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Oral cavity cancer incidence rates in Osaka, Japan between 2000 and 2014
Oral Oncology 105 (2020) 104653
Contents lists available at ScienceDirect
Oral Oncology journal homepage: www.elsevier.com/locate/oraloncology
Oral cavity cancer incidence rates in Osaka, Japan between 2000 and 2014 a,⁎
a
a
T
a
Shihoko Koyama , Takahiro Tabuchi , Sumiyo Okawa , Toshitaka Morishima , Shunsuke Ishimotob, Miki Ishibashib, Isao Miyashiroa a b
Cancer Control Center, Osaka International Cancer Institute, 3-1-69, Otemae, Chuo-ku, Osaka, Osaka 541-8567, Japan Dentistry, Osaka International Cancer Institute, 3-1-69, Otemae, Chuo-ku, Osaka, Osaka 541-8567, Japan
A R T I C LE I N FO
A B S T R A C T
Keywords: Epidemiology Oral cancer Japan
Background: We investigated trends in oral cavity cancer incidence from 2000 to 2014 in Osaka, Japan. Methods: Using Osaka Cancer Registry (OCR) data, oral cavity cancer incidence number and age-standardized incidence rates were calculated according to three 5-year-time-periods: 2000–2004, 2005–2009 and 2010–2014. We calculated the distribution of clinical stage for each 5-year period and the proportion of oral cavity cancer among all cancers. Results: A total of 6,086 oral cavity cancers were registered in OCR in 2000–2014. Across the period, between 55.6% and 65.0% were 65 years+ and approximately 60% were men. Tongue cancer accounted for 30.4% to 43.8% of the registrations, while gum accounted for 30.7% to 34.7%. 36.3% to 37.3% were regional, while 1.8% to 2.8% were distant. The age-standardized incidence rate of oral cavity cancer increased from 2.1/100,000 in 2000 to 3.8/100,000 in 2014, although the proportion of oral cavity cancer among all cancers only increased slightly from 0.71% in 2000 to 0.92% in 2014. Proportion of localized stage cancer was 60.8%–67.5% for tongue and 31.0%–49.5% for gum or floor of mouth. Proportion of distant stage cancer was 0.3%–1.0% for tongue and 2.5%–4.2% for gum or floor of mouth. Conclusions: Age-standardized incidence rate of oral cavity cancer increased, but was not higher than other countries. The proportion of localized stage tongue cancer was higher, while that of distant stage cancer was lower than other sites. Tongue cancer might be easier to detect in its earlier stages than other sites.
Introduction Oral cavity cancer is an important global public health problem. The latest report from the International Agency for Research on Cancer (IARC) showed that lip and oral cancers which include lips, tongue, gum, and floor of mouth, have an annual incidence of over 350,000 diagnosed cases, and an annual mortality of about 177,000 deaths worldwide [1]. Oral cavity cancer has usually been included as part of oral and pharyngeal cancer or head and neck cancer [2]. For example, the National Cancer Center Japan report ‘oral and pharygeal cancer’ incidence in online publications every year [3,4], but do not report the incidence of oral cavity cancer alone. As a result, reports/studies of trends in oral cavity cancer are rare, and trends in oral and pharyngeal cancer are often used as substitutes in Japan. Oral cavity cancers differ from pharyngeal cancers in their association with human papilloma virus (HPV): i.e., a meta-analysis carried out in 2015 [5] found that the proportion of HPV-attributable cases was
⁎
45.8% for oropharyngeal cancer and 24.2% for oral cavity cancer. Therefore, it may be important to use distinct terms: oral cavity cancer and pharyngeal cancer [6]. General dental practitioners more routinely examined patients’ oral mucosa than general medical practitioner [7]. Dentists' familiarity with, and access to, their patients' oral cavities make them particularly well suited to perform early detection examinations [8]. The percentage of people that visit a dental office at least once a year (regular dental check-up) increased from 34.1% in 2009 to 52.9% in 2016 [9]. However, it is not known whether early detection of oral cavity cancer has increased. The incidence rates of oral cancers vary considerably worldwide, ranging from 16.4 per 100,000 for men in India, to 5.0 per 100,000 for men in Singapore, to 10.6 per 100,000 for women in India, to 1.7 per 100,000 for women in Slovakia [10]. Although oral cavity cancer incidence has been reported in other countries [6,11], no study has updated the trends in incidence of oral cavity cancer in Japan. The objective of this study was to examine the trends in incidence of oral
Corresponding author. E-mail address: [email protected] (S. Koyama).
https://doi.org/10.1016/j.oraloncology.2020.104653 Received 16 November 2019; Received in revised form 27 February 2020; Accepted 14 March 2020 1368-8375/ © 2020 Elsevier Ltd. All rights reserved.
Oral Oncology 105 (2020) 104653
S. Koyama, et al.
cavity cancer from 2000 to 2014 in Osaka, Japan.
Table 1 Number and percentage of oral cavity cancer cases by characteristics reported to the OCR 2000–2014 : age, sex, site, and stage (N = 6,086).
