
1.82 1.10 1.02 1.40 1.70
0.00 0.55 0.12 0.00 0.00
2.33 0.81 1.56 2.99 0.68 2.07 1.75 1.75 2.34
3.08 1.62 2.18 2.65 0.89 2.18 2.20 2.75 3.80
1.32 2.00 1.40 0.89 1.29 1.05 1.26 1.57 1.62
1.15 1.34 1.18 0.45 0.89 0.88 1.10 1.42 1.41
1.53 3.00 1.67 1.75 1.87 1.26 1.43 1.74 1.86
0.00 0.00 0.00 0.72 0.18 0.57 0.00 0.00 0.00
21.93 13.15 10.57
15.25 13.11 10.17
0.70 1.00 0.96
0.65 0.85 0.83
0.75 1.16 1.11
0.00 0.96 0.61
2.13 1.77 2.33
3.12 3.35 3.96
1.46 1.89 1.70
1.22 1.35 1.33
1.76 2.64 2.18
0.00 0.00 0.00
3.95 4.24
4.90 6.13
1.24 1.45
0.92 1.06
1.67 1.98
0.17 0.03
2.05 1.74
3.11 2.76
1.51 1.59
1.04 0.99
2.20 2.54
0.04 0.07
6.97 13.68 7.85
6.08 11.02 8.66
0.87 0.81 1.10
0.78 0.72 0.98
0.98 0.91 1.24
0.02 0.00 0.11
1.66 1.22 0.97
2.41 1.97 2.17
1.45 1.62 2.23
1.20 1.19 1.73
1.76 2.20 2.88
0.00 0.00 0.00
6.99 1.96 3.98
4.72 1.97 4.43
0.68 1.01 1.11
0.60 0.85 1.03
0.76 1.19 1.20
0.00 0.95 0.01
3.02 1.51 1.61
2.38 1.71 1.98
0.79 1.13 1.23
0.67 0.94 1.11
0.92 1.35 1.37
0.00 0.19 0.00
19.14 16.65
15.49 15.96
0.81 0.96
0.76 0.87
0.87 1.06
0.00 0.41
9.83 14.10
8.12 9.83
0.83 0.70
0.75 0.62
0.91 0.79
0.00 0.00
7.99
5.30
0.66
0.54
0.81
0.00
9.19
3.97
0.43
0.36
0.53
0.00
5.35 14.73
4.64 6.43 2.83 5.95
0.87 0.44
0.69 0.27
1.09 0.71
0.21 0.00
1.42
1.78 6.08
1.26
0.89
1.78
0.22
0.53
0.40
0.68
0.00
5.44
3.59
0.66
0.48
0.90
0.01
2.64 2.49
1.21
0.07
1.77
1.59
0.89
0.71
1.13
0.34
11.33
2.18
0.98
1.49
2.83
2.13
0.75
0.37
1.55
0.44
7.08
5.70
0.80
0.76
0.85
0.00
3.22
2.92
0.91
0.84
0.97
0.01
14.61 8.92
9.65 7.16
0.66 0.80
0.58 0.76
0.76 0.84
0.00 0.00
4.49 4.32
3.31 3.41
0.74 0.79
0.60 0.74
0.91 0.84
0.00 0.00
14.10
9.93
0.70
0.50
0.98
0.04
1.67
3.56
2.69
0.76
0.56
1.02
0.06
1.74
1.27
0.73
0.48
1.10
0.11
0.22 0.07
2.66 2.81 1.35 2.54
1.16
0.80
1.69
0.45
1.07
0.98
1.17
0.16
9.72 3.67
7.01
12.73 2.57 1.01 3.44
1.31 0.70
6.32
0.90
0.88 0.47
1.96 1.05
2.42
0.85
0.96
0.00
Source: Cancer Incidence in Five Continents. Incidence rates per 100,000 population, age-standardized to the 1960 standard world population. Abbreviation: 95% CI, 95% confidence interval. Rate ratio comparing 1998–2002 to 1983–1987. Significant rate ratios in bold. Rates not reported if the numerator included fewer than 16 cases.
2.82
3.01
E.P. Simard et al. / Oral Oncology 50 (2014) 387–403
389
Figure 1. Trends in oral cavity cancer incidence rates in select countries by sex (Cancer Incidence in Five Continents, 1983–2002). Notes: Rates are displayed on the log scale. Rates not reported if numerator included fewer than 16 cases. Registries without data for all four time periods are not displayed. Oral cavity includes tongue and mouth.
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Table 2 Age-standardized oropharynx cancer (tonsil and oropharynx; C09-10) incidence rates and rate ratios by sex among adults P 15 years, select registries. Males
Europe Eastern Europe Belarus Czech Republic Poland Cracow Warsaw City Russia (St Petersburg) Slovak Republic Northern Europe Denmark Estonia Finland Iceland Latvia Norway Sweden United Kingdom (4 registries) UK, Scotland Western Europe France (6 registries) Germany (Saarland) Switzerland (4 registries) The Netherlands Eindhoven Maastricht Southern Europe Italy (6 registries) Slovenia Spain (5 registries) Asia Eastern Asia China Hong Kong Shanghai Japan (5 registries) Southern Asia India Mumbai (Bombay) Chennai (Madras) South-Eastern Asia Philippines (Manila) Singapore Chinese Indian Malay Thailand (Chiang Mai) Western Asia Israel Jews Non-Jews Kuwait Kuwaitis Non-Kuwaitis North America Canada (9 registries) United States SEER (9 Registries): Black SEER (9 Registries): White South America Caribbean Martinique (France) Central America Costa Rica South America Brazil (Goiania) Colombia (Cali) Ecuador (Quito) Peru (Trujillo) Oceania Australia (6 registries)
Females
1983–1987
1998–2002
Rate ratio
(95% CI)
p Value
1983–1987
1998–2002
Rate ratio
(95% CI)
p Value
1.00 2.55
4.75 4.36
4.74 1.71
4.11 1.54
5.47 1.90
0.00 0.00
0.15 0.41
0.23 0.72
1.50 1.73
1.00 1.37
2.26 2.19
0.05 0.00
1.45 3.25 1.21 5.41
2.64 3.57 3.43 8.63
1.82 1.10 2.84 1.60
1.07 0.85 2.30 1.43
3.10 1.41 3.50 1.78
0.04 0.47 0.00 0.00
0.68 0.33 0.37
1.15 0.39 0.41
1.69 1.17 1.12
1.11 0.80 0.74
2.58 1.73 1.69
0.02 0.42 0.59
1.90 3.21 0.60
3.81 4.21 1.22
2.00 1.31 2.04
1.72 1.00 1.54
2.34 1.73 2.72
0.00 0.05 0.00
0.64 0.44 0.18
1.45 0.40 0.34
2.26 0.90 1.91
1.75 0.45 1.19
2.92 1.80 3.07
0.00 0.77 0.01
1.24 1.09 1.05 1.26 1.07
3.21 2.06 1.81 2.13 2.44
2.59 1.89 1.72 1.70 2.28
1.95 1.50 1.46 1.50 1.86
3.45 2.39 2.03 1.92 2.80
0.00 0.00 0.00 0.00 0.00
0.30 0.46 0.43 0.43 0.34
0.42 0.68 0.80 0.65 0.78
1.38 1.48 1.87 1.52 2.28
0.78 1.02 1.45 1.23 1.62
2.42 2.15 2.41 1.87 3.20
0.27 0.04 0.00 0.00 0.00
13.68 3.42 5.43
9.43 6.42 5.89
0.69 1.88 1.08
0.63 1.45 0.89
0.76 2.43 1.32
0.00 0.00 0.43
0.74 0.76 1.05
1.48 1.21 1.68
2.01 1.59 1.60
1.50 0.92 1.10
2.69 2.76 2.33
0.00 0.10 0.02
1.31 2.13
2.18 2.99
1.67 1.41
1.04 0.91
2.67 2.18
0.05 0.15
0.67 0.84
3.13 9.45 2.02
2.80 8.20 2.41
0.89 0.87 1.20
0.75 0.75 0.95
1.06 1.00 1.51
0.21 0.05 0.14
0.59 0.54 0.31
0.57 0.99 0.19
0.97 1.84 0.61
0.67 1.17 0.31
1.40 2.90 1.22
0.86 0.01 0.15
1.63 0.48 0.68
1.25 0.38 1.33
0.77 0.78 1.95
0.61 0.54 1.67
0.97 1.11 2.28
0.02 0.17 0.00
0.48 0.33 0.16
0.26 0.15 0.18
0.54 0.48 1.15
0.34 0.29 0.80
0.84 0.77 1.63
0.00 0.00 0.46
4.68 2.42
2.82 3.58
0.60 1.48
0.52 1.17
0.70 1.87
0.00 0.00
0.98 0.60
0.61 0.52
0.62 0.86
0.44 0.50
0.87 1.48
0.00 0.58
0.96
0.93
0.97
0.59
1.59
0.91
1.02
0.62
0.61
0.36
1.02
0.05
0.94
0.32
0.55
0.26
1.16
0.08
1.53
1.55
1.01
0.68
1.51
3.70
2.14
0.58
0.37
0.91
0.01
1.06
0.58
2.05
1.23
3.40
0.01
0.28
0.57
0.18
1.98
2.36
1.19
1.08
1.31
0.00
0.79
0.70
0.89
0.76
1.03
0.12
6.48 2.39
4.93 2.90
0.76 1.21
0.62 1.11
0.93 1.32
0.01 0.00
1.55 0.96
0.95 0.73
0.61 0.77
0.42 0.66
0.90 0.89
0.01 0.00
8.83
6.93
0.78
0.52
1.18
0.24
0.98
1.07
1.10
0.66
1.84
0.72
4.56 1.20
2.47
2.46
0.76
0.66
0.86
0.71
1.04
0.13
0.99
0.90
1.10
0.92
Source: Cancer Incidence in Five Continents. Incidence rates per 100,000 population, age-standardized to the 1960 standard world population. Abbreviation: 95% CI, 95% confidence interval. Rate ratio comparing 1998–2002 to 1983–1987. Significant rate ratios in bold. Rates not reported if the numerator included fewer than 16 cases.
