==== Front Ann Saudi MedAnn Saudi MedAnnals of Saudi Medicine0256-49470975-4466King Faisal Specialist Hospital and Research Centre 1714301810.5144/0256-4947.2006.433asm-6-433Original ArticleThe incidence of lung cancer in the Gulf Cooperation Council countries Al-Hamdan Nasser *Al-Jarallah Mohammed †Ravichandran Kandasamy ‡Al-Sayyad Jamal §Al-Lawati Jawad ||Khazal Zainab ¶Al-Khateeb Falah ¶Abdulwahab Abdulaziem #Al-Mulla Ahmed #Al-Asfour Adel †Bazarbashi Shouki ** * Ministry of Health, Kingdom of Saudi Arabia † Ministry of Health, State of Kuwait ‡ Department of Biostatistics, Epidemiology and Scientific Computing, King Faisal Specialist Hospital and Research Center, Riyadh, Kingdom of Saudi Arabia § Ministry of Health, Kingdom of Bahrain || Ministry of Health, Sultanate of Oman ¶ Ministry of Health, United Arab Emirates # Ministry of Health, State of Qatar ** King Faisal Cancer Center, King Faisal Specialist Hospital and Research Center, Riyadh, Kingdom of Saudi ArabiaCorrespondence and reprint requests: Nasser Al Hamdan, MD, Ministry of Health, P.O. Box 6344, Riyadh 11442, Saudi Arabia, T: +966-1-497 2272, F: +966-1-496 0163, nhamdan@kfshrc.edu.saNov-Dec 2006 26 6 433 438 01 8 2006 Copyright © 2006, Annals of Saudi Medicine2006This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.BACKGROUND Lung cancer is the most common cancer in the world, with an estimated number of 1.3 million new cases as of 2002. This is the first report from the countries that comprise the Gulf Cooperation Council (GCC). PATIENTS AND METHODS All the primary lung cancer cases registered in the Gulf Center for Cancer Registration during 1998 to 2001 were used to calculate the age-standardized incidence rate (ASR) per 100 000 person-years by the direct standardization method. RESULTS Overall, there were 1607 (1261 males, 346 females) primary lung cancer cases registered during this period with the male to female ratio of 3.6:1. The highest ASR was in Bahrain (34.3 for males, 12.1 for females) followed by Qatar (18.5 for males, 5.5 for females) and Kuwait (13.8 for males, 4.0 for females); the lowest rate was in Saudi Arabia (4.8 for males, 1.3 for females). The mean age at diagnosis for males ranged from 68.7 years in Bahrain to 59.2 years in Oman. For females it ranged from 68.2 years in Bahrain to 58.0 years in Oman. Squamous cell carcinoma in males (except in Qatar) and adenocarcinoma in females were the predominant histological type. CONCLUSIONS Cancer of the lung is one of the common cancers among males in all the GCC countries and ranks second among Bahraini females. Adenocarcinomas were more common in women than men. ==== Body Lung cancer was the most common cancer in the world in 2002 with an estimated 1.3 million new cases. Almost half of these cases arise from developing countries where resources for treatment and prevention are scarce. Further, with 71% of the world total occurring in men, the disease is more common in men than women. The highest incidence rates in men are seen in Europe (especially eastern Europe) and North America. The rates in Australia/New Zealand, China, Japan and Southeast Asia are moderately high. In women, high incidence rates are observed in North America and northwest Europe (UK, Iceland, Denmark) with moderate incidence rates in Australia/New Zealand and China.1 Adenocarcinomas are more common in women than in men, in both smokers and non-smokers. In nonsmoking patients with lung cancer, adenocarcinoma is the most frequently observed histological tumor type.2–3 This paper describes lung cancer incidence among nationals of the Gulf Cooperation Council (GCC) countries, based on four years data. There are no earlier studies, based on the population data, describing the incidence and patterns of lung cancer in the GCC countries. Patients and methods A National Cancer Registry (NCR) exist in each GCC country and they are networked through the Gulf Center for Cancer Registration (GCCR), which has been functioning since 