Policy Review

Tackling cancer control in the Gulf Cooperation Council Countries Saleh Al-Othman, Abdelali Haoudi, Samar Alhomoud, Abdullah Alkhenizan, Tawfik Khoja, Ali Al-Zahrani

Cancer is a major health problem in both high income and middle-to-low income countries, and is the second leading cause of death in the world. Although more than a third of cancer could be prevented and another third could be cured if diagnosed early, it remains a huge challenge to health-care systems worldwide. Despite substantial improvements in health services some of the countries in the Gulf region, the burden of non-communicable diseases is a major threat, primarily due to the rapid socioeconomic shifts that have led to unfavourable changes in lifestyle such as increased tobacco use, decreased physical activity, and consumption of unhealthy food. In the Gulf Cooperation Council states (United Arab Emirates, Bahrain, Saudi Arabia, Oman, Qatar, and Kuwait), advanced breast cancer, colorectal cancer, leukaemia, thyroid cancer, and non-Hodgkin lymphomas are the most common cancers affecting younger populations compared with other countries. By contrast with cancer prevalence in developed countries, prostate, lung, and cervical cancers are not among the most common cancers in the Gulf region. In view of the increased cost of cancer management worldwide, integrated approaches between primary, secondary, and tertiary health-care systems with special focus on prevention and early detection is an essential step in the countries’ efforts in the fight against cancer.

Introduction Cancer is a major health problem in both high income and low-to-middle-income countries, and is the second leading cause of death in the world. The global incidence of cancer in 2012 was 14 million.1 The estimated number of new cases of cancer is expected to continue to rise by 3–4% every year, and more than 65% of this increase will occur in low-to-middle-income countries where healthcare facilities and patient care are restricted.1 In the WHO eastern Mediterranean region, the incidence of cancer is predicted to rise by 80% over the next decade. Although two-thirds of cancers could be prevented or cured if diagnosed early, cancer constitutes a profound challenge to health-care systems, patients and their families, and society as a whole. Therefore, combating cancer necessitates integration between primary, secondary, and tertiary medical care in all countries. People in the Gulf region have achieved rapid improvements in health care over the past 20 years, better control of communicable diseases, and have longer life expectancy. These improvements have happened alongside rapid socioeconomic changes that have modified the populations’ lifestyles, such as increased tobacco use, decreased physical activity, and increased consumption of unhealthy food. In combination, all of these factors have likely influenced the prevalence of some types of cancer.3 In 1997, the Gulf Centre for Cancer Registration (GCCR) was established to provide cancer incidence data for nationals of the Gulf Cooperation Council (GCC; United Arab Emirates [UAE], Bahrain, Saudi Arabia, Oman, Qatar, and Kuwait) states. GCCR works under the jurisdiction of the executive office of the health ministers’ council for GCC states. Raw data for cancer prevalence and population estimates are provided by each national cancer registry in the six GCC states. The primary objectives of the GCCR are to collect and classify www.thelancet.com/oncology Vol 16 May 2015

information on all cancer cases to produce statistics on the occurrence in a defined population, to provide technical support for early detection and screening programmes, and to facilitate epidemiological studies to provide a framework for assessment and control. This initiative was the groundwork for the strategic plans (2004–09 and 2010–20) for cancer prevention and control in the GCC states. Furthermore, a framework comprising seven approaches and strategic actions has been developed to support member states in developing national action plans and implementation of cancer control activities.4 These strategies are in line with the WHO global strategy for the prevention and control of non-communicable diseases (2008–13), and the WHO strategy against cancer through effective integration between primary, secondary, and tertiary prevention programmes, which aim to prevent preventable cancers, cure applicable cancers through early detection and management, and relieve pain and improve quality of life through palliative care services.