Methods
Characteristic
Data and definition of oral cavity cancer Total Age < 30 30–44 45–54 55–64 65–74 75–84 85+ Sex Men Women Site Tongue Gum Floor of mouth Other* and unspecified parts of mouth Stage Localized Regional Distant site Unknown
We used data from the Osaka Cancer Registry (OCR), which is a population-based cancer registry that covers all cancer incidence observed in the Osaka prefecture [population: 8.8 million (2015 census)] [12]. Oral cavity cancer cases who were diagnosed between 2000 and 2014 were analyzed. Oral cavity cancers were defined by the International Classification of Diseases, 10th revision (ICD-10); tongue (C02.0, C02.1, C02.2, C02.3), gum (C03.0, C03.1, C03.9), floor of mouth (C04.0, C04.1, C04.8, C04.9, C05.0), inner lip and other and unspecified parts of mouth (Others) (C00.3, C00.4, C00.5, C00.6, C00.8, C00.9, C06.0, C06.1, C06.2, C06.8, C06.9)] [13]. Variables Year of diagnosis was divided into three groups: 2000–2004, 2005–2009 and 2010–2014. Age group was divided into seven groups; < 30, 30–44, 45–54, 55-64, 65–74, 75–84, and 85+. Cancer stage at diagnosis was classified into four groups; (1) Localized: cancer is confined to the original organ (T1, T2), (2) Regional: cancer has spread to regional lymph nodes and/or to immediately adjacent tissues (T3, T4a, T4b, N1, N2, N3), (3) Distant: cancer has metastasized to distant organs (M1), and (4) Unknown [14].
2000–2004 n %
2005–2009 n %
2010–2014 n %
1301
100.0
2084
100.0
2701
100.0
10 72 173 323 377 250 96
0.8 5.5 13.3 24.8 29.0 19.2 7.4
20 126 216 445 656 426 195
1.0 6.1 10.4 21.4 31.5 20.4 9.4
25 147 231 543 784 688 283
1.0 5.4 8.6 20.1 29.0 25.5 10.5
794 507
61.0 39.0
1,229 855
59.0 41.0
1572 1129
58.2 41.8
395 452 255 199
30.4 34.7 19.6 15.3
839 648 322 275
40.3 31.1 15.5 13.2
1182 829 368 322
43.8 30.7 13.6 11.9
559 483 37 222
43.0 37.1 2.8 17.1
1047 756 40 241
50.2 36.3 1.9 11.6
1451 1007 49 194
53.7 37.3 1.8 7.2
Abbreviations: OCR; Osaka cancer registry. * Other: inner lip, oral cavity cancer not otherwise specified.
Statistical analyses
The proportion of distant stage tongue cancer was 0.3%–1.0% and 2.5%–4.2% for gum or floor of mouth.
We calculated the incidence number and proportion by characteristics according to time period. Age-standardized incidence rates (ASRs) were calculated by sex and year of cancer diagnosis (between 2000 and 2014), using the population data by age group from Osaka Prefecture (the Population Census) [15], adjusting to the Japanese model population in 1985 (direct method). To validate the trend of oral cavity cancer, the proportion among all cancers (C00-C96) except in-situ cancers was also calculated for each year. In addition, we used joinpoint regression to observe ASR trends with an annual percent change (APC) [16]. Analyses were carried out using Stata version 15 (Stata Corporation, College Station, Texas, USA) and the Joinpoint Regression Program, Version 4.7.0.0 (Statistical Research and Applications Branch, National Cancer Institute). The study was reviewed and approved by the Research Ethics Committee of the Osaka International Cancer Institute (No.19149).
Discussion The present study is the first to examine the incidence rate of oral cavity cancer between 2000 and 2014 in Japan, suggesting that the agestandardized incidence rate increased from 2.1 per 100,000 persons in 2000 to 3.8 in 2014. ASRs for both sexes significantly increased in the joinpoint analysis (men:APC = 5.1%; women:APC = 5.7%; and both sexes:APC = 5.3%). However, this result should be interpreted cautiously as the proportion of oral cavity cancer among all cancers only increased slightly (from 0.71% in 2000 to 0.92%) in 2014. Lip and oral cavity cancers (C00-C06) accounted for approximately 2.0% of all cancers worldwide in 2018 [1]. Therefore, the incidence rate of oral cavity cancer in Japan found in this study may not be high. Smoking and use of chewed forms of tobacco are the most common causes of oral cavity cancer [17,18]. Although smoking rates are still increasing in developing countries, they are decreasing in developed economies such as Japan, England, and South Korea. The smoking rate in Japan decreased from 47.4% to 32.1% among men and from 11.5% to 8.5% among women between 2000 and 2014. A previous study has shown that the ASRs of oral cavity cancer have been declining worldwide, consistent with a decline in tobacco use between 1983 and 2003 [19]; the APC of the ASR was −0.9% between 2000 and 2013 [18]. However, in addition to the trends shown in this study, other countries have also indicated different trends: oral cavity cancer incidence rates increased for both sexes between 1995 and 2011 in England (men: APC 2.8%, women: APC 3.0%) [20], and also increased between 1999 and 2010 in South Korea (APC 1.2%) [11]. Among all sites of oral cavity cancer, the proportion of localized cases increased, while that of distant stage cases decreased. A possible reason for the increase in localized stage cancer may be that the number of Japanese people who visit dental clinics is increasing (as mentioned in the introduction) [9]. Distribution of stage varied by cancer site. In particular, the proportion of localized stage tongue cancer was higher, and the proportion of distant stage tongue cancer lower than other sites.