E.P. Simard et al. / Oral Oncology 50 (2014) 387–403
391
Figure 2. Trends in tonsil and oropharynx cancer incidence rates in select countries by sex (Cancer Incidence in Five Continents, 1983–2002). Notes: Rates are displayed on the log scale. Rates not reported if numerator included fewer than 16 cases. Registries without data for all four time periods are not displayed. Oropharynx includes tonsils and oropharynx.
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Europe) HPV may be responsible for more than 60% of HNC cases at these specific sub-sites [6]. While previous studies have described trends in HNC incidence rates at the country or regional level [7,8], we sought to describe trends in rates internationally with a focus on differences by anatomic sub-site and sex. As more precise estimates of the contribution of various risk factors to HNC emerge at the country-level such an evaluation of HNC incidence trends would inform both clinicians treating patients as well as cancer prevention and control programs with regards to areas that warrant focused attention and intervention.
Methods Incident HNC cases among individuals aged 15 years or greater were obtained from the International Agency for Research on Cancer’s (IARCs) Cancer Incidence in Five Continents (CI5) databases. Volumes 6 [9] (including cancers diagnosed during 1983–1987), 7 [10] (1988–1992), 8 [11] (1993–1987), and 9 [12] (1998–2002) of CI5 were used to obtain country and/or registry level data for different HNC sub-sites for males and females separately (the different years of data contributing from each registry are shown in Appendix A). Data from 85 population-based cancer registries with high-quality data representing 37 countries were used in the current analysis. In order to describe HNC rates and changes in rates over time and across countries, we focused on incidence rates reported during two combined calendar periods: 1983–1987 (from CI5 volume 6) and 1998–2002 (from CI5 volume 9). HNC cases reported from local registries were coded using combinations of International Classification of Diseases (ICD) codes (versions 7–10) and International Classification of Diseases for Oncology (ICD-O, versions 1–3) [11,12]. To allow for comparisons between registries over time, cases were converted to ICD-9 [13] (used during 1979–1988) and ICD-10 [14] (used from 1999 onwards). Invasive HNC cases (of any histology) were categorized into three broad groups using information regarding anatomic site available across CI5 volumes based on their different etiologic risk factors. Oral cavity cancers included cancers of the tongue and mouth (ICD-9 codes 141 and 143-5 and ICD-10 codes C01-02 and C03-06) and were considered in large part to be associated with tobacco and alcohol use. Oropharyngeal cancers included the tonsils and oropharynx (ICD-9 code 146 and ICD-10 codes C09-10) and were considered to be associated with HPV infection, in addition to tobacco and alcohol use. The last category was other HNCs which included poorly-defined tumors of the lip/oral cavity/pharynx (ICD-9 code 149 and ICD-10 code C14), the hypopharynx (ICD-9 code 148 and ICD-10 codes C12-13) as well as the larynx (ICD-9 code 161 and ICD-10 code C32). Consistent with prior HNC studies [15–18], tumors of the salivary gland, nasal cavity and sinuses and nasopharynx were excluded because they have different etiologic associations and incidence trends [19,20]. Five-year average annual incidence rates for the three categories of HNC were calculated during the two calendar periods (1983–1987 and 1998–2002) for each registry and sex (cancer counts and corresponding population estimates are provided in aggregate by IARC although annual data may not be available for every registry during every 5-year period). In instances where data from multiple regional registries were available for an economically developed country, registry specific data were aggregated to obtain a national estimate so as to simplify the interpretation of trends for multiple registries and countries. This was done for the United Kingdom (n = 4 registries), France (n = 6), Switzerland (n = 4), Italy (n = 6), Spain (n = 5), Canada (n = 9), Australia (n = 6), and Japan (n = 5). The United States also aggregates nine registries
by black and white race. For the other countries either a national registry was available or data from one or more registries are provided at the registry-level. HNC incidence rates were age-standardized to the 1960 world standard population using the Segi method [21] as modified by Doll [22] by 5-year age increments (15–19, 20–24, . . ., 80–84, 85+) to account for the different age structures across and within countries over the study period [22]. To assess changes in rates the rate ratio (RR) was calculated with corresponding 95% confidence intervals (95% CIs) as the ratio of rates during 1998–2002 divided by those during 1983–1987 [23]. A two-sided Z-test was calculated to evaluate the significance of the RR with a corresponding P-value and P-values less than 0.05 were considered statistically significant. Sex-specific HNC rates are also presented graphically on the log scale for selected countries/registries with noteworthy trends for the entire study period using CI5 data from volumes 6–9 (covering years 1983–1987, 1988–1992, 1993–1997, 1998–2002, respectively) [24]. For stability and reliability, rates were not reported if the numerator contained fewer than 16 cases (numerators for all rates are shown in Appendix B). All analyses were conducted SAS version 9.3 (SAS Institute, Cary, North Carolina).