Lancet Oncol 2015; 16: e246–57 Gulf Centre for Cancer Control and Prevention (S Al-Othman MD, A Al-Zahrani MD), Department of Surgery (S Alhomoud MD), and Department of Family Medicine (A Alkhenizan MD), King Faisal Special Hospital and Research Centre, Riyadh, Saudi Arabia; King Abdullah International Medical Research Center, King Abdulaziz Medical Citty, Riyadh, Saudi Arabia (A Haoudi PhD); Division of Genetics and Genomics, Boston Children’s Hospital, Harvard Medical School, Boston, MA, USA (A Haoudi); and Health Ministers Council for Cooperation Council, Riyadh, Saudi Arabia (Prof T Khoja MD) Correspondence to: Dr Saleh Al-Othman, Gulf Centre for Cancer Control and Prevention, King Faisal Special Hospital and Research Centre, PO Box 3354, Riyadh 11211, Saudi Arabia [email protected]

Incidence From January, 1998, to December, 2009, 119 288 newly diagnosed cancer cases among nationals of the GCC states were reported by the six cancer registries to the GCCR. Of these, 58 629 patients (49·1%) were male and 60 659 (50·9%) were female. Most cases were reported from Saudi Arabia, followed by Oman, Kuwait, Bahrain, UAE, and Qatar (table 1).4 Direct age standardisation is a common method used to compare several populations that differ with respect to age structure. The calculated incidence is known as the world standardised incidence rate, which is usually expressed per 100 000 individuals. For a 12-year period (1998–2009), we calculated the age-standardised rate (ASR) by obtaining the age-specific rates and applying these rates to the standard world population for each age e246

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Male

Female

Total

Bahrain

2442 (4·2%)

2687 (4·4%)

5129 (4·3%)

Kuwait

3743 (6·4%)

4947 (8·2%)

8690 (7·3%)

Oman

5570 (9·5%)

5142 (8·5%)

Qatar

964 (1·6%)

1109 (1·8%)

2073 (1·7%)

43 920 (74·9%)

44 557 (73·5%)

88 477 (74·2%)

Saudi Arabia UAE

1990 (3·4%)

2217 (3·7%)

Total

58 629 (100%)

60 659 (100%)

10 712 (9·0)

4207 (3·5%) 119 288 (100%)

UAE=United Arab Emirates.

Table 1: Cancer cases reported to Gulf Centre for Cancer Registration by nationality and sex, 1998–2009

account GCC nationals.5 However, the 2010 Saudi Arabian cancer registry reported 13 159 cases of cancer, of which 3188 cases (24·2%) were in non-Saudi Arabian nationals.6 Breast, colorectal, skin, non-Hodgkin lymphoma, and leukaemia were the five most common cancers among expatriates.6 The main difference was that skin cancer was ranked the second most common cancer among nonSaudi Arabian male individuals, after colorectal cancer, which represented 7·9% of the total number of cases. Similarly, cervical cancer (4·8%) ranked fourth in nonSaudi Arabian female individuals after breast, colorectal, and thyroid cancer.6

Breast and cervical cancer Colorectal 9·2

24·2 Breast

Non-Hodgkin lymphoma 8·8

9·2 Thyroid

Leukaemia 7·8

7·6 Colorectal

Lung 7·4

5·9 Non-Hodgkin lymphoma

Liver 7·3

5·5 Leukaemia

Prostate 6·5

3·7 Ovary

Bladder 4·8

3·3 Corpus Uteri

Stomach 4·6

2·9 Cervix Uteri

Hodgkin’s disease 4·0

2·9 Liver

Brain 3·8 50

40

30

20

2·7 Other Skin 10

Cancers in males (%)

0

10

20

30

40 50

Cancers in females (%)

Figure: Most common cancers among GCC nationals, 1998–2009 Data for 58 629 male patients and 60 659 female patients. Adapted from Salim and colleagues,2 with permission.

group.4 We used the SAS statistical package to generate the annual ASR and the mean annual ASR for all nationals of the GCC states. We calculated average annual ASR in the same way from the midpoint population (average of the total populations in 2003 and 2004) to obtain summary unbiased weighted cancer incidence rate for the 12 years from 1998–2009.4 The mean annual ASR for cancer incidence in the GCC states per 100 000 individuals was 82·9 for the period between 1998 and 2009. In the male population, colorectal cancer was the most common type of cancer at 9·2%, followed by non-Hodgkin lymphoma (8·8%), leukaemia (7·8%), lung (7·4%), and liver (7·3%). In the female population, breast cancer was the most common type of cancer, (24·2% of total cancers), followed by thyroid (9·2%), colorectal (7·6%), non-Hodgkin lymphoma (5·9%), and leukaemia (5·5%; figure). Overall, 48·5% of patients, both male and female, with cancer presented with advanced tumours (defined as either regional or distant metastasis) at the time of diagnosis.4 There is little published data on the incidence of cancer among expatriates in GCC states because most of the national registry data in the GCC countries only take into e247