Results A total of 6,086 oral cavity cancer cases were registered in OCR between 2000 and 2014. Basic characteristics of oral cavity cancers according to age, sex, site and stage are shown in Table 1. Among oral cavity cancer patients, 55.6% to 65.0% were 65 years or older; approximately 60% were men. Tongue cancer accounted for 30.4% to 43.8%, while gum cancer accounted for 30.7% to 34.7%. In terms of clinical cancer stage, 36.3% to 37.3% were regional, while 1.8% to 2.8% were distant. ASRs of oral cavity cancer, and proportion of oral cavity cancer among all cancers are shown in Fig. 1 and supplementary Table S1. The ASR of oral cavity cancer (per 100,000 people) was 2.1 in 2000, 2.5 in 2005, 3.3 in 2010, and 3.8 in 2014. The proportion of oral cavity cancer among all cancers was 0.67%–1.00%. The results of the joinpoint analysis of ASRs are presented in Fig. 2. All ASRs significantly increased in 2000–2014 (men:APC = 5.1%; women: APC = 5.7%; and both sexes:APC = 5.3%). Table 2 shows the proportion of stage at diagnosis by site in the oral cavity. The proportion of localized stage tongue cancer was 60.8%–67.5% and 31.0%–49.5% for gum or floor of mouth. 2
Oral Oncology 105 (2020) 104653
S. Koyama, et al.
Fig. 1. Annual age-standardized incidence rate per 100,000 population of oral cavity cancer by sex (left axis), and proportion of oral cavity cancer within all cancers (C00-C96) (right axis).
oral cavity cancer registration in the OCR was not perfect. However, the proportion of death certificate only (DCO) for oral and pharyngeal cancer (C00-C14), which is often regarded as an index of completeness, was low at approximately 2.8% in 2014. In addition, cancer control has been systematically promoted by the national government of Japan since 2006 [25]. As a result, the number of cancer cases submitted to the registry from each hospital has gradually increased in the last 15 years. The increase in age-sex adjusted oral cavity cancer incidence in Osaka may be affected by the increased number of registered cases. Second, because we used data from the OCR, we need to interpret the findings with limited generalizability to the whole of Japan. Nevertheless, in 2014, the ASR of oral and pharyngeal cancer (C00-C14) in Osaka (men:13.8, women:5.3) was almost equal to that for the whole of Japan (men:12.8, women:4.3) [4]. In conclusion, we have described trends in oral cavity cancer incidence using population-based data from a cancer registry in Osaka, Japan. The ASR of oral cavity cancer increased, but may not be high compared with other countries. We suggest dentists should be given additional training on oral cancer screening programs so that patients
Tongue cancer might be easier to detect in its earlier stage than other sites. This may, in part, be a result of the National Health Promotion Campaign for the 21st century, ‘Healthy Japan 21′, which was proposed to prevent lifestyle-related diseases. In 2000, Healthy Japan 21 included a focus on oral health. Nationwide health promotion activities were suggested, including the oral health-related goal of increasing the number of people attending regular dental check-ups [21]. It has been reported that regular dental check-ups are associated with earlier-stage diagnosis for oral cavity cancer [22]. However, in Japan only 34.1% of dentists in private clinics always or usually perform oral cavity cancer screening, which is significantly lower than in other countries such as Australia (89.3%) [23]. Therefore, further education and training programs for oral cavity cancer screening should be given to dentists to improve prevention and early detection [23]. Early detection has a large impact on prognosis. The survival of oral cavity cancer patients depends on the stage at diagnosis; i.e., the 5-year survival rate of patients with localized stage tongue cancer was 79.8%, but 38.8% for distant stage [24]. The present study has some limitations. First, the completeness of
Fig. 2. Age-standardized incidence rate trends using joinpoint regression. 3
Oral Oncology 105 (2020) 104653
S. Koyama, et al.
Table 2 Distribution of stage at diagnosis by site in oral cavity. 2000–2004
Site Tongue Gum Floor of mouth Other* Total
2005–2009
2010–2014
Localized %
Regional %
Distant site %
Unknown %
Localized %
Regional %
Distant site %
Unknown %
Localized %
Regional %
Distant site %
Unknown %
60.8 31.0 40.0 38.7 43.0
31.4 42.3 37.6 36.2 37.1
1.0 4.2 3.5 2.5 2.8
6.8 22.6 18.8 22.6 17.1
66.9 35.3 44.1 41.8 50.2
28.6 45.2 36.6 38.2 36.3
0.5 2.6 2.8 3.6 1.9
4.1 16.8 16.5 16.4 11.6
67.5 40.0 49.5 43.2 53.7
29.1 46.8 41.0 38.5 37.3
0.3 2.5 2.7 4.3 1.8
3.0 10.6 6.8 14.0 7.2
* Other: inner lip, oral cavity cancer not otherwise specified.
can be screened in regular dental check-ups. Similarly, patients should maintain regular check-up visits not only for the prevention of caries and periodontal treatment but also for the prevention and early detection of oral cancer.