Results Changes in HNC incidence rates from 1983–1987 to 1998–2002 varied substantially across countries for both men and women for all of the major HNC categories (oral cavity, oropharynx and other HNC). Oral cavity cancer rates increased among both men and women in 7 out of 37 countries located in Europe and Asia (Czech Republic, Slovak Republic, Denmark, Estonia, Finland, the United Kingdom and Japan) (Table 1 and Fig. 1). The largest increases were among men in Finland (RR = 1.61, 95% CI: 1.39–1.86) and women in Spain (RR = 2.23, 95% CI: 1.73–2.88). Oral cavity cancer rates decreased for men and women in 6 countries (China [Hong Kong registry], India [Mumbai registry], Philippines, Thailand, Canada and the United States). The greatest decrease among men was in the Indian registry in Singapore (RR = 0.44, 95% CI: 0.27–0.71) and among women in the Philippines (RR = 0.43, 95% CI: 0.36–0.53). Oral cavity cancer rates were stable in many South American registries (except in Martinique where rates decreased by 30% among men). In Australia, rates were stable among women but decreased by 10% among men. The first and second-highest oral cavity cancer rates in 1998–2002 among both men (15.96, 15.49) and women (9.83, 8.12) were in the two Indian registries with available data: Chennai and Mumbai, respectively. Rates were also elevated among men in France (15.25). Rates were generally more than two-times as high among men versus women, except notably in the Slovak Republic and Belarus where rates were more than 10-fold higher among men versus women. Approximately two-thirds of oropharyngeal cancers were located in the tonsil and the remaining in the oropharynx. During 1983–1987 and 1998–2002, rates of oropharyngeal cancer increased among men and women in 7 countries (Belarus, Czech Republic, Denmark, Finland, Norway, Sweden, and the United Kingdom) (Table 2 and Fig. 2). While oropharyngeal cancer rates decreased among men in France (RR = 0.69, 95% CI: 0.63–0.76), they increased among women (RR = 2.01, 95% CI: 1.50–2.69). Oropharyngeal cancer rates also decreased among men and women in China (Hong Kong) and India (Mumbai). In other global regions the trends differed by sex. For example, rates increased among men only in India (Chennai), Germany, Japan, and Canada. In the United States, the increase in oropharyngeal cancer rates was restricted to white men (RR = 1.21, 95% CI: 1.11–1.32) whereas rates significantly decreased among black men and white and
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Table 3 Age-standardized other head and neck cancer (pyriform sinus, hypopharnyx, lip/oral cavity/pharynx not otherwise specified, and larynx; C12-14, 32) incidence rates and rate ratios by sex among adults P 15 years, select registries. Males
Europe Eastern Europe Belarus Czech Republic Poland Cracow Warsaw City Russia (St Petersburg) Slovak Republic Northern Europe Denmark Estonia Finland Iceland Latvia Norway Sweden United Kingdom (4 registries) UK, Scotland Western Europe France (6 registries) Germany (Saarland) Switzerland (4 registries) The Netherlands Eindhoven Maastricht Southern Europe Italy (6 registries) Slovenia Spain (5 registries) Asia Eastern Asia China Hong Kong Shanghai Japan (5 registries) Southern Asia India Mumbai (Bombay) Chennai (Madras) South-Eastern Asia Philippines (Manila) Singapore Chinese Indian Malay Thailand (Chiang Mai) Western Asia Israel Jews Non-Jews Kuwait Kuwaitis Non-Kuwaitis North America Canada (9 registries) United States SEER (9 Registries): Black SEER (9 Registries): White South America Caribbean Martinique (France) Central America Costa Rica South America Brazil (Goiania) Colombia (Cali) Ecuador (Quito) Peru (Trujillo) Oceania Australia (6 registries)
Females
1983–1987
1998–2002
Rate ratio
(95% CI)
p Value
1983–1987
1998–2002
Rate ratio
(95% CI)
p Value
14.89 12.89
18.93 11.93
1.27 0.93
1.21 0.88
1.34 0.98
0.00 0.00
0.73 0.83
0.34 1.09
0.46 1.31
0.36 1.10
0.60 1.56
0.00 0.00
19.11 17.41 16.56 20.14
14.81 13.15 13.95 20.71
0.77 0.76 0.84 1.03
0.64 0.67 0.78 0.97
0.94 0.85 0.91 1.10
0.01 0.00 0.00 0.38
1.45 2.47 0.62 0.86
2.37 2.07 0.63 0.91
1.64 0.84 1.01 1.06
0.99 0.63 0.75 0.80
2.71 1.10 1.35 1.40
0.07 0.20 0.96 0.70
9.19 12.73 6.98 4.85 13.30 6.41 5.06 7.83 9.53
8.84 15.18 4.52 5.59 15.20 5.43 3.88 7.74 11.94
0.96 1.19 0.65 1.15 1.14 0.85 0.77 0.99 1.25
0.89 1.04 0.58 0.67 1.03 0.76 0.70 0.94 1.16
1.05 1.37 0.73 1.99 1.27 0.95 0.84 1.05 1.35
0.36 0.01 0.00 0.61 0.01 0.00 0.00 0.70 0.00
2.16 0.63 0.72
1.96 0.75 0.50
0.91 1.19 0.69
0.77 0.69 0.51
1.08 2.07 0.94
0.27 0.53 0.02
0.93 0.69 0.74 1.95 2.41
0.61 0.94 0.77 1.69 2.83
0.66 1.36 1.04 0.86 1.18
0.45 1.01 0.84 0.78 1.01
0.97 1.84 1.29 0.96 1.36
0.03 0.05 0.73 0.01 0.03
33.81 15.35 16.31
22.69 13.67 12.78
0.67 0.89 0.78
0.63 0.77 0.69
0.71 1.03 0.89
0.00 0.11 0.00
1.24 1.24 1.51
1.70 1.88 2.12
1.37 1.52 1.40
1.07 0.98 1.01
1.75 2.36 1.94
0.01 0.07 0.05
9.39 10.12
9.75 10.17
1.04 1.00
0.85 0.80
1.27 1.26
0.71 0.97
1.32 1.29
1.57 1.65
1.19 1.28
0.72 0.72
1.99 2.25
0.50 0.42
22.35 17.72 23.92
14.36 16.03 23.15
0.64 0.90 0.97
0.60 0.82 0.90
0.69 1.00 1.04
0.00 0.05 0.36
1.42 1.07 0.47
1.08 1.29 0.67
0.76 1.20 1.42
0.59 0.84 0.92
0.98 1.70 2.19
0.03 0.31 0.13
16.19 4.40 6.87
8.52 4.41 6.63
0.53 1.00 0.96
0.49 0.90 0.91
0.57 1.12 1.03
0.00 0.97 0.24
1.93 0.87 0.69
0.61 0.41 0.53
0.32 0.47 0.76
0.25 0.36 0.63
0.41 0.63 0.92
0.00 0.00 0.00
27.93 15.11
16.66 15.00
0.60 0.99
0.56 0.89
0.64 1.10
0.00 0.89
6.11 4.15
2.89 3.81
0.47 0.92
0.41 0.75
0.55 1.12
0.00 0.40
10.23
9.81
0.96
0.82
1.12
0.60
3.42
1.96
0.57
0.43
0.76
0.00
10.77 15.87
0.81 0.35
0.69 0.20
0.96 0.60
0.01 0.00
1.24
0.55
0.44
0.26
0.75
0.00
17.54
8.73 5.49 5.35 6.58
0.38
0.30
0.48
0.00
5.19
1.46
0.28
0.18
0.44
0.00
7.60 6.96
7.09 9.45
0.93 1.36
0.83 0.95
1.05 1.95
0.25 0.11
1.22
0.91
1.64
0.19
4.29 18.78
4.37 5.09
1.02 0.27
0.57 0.14
1.83 0.52
10.86
7.39
0.68
0.65
22.63 12.67
15.81 8.31
0.70 0.66
16.08
13.12
7.50 10.92 8.17 3.15
10.52
0.95
1.16
0.95 0.00
0.71
0.00
2.04
1.44
0.70
0.64
0.78
0.00
0.63 0.63
0.78 0.69
0.00 0.00
4.65 2.85
3.50 2.07
0.75 0.73
0.61 0.67
0.93 0.79
0.01 0.00
0.82
0.61
1.10
0.17
1.83
5.95
0.79
0.64
0.98
0.02
1.14
0.42
0.37
0.19
0.71
0.00
16.12 8.63 2.32 2.83
1.48 1.06 0.73
1.03 0.83 0.40
2.11 1.35 1.34
0.06 0.67 0.28
1.63
1.73 1.78
1.09
0.68
1.76
0.72
7.34
0.70
1.31
1.03
0.79
0.68
0.91
0.00
0.66
0.74
0.00
Source: Cancer Incidence in Five Continents. Incidence rates per 100,000 population, age-standardized to the 1960 standard world population. Abbreviation: 95% CI, 95% confidence interval. Rate ratio comparing 1998–2002 to 1983–1987. Significant rate ratios in bold. Rates not reported if the numerator included fewer than 16 cases.
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Figure 3. Trends in other head and neck cancer incidence rates in select countries by sex (Cancer Incidence in Five Continents, 1983–2002). Notes: Rates are displayed on the log scale. Rates not reported if numerator included fewer than 16 cases. Registries without data for all four time periods are not displayed. Other head and neck includes hypopharnyx, lip/oral cavity/pharnyx not otherwise specified, and larynx.
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E.P. Simard et al. / Oral Oncology 50 (2014) 387–403 Table A1 Years of data by volume and registry, Cancer Incidence in Five Continents.