The mean ASR for breast cancer was 20·4 cases per 100 000 women, and ranged between 16·9 per 100 000 in Saudi Arabia and 55·9 per 100 000 in Bahrain. Breast cancer incidence increased by 40% among GCC women during the 12-year period.4 Although advanced breast cancer is less common in developed countries, most patients with breast cancer in the GCC states presented at late stage with 58·1% at either regional or distant metastasis. Moreover, GCC women appeared to develop breast cancer at a younger age compared with women in high income countries; in these countries, less than 5% of all breast cancer cases occur in women younger than 40 years, compared to 25·5% for women in the GCC states.4 Similarly, cervical cancer was the fourth most common cancer affecting women worldwide,1–10 but was ranked seventh for women in the GCC states, at 2·9% of all cancers.4 These differences might be attributed to differences in environmental carcinogens, lifestyle, dietary habits, or cultural practices.7

Colorectal cancer Globally, the ASR of colorectal cancer was 20·1 per 100 000 in men and 14·6 per 100 000 in women.4 In high income countries, colorectal cancer ASR is 40·0 per 100 000 in men and 26·6 per 100 000 in women; in low to middle income countries, the rates are 10·2 per 100 000 and 7·7 per 100 000, respectively.4 Several studies have shown a decreased incidence of colorectal cancer among Arab populations when compared with other world populations.2 In spite of the low overall incidence of colon cancer in Arab countries, the Gulf countries show relatively high incidence in people younger than 40 years. In the GCC states, colorectal cancer was ranked as the second most common cancer with overall ASRs of 8·5 per 100 000 for men and 7·2 per 100 000 for women.4 In men, the ASR ranged between 6·6 per 100 000 in Oman and 16·4 per 100 000 in Kuwait, and in women the ASR ranged between 5·3 per 100 000 in Oman and 18·7 per 100 000 in Qatar. The reported incidence continued to increase between 1998 and 2009 in both sexes, with the total number of newly diagnosed colorectal cancer cases increasing by 3·4-times in men and 2·1-times in women, with most colorectal cancer www.thelancet.com/oncology Vol 16 May 2015

Policy Review

cases presented at advanced stage (61·5% of cases for both men and women). Only 20·7% of colorectal cases presented with localised disease, suggesting absence of screening and early detection programmes.4

Non-Hodgkin lymphoma Incidence of non-Hodgkin lymphoma in the GCC states accounted for 7·4% of all cancers, and ranked as the second most common malignancy among men (8·8%), and the fourth most common cancer in women (5·9%). Compared with how common non-Hodgkin lymphoma is globally (the seventh most common cancer in men and eighth in women), non-Hodgkin lymphoma appears to be more common in the GCC states. This finding is consistent with findings from previous studies that reported a substantial degree of association between nonHodgkin cancer incidence and geography.8

Lung cancer Lung cancer was the most commonly diagnosed cancer and the most common cause of cancer deaths worldwide (1·8 million new cases and 13·0% of total deaths),10 but ranked the seventh most common cancer in the GCC states with a prevalence of 4·7% of all cancers and an overall ASR of 7·2 per 100 000 for men and 2·2 per 100 000 for women. In men, the average ASR for lung cancer ranged between 5·9 per 100 000 in Saudi Arabia and 29·0 per 100 000 in Bahrain, whereas in women, it ranged between 2·9 per 100 000 in UAE and 11·0 per 100 000 in Bahrain.4,11,12

Liver cancer In the GCC states, liver cancer accounted for 5·0% of all newly diagnosed cancers during the period from 1998 to 2009.4 The overall ASR of liver cancer for all GCC nationals were 7·1 per 100 000 for men and 2·9 per 100 000 for women. The reported declining trend4 in liver cancer continued during the same period (male p=0·02, female p=0·38) and can be partly attributed to the extended national vaccination programme for hepatitis B virus that was introduced to all GCC states in the early 1990s. A few years later, the immunisation programme was extended to include adults and elderly people as well as children. This reduction is consistent with findings from several studies that showed significant evidence for the effectiveness of hepatitis B virus vaccine against hepatocellular carcinoma.13,14