[7] Carter LM, Ogden GR. Oral cancer awareness of general medical and general dental practitioners. Br Dent J 2007;E10. 203, discussion 248–9. [8] Mashberg A. Diagnosis of early oral and oropharyngeal squamous carcinoma: obstacles and their amelioration. Oral Oncol 2000;36:253–5. [9] The Japan National Health. Nutrition Suevey 2016https://www.mhlw.go.jp/file/ 04-Houdouhappyou-10904750-Kenkoukyoku-Gantaisakukenkouzoushinka/ kekkagaiyou_7.pdf. [10] Adami HO, Hunter DJ, Lagiou P, Mucci L. Textbook of cancer epidemiology. Oxford University Press; 2018. [11] Choi SW, Moon EK, Park JY, Jung KW, Oh CM, Kong HJ, et al. Trends in the incidence of and survival rates for oral cavity cancer in the Korean population. Oral Dis 2014;20:773–9. [12] Toyoda Y, Tabuchi T, Nakata K, Morishima T, Nakayama T, Miyashiro I, et al. Increase in incidental detection of thyroid cancer in Osaka. Japan Cancer Sci 2018;109:2310–4. [13] Friz. International classification of diseases for oncology: World Health Organization; 2012. [14] Ruhl JLCC, Hurlbut A, Ries LAG, Adamo P, Dickie L, Schussler N. Summary stage 2018: Codes and coding instructions. National Cancer Institute: Bethesda, MD; 2018. [15] Director-general for statistics and information policy ministry of health. Vital statistics. Labour and Welfare Japan. [16] Ito Y, Ioka A, Tanaka M, Nakayama T, Tsukuma H. Trends in cancer incidence and mortality in Osaka, Japan: evaluation of cancer control activities. Cancer Sci 2009;100:2390–5. [17] Chaturvedi P, Singh A, Chien CY, Warnakulasuriya S. Tobacco related oral cancer. BMJ 2019;365:l2142. [18] Thun MJ, Linet MS, Haiman CA, Cerhan JR, Schottenfeld D. Cancer epidemiology and prevention. Oxford University Press; 2017. [19] Chaturvedi AK, Anderson WF, Lortet-Tieulent J, Curado MP, Ferlay J, Franceschi S, et al. Worldwide trends in incidence rates for oral cavity and oropharyngeal cancers. J Clin Oncol 2013;31:4550–9. [20] Louie KS, Mehanna H, Sasieni P. Trends in head and neck cancers in England from 1995 to 2011 and projections up to 2025. Oral Oncol 2015;51:341–8. [21] Zaitsu T, Saito T, Kawaguchi Y. The oral healthcare system in Japan. Healthcare (Basel), 6; 2018. [22] Langevin SM, Michaud DS, Eliot M, Peters ES, McClean MD, Kelsey KT. Regular dental visits are associated with earlier stage at diagnosis for oral and pharyngeal cancer. Cancer Causes Control 2012;23:1821–9. [23] Haresaku S, Makino M, Sugiyama S, Naito T, Mario RJ. Comparison of practices, knowledge, confidence, and attitude toward oral cancer among oral health professionals between Japan and Australia. J Cancer Educ 2018;33:429–35. [24] Howlader NNA, Krapcho M, Miller D, Bishop K, Kosary CL, Yu M, et al. SEER cancer statistics review, 1975-2014, National Cancer Institute. Bethesda, MD. [25] Matsuda T, Sobue T. Recent trends in population-based cancer registries in Japan: the act on promotion of cancer registries and drastic changes in the historical registry. Int J Clin Oncol 2015;20:11–20.
Acknowledgements This study was supported by JSPS (Japan Society for the Promotion of Science) KAKENHI Grant Number (JP18K17107, JP18H03062), Health Labour Sciences Research Grant (H30-Gantaisaku-Ippan-009) from the Ministry of Health, Labour and Welfare, Japan. The funders had no role in the study design, data collection and analysis. The views and opinions expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the respective funding organisations. Appendix A. Supplementary material Supplementary data to this article can be found online at https:// doi.org/10.1016/j.oraloncology.2020.104653. References [1] Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018;68:394–424. [2] Marugame T, Matsuda T, Kamo K, Katanoda K, Ajiki W, Sobue T, et al. Cancer incidence and incidence rates in Japan in 2001 based on the data from 10 population-based cancer registries. Jpn J Clin Oncol 2007;37:884–91. [3] Hori M, Matsuda T, Shibata A, Katanoda K, Sobue T, Nishimoto H, et al. Cancer incidence and incidence rates in Japan in 2009: a study of 32 population-based cancer registries for the Monitoring of Cancer Incidence in Japan (MCIJ) project. Jpn J Clin Oncol 2015;45:884–91. [4] Cancer Registry and Statistics. Cancer Information Service, National Cancer Center, Japan. [Accessed October 2019]. [5] Gillison ML, Chaturvedi AK, Anderson WF, Fakhry C. Epidemiology of human papillomavirus-positive head and neck squamous cell carcinoma. J Clin Oncol 2015;33:3235–42. [6] Conway DI, Purkayastha M, Chestnutt IG. The changing epidemiology of oral cancer: definitions, trends, and risk factors. Br Dent J 2018;225:867–73.