Europe Eastern Europe Belarus Czech Republic Poland Cracow Warsaw City Russia (St Petersburg) Slovak Republic Northern Europe Denmark Estonia Finland Iceland Latvia Norway Sweden United Kingdom (4 registries) Merseyside and Cheshire North Western Oxford Region West Midlands UK, Scotland Western Europe France (6 registries) Bas-Rhin Calvados Doubs Isere Somme Tarn Germany (Saarland) Switzerland (4 registries) Geneva Neuchatel St Gall-Appenzell Vaud The Netherlands Eindhoven Maastricht Southern Europe Italy (6 registries) Genoa Province Florence and Prato Parma Province Ragusa Province Torino Varese Province Slovenia Spain (5 registries) Granada Murcia Navarra Tarragona Zaragoza Asia Eastern Asia China Hong Kong Shanghai Japan (5 registries) Hiroshima Miyagi Prefecture Nagasaki Prefecture Osaka Prefecture Yamagata Prefecture Southern Asia India Mumbai (Bombay) Chennai (Madras) South-Eastern Asia Philippines (Manila) Singapore Chinese
Vol. 6
Vol. 7
Vol. 8
Vol. 9
1983–1987 1983–1987
1988–1992 1988–1992
1993–1997 1993–1997
1998–2002 1998–2002
1983–1986 1983–1987 1983–1987 1983–1987
1988–1992 1989–1992 – 1988–1992
1993–1997 1993–1997 1994–1997 1993–1997
1998–2002 1998–2002 1998–2002 1998–2002
1983–1987 1983–1987 1982–1986 1983–1987 1983–1987 1983–1987 1983–1987
1988–1992 1988–1992 1987–1992 1988–1992 1988–1992 1988–1992 1988–1992
1993–1997 1993–1997 1993–1997 1993–1997 1993–1997 1993–1997 1993–1997
1998–2002 1998–2002 1998–2002 1998–2002 1998–2002 1998–2002 1998–2002
1983–1987 1983–1987 1983–1987 1983–1986 1983–1987
1988–1992 1988–1992 1988–1992 1988–1992 1988–1992
1993–1997 1993–1997 1993–1997 1993–1997 1993–1997
1998–2002 1998–2002 1998–2002 1998–2002 1998–2002
1983–1987 1983–1987 1983–1987 1983–1987 1983–1984 1983–1987 1983–1987
1988–1992 1988–1992 1988–1992 1988–1992 1988–1992 1988–1992 1988–1992
1993–1997 1993–1997 1993–1997 1993–1997 1993–1997 1993–1997 1993–1997
1998–2002 1998–2002 1998–2002 1998–2002 1998–2002 1998–2002 1998–2002
1983–1987 1983–1987 1983–1987 1983–1987
1988–1992 1988–1992 1988–1992 1988–1992
1993–1997 1993–1996 1993–1997 1993–1996
1998–2002 1998–2002 1998–2002 1998–2002
1983–1987 1986–1988
1988–1992 1988–1992
1993–1997 1993–1997
1998–2002 1998–2002
1986–1987 1985–1987 1983–1987 1983–1987 1985–1987 1983–1987 1982–1987
1988–1992 1988–1991 1988–1992 1988–1992 1988–1991 1988–1992 1988–1992
1993–1996 1993–1997 1993–1997 1993–1997 1993–1997 1993–1997 1993–1997
1998–2000 1998–2002 1998–2002 1998–2002 1998–2002 1998–2000 1998–2002
1985–1987 1984–1987 1983–1986 1984–1987 1983–1985
1988–1992 1988–1992 1987–1991 1988–1992 1986–1990
1993–1997 1993–1996 1993–1997 1993–1997 1991–1995
1998–2002 1997–2001 1998–2002 1998–2001 1996–2000
1983–1987 1983–1987
1988–1992 1988–1992
1993–1997 1993–1997
1998–2002 1998–2002
1981–1985 1983–1987 1983–1987 1983–1987 1983–1986
1986–1990 1988–1992 1988–1992 1988–1992 1988–1992
1991–1995 1993–1997 1993–1997 1993–1997 1993–1997
1996–2000 1998–2002 1998–2002 1998–2002 1998–2002
1983–1987 1983–1987
1988–1992 1988–1992
1993–1997 1993–1997
1998–2002 1998–2002
1983–1987
1988–1992
1993–1997
1998–2002
1983–1987
1988–1992
1993–1997
1998–2002 (continued on next page)
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Table A1 (continued)
Indian Malay Thailand (Chiang Mai) Western Asia Israel Jews Non-Jews North America Canada (9 registries) Alberta British Columbia Manitoba New Brunswick Newfoundland and Labrador Nova Scotia Ontario Prince Edward Island Saskatchewan United States SEER (9 Registries): Black SEER (9 Registries): White South America Caribbean Martinique (France) Central America Costa Rica South America Brazil (Goiania) Colombia (Cali) Ecuador (Quito) Peru (Trujillo) Oceania Australia (6 registries) New South Wales South Tasmania Victoria Western Capital Territory
Vol. 6
Vol. 7
Vol. 8
Vol. 9
1983–1987 1983–1987 1983–1987
1988–1992 1988–1992 1988–1992
1993–1997 1993–1997 1993–1997
1998–2002 1998–2002 1998–2002
1982–1986 1982–1986
1988–1992 1988–1992
1993–1997 1993–1997
1998–2002 1998–2002
1983–1987 1983–1987 1983–1987 1983–1986 1983–1987 1983–1987 1983–1987 1983–1987 1983–1987
1988–1992 1988–1992 1988–1992 1988–1992 1988–1992 1988–1992 1988–1992 1988–1992 1988–1992
1993–1997 1993–1997 1993–1997 1993–1997 1993–1997 1993–1997 1993–1997 1993–1997 1993–1997
1998–2002 1998–2002 1998–2002 1998–2002 1998–2002 1998–2002 1998–2002 1998–2002 1998–2002
1983–1987 1983–1987
1988–1992 1988–1992
1993–1997 1993–1997
1998–2002 1998–2002
1983–1987
–
1993–1997
1998–2002
1984–1987
1988–1992
1995–1996
1998–2002
1988–1989 1982–1986 1985–1987 1984–1987
1990–1993 1987–1991 1988–1992 1988–1990
1995–1998 1992–1996 1993–1997 –
1999–2002 1998–2002 1998–2002 1998–2002
1983–1987 1983–1987 1983–1987 1983–1987 1983–1987 1983–1987
1988–1992 1988–1992 1988–1992 1988–1992 1988–1992 1988–1992
1993–1997 1993–1997 1993–1997 1993–1997 1993–1997 1993–1997
1998–2002 1998–2002 1998–2002 1998–2002 1998–2002 1998–2002
black women. During 1998–2002 oropharyngeal cancer rates were highest among men in France (9.43) and among women in Switzerland (1.68). Generally, oropharyngeal cancer rates were 2–5 times as high among men compared to women, except in Belarus and the Slovak Republic where the sex disparity was more than 20-fold. With respect to rates and trends of other HNC (which included poorly-defined tumors of the lip/oral cavity/pharynx as well as the hypopharynx and larynx), they reflect patterns of laryngeal cancer which accounted for more than two-thirds of the cases during 1983–1987 and 1998–2002. Trends in other HNC incidence rates varied during 1983–1987 and 1998–2002 by country/registry and sex (Table 3 and Fig. 3). Incidence rates increased for both men and women in the United Kingdom (Scotland registry only) whereas they decreased for both sexes in 10 countries (Finland, Italy, China [Hong Kong], India [Mumbai], Singapore [Chinese], Thailand [Chang Mai], Canada, United States, Costa Rica, and Australia). The largest increase in rates between 1983–1987 and 1998–2008 among men occurred in Belarus (RR = 1.27, 95% CI: 1.21–1.34) and among women occurred in Switzerland (RR = 1.40, 95% CI: 1.01–1.94). Whereas the largest decreases were among non-Kuwaiti men in Kuwait (RR = 0.27, 95% CI: 0.14–0.52) and among women in Thailand (RR = 0.28, 95% CI: 0.18–0.44). Rates of other HNCs during 1998–2002 were highest among men in Spain (23.15) and France (22.69) and among women in the Indian registry of Chennai (3.81) and among black women in the United States (3.50). Rates of other HNC were generally at least
five-fold higher among men compared to women, with notable exceptions in Belarus and Spain where they were more than 50- and 30-times as high in men versus women, respectively. Discussion This analysis of international variations in HNC incidence rates documents significant heterogeneity in trends by sub-site, country and sex. Rates of oral cavity cancer increased among both men and women in a number of European countries but were stable or decreased in a number of Asian countries and rates decreased for men and women in Canada and the United States. Rates of oropharyngeal cancer also increased among both men and women in a number of European nations. These trends were concentrated mainly among eastern (Belarus, Czech Republic) and some northern European nations (the United Kingdom, Denmark, Estonia, Finland, Latvia, Norway, Sweden) as well as some Asian countries (Japan and India [Chennai]). In contrast, oropharyngeal cancer rates declined among men and women in China (Hong Kong) and India (Mumbai). For other HNCs (mainly of the larynx), incidence rates declined for men and women in nine countries and trends varied by sex in other areas. The different trends in incidence rates across countries by HNC sub-site and sex likely reflect differences in the prevalence of known HNC risk factors. Tobacco use is the strongest HNC risk factor, especially for oral cavity and other HNCs. Exposure to this carcinogen via active or