Health systems Worldwide spending on new cases of cancer in 2010 was estimated at US$290 billion. Medical costs accounted for $154 billion (53%), non-medical costs accounted for $67 billion (23%), and income losses $69 billion (24%).15 The income losses cost does not include the cost of cancer screening and prevention, lost income due to cancer mortality, or future treatment costs. A study by the World Economic Forum showed that high income www.thelancet.com/oncology Vol 16 May 2015

countries have the highest burden of lost output from health-care costs reflecting their high income, followed by upper-middle-income countries and then lowermiddle-income countries. Low income countries have the lowest burden of lost output because the value of lost earnings in this group is smaller in relation to healthcare costs, and the total population of this group is much smaller than that of middle-income countries.15,16 Saudi Arabia, which comprises more than two-thirds of the GCC population, is the largest spender on health care among the GCC states.17 The GCC national population grew about 3% per year between 2008 and 2012—among the highest growth in the world—and about 60% of the GCC national population are aged between 14–27 years.18 Furthermore, the number of migrant workers in the GCC states has increased from 9 million to 13 million from 1990 to 2005.20 The total health-care spending in the Gulf region will reach $60 billion in 2025, up from $12 billion in 2012.21 The mean GCC health-care expenditure per head was $690 in 2011, with a range between $598 in Oman and $1776 in Qatar, compared with $8608 in the USA and $3609 in the UK.22 Despite the substantial increase in health-care expenditure in the GCC states, per head spending remains much lower than in developed countries. Health services in Gulf countries have increased and improved significantly in recent decades.17,21 At present, the Ministries of Health for the GCC states are the major government providers of health-care services in the GCC states, with a total of 415 hospitals (65 571 beds) and 2648 primary health-care centres, with about 70% of these services in Saudi Arabia countries (table 2).23 In 2009 and 2011, the Governments of Saudi Arabia and Qatar set a national strategy for health-care services to focus on diversification of funding sources; development of information systems; development of the human workforce; activation of the supervision and monitoring role of the Ministries of Health over health services; encouragement of the private sector to take its position in the provision of health services; improvement of the quality of preventive, curative, and rehabilitative care; and distribution of health-care services equally to all regions.24 Health-care system improvement has become a priority in many Gulf countries to reduce the poor quality of health-care provision compared with non-GCC high-income. Ministerial announcements in the Gulf countries have made notification of cancer policies mandatory for all ministries of health hospitals, government and private hospitals, clinics, and laboratories through the creation of the GCCR. Despite these achievements, cancer-care services, non-communicable disease surveillance, and the monitoring systems of four diseases including cancer in the GCC countries continue to show insufficient and uneven progress (table 3).25 However, early detection of cancer and reliability of diagnoses and treatment are e248

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Hospital

Saudi Arabia

Beds

Government

Private

Government Private

Clinics

Radiotherapy

Total beds per 10 000 population

Government Private

Government Private EBTE centres centres units

BTE units

283

125

44 099

11 833

22

2037

2308

9

3

30

9

UAE

32

58

6627

2549

19

243

2057

2

1

7

2

Kuwait

30

15

5149

653

18

97

98

1

0

4

1

Qatar

5

4

2564

394

14

30

177

1

0

2

1

Oman

55

5

5430

189

19

217

817

1

0

2

1

Bahrain

10

13

1702

384

19

24

NA

1

0

1

0

Data from Ng and colleagues,26 Karageorgi and colleagues,27 and Ballard-Barbash and colleagues.28 EBTE=external beam radiotherapy equipment. BTE=brachytherapy equipment. UAE=United Arab Emirates. NA=Not applicable.