4
Contents lists available at ScienceDirect
Oral Oncology journal homepage: www.elsevier.com/locate/oraloncology
Oral cavity cancer incidence rates in Osaka, Japan between 2000 and 2014 a,⁎
a
a
T
a
Shihoko Koyama , Takahiro Tabuchi , Sumiyo Okawa , Toshitaka Morishima , Shunsuke Ishimotob, Miki Ishibashib, Isao Miyashiroa a b
Cancer Control Center, Osaka International Cancer Institute, 3-1-69, Otemae, Chuo-ku, Osaka, Osaka 541-8567, Japan Dentistry, Osaka International Cancer Institute, 3-1-69, Otemae, Chuo-ku, Osaka, Osaka 541-8567, Japan
A R T I C LE I N FO
A B S T R A C T
Keywords: Epidemiology Oral cancer Japan
Background: We investigated trends in oral cavity cancer incidence from 2000 to 2014 in Osaka, Japan. Methods: Using Osaka Cancer Registry (OCR) data, oral cavity cancer incidence number and age-standardized incidence rates were calculated according to three 5-year-time-periods: 2000–2004, 2005–2009 and 2010–2014. We calculated the distribution of clinical stage for each 5-year period and the proportion of oral cavity cancer among all cancers. Results: A total of 6,086 oral cavity cancers were registered in OCR in 2000–2014. Across the period, between 55.6% and 65.0% were 65 years+ and approximately 60% were men. Tongue cancer accounted for 30.4% to 43.8% of the registrations, while gum accounted for 30.7% to 34.7%. 36.3% to 37.3% were regional, while 1.8% to 2.8% were distant. The age-standardized incidence rate of oral cavity cancer increased from 2.1/100,000 in 2000 to 3.8/100,000 in 2014, although the proportion of oral cavity cancer among all cancers only increased slightly from 0.71% in 2000 to 0.92% in 2014. Proportion of localized stage cancer was 60.8%–67.5% for tongue and 31.0%–49.5% for gum or floor of mouth. Proportion of distant stage cancer was 0.3%–1.0% for tongue and 2.5%–4.2% for gum or floor of mouth. Conclusions: Age-standardized incidence rate of oral cavity cancer increased, but was not higher than other countries. The proportion of localized stage tongue cancer was higher, while that of distant stage cancer was lower than other sites. Tongue cancer might be easier to detect in its earlier stages than other sites.
Introduction Oral cavity cancer is an important global public health problem. The latest report from the International Agency for Research on Cancer (IARC) showed that lip and oral cancers which include lips, tongue, gum, and floor of mouth, have an annual incidence of over 350,000 diagnosed cases, and an annual mortality of about 177,000 deaths worldwide [1]. Oral cavity cancer has usually been included as part of oral and pharyngeal cancer or head and neck cancer [2]. For example, the National Cancer Center Japan report ‘oral and pharygeal cancer’ incidence in online publications every year [3,4], but do not report the incidence of oral cavity cancer alone. As a result, reports/studies of trends in oral cavity cancer are rare, and trends in oral and pharyngeal cancer are often used as substitutes in Japan. Oral cavity cancers differ from pharyngeal cancers in their association with human papilloma virus (HPV): i.e., a meta-analysis carried out in 2015 [5] found that the proportion of HPV-attributable cases was
⁎
45.8% for oropharyngeal cancer and 24.2% for oral cavity cancer. Therefore, it may be important to use distinct terms: oral cavity cancer and pharyngeal cancer [6]. General dental practitioners more routinely examined patients’ oral mucosa than general medical practitioner [7]. Dentists' familiarity with, and access to, their patients' oral cavities make them particularly well suited to perform early detection examinations [8]. The percentage of people that visit a dental office at least once a year (regular dental check-up) increased from 34.1% in 2009 to 52.9% in 2016 [9]. However, it is not known whether early detection of oral cavity cancer has increased. The incidence rates of oral cancers vary considerably worldwide, ranging from 16.4 per 100,000 for men in India, to 5.0 per 100,000 for men in Singapore, to 10.6 per 100,000 for women in India, to 1.7 per 100,000 for women in Slovakia [10]. Although oral cavity cancer incidence has been reported in other countries [6,11], no study has updated the trends in incidence of oral cavity cancer in Japan. The objective of this study was to examine the trends in incidence of oral
Corresponding author. E-mail address: [email protected] (S. Koyama).
https://doi.org/10.1016/j.oraloncology.2020.104653 Received 16 November 2019; Received in revised form 27 February 2020; Accepted 14 March 2020 1368-8375/ © 2020 Elsevier Ltd. All rights reserved.
Oral Oncology 105 (2020) 104653
S. Koyama, et al.
cavity cancer from 2000 to 2014 in Osaka, Japan.
Table 1 Number and percentage of oral cavity cancer cases by characteristics reported to the OCR 2000–2014 : age, sex, site, and stage (N = 6,086).