397
E.P. Simard et al. / Oral Oncology 50 (2014) 387–403
Table B1 Number of cases by sex, registry, and volume of Cancer Incidence in Five Continents. Males
Oral cavity (C01-06) Europe Eastern Europe Belarus Czech Republic Poland Cracow Warsaw City Russia (St Petersburg) Slovak Republic Northern Europe Denmark Estonia Finland Iceland Latvia Norway Sweden United Kingdom (4 registries) Merseyside and Cheshire North Western Oxford Region Trent West Midlands UK, Scotland Western Europe France (6 registries) Bas-Rhin Calvados Doubs Isere Somme Tarn Germany (Saarland) Switzerland (4 registries) Geneva Neuchatel St Gall-Appenzell Vaud The Netherlands Eindhoven Maastricht Southern Europe Italy (6 registries) Genoa Province Florence and Prato Parma Province Ragusa Province Romagna Region Torino Varese Province Slovenia Spain (5 registries) Basque Country Granada Murcia Navarra Tarragona Zaragoza Asia Eastern Asia China Hong Kong Shanghai Japan (5 registries) Hiroshima Miyagi Prefecture Nagasaki Prefecture Osaka Prefecture Yamagata Prefecture
Females
Vol. 6
Vol. 7
Vol. 8
Vol. 9
Vol. 6
Vol. 7
Vol. 8
Vol. 9
1019 1196
1620 1318
1803 1553
1742 1722
191 270
275 323
215 374
225 420
64 190 845 1095
61 143
82 196 817 1554
88 193 901 1506
11 73 167 103
17 57
30 87 202 168
31 85 226 188
961 250 535 22 350 480 883 1871 360 678 261 601 572 1089
391 36 249 18 55 299 537 707 145 227 117 224 218 385
422 58 359 17 61 300 626 800 148 231 125 296 468
484 60 408 27 82 337 669 968 167 303 155 294 343 557
535 82 393 24 78 333 690 1226 211 384 205 393 426 614
1383
121
537 165 252 13 214 457 856 1196 294 424 136 426 342 658
683 285 367 21 352 461 826 1559 308 503 187 561 789
828 272 416 18 355 526 899 1611 315 547 215 520 534 939
1506 582 281 168 306 84 85 310 357 110 31 71 145
1650 548 286 176 280 273 87 342 399 110 49 74 166
1592 458 293 161 313 284 83 337 319 95 27 59 138
1458 389 267 158 274 271 99 367 414 110 41 79 184
197 60 30 25 45 12 25 55 114 29 12 23 50
279 71 45 41 64 40 18 79 156 47 15 29 65
285 79 45 30 56 52 23 110 131 43 14 22 52
370 85 67 50 76 55 37 118 199 57 29 36 77
65 47
89 92
126 143
121 142
41 22
56 51
67 63
85 66
546 58 109 84 21 21 122 152 593 430 241 82 131 85 61 71
705 142 124 78 22
791 187 150 73 12 133 198 171 479 792
691 115 169 91 22
184 29 46 18 7
342 71 102 35 5
376 67 113 40 14
42 42 74 72 45 9 26 8 6 23
87 42 84 209
153 182 121 127 209
193 101 516 798 577 153 258 97 128 162
283 77 73 24 11 69 58 40 69 179 76 46 59 22 28 24
40 55 33 30 51
104 38 111 261 161 54 91 40 25 51
662 270 1018 64 159 54 701 40
619 374 1351 107 186 189 804 65
747 282 1716 122 229 267 999 99
694 321 1915 155 279 251 1070 160
309 223 510 50 72 20 350 18
326 327 737 54 115 96 426 46
326 264 900 76 119 154 494 57
383 316 1128 71 187 151 629 90
142 197 486 759 515 164 216 103 117 159
(continued on next page)
398
E.P. Simard et al. / Oral Oncology 50 (2014) 387–403
Table B1 (continued) Males
Southern Asia India Mumbai (Bombay) Chennai (Madras) South-Eastern Asia Philippines (Manila) Singapore Chinese Indian Malay Thailand (Chiang Mai) Western Asia Israel Jews Non-Jews Kuwait Kuwaitis Non-Kuwaitis North America Canada (9 registries) Canada (Excluding Quebec, Yukon and Nunavut) Alberta British Columbia Manitoba New Brunswick Newfoundland and Labrador Nova Scotia Ontario Prince Edward Island Saskatchewan United States SEER (9 Registries): Black SEER (9 Registries): White
Females
Vol. 6
Vol. 7
Vol. 8
Vol. 9
Vol. 6
Vol. 7
Vol. 8
Vol. 9
1864 679
1972 835
2188 924
2506 1020
770 551
869 610
1006 518
1132 585
231
273
289
246
294
285
289
218
133 50 8 129
130 37 11 136
153 41 8 142
207 32 20 160
45 15 10 79
71 13 5 102
73 22 9 86
101 22 11 104
145 9
164 6
206 13
256 27
141 7
159 11
208 4
216 8
8 35
4 19
11 27
15 40
6 13
6 6
6 9
14 13
2578 3648 197 404 138 75 45 122 1470 17 110
2862 3910 225 537 145 93 53 144 1552 24 89
2859 3966 275 496 151 92 58 129 1555 18 85
3046 3047 346 504 151 87 63 137 1646 22 90
1433 1788 125 282 84 40 19 43 762 4 74
1583 1960 146 297 102 40 24 60 839 12 63
1744 2192 191 302 108 48 16 75 925 8 71
1890 1892 224 377 111 45 17 75 938 16 87
460 3239
496 3097
469 3167
448 3277
175 2035
191 1953
198 2038
205 2037
72
7
33
133
42
59
76 74 13
128 61 21 21
8 43 13 8
64 10 4
South America Caribbean Martinique (France) Central America Costa Rica South America Brazil (Goiania) Colombia (Cali) Ecuador (Quito) Peru (Trujillo)
76
87
27 50 5 12
78 18 9
Oceania Australia (6 registries) New South Wales South Tasmania Victoria Western Capital Territory
1795 821 166 57 544 192 15
1960 881 194 50 578 235 22
2164 1021 177 56 603 277 30
2245 992 198 88 656 274 37
878 371 91 29 305 69 13
174 518
420 647
817 827
927 1037
16 115 100 484
41 108 673
40 156 225 824
226 89 58 5 57 105 235 368 78
294 133 81 3 114 110 274 458 97
411 130 94 3 122 164 333 549 121
Tonsil and oropharynx (C09-10) Europe Eastern Europe Belarus Czech Republic Poland Cracow Warsaw City Russia (St Petersburg) Slovak Republic Northern Europe Denmark Estonia Finland Iceland Latvia Norway Sweden United Kingdom (4 registries) Merseyside and Cheshire
74
17 26
73
33 86 28
33 90 31 20
1053 473 112 32 326 96 14
1166 485 101 33 393 138 16
1302 584 128 42 411 117 20
40 126
62 113
79 164
70 211
45 142 327 927
10 35 50 45
11 27 44
17 40 46 82
9 65 64 54
511 122 156 5 165 216 416 729 139
90 17 31 1 25 53 99 163 31
125 10 30 2 10 31 121 166 31
136 21 35 1 37 59 138 198 44
203 19 51 2 34 83 191 247 54
399
E.P. Simard et al. / Oral Oncology 50 (2014) 387–403 North Western Oxford Region Trent West Midlands UK, Scotland Western Europe France (6 registries) Bas-Rhin Calvados Doubs Isere Somme Tarn Germany (Saarland) Switzerland (4 registries) Geneva Neuchatel St Gall-Appenzell Vaud The Netherlands Eindhoven Maastricht Southern Europe Italy (6 registries) Genoa Province Florence and Prato Parma Province Ragusa Province Romagna Region Torino Varese Province Slovenia Spain (5 registries) Basque Country Granada Murcia Navarra Tarragona Zaragoza Asia Eastern Asia China Hong Kong Shanghai Japan (5 registries) Hiroshima Miyagi Prefecture Nagasaki Prefecture Osaka Prefecture Yamagata Prefecture Southern Asia India Mumbai (Bombay) Chennai (Madras) South-Eastern Asia Philippines (Manila) Singapore Chinese Indian Malay Thailand (Chiang Mai) Western Asia Israel Jews Non-Jews Kuwait Kuwaitis Non-Kuwaitis North America Canada (9 registries) Canada (Excluding Quebec, Yukon and Nunavut) Alberta British Columbia Manitoba New Brunswick Newfoundland and Labrador Nova Scotia
154 41 74 95 124
172 40
259 95 166 236 299
63 16 42 53 50
69 22
149 178
177 72 119 179 231
44 70
70 28 56 56 104
69 34 47 90 118
944 310 187 160 170 62 55 78 183 66 16 24 77
1095 317 199 131 175 211 62 112 234 70 24 35 105
1068 297 233 122 200 173 43 139 212 75 13 49 75
899 212 177 112 203 145 50 179 237 84 19 45 89