Table 2: Availability of health-care services in GCC countries

Saudi Arabia

Bahrain

Kuwait

Qatar

UAE

Oman

Yes

Yes

Yes

Yes

No

Yes

Operational multisectoral national policy, strategy, or action plan that integrates No several NCDs and shared risk factors

Yes

No

Yes

No

No

Operational NCD unit, branch, or department within the Ministry of Health, or equivalent

Operational policy, strategy, or action plan to reduce the harmful use of alcohol

No

Yes

No

Yes

No

No

Operational policy, strategy, or action plan to reduce physical inactivity or promote physical activity

Yes

Yes

No

Yes

No

Yes

Operational policy, strategy, or action plan to reduce the burden of tobacco use

Yes

Yes

No

Yes

No

Yes

Operational policy, strategy, or action plan to reduce unhealthy diet or promote healthy diets

Yes

Yes

No

Yes

No

Yes

Evidence-based national guidelines, protocols, or standards for the management of major NCDs through a primary-care approach

Unknown

Yes

Unknown

Yes

Yes

No

NCD surveillance and monitoring system in place to enable reporting against the nine global NCD targets

No

No

No

No

No

No

National, population-based cancer registry

Yes

No

Yes

Yes

Yes

Yes

NCD=non-communicable diseases. UAE=United Arab Emirates. Data from Anand and colleagues.25

Table 3: WHO non-communicable diseases: GCC country profiles

improving in the GCC countries because of the availability of modern medical facilities.29 In many countries, including the UAE, the introduction of screening programmes has reduced the late diagnosis of breast cancer to a lower frequency than other countries such as Kuwait and Saudi Arabia, where routine screening is not implemented.29,30 Despite these achievements, cancer care is still facing many challenges including human resource development, implementation of cooperative health insurance, privatisation of public hospitals, effective management of cancer, development of practical policies for national crises, establishment of an efficient national health information system, the introduction of e-health (including electronic storage of health records), and optimisation of collaboration with international experts and partners.16,29 To address these challenges and to continue to improve cancer care in particular, the Ministries of Health of all GCC states need to develop and implement cancer-control programmes within a national cancer control institute. This institute will coordinate public health strategies for cancer e249

prevention and control, and will coordinate national cancer registries, national oncology and radiotherapy institutes and cancer research within each country. Such an umbrella structure will lead to, and facilitate, the coordination of many fragmented programmes and initiatives, and maximise benefits of large investments for better integration of cancer care.

Primary and secondary cancer prevention The most cost-effective strategy for cancer control is through primary prevention: reduction of the main risk factors for cancer, and protection of the population’s health and wellbeing. Several cancer risk factors have been identified as the cause of 35% of cancer deaths worldwide, including tobacco use, excess weight, poor diet, unsafe sex, and urban air pollution.31 According to a WHO report on the global tobacco epidemic, the estimated standardised prevalence rates for adult daily smokers of tobacco (both sexes) in GCC countries, ranged from more than 13% in Bahrain, UAE, Saudi Arabia, Qatar, and Kuwait to 8·5% in www.thelancet.com/oncology Vol 16 May 2015

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ASR for adult daily smokers of tobacco, both sexes, 2012

ASR for adult daily smokers of tobacco, male, 2012

ASR for adult daily smokers of tobacco, female, 2012

Rate of change (%), both sexes 1996–2012

Rate of change (%), male 1996–2012

Rate of change (%), female 1996–2012

Mean annual cigarette consumption per head

Mean daily cigarette consumption per head

Bahrain

17·5

23·9

5·9

2·5

–0·2

–2·2

1180

17·0

Qatar

15·5

19·3

1·4

1·8

–0·3

–0·1

921

13·9

UAE

13·7

18·2

2·5

–3·0

–3·5

1·7

1013

17·0

Saudi Arabia

13·9

22·1

2·2

12·5

2·1

1·2

1912

35·0

Kuwait

20·9

31·3

3·5

–8·3

0·7

0·1

1965

21·0

Oman

8·5

12·9

0·9

–1·1

–2·1

–0·3

1113

33·5

UAE=United Arab Emirates. ASR=age-standardised rate.