1997 and accumulating incidence data since 1 January 1998. In the GCC countries there is mandatory cancer case reporting, but data is collected by active and passive methods. The data collected includes personal identity details, age, sex, date of diagnosis, histology, and topography. The International Classification of Diseases for Oncology second edition (ICDO-2, WHO, 1990) is used to classify the topography and morphology of the tumor. The lung cancer cases included in this study were defined as code numbers C33 and C34 of ICDO-2. All the primary lung cancer cases registered in the GCCR during 1998 to 2001 were included in this study. The age-standardized incidence rate (ASR) per 100 000 person-years was calculated by direct standardization, using the world standard population. To calculate the ASR, the gender specific population of GCC nationals was estimated with 5-year age spans. Information on prevalence of smoking in GCC countries were obtained from the Family Health Survey conducted in all the GCC countries.4–9 The fraction of lung cancer cases associated with tobacco smoking was calculated by assuming that, if no one smoked, the incidence of lung cancer would be the same as a population of non-smokers in the USA and the method used was that described by Parkin et al.10 Results Overall, there were 1607 (1261 males, 346 females) primary lung cancer cases registered during this period among GCC nationals with a male to female ratio of 3.6:1. The male to female ratio ranged from 2.8 in the Emirates and Bahrain to 4.4 in Oman (Table 1). Lung cancer was the most common cancer among males in Bahrain, Qatar and the Emirates; it ranked second, third and fourth in Kuwait, Oman and Saudi Arabia, respectively. In males, the highest ASR was in Bahrain followed by Qatar, Kuwait, Oman, the Emirates and Saudi Arabia. In females, the highest ASR was in Bahrain followed by Qatar, Kuwait, the Emirates, Oman and Saudi Arabia (Table 1). Among males, the mean age at diagnosis was higher in Bahrain (68.7±11.8 years, mean±SD) than in the Emirates (63.4±13.1 years), Saudi Arabia (63.4±13.1 years), Kuwait (63.4±12.4 years), Qatar (60.8±15.7 years) and Oman (59.2±13.5 years). Among females the mean age was higher in Bahrain (68.2±12.7 years) than in the Emirates (64.5±12.6 years), Qatar (63.9±10.0 years), Saudi Arabia (63.1±13.8 years), Kuwait (62.9±15.7 years) and Oman (58.0±12.1 years). In general, the incidence of lung cancer increases with age up to 69 years in males and up to 60 years in females (Figures 1a, 1b). The microscopic verification (histological or cytological method) of diagnosis ranged from 62% in the Emirates to 93% in Saudi Arabia. Within the four major histologically distinct types (squamous-cell carcinoma, adenocarcinoma, small-cell carcinoma, and large-cell carcinoma), the predominant types were squamous cell carcinoma in males (except in Qatar) and adenocarcinoma in females (Figures 2a, 2b). The above four types together accounted for 89.7%, 87.5%, 81.7%, 64.9%, 54.7% and 49.0% of total male lung cancers in Qatar, the Emirates, Saudi Arabia, Bahrain, Oman and Kuwait. Among females, these four types together ranged from 53.1% in Kuwait to 85.7% in Qatar. There were only 8 sarcoma cases in our data (one male each in Oman and Kuwait; three in each gender in Saudi Arabia). Figure 3 shows the smoking prevalence (current smoker of any tobacco product) among males and females aged 15 years or older during the mid 1990s. The highest prevalence, among males, was observed in Kuwait (32.4%) followed by Bahrain (25.8%), Qatar (23.6%), the Emirates (20.9%), Saudi Arabia (20.3%) and Oman (15.5%). In females, the prevalence in Bahrain (8.8%) was at least 6-fold higher compared with other GCC countries (ranging from 0.5% in Qatar to 1.5% in Oman and Kuwait). The fraction of lung cancer cases associated with tobacco smoking in the GCC countries, among males, ranged from 5% in Saudi Arabia to 84% in Bahrain. In females, the fraction was 