Methods
Characteristic
Data and definition of oral cavity cancer Total Age < 30 30–44 45–54 55–64 65–74 75–84 85+ Sex Men Women Site Tongue Gum Floor of mouth Other* and unspecified parts of mouth Stage Localized Regional Distant site Unknown
We used data from the Osaka Cancer Registry (OCR), which is a population-based cancer registry that covers all cancer incidence observed in the Osaka prefecture [population: 8.8 million (2015 census)] [12]. Oral cavity cancer cases who were diagnosed between 2000 and 2014 were analyzed. Oral cavity cancers were defined by the International Classification of Diseases, 10th revision (ICD-10); tongue (C02.0, C02.1, C02.2, C02.3), gum (C03.0, C03.1, C03.9), floor of mouth (C04.0, C04.1, C04.8, C04.9, C05.0), inner lip and other and unspecified parts of mouth (Others) (C00.3, C00.4, C00.5, C00.6, C00.8, C00.9, C06.0, C06.1, C06.2, C06.8, C06.9)] [13]. Variables Year of diagnosis was divided into three groups: 2000–2004, 2005–2009 and 2010–2014. Age group was divided into seven groups; < 30, 30–44, 45–54, 55-64, 65–74, 75–84, and 85+. Cancer stage at diagnosis was classified into four groups; (1) Localized: cancer is confined to the original organ (T1, T2), (2) Regional: cancer has spread to regional lymph nodes and/or to immediately adjacent tissues (T3, T4a, T4b, N1, N2, N3), (3) Distant: cancer has metastasized to distant organs (M1), and (4) Unknown [14].
2000–2004 n %
2005–2009 n %
2010–2014 n %
1301
100.0
2084
100.0
2701
100.0
10 72 173 323 377 250 96
0.8 5.5 13.3 24.8 29.0 19.2 7.4
20 126 216 445 656 426 195
1.0 6.1 10.4 21.4 31.5 20.4 9.4
25 147 231 543 784 688 283
1.0 5.4 8.6 20.1 29.0 25.5 10.5
794 507
61.0 39.0
1,229 855
59.0 41.0
1572 1129
58.2 41.8
395 452 255 199
30.4 34.7 19.6 15.3
839 648 322 275
40.3 31.1 15.5 13.2
1182 829 368 322
43.8 30.7 13.6 11.9
559 483 37 222
43.0 37.1 2.8 17.1
1047 756 40 241
50.2 36.3 1.9 11.6
1451 1007 49 194
53.7 37.3 1.8 7.2
Abbreviations: OCR; Osaka cancer registry. * Other: inner lip, oral cavity cancer not otherwise specified.
Statistical analyses
The proportion of distant stage tongue cancer was 0.3%–1.0% and 2.5%–4.2% for gum or floor of mouth.
We calculated the incidence number and proportion by characteristics according to time period. Age-standardized incidence rates (ASRs) were calculated by sex and year of cancer diagnosis (between 2000 and 2014), using the population data by age group from Osaka Prefecture (the Population Census) [15], adjusting to the Japanese model population in 1985 (direct method). To validate the trend of oral cavity cancer, the proportion among all cancers (C00-C96) except in-situ cancers was also calculated for each year. In addition, we used joinpoint regression to observe ASR trends with an annual percent change (APC) [16]. Analyses were carried out using Stata version 15 (Stata Corporation, College Station, Texas, USA) and the Joinpoint Regression Program, Version 4.7.0.0 (Statistical Research and Applications Branch, National Cancer Institute). The study was reviewed and approved by the Research Ethics Committee of the Osaka International Cancer Institute (No.19149).
Discussion The present study is the first to examine the incidence rate of oral cavity cancer between 2000 and 2014 in Japan, suggesting that the agestandardized incidence rate increased from 2.1 per 100,000 persons in 2000 to 3.8 in 2014. ASRs for both sexes significantly increased in the joinpoint analysis (men:APC = 5.1%; women:APC = 5.7%; and both sexes:APC = 5.3%). However, this result should be interpreted cautiously as the proportion of oral cavity cancer among all cancers only increased slightly (from 0.71% in 2000 to 0.92%) in 2014. Lip and oral cavity cancers (C00-C06) accounted for approximately 2.0% of all cancers worldwide in 2018 [1]. Therefore, the incidence rate of oral cavity cancer in Japan found in this study may not be high. Smoking and use of chewed forms of tobacco are the most common causes of oral cavity cancer [17,18]. Although smoking rates are still increasing in developing countries, they are decreasing in developed economies such as Japan, England, and South Korea. The smoking rate in Japan decreased from 47.4% to 32.1% among men and from 11.5% to 8.5% among women between 2000 and 2014. A previous study has shown that the ASRs of oral cavity cancer have been declining worldwide, consistent with a decline in tobacco use between 1983 and 2003 [19]; the APC of the ASR was −0.9% between 2000 and 2013 [18]. However, in addition to the trends shown in this study, other countries have also indicated different trends: oral cavity cancer incidence rates increased for both sexes between 1995 and 2011 in England (men: APC 2.8%, women: APC 3.0%) [20], and also increased between 1999 and 2010 in South Korea (APC 1.2%) [11]. Among all sites of oral cavity cancer, the proportion of localized cases increased, while that of distant stage cases decreased. A possible reason for the increase in localized stage cancer may be that the number of Japanese people who visit dental clinics is increasing (as mentioned in the introduction) [9]. Distribution of stage varied by cancer site. In particular, the proportion of localized stage tongue cancer was higher, and the proportion of distant stage tongue cancer lower than other sites.