32

Table 4: Smoking prevalence in GCC countries

Oman. Estimated prevalence for smoking for both sexes between 1996 and 2012 increased by 12·5% in Saudi Arabia, 2·5% in Bahrain, and 1·8% in Qatar. Conversely, in Kuwait, UAE, and Oman the estimated prevalence declined by 8·3%, 3%, and 1·1%, respectively.32 For men, estimated prevalence in 2012 was 8·5–20·9% in all six countries within the GCC states. Conversely, Saudi Arabia showed the highest increase in smoking prevalence between 1996 and 2012 for both sexes at 12·5%, followed by Bahrain at 2·5% for both sexes. In 2012, estimated prevalence for women ranged between 0·9% in Oman and 5·9% in Bahrain. Conversely, Bahrain showed a decline in smoking prevalence among women, whereas UAE and Saudi Arabia had increases in smoking prevalence for women (table 4).32 In 2012, the average number of cigarettes per smoker per day in the GCC states was 23·4 cigarettes, which is more than the global average of about 18·0 cigarettes per smoker per day. The greatest health risks are likely to occur in countries with the highest tobacco use, such as Kuwait and Saudi Arabia. Both countries showed substantial increases in smoking among both sexes between 1980 and 2012.32 UAE showed a substantial increase in smoking among women for the same period. Moreover, smoking prevalence for students at schools was 16%, and 13·5% for those at university in Saudi Arabia.32,33 Smoking prevention strategies and education in health risks in both the clinical and community setting will be necessary to curb the epidemic. Responsibilities for health-care providers include advice and counselling, referrals to behavioural therapy, and support groups and prescriptions for nicotine replacement and other medications.34 Currently, all the GCC countries are moving aggressively towards strict legislations on banning smoking in all indoor public places and workplaces, implementing regulations on the packaging and labelling of tobacco products, and banning tobacco advertisement. Taxation has increased from 30% to 50% for all GCC states over the past 5 years, and importation of chewing tobacco banned for all GCC states.35 www.thelancet.com/oncology Vol 16 May 2015

The results of studies have shown that bodyweight and physical inactivity play an important part in cancer development and account for about a fifth to a third of some of the most commonly occurring cancers such as breast, colon, kidney, and oesophagus cancer across the globe.36 The rapid increase in wealth and economic development of the GCC states has led to changes in lifestyle, where the consumption of fast food and reduced physical activity have contributed to a notable increase in obesity in the GCC states.36,37 In a study conducted on schoolchildren aged 7–12 years in Riyadh, Saudi Arabia, more than half the students were not participating in any form of group physical activity that raised the heart rate to above 139 beats per min, for 30 min or more.37 According to WHO reports, Kuwait, Bahrain, Saudi Arabia, and UAE are among the top ten countries worldwide with the highest rates of obesity. Recent surveys have shown that 28% of men and 44% of women are obese in Saudi Arabia.38 Similarly, 36% of men and 48% of women are obese in Kuwait.39 Many studies have shown close association between increased physical activities and reduced weight, and subsequently decreased risk of development of cancer.36,37 A combination of many factors in the GCC states has led to people becoming overweight, including limited access to culturally acceptable exercise activities, multiple pregnancies in women, and an increase in sedentary lifestyle activities. GCC countries have been working together to apply policies to overcome the increase in the incidence of obesity. UAE and Saudi Arabia have banned high-fat snacks in schools, and fast food is banned in all public school canteens.36,37 Globally, the estimated incidence of cancer related to infectious diseases ranges between 25% in developing countries and less than 10% in developed countries.40,41 For example, hepatitis B and C infection accounts for more than 75% of all hepatocellular carcinoma cases across the world.41 Hepatitis B infection and exposure to aflatoxin increases the risk of liver cancer. A study reported that the overall prevalence of hepatitis B infection in Saudi Arabia was 6·7%.40,43 In the GCC region, the prevalence of hepatitis B surface antigen e250