0 in three countries (the Emirates, Saudi Arabia and Oman), 2% in Kuwait, 26% in Qatar and 65% in Bahrain (Table 2). Discussion In comparing the ASR for lung cancer in the GCC countries with other countries listed in Cancer Incidence in Five Continents,11 the incidence in Bahraini males was greater than the African and most of the Asian populations. The incidence in Bahraini females was greater than in females in African, Asian (except China) and most of the European countries. The most important risk factor for lung cancer is tobacco smoking and the supportive evidence for this association has been reviewed many times by different scientific groups and institutions.12–13 By 1985, it was estimated that lung cancer was the most common malignant disease, and about 85% to 90% of lung cancer cases were attributed to tobacco smoking.10,14 At the beginning of the 1990s some 86% of lung cancer cases in men and 49% in women were attributed to tobacco smoking.15 In women, the proportion of tobacco-related lung cancer is much more variable throughout the world, reflecting differences in the development of the tobacco smoking epidemic. The proportion of cancers in women that can be attributed to tobacco varies from about 80% in the UK to virtually nothing in Spain and Portugal.15 Since the risk associated with tobacco smoking in the GCC countries is not known, the fraction of lung cancer cases associated with tobacco smoking was calculated by assuming that, if no one smoked, the incidence of lung cancer would be the same as a population of non-smokers in the USA. For both genders, the estimates from Bahrain precisely reflect the world pattern and estimates from other GCC countries closely approximate the world pattern. The prevalence of smoking in the GCC countries, obtained from surveys conducted in the mid-1990s (Emirates, Bahrain and Oman in 1995; Saudi Arabia and Kuwait in 1996; Qatar in 1998), are published elsewhere.4–9 Because this information was collected from the household head, it is likely to underestimate smoking prevalence, particularly among young adults and women, because of either a lack of knowledge or reluctance to answering questions truthfully. Despite these drawbacks, the results of these surveys were used in this study because of the uniformity in the study design, sampling procedure, data collection and analysis. Though the incidence of cancer in our study cannot be directly attributed to the smoking prevalence from these surveys, the higher prevalence and longer history of smoking among Bahrainis (both men and women) than other GCC nationalities was reflected in the higher incidence of lung cancer and the higher proportion of lung cancer attributable to tobacco smoking compared with other GCC countries. The relationship between passive exposure to smoke and lung cancer was first shown by Hirayama at the beginning of the 1980s,16 and soon after by two other groups.17–18 It is now estimated that environmental exposure to tobacco smoke increases risk by 15% to 25%,19–21 even after adjustment for other possible confounding factors.22–23 Environmental exposure can be the result of exhaled smoke from smokers and sidestream smoke from burning tobacco products (cigarettes, cigars, and pipes). Sidestream smoke has a higher concentration of carcinogenic compounds than mainstream smoke.24 As such there is no information, to the knowledge of the authors, on the level of environmental exposure in the GCC countries. Other factors known to increase the risk of lung cancer are occupational exposure to asbestos, some metals (e.g., nickel, arsenic, cadmium), radon (particularly amongst miners) and ionizing radiation.15 Though the contribution of environmental factors other than tobacco smoke to total population rates of cancer is small15, the effect of these factors remains unstudied in GCC countries. Carcinoma of the lung can be divided into four histologically distinct types: squamous-cell carcinoma, adenocarcinoma, small-cell