Results A total of 6,086 oral cavity cancer cases were registered in OCR between 2000 and 2014. Basic characteristics of oral cavity cancers according to age, sex, site and stage are shown in Table 1. Among oral cavity cancer patients, 55.6% to 65.0% were 65 years or older; approximately 60% were men. Tongue cancer accounted for 30.4% to 43.8%, while gum cancer accounted for 30.7% to 34.7%. In terms of clinical cancer stage, 36.3% to 37.3% were regional, while 1.8% to 2.8% were distant. ASRs of oral cavity cancer, and proportion of oral cavity cancer among all cancers are shown in Fig. 1 and supplementary Table S1. The ASR of oral cavity cancer (per 100,000 people) was 2.1 in 2000, 2.5 in 2005, 3.3 in 2010, and 3.8 in 2014. The proportion of oral cavity cancer among all cancers was 0.67%–1.00%. The results of the joinpoint analysis of ASRs are presented in Fig. 2. All ASRs significantly increased in 2000–2014 (men:APC = 5.1%; women: APC = 5.7%; and both sexes:APC = 5.3%). Table 2 shows the proportion of stage at diagnosis by site in the oral cavity. The proportion of localized stage tongue cancer was 60.8%–67.5% and 31.0%–49.5% for gum or floor of mouth. 2
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Fig. 1. Annual age-standardized incidence rate per 100,000 population of oral cavity cancer by sex (left axis), and proportion of oral cavity cancer within all cancers (C00-C96) (right axis).
oral cavity cancer registration in the OCR was not perfect. However, the proportion of death certificate only (DCO) for oral and pharyngeal cancer (C00-C14), which is often regarded as an index of completeness, was low at approximately 2.8% in 2014. In addition, cancer control has been systematically promoted by the national government of Japan since 2006 [25]. As a result, the number of cancer cases submitted to the registry from each hospital has gradually increased in the last 15 years. The increase in age-sex adjusted oral cavity cancer incidence in Osaka may be affected by the increased number of registered cases. Second, because we used data from the OCR, we need to interpret the findings with limited generalizability to the whole of Japan. Nevertheless, in 2014, the ASR of oral and pharyngeal cancer (C00-C14) in Osaka (men:13.8, women:5.3) was almost equal to that for the whole of Japan (men:12.8, women:4.3) [4]. In conclusion, we have described trends in oral cavity cancer incidence using population-based data from a cancer registry in Osaka, Japan. The ASR of oral cavity cancer increased, but may not be high compared with other countries. We suggest dentists should be given additional training on oral cancer screening programs so that patients
Tongue cancer might be easier to detect in its earlier stage than other sites. This may, in part, be a result of the National Health Promotion Campaign for the 21st century, ‘Healthy Japan 21′, which was proposed to prevent lifestyle-related diseases. In 2000, Healthy Japan 21 included a focus on oral health. Nationwide health promotion activities were suggested, including the oral health-related goal of increasing the number of people attending regular dental check-ups [21]. It has been reported that regular dental check-ups are associated with earlier-stage diagnosis for oral cavity cancer [22]. However, in Japan only 34.1% of dentists in private clinics always or usually perform oral cavity cancer screening, which is significantly lower than in other countries such as Australia (89.3%) [23]. Therefore, further education and training programs for oral cavity cancer screening should be given to dentists to improve prevention and early detection [23]. Early detection has a large impact on prognosis. The survival of oral cavity cancer patients depends on the stage at diagnosis; i.e., the 5-year survival rate of patients with localized stage tongue cancer was 79.8%, but 38.8% for distant stage [24]. The present study has some limitations. First, the completeness of
Fig. 2. Age-standardized incidence rate trends using joinpoint regression. 3
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Table 2 Distribution of stage at diagnosis by site in oral cavity. 2000–2004
Site Tongue Gum Floor of mouth Other* Total
2005–2009
2010–2014
Localized %
Regional %
Distant site %
Unknown %
Localized %
Regional %
Distant site %
Unknown %
Localized %
Regional %
Distant site %
Unknown %
60.8 31.0 40.0 38.7 43.0
31.4 42.3 37.6 36.2 37.1
1.0 4.2 3.5 2.5 2.8
6.8 22.6 18.8 22.6 17.1
66.9 35.3 44.1 41.8 50.2
28.6 45.2 36.6 38.2 36.3
0.5 2.6 2.8 3.6 1.9
4.1 16.8 16.5 16.4 11.6
67.5 40.0 49.5 43.2 53.7
29.1 46.8 41.0 38.5 37.3
0.3 2.5 2.7 4.3 1.8
3.0 10.6 6.8 14.0 7.2
* Other: inner lip, oral cavity cancer not otherwise specified.
can be screened in regular dental check-ups. Similarly, patients should maintain regular check-up visits not only for the prevention of caries and periodontal treatment but also for the prevention and early detection of oral cancer.