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(HBsAg) for patients with hepatocellular carcinoma ranged from 7·4% to 17·0% between 1997 and 2010 in Saudi Arabia, denoting high endemicity.42 Some evidence suggests that introduction of the hepatitis B virus vaccine in 26 Latin American countries from the 1980s to 2000 coincided with decreasing incidences of liver cancer.15 Under the GCC regulations, screening for hepatitis B and hepatitis C is mandatory for every migrant wishing to live or work in a GCC member state, which is especially important in employment categories with a high risk of transmission, such as babysitters, home maids, those working in the food industry, health clubs, beauty centres, and hair salons.42,43 A 2008 study reported that the full effect of the hepatitis B vaccination programme done in 1989 for all Saudi-Arabian children has not yet reached all pregnant women, with 79·9% being non-immune and thus liable to hepatitis B virus infection.43 However, the 12-year cancer report from the GCC shows a significant (p=0·02) decline of liver cancer incidence in the male population by more than 10% during the same period, which might be used to encourage other GCC states to expand hepatitis B virus vaccination programmes to include adults as well.4 More than 660 million people annually are infected by herpes simplex virus and human papillomavirus (HPV), the world’s most common sexually transmitted viral infection associated with almost all cases of cervical cancer, 90% of anal cancers, and 40% of cancers of the external genitalia.44,45 Analysis of HPV vaccination programmes within the eastern Mediterranean vaccinating 6·2 million 12-year-old girls proved to be very cost effective, because it prevented 29 000 cases of cervical cancer and 18 000 deaths at a total cost of $360 million.45 Bahrain, Kuwait, Oman, UAE, and Saudi Arabia have licensed HPV vaccines, and a bivalent HPV vaccine is licensed in Qatar. UAE was the first country in the European, Middle Eastern, and north African region to implement an HPV vaccination programme in Abu Dhabi, and to introduce a voluntary school-based vaccination programme for girls aged 15–17 years.46 As cervical cancer is not among the most common cancers in the GCC region,4 Cost-effectiveness of HPV vaccination programmes is debatable. However, further evaluation is required, especially with current changes in the socioeconomic status, lifestyles, and reproductive patterns of individuals in the GCC region. Infection with Helicobacter pylori is considered one of the primary identified causes of gastric cancer,47 and is also associated with gastric mucosa-associated lymphoid tissue (MALT) lymphoma. Similarly, epidemiological evidence suggests that H pylori infection might be associated with a reduced risk of oesophageal adenocarcinoma.48 Several reports have shown high prevalence of H pylori infection in Saudi Arabia, and strong association with B-cell MALT lymphoma. The most direct approach to reduce H pylori infection is a regimen of proton-pump inhibitors and antibiotics.49,50 This strategy could be very cost effective e251

among high-risk populations and where gastric cancer is very common, such as in Oman.50 GCC states have witnessed a shift due to rapid urbanisation and lifestyle changes, with the rise of hydrocarbon and chemical industries leading to a major economic boom in the GCC states. 15 industrial processes or occupations have been classified by the International Agency for Research on Cancer as being carcinogenic.51 Epidemiological evidence shows there is a link between the use of organochlorine insecticides, organophosphorus, aflatoxins, dioxins, and asbestos compounds, and incidences of soft-tissue sarcoma, nonHodgkin lymphoma, leukaemia, and, albeit less consistently, with cancers of the lung and breast.31,53 Although arsenic is listed as a carcinogen for human beings, 90% of all commercial chickens are raised using arsenic to stimulate early maturation to produce more eggs.54 Broiler meat remains the most competitive source of animal protein in the GCC states, where total consumption in Saudi Arabia was more than 700 000 tonnes in 2014. The GCC states have implemented very restricted regulations on importation of poultry products. Birds must be fed on vegetable-only protein sources, and must be free of growth hormones and chemicals.55 GCC states have large petroleum resources, and they are home to most of the world’s oil production. The region is also a global hub for chemical industries and the largest industrial area in the Middle East. A study done in Saudi Arabia shows that there was significant association between the concentration of NO2 air pollution and the most common cancers, such as lung and breast.53 In order to carry out effective cancer prevention, all possible potential risk factors associated with increased chance of development of cancer first need to be identified.31,52 Only then can decisions regarding their prevention be taken.

National screening programmes Early cancer detection programmes in the GCC countries have recently been the focus of health-care providers in the region and recognised as a much-needed priority in the current and future strategic planning of health-care policies. According to the latest cancer incidence report from the Gulf Centre for Cancer Control and Prevention, most cancers among nationals from the GCC countries were diagnosed at late stages, and affected a much younger population than in other countries.4 Screening programmes help to reduce the burden of cancer in the population by preventing cancer from developing, thus reducing mortality and morbidity, improving outcomes and quality of life, as well as helping to reduce the economic burden. Data from breast cancer studies showed reduction of mortality between 25% and 30% for those patients who were screened early,56 while the UK’s www.thelancet.com/oncology Vol 16 May 2015