61 17 9 6 17 8 4 25 46 14 3 7 22
112 28 16 16 34 14 4 27 53 22 6 5 20
113 24 22 16 26 18 7 43 73 35 8 6 24
155 42 28 15 28 31 11 37 79 30 8 9 32
22 24
32 32
36 67
55 71
8 5
8 21
18 16
17 21
244 15 29 23 6 6 58 113 409 110 90 17 24 21 21 27
299 68 45 28 1
355 55 71 41 4
61 7 18 4 0 1 18 14 32 22 11 5 3 0 6 8
72 17 17 5 1
78 14 15 3 0
20 12 27 15 12 0 4 3 2 6
29 17 36 9
37 48 39 52 28
307 47 59 32 7 61 109 53 383 212 211 44 57 41 35 35
1 1 2 3 2
75 16 20 7 3 13 23 6 55 19 15 4 4 1 4 6
58 99 382 195 190 30 64 29 35 37
86 98 445 204
147 70 175 15 31 9 114 6
145 61 261 21 29 26 177 8
116 61 428 23 72 52 263 18
183 57 580 44 119 52 321 44
50 48 51 8 9 2 30 2
33 35 64 3 2 9 45 5
33 40 60 3 10 7 37 3
43 31 94 8 13 8 54 11
454 98
482 162
461 174
423 223
75 24
57 31
56 32
83 32
28
52
39
50
36
40
45
33
40 2 2 41
39 7 6 50
41 6 4 44
67 8 5 56
8 0 0 16
13 3 1 29
10 2 2 18
17 1 1 18
17 1
26 1
29 2
54 3
11 1
10 0
18 1
21 2
1 9
2 4
3 1
1 0
0 2
3 0
0 1
0 1
706 1022 46 128 36 17 7 18
834 1175 66 165 63 31 20 42
922 1290 76 187 42 30 22 41
1214 1215 125 232 66 55 23 85
317 396 20 57 13 11 2 8
324 434 20 63 18 9 7 15
370 483 27 82 17 8 5 16
423 423 41 73 27 14 9 22
(continued on next page)
400
E.P. Simard et al. / Oral Oncology 50 (2014) 387–403
Table B1 (continued) Males
Ontario Prince Edward Island Saskatchewan United States SEER (9 Registries): Black SEER (9 Registries): White
Females
Vol. 6
Vol. 7
Vol. 8
Vol. 9
Vol. 6
Vol. 7
Vol. 8
Vol. 9
430 3 21
420 3 24
489 4 31
583 5 40
191 3 12
182 1 9
197 0 18
218 2 17
200 865
178 903
207 1045
228 1299
59 412
62 429
57 380
58 386
50
4
16
51
12
20
25 20 11
47 30 8 3
1 15 3 0
10 2 0
610 246 57 17 221 59 10
855 359 97 28 249 111 11
213 119 12 8 55 14 5
South America Caribbean Martinique (France) Central America Costa Rica South America Brazil (Goiania) Colombia (Cali) Ecuador (Quito) Peru (Trujillo)
20
37
4 13 0 2
20 3 4
Oceania Australia (6 registries) New South Wales South Tasmania Victoria Western Capital Territory
632 284 64 19 202 59 4
702 275 78 21 242 83 3
47
Other head and neck (pyriform sinus, lip/oral cavity/pharynx not otherwise specified, Europe Eastern Europe Belarus 2459 3433 Czech Republic 2717 2661 Poland Cracow 198 212 Warsaw City 573 495 Russia (St Petersburg) 1323 Slovak Republic 1840 2065 Northern Europe Denmark 1152 1160 Estonia 357 481 Finland 698 741 Iceland 23 30 Latvia 638 828 Norway 670 647 Sweden 1226 1198 United Kingdom (4 registries) 2453 3035 Merseyside and Cheshire 491 555 North Western 863 995 Oxford Region 303 347 Trent 883 West Midlands 796 1138 UK, Scotland 1138 1310 Western Europe France (6 registries) 2369 2727 Bas-Rhin 758 765 Calvados 448 491 Doubs 299 341 Isere 515 511 Somme 187 463 Tarn 162 156 Germany (Saarland) 368 452 Switzerland (4 registries) 561 584 Geneva 152 171 Neuchatel 66 57 St Gall-Appenzell 121 94 Vaud 222 262 The Netherlands Eindhoven 153 251 Maastricht 112 232 Southern Europe Italy (6 registries) 1759 2046 Genoa Province 186 433 Florence and Prato 437 532 Parma Province 256 236 Ragusa Province 74 57
8 5
10
11 8 2
5 15 1 3
193 84 20 5 63 20 1
215 97 22 3 65 24 4
253 108 29 6 82 24 4
and larynx; C12-14,32)
3732 2844
3733 2902
179 233
135 212
97 240
93 333
253 616 1063 2212
247 535 1336 2177
20 111 100 92
37 78
35 110 83 115
51 106 102 117
1272 462 618 25 787 668 1075 3036 582 1001 391 901 1062 1477
1244 447 621 34 787 663 1032 2983 549 995 372 907 1067 1573
287 25 104 9 69 87 206 753 193 265 100 268 195 361
279 30 117 2 61 95 189 844 171 291 93 289 386
276 33 86 4 44 132 193 819 159 267 111 278 282 452
305 32 94 11 50 128 221 785 160 268 97 227 260 447
2556 717 440 313 494 450 142 459 492 153 51 96 192
2225 542 414 254 471 404 140 404 523 133 75 104 211
110 28 16 15 27 8 16 36 65 24 3 12 26
158 49 19 16 30 29 15 51 84 27 10 5 42
166 48 19 20 43 21 15 64 69 23 4 17 25
184 43 32 23 53 18 15 58 103 21 15 18 49
244 262
245 244
23 17
21 27
39 40
41 41
2244 479 636 197 54
1759 360 516 204 56
143 22 48 23 8
199 45 59 21 4
213 47 70 16 4
170 36 59 13 3
91
401
E.P. Simard et al. / Oral Oncology 50 (2014) 387–403 Romagna Region Torino Varese Province Slovenia Spain (5 registries) Basque Country Granada Murcia Navarra Tarragona Zaragoza Asia Eastern Asia China Hong Kong Shanghai Japan (5 registries) Hiroshima Miyagi Prefecture Nagasaki Prefecture Osaka Prefecture Yamagata Prefecture Southern Asia India Mumbai (Bombay) Chennai (Madras) South-Eastern Asia Philippines (Manila) Singapore Chinese Indian Malay Thailand (Chiang Mai) Western Asia Israel Jews Non-Jews Kuwait Kuwaitis Non-Kuwaitis North America Canada (9 registries) Canada (Excluding Quebec, Yukon and Nunavut) Alberta British Columbia Manitoba New Brunswick Newfoundland and Labrador Nova Scotia Ontario Prince Edward Island Saskatchewan United States SEER (9 Registries): Black SEER (9 Registries): White South America Caribbean Martinique (France) Central America Costa Rica South America Brazil (Goiania) Colombia (Cali) Ecuador (Quito) Peru (Trujillo) Oceania Australia (6 registries) New South Wales South Tasmania Victoria Western Capital Territory
85 355 451 772 1336 659 234 388 263 166 285
370 418 731 2092 1302 412 559 321 254 546
1484 608 1709 124 270 86 1106 123
430 468 410 728 2118 413 455 314 320 616
413 210 751 2203 1404 378 627 349 287 562
21 21 62 32 20 5 10 6 4 7
53 36 34 54 37 33 7 12 7 5 6
6 19 11 13 16
49 10 74 69 80 7 28 11 7 16
1446 808 2194 160 344 262 1245 183
1367 664 2697 196 483 383 1442 193
1277 729 3029 273 506 422 1552 276
207 133 218 12 26 15 146 19
154 113 272 16 39 27 174 16
126 99 233 15 38 24 129 27
109 90 287 30 52 30 141 34
2443 612
2483 780
2336 807
2373 937
480 179
503 217
503 191
408 242
298
337
438
420
118
111
153
108
264 47 10 199
312 35 16 241
395 42 23 208
365 29 33 176
38 2 6 71
40 6 7 76
32 6 2 61
31 6 5 42
494 41
521 40
656 68
695 95
71 2
95 2
98 6
139 14
20 84
20 39
22 41
27 59
7 7
11 1
6 5
6 5
3991 6287 321 625 226 126 82 212 2206 21 172
4251 6538 353 680 216 179 114 253 2235 34 187
4131 6353 332 691 218 187 118 205 2164 33 183
4012 4016 394 629 184 173 126 210 2076 44 176
838 1314 65 117 40 21 14 37 499 9 36
916 1444 74 145 45 26 13 49 529 4 31
933 1472 90 164 51 40 16 48 489 5 30
866 867 97 126 37 40 18 43 457 7 41
708 4700
742 4589
745 4252
714 3833
176 1215
202 1278
200 1179
203 1094
104
7
92
291
27
47
107 153 32
157 207 43 17
10 26 3 0
32 7 3
2869 1290 240 82 915 310 32
2719 1251 223 86 814 312 33
385 159 40 11 134 39 2
399 173 37 9 136 42 2
84 152
225
31 99 18 9
127 27 12
2713 1208 277 99 866 236 27
2905 1307 291 90 879 307 31
41 35 60 65
16 8
24
31 40 4
21 53 9 6
429 184 26 23 147 44 5
439 184 38 21 145 47 4
402
E.P. Simard et al. / Oral Oncology 50 (2014) 387–403