[7] Carter LM, Ogden GR. Oral cancer awareness of general medical and general dental practitioners. Br Dent J 2007;E10. 203, discussion 248–9. [8] Mashberg A. Diagnosis of early oral and oropharyngeal squamous carcinoma: obstacles and their amelioration. Oral Oncol 2000;36:253–5. [9] The Japan National Health. Nutrition Suevey 2016https://www.mhlw.go.jp/file/ 04-Houdouhappyou-10904750-Kenkoukyoku-Gantaisakukenkouzoushinka/ kekkagaiyou_7.pdf. [10] Adami HO, Hunter DJ, Lagiou P, Mucci L. Textbook of cancer epidemiology. Oxford University Press; 2018. [11] Choi SW, Moon EK, Park JY, Jung KW, Oh CM, Kong HJ, et al. Trends in the incidence of and survival rates for oral cavity cancer in the Korean population. Oral Dis 2014;20:773–9. [12] Toyoda Y, Tabuchi T, Nakata K, Morishima T, Nakayama T, Miyashiro I, et al. Increase in incidental detection of thyroid cancer in Osaka. Japan Cancer Sci 2018;109:2310–4. [13] Friz. International classification of diseases for oncology: World Health Organization; 2012. [14] Ruhl JLCC, Hurlbut A, Ries LAG, Adamo P, Dickie L, Schussler N. Summary stage 2018: Codes and coding instructions. National Cancer Institute: Bethesda, MD; 2018. [15] Director-general for statistics and information policy ministry of health. Vital statistics. Labour and Welfare Japan. [16] Ito Y, Ioka A, Tanaka M, Nakayama T, Tsukuma H. Trends in cancer incidence and mortality in Osaka, Japan: evaluation of cancer control activities. Cancer Sci 2009;100:2390–5. [17] Chaturvedi P, Singh A, Chien CY, Warnakulasuriya S. Tobacco related oral cancer. BMJ 2019;365:l2142. [18] Thun MJ, Linet MS, Haiman CA, Cerhan JR, Schottenfeld D. Cancer epidemiology and prevention. Oxford University Press; 2017. [19] Chaturvedi AK, Anderson WF, Lortet-Tieulent J, Curado MP, Ferlay J, Franceschi S, et al. Worldwide trends in incidence rates for oral cavity and oropharyngeal cancers. J Clin Oncol 2013;31:4550–9. [20] Louie KS, Mehanna H, Sasieni P. Trends in head and neck cancers in England from 1995 to 2011 and projections up to 2025. Oral Oncol 2015;51:341–8. [21] Zaitsu T, Saito T, Kawaguchi Y. The oral healthcare system in Japan. Healthcare (Basel), 6; 2018. [22] Langevin SM, Michaud DS, Eliot M, Peters ES, McClean MD, Kelsey KT. Regular dental visits are associated with earlier stage at diagnosis for oral and pharyngeal cancer. Cancer Causes Control 2012;23:1821–9. [23] Haresaku S, Makino M, Sugiyama S, Naito T, Mario RJ. Comparison of practices, knowledge, confidence, and attitude toward oral cancer among oral health professionals between Japan and Australia. J Cancer Educ 2018;33:429–35. [24] Howlader NNA, Krapcho M, Miller D, Bishop K, Kosary CL, Yu M, et al. SEER cancer statistics review, 1975-2014, National Cancer Institute. Bethesda, MD. [25] Matsuda T, Sobue T. Recent trends in population-based cancer registries in Japan: the act on promotion of cancer registries and drastic changes in the historical registry. Int J Clin Oncol 2015;20:11–20.
Acknowledgements This study was supported by JSPS (Japan Society for the Promotion of Science) KAKENHI Grant Number (JP18K17107, JP18H03062), Health Labour Sciences Research Grant (H30-Gantaisaku-Ippan-009) from the Ministry of Health, Labour and Welfare, Japan. The funders had no role in the study design, data collection and analysis. The views and opinions expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the respective funding organisations. Appendix A. Supplementary material Supplementary data to this article can be found online at https:// doi.org/10.1016/j.oraloncology.2020.104653. References [1] Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018;68:394–424. [2] Marugame T, Matsuda T, Kamo K, Katanoda K, Ajiki W, Sobue T, et al. Cancer incidence and incidence rates in Japan in 2001 based on the data from 10 population-based cancer registries. Jpn J Clin Oncol 2007;37:884–91. [3] Hori M, Matsuda T, Shibata A, Katanoda K, Sobue T, Nishimoto H, et al. Cancer incidence and incidence rates in Japan in 2009: a study of 32 population-based cancer registries for the Monitoring of Cancer Incidence in Japan (MCIJ) project. Jpn J Clin Oncol 2015;45:884–91. [4] Cancer Registry and Statistics. Cancer Information Service, National Cancer Center, Japan. [Accessed October 2019]. [5] Gillison ML, Chaturvedi AK, Anderson WF, Fakhry C. Epidemiology of human papillomavirus-positive head and neck squamous cell carcinoma. J Clin Oncol 2015;33:3235–42. [6] Conway DI, Purkayastha M, Chestnutt IG. The changing epidemiology of oral cancer: definitions, trends, and risk factors. Br Dent J 2018;225:867–73.
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