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flexible sigmoidoscopy trial showed a 43% reduction in colorectal cancer mortality and a 33% reduction in incidence for those patients who had previously been screened for colorectal cancer.57 The European Union recommends population-based screening for breast, cervical, and colorectal cancer using evidence-based methods with quality assurance of the entire screening process provided that those programmes are implemented cost-effectively and with high quality.58 In the UAE, the introduction of a screening programme in 2013 has reduced late diagnosis of breast cancer compared with other GCC countries, such as Kuwait and Saudi Arabia, where routine screening is not yet available.59 Overall acceptance of screening programmes in Arab populations is below expectation, which might be due to lack of health knowledge and inaccurate public beliefs in their benefits.60 Poor acceptance might be attributed to a feeling of embarrassment, family relationships, fatalism, social stigma, fear of pain, or a feeling of discomfort from the screening procedure itself.61–63 In a recent knowledge, attitudes, practices, and barriers study conducted in Qatar only 249 (24·9%) of the women surveyed did regular breast self-examinations; 233 (23·3%) had clinical breast examination, and 225 (22·5%) had mammography. Some of the reasons given for low participation were the embarrassment of having clinical breast examination (534 [53·3%]), and fear of mammography results (550 54·9%]).64 Similar results of low participation in breast cancer screenings were reported from Saudi Arabia, Bahrain, and Oman.65,66 Not enough data have been published regarding colorectal screening in the GCC region to draw similar conclusions. Although screening seems to have obvious benefits, recommendations should be supported by evidence using operational and outcome measures from appropriately designed and conducted studies.58 Successful implementation of screening programmes entails not only doing the test, but must also include a system for identification and encouragement of the target population to attend screenings. Protocols are also required for management of patients in the diagnosis, treatment, and surveillance phases to ensure that all individuals have timely access to appropriate diagnostic and treatment options. In addition, irrespective of the organisational approach, political and financial support are crucial to the successful implementation of any screening programme.67 Cancer screening in the European Union shows that Europe leads the way worldwide in the implementation of population-based screening, with more than 50 nationwide programmes for breast, cervical, and colorectal cancer currently being run or established, in Sweden, Denmark, and the Netherlands.58 GCC countries should consider carrying out similar trials. Further collaboration between GCC countries in the planning and implementation of screening programmes www.thelancet.com/oncology Vol 16 May 2015

is essential with appropriate governmental commitment. Therefore, regional guidelines need to be established, detailing who should be screened, at what age, and how frequently. National screening programmes should be established in all the countries, or wait and observe costeffectiveness in countries where they have already been established. A consensus should be formed on how to provide comprehensive strategies, focusing on improving access to health care with emphasis on improving early diagnosis. Equally important is building structured networks to drive clinical trials to improve standard of care, and to raise public awareness and knowledge through school education and social networks, aiming at providing an improved quality of life.

Primary care systems Primary health-care services in the Gulf region have improved strikingly in the past two decades. Several postgraduate training programmes were established in the specialties of family medicine and primary care. However, owing to increased demands, this field is still suffering from shortage of trained primary care physicians and inadequate infrastructure of primary health care centres, especially in rural and remote cities.65 Early diagnosis of patients with cancer at the primary care level is a challenging task because most patients present with non-specific symptoms with wide differential diagnosis. However, trained primary care physicians were shown to play a major part in the early diagnosis of cancer in countries with well-established primary health-care systems. In such systems, most patients with cancer presented first to their primary care physicians and were subsequently diagnosed by them.66,68 To overcome such challenges, primary care services in the GCC region need to recruit skilled practitioners with access to the appropriate laboratory and radiological diagnostic facilities. In addition, primary care services require access to an efficient referral system to specialised health care services. Coordination of care between primary, secondary, and tertiary care services within the health care system need to be encouraged in order to improve the care of patients with cancer within the GCC states. Such coordination should involve the development of shared evidence-based guidelines for the screening and management of common cancer diseases in the region. Follow-up of cancer patients by trained primary care physicians was shown to be as effective as follow-up by secondary care facilities.69 In addition, management of patients with cancer by primary care services was shown to be more cost-effective than the care provided by secondary care services, and resulted in similar patient satisfaction.69 Increased investment is needed in primary care services in the Gulf region to improve the efficiency of health-care systems. Such resources can be used to train more health-care providers in family medicine and primary