passive smoking has substantially declined over the past few decades in many economically developed countries, where the health hazards of smoking are well-recognized and tobacco prevention programs have long been established [25,26]. For example, in the United States, smoking prevalence peaked in the 1960s and has since declined [25]. These patterns may have contributed, at least in part, to the declines in incidence rates for oral cavity and other HNCs noted in the current study. Consistent with previous findings [7,8,16,27–29], rates of oral cavity cancer increased among men and women in some eastern and northern European countries where tobacco use remained common such as the Czech and Slovak Republics, Denmark, Estonia, and Finland. In addition, rates of oral cavity cancer increased among women only in a number of European nations, perhaps reflecting the delayed peak in smoking prevalence among women compared to men, as has been seen in other countries [25]. Rates of oral cavity and oropharyngeal cancer also increased in the United Kingdom and it has been suggested that these trends are largely driven by increases among individuals with low socioeconomic status (among whom smoking prevalence is elevated) [30]. In addition, the high rates of oral cavity cancer among men and women in India and other Asian countries are largely due to the consumption of betel quid which can result in exposure to carcinogenic tobacco-specific nitrosamines [31,32]. The important role of alcohol consumption with regards to HNC (oral cavity cancer) also deserves mention, specifically in Hungary and other central and eastern European countries where alcohol consumption has increased or stabilized at high levels [26,33]. In these regions, the type of alcohol consumed is important. For example, in some eastern European nations alcohol is derived from fruits (e.g., plums, peaches, and apricots) which are believed to contain acetaldehyde, a compound considered possibly carcinogenic to humans [28,32,34–37]. We also documented extremely high rates of all HNCs among men in France, underscoring the importance of understanding area-specific tobacco (and alcohol) consumption practices for HNC prevention and control. A previous study [38] found the overall increase in HNC rates in France was driven by increases in pharyngeal cancer (versus oral cavity alone) but our analysis using updated data showed broad increases across all three categories of HNC. Increasing HNC rates in these regions underscore the need for prevention programs that address not only tobacco, but also alcohol consumption. With regards to oropharyngeal cancers, the role of persistent HPV infection is rising in prominence in many economically developed countries where tobacco use has declined [1]. Globally, approximately 25% of oropharyngeal cancers are due to HPV infection [39] although this attribution is higher in some economically developed countries such as the United States where the figure exceeds 60% [6]. Similar to previous studies [4,40–45], the current analysis found increases in oropharyngeal sub-sites most often associated with HPV infection in the United States and Canada, as well as a number of other economically developed European countries such as Denmark and Sweden. In other countries where data is absent regarding the role of HPV in oropharyngeal cancer and where tobacco use remains common, the cases are likely due to tobacco. Additional, representative studies from other economically developed regions with data on the prevalence of HPV DNA in tumor blocks (or other markers) is needed to quantify the contribution of HPV infection to oropharyngeal cancers in these settings. Rates of HNC stratified by subtype warrant continued monitoring in countries undergoing economic transitions because of associated increases in the prevalence of cancer risk factors (e.g., tobacco use, energy imbalance, and HPV exposure) [26]. In terms of prevention, one recent study found a reduced prevalence of oral HPV infection after bivalent HPV vaccination, suggesting the
vaccine may have a protective effect against infections associated with oropharyngeal cancer risk [46]. The trends presented for the heterogeneous grouping of other HNCs also deserve brief comment. This category included mainly laryngeal cancers, for which the strongest risk factor is also tobacco use [47]. The country-specific incidence trends were generally similar to those of oral cavity cancers with rates increasing in some European countries such as Belarus, Estonia and Latvia and decreasing in countries where the tobacco epidemic was established first such as the United States and Canada [29]. It should be noted that alcohol consumption is also a risk factor for laryngeal cancer (as well as some other HNCs), although the effect is much smaller than that of tobacco use [47]. Nonetheless, the synergistic role of dual use (joint tobacco and alcohol consumption) results in higher laryngeal cancer risks than either alone. The role of diet and nutrition and body mass index (BMI) may also be important to consider in light of the current HNC trends. Diets rich in fruits and vegetables are generally associated with a decreased risk of HNCs [1,47]. It is possible that fruit and vegetable consumption may decrease in economically transitioning countries possibly attenuating declines in tobacco-associated HNCs. However, the precise role of diet and obesity in HNC etiology is unclear. Large pooled studies are needed to evaluate the contribution of various dietary practices to HNC while controlling for tobacco and alcohol consumption, as smokers tend to be leaner but also drink more than non-smokers [17]. With regards to BMI, one recent prospective study found no association between BMI and HNC incidence but additional studies in other countries are needed to clarify the complex relationship between smoking, alcohol, diet, BMI, and HNC incidence [18]. Strengths of this descriptive study include the use of high-quality population-based cancer registry data from a number of countries included in the IARC CI5 databases. By grouping HNCs into broad categories, we were able to describe incidence rates and trends in relation to underlying trends in causal risk factors such as tobacco and alcohol consumption and HPV infection. In addition, we present 5-year average annual rates and compare changes over time across broad calendar periods, avoiding the instability associated with comparing annual rates based on small sample sizes. Nonetheless, the study also has limitations. IARC incidence data are limited in their global coverage, and data from Africa, where the cancer burden is substantial, are notably scarce [48]. In addition, estimates of rates and trends within countries should also be interpreted with caution as they are usually based upon a small number of registries that may not accurately represent national-level data. Also, consistent histologic classification data for the majority of CI5 registries with regards to the other HNC category precluded a more detailed evaluation of trends for this site. While the most up-to-date data were used for this analysis, incident cases are only available through 2002. When new volumes of CI5 data are released an updated analysis will be necessary for more contemporary estimates of both rates and trends. We documented trends in HNC incidence rates by country, sex, and anatomic site. For many tobacco-related HNCs, incidence rates increased in countries where tobacco use remains common (e.g., in some European and Asian countries). In contrast, in areas where tobacco use has declined, rates of HPV-associated oropharyngeal cancer increased. Continued monitoring of HNC incidence trends is warranted as many countries undergo economic transition that may be associated with the acquisition of risk factor for HNC including tobacco and alcohol use as well as HPV exposure. Establishing tobacco control programs in many regions may aid in reversing the increasing HNC incidence trends noted in the current study.