carcinoma, and large-cell carcinoma.25 The four types differ not only in terms of their clinical features, responses to treatment, and prognosis, but their distribution varies among smokers and non-smokers also.26 Smoking increases the risk of all histological types of lung cancer, although the relative risk is greater for squamous-cell and small-cell carcinomas than for adenocarcinomas.27–29 Adenocarcinoma has always been more common in women than in men, in both smokers and non-smokers. In non-smoking patients with lung cancer, adenocarcinoma is the most frequently observed histological tumor type.2–3 However, the proportion of lung cancers that are adenocarcinomas is lower in Europe than in Asia or North America.30 Our study also shows that adenocarcinomas in women are more common than in men and the proportion is higher than in European women. There is no doubt that smoking cessation is the best way to reduce risk of lung cancer and many observational studies (both cohort and case-control) have confirmed this fact. For men, the evidence shows that several populations have now passed the peak of the tobacco-related epidemic and incidence rates are now declining (for example, in the United States, Australia, Singapore and the countries of Northern and Western Europe).15 As 85% to 90% of lung cancers are attributable to tobacco use, the incidence of lung cancer in the GCC countries will rise in coming decades due to an increase in cigarette smoking unless extensive control measures on tobacco are implemented. From a public health point of view, more benefit in terms of an immediate impact on number of deaths from lung cancer can be gained by persuading adult smokers to give up rather than focusing on smoking prevention in adolescents.31–33 Antismoking programs should therefore be a public health priority in these countries and further work should be done to identify environmental causes in addition to finding the risk associated with tobacco smoking. Figure 1a Age specific incidence rate of lung cancer among male GCC nationals in the GCC countries, 1998–2001. Figure 1b Age specific incidence rate of lung cancer among female GCC nationals in the GCC countries, 1998–2001. Figure 2a Histological distribution among male lung cancer cases in the GCC countries: 1998–2001. Figure 2b Histological distribution among female lung cancer cases in the GCC countries: 1998–2001. Figure 3 Prevalence of smoking by gender among GCC nationals in GCC countries. Table 1 Number, percentage, age-standardised incidence rate (ASR) and ranking of lung cancer in the GCC countries by gender (1998–2001). Country Male Female Sex Ratio No. % ASR Rank No. % ASR Rank Emirates 48 8.8 7.2 1 17 2.9 2.9 10 2.8:1 Bahrain 151 20.0 34.3 1 53 6.8 12.1 2 2.8:1 Saudi Arabia 778 6.5 4.8 4 201 1.8 1.3 18 3.9:1 Oman 159 8.4 9.2 3 36 2.2 2.2 13 4.4:1 Qatar 29 9.9 18.5 1 7 2.3 5.5 11 4.1:1 Kuwait 96 10.8 13.8 2 32 2.8 4.0 9 3.0:1 Table 2 Total (average per year, based on 1998–2001 cases) and percentage of lung cancer cases attributable to tobacco smoking in GCC countries. Country Males Females Total cases % Tobacco attributable Total cases % Tobacco attributable Emirates 12 28 4 0 Bahrain 38 84 13 65 Saudi Arabia 195 5 50 0 Oman 40 40 9 0 Qatar 7 69 2 26 Kuwait 24 61 8 2 ==== Refs References 1 Ferlay J Bray F Pisani P Parkin DM GLOBOCAN 2002: Cancer Incidence, Mortality and Prevalence Worldwide, Version 2.0 IARC Cancer Base No. 5 IARC Press Lyon 2004 2 Muscat JE Wynder EL Lung cancer pathology in smokers, ex-smokers and never smokers Cancer Lett 1995 88 1 5 7850764 3 Boffetta P Jarvholm B Brennan P Nyren O Incidence of lung cancer in a large cohort of non-smoking men from Sweden Int J Cancer 2001 94 591 593 11745449 4 Naseeb T Farid SM Bahrain Family Health Survey 1996 Ministry of Health State of Bahrain 2000 5 Fikri M Farid SM United Arab Emirates Family Health Survey 1996 Ministry of Health United Arab Emirates 2000 6 Alnesef Y Al-Rashoud R Farid SM Kuwait Family Health