E.P. Simard et al. / Oral Oncology 50 (2014) 387–403
Conflict of interest statement None declared. Appendix A See Table A1. Appendix B See Table B1. References [1] Mayne S, Morse D, Winn D. Cancers of the oral cavity and pharynx. In: Schottenfeld D, Fraumeni J, editors. Cancer epidemiology and prevention. New York: Oxford; 2006. p. 674–96. [2] Hashibe M, Brennan P, Chuang SC, et al. Interaction between tobacco and alcohol use and the risk of head and neck cancer: pooled analysis in the International Head and Neck Cancer Epidemiology Consortium. Cancer Epidemiol Biomarkers Prevent 2009;18(2):541–50. [3] Danaei G, Vander Hoorn S, Lopez AD, Murray CJ, Ezzati M, Comparative Risk Assessment collaborating g. Causes of cancer in the world: comparative risk assessment of nine behavioural and environmental risk factors. Lancet 2005;366(9499):1784–93. [4] Chaturvedi AK, Engels EA, Anderson WF, Gillison ML. Incidence trends for human papillomavirus-related and -unrelated oral squamous cell carcinomas in the United States. J Clin Oncol: Off J Am Soc Clin Oncol 2008;26(4):612–9. [5] Gillison ML, Alemany L, Snijders PJ, et al. Human papillomavirus and diseases of the upper airway: head and neck cancer and respiratory papillomatosis. Vaccine 2012;30(Suppl. 5):F34–54. [6] Gillison ML, Chaturvedi AK, Lowy DR. HPV prophylactic vaccines and the potential prevention of noncervical cancers in both men and women. Cancer 2008;113(10 Suppl):3036–46. [7] de Camargo Cancela M, de Souza DL, Curado MP. International incidence of oropharyngeal cancer: a population-based study. Oral Oncol 2012;48(6):484–90. [8] Warnakulasuriya S. Global epidemiology of oral and oropharyngeal cancer. Oral Oncol 2009;45(4–5):309–16. [9] International Agency for Research on Cancer. Cancer incidence in five continents, Vol. VI. Lyon, France: IARC Scientific Publications, No. 120; 1992. [10] International Agency for Research on Cancer. Cancer incidence in five continents, vol. VII. Lyon, France: IARC Scientific Publications, No. 143; 1997. [11] International Agency for Research on Cancer. Cancer incidence in five continents, vol. VIII. Lyon, France: IARC Scientific Publications, No. 155; 2002. [12] International Agency for Research on Cancer. Cancer incidence in five continents, vol. IX. Lyon, France: IARC Scientific Publications, No. 160; 2007. [13] World Health Organization. Manual of the international statistical classification of diseases, injuries, and causes of death. Geneva, Switzerland: World Health Organization; 1977 [9th Rev]. [14] World Health Organization. Manual of the international statistical classification of diseases, injuries, and causes of death. 2nd ed. Geneva, Switzerland: World Health, Organization; 2004 [10th Rev]. [15] Hashibe M, Brennan P, Benhamou S, et al. Alcohol drinking in never users of tobacco, cigarette smoking in never drinkers, and the risk of head and neck cancer: pooled analysis in the International Head and Neck Cancer Epidemiology Consortium. J Natl Cancer Inst 2007;99(10):777–89. [16] Curado MP, Hashibe M. Recent changes in the epidemiology of head and neck cancer. Curr Opin Oncol May 2009;21(3):194–200. [17] Gaudet MM, Olshan AF, Chuang SC, et al. Body mass index and risk of head and neck cancer in a pooled analysis of case-control studies in the International Head and Neck Cancer Epidemiology (INHANCE) Consortium. Int J Epidemiol Aug 2010;39(4):1091–102. [18] Gaudet MM, Patel AV, Sun J, et al. Prospective studies of body mass index with head and neck cancer incidence and mortality. Cancer Epidemiol Biomarkers Prevent 2012;21(3):497–503. [19] Sun EC, Curtis R, Melbye M, Goedert JJ. Salivary gland cancer in the United States. Cancer epidemiology, biomarkers & prevention: a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology 1999;8(12):1095–100. [20] Sun X, Tong LP, Wang YT, et al. Can global variation of nasopharynx cancer be retrieved from the combined analyses of IARC Cancer Information (CIN) databases? PloS one 2011;6(7):e22039.
403
[21] Segi M. Cancer mortality for selected sites in 24 countries (1950–57) Sendai. Japan: Department of Public Health, Tohoku University of Medicine; 1960. [22] Doll R, Cook P. Summarizing indices for comparison of cancer incidence data. Int J Cancer 1967;2(3):269–79. [23] International Agency for Research on Cancer. Cancer registration principles and methods. Lyon, France: IARC Scientific Publications, No. 95; 1991. [24] Devesa SS, Donaldson J, Fears T. Graphical presentation of trends in rates. Am J Epidemiol 1995;141(4):300–4. [25] Thun M, Peto R, Boreham J, Lopez AD. Stages of the cigarette epidemic on entering its second century. Tobacco Control Mar 2012;21(2):96–101. [26] Ezzati M, Riboli E. Behavioral and dietary risk factors for noncommunicable diseases. New Engl J Med 2013;369(10):954–64. [27] Boyle P, Ferlay J. Cancer incidence and mortality in Europe, 2004. Ann Oncol: Off J Eur Soc Med Oncol/ESMO 2005;16(3):481–8. [28] Garavello W, Bertuccio P, Levi F, et al. The oral cancer epidemic in central and eastern Europe. Int J Cancer 2010;127(1):160–71. [29] Sturgis EM, Cinciripini PM. Trends in head and neck cancer incidence in relation to smoking prevalence: an emerging epidemic of human papillomavirus-associated cancers? Cancer 2007;110(7):1429–35. [30] Conway DI, Stockton DL, Warnakulasuriya KA, Ogden G, Macpherson LM. Incidence of oral and oropharyngeal cancer in United Kingdom (1990–1999) – recent trends and regional variation. Oral Oncol 2006;42(6):586–92. [31] Nair U, Bartsch H, Nair J. Alert for an epidemic of oral cancer due to use of the betel quid substitutes gutkha and pan masala: a review of agents and causative mechanisms. Mutagenesis 2004;19(4):251–62. [32] International Agency for Research on Cancer. IARC monographs on carcinogenic risks to humans, Part E, vol. 100. Review of human carcinogens: personal habits and indoor combustions. Lyon, France: IARC Scientific Publications; 2009. [33] Bosetti C, Levi F, Lucchini F, Zatonski WA, Negri E, La Vecchia C. Worldwide mortality from cirrhosis: an update to 2002. J Hepatol May 2007;46(5):827–39. [34] Boffetta P, Hashibe M, La Vecchia C, Zatonski W, Rehm J. The burden of cancer attributable to alcohol drinking. Int J Cancer 2006;119(4):884–7. [35] Popova S, Rehm J, Patra J, Zatonski W. Comparing alcohol consumption in central and eastern Europe to other European countries. Alcohol Alcoholism 2007;42(5):465–73. [36] International Agency for Research on Cancer. IARC monograps on carcinogenic risks to humans, vol. 71. Re-evalution of some organic chemicals, hydrazine and hydrogen peroxide. Lyon, France: IARC Scientific Publications; 1999. [37] International Agency for Research on Cancer. IARC monographs on the evaluation of carcinogenic risks to humans, vol. 96. Alcohol consumption and ethyl carbamate. Lyon, France: IARC Scientific Publications; 2010. [38] Franceschi S, Bidoli E, Herrero R, Munoz N. Comparison of cancers of the oral cavity and pharynx worldwide: etiological clues. Oral Oncol Jan 2000;36(1):106–15. [39] de Martel C, Ferlay J, Franceschi S, et al. Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol Jun 2012;13(6):607–15. [40] Chaturvedi AK, Engels EA, Pfeiffer RM, et al. Human papillomavirus and rising oropharyngeal cancer incidence in the United States. J Clin Oncol: Off J Am Soc Clin Oncol 2011;29(32):4294–301. [41] Jemal A, Simard EP, Dorell C, et al. Annual Report to the Nation on the Status of Cancer, 1975–2009, featuring the burden and trends in human papillomavirus (HPV)-associated cancers and HPV vaccination coverage levels. J Natl Cancer Inst 2013;105(3):175–201. [42] Simard EP, Ward EM, Siegel R, Jemal A. Cancers with increasing incidence trends in the United States: 1999 through 2008. CA: Cancer J Clin 2012;January 4. [43] Johnson-Obaseki S, McDonald JT, Corsten M, Rourke R. Head and neck cancer in Canada: Trends 1992 to 2007. Otolaryngol – Head Neck Surg: Off J Am Acad Otolaryngol – Head Neck Surg 2012;February 10. [44] Blomberg M, Nielsen A, Munk C, Kjaer SK. Trends in head and neck cancer incidence in Denmark, 1978–2007: focus on human papillomavirus associated sites. Int J Cancer 2011;129(3):733–41. [45] Ramqvist T, Dalianis T. An epidemic of oropharyngeal squamous cell carcinoma (OSCC) due to human papillomavirus (HPV) infection and aspects of treatment and prevention. Anticancer Res May 2011;31(5):1515–9. [46] Herrero R, Quint W, Hildesheim A, et al. Reduced prevalence of oral human papillomavirus (HPV) 4 years after bivalent HPV vaccination in a randomized clinical trial in Costa Rica. PloS one 2013;8(7):e68329. [47] Olshan AF. Cancer of the larynx. In: Schottenfeld D, Fraumeni J, editors. Cancer epidemiology and prevention. New York: Oxford; 2006. p. 627–37. [48] Jemal A, Bray F, Forman D, et al. Cancer burden in Africa and opportunities for prevention. Cancer 2012;118(18):4372–84.