Survey 1996 Ministry of Health State of Kuwait 2000 7 Sulaiman AJM Al-Riyami A Farid SM Oman Family Health Survey 1996 Ministry of Health Sultanate of Oman 2000 8 Jaber KA Farid SM Qatar Family Health Survey 1996 Ministry of Health State of Qatar 2000 9 Khoja TA Farid SM Saudi Arabia Family Health Survey 1996 Ministry of Health Kingdom of Saudi Arabia 2000 10 Parkin DM Pisani P Lopez AD Masuyer E At least one in seven cases of cancer is caused by smoking: global estimates for 1985 Int J Cancer 1994 59 494 504 7960219 11 Parkin DM Whelan SL Ferlay J Teppo L Thomas B Cancer Incidence in Five Continents VIII Publication No 155 IARC Lyon 2002 12 International Agency for Research on Cancer Tobacco smoking: evaluation of carcinogenic risk to humans IARC monographs on the evaluation of carcinogenic risk to humans Publication No 38 IARC Press Lyon 1986 13 Royal College of Physicians Smoking or health: the third report from the Royal College of Physicians of London Pitman Medical London 1977 14 Schottenfeld D Fraumeni JF Jr Cancer epidemiology and prevention 2nd edn Oxford University Press New York 1986 15 Parkin DM Bray FI Devesa SS Cancer burden in the year 2000. The global picture Euro J Cancer 2001 37 S4 S66 16 Hirayama T Non-smoking wives of heavy smokers have a higher risk of lung cancer: a study from Japan B M J 1981 282 183 185 17 Trichopoulos D Kalandidi A Sparros L MacMahon B Lung cancer and passive smoking Int J Cancer 1981 27 1 4 7251227 18 Garfinkel L Time trends in lung cancer mortality among nonsmokers and a note on passive smoking J Natl Cancer Inst 1981 66 1061 1066 6941041 19 Dockery DW Trichopoulos D Risk of lung cancer from environmental exposures to tobacco smoke Cancer Causes Control 1997 8 333 345 9498897 20 Boffetta P Agudo A Ahrens W Multicenter case-control study of exposure to environmental tobacco smoke and lung cancer in Europe J Natl Cancer Inst 1998 90 1440 1450 9776409 21 Zhong L Goldberg MS Parent ME Hanley JA Exposure to environmental tobacco smoke and the risk of lung cancer: a meta-analysis Lung Cancer 2000 27 3 18 10672779 22 Fontham ETH Correa P Reynolds P Environmental tobacco smoke and lung cancer in nonsmoking women: a multicenter study J A M A 1994 271 1752 1759 23 Cardenas VM Thun MJ Austin H Environmental tobacco smoke and lung cancer mortality in the American Cancer Society’s Cancer Prevention Study II Cancer Causes Control 1997 8 57 64 9051323 24 Jenkins RA Guerin MR Tomkins BA The chemistry of environmental tobacco smoke: composition and measurement CRC Press LLC Boca Raton 2000 25 Churg A Lung cancer cell type and occupational exposure Samet JM Epidemiology of lung cancer Marcel Dekker Inc New York 1994 413 436 26 Tyczynski JE Bray F Parkin DM Lung cancer in Europe in 2000: epidemiology, prevention, and early detection Lancet Oncol 2003 4 45 55 12517539 27 Simonato L Agudo A Ahrens W Lung cancer and cigarette smoking in Europe: an update of risk estimates and an assessment of inter-country heterogeneity Int J Cancer 2001 91 876 887 11275995 28 Jedrychowski W Becher H Wahrendorf J Basa-Cierpialek Z Gomola K Effect of tobacco smoking on various histological types of lung cancer J Cancer Res Clin Oncol 1992 118 276 282 1315780 29 Dosemeci M Gokmen I Unsal M Hayes RB Blair A Tobacco, alcohol use, and risks of laryngeal and lung cancer by subsite and histologic type in Turkey Cancer Causes Control 1997 8 729 737 9328195 30 Parkin DM Sankaranarayanan R Overview on small cell lung cancer in the world: industrialized countries, Third World, Eastern Europe Anticancer Res 1994(b) 14 277 282 8166467 31 Hakulinen T Pukkala E Future incidence of lung cancer: forecast based on hypothetical changes in the smoking habits of males Int J Epidemiol 1981 10 233 240 7287283 32 Doll R Peto R Wheatley K Gray R Sutherland I Mortality in relation to smoking: 40 years’ observations on male British doctors B M J 1994 309 901 911 33 Peto R Smoking and deaths: the past 40 years and the next 40 B M J 1994 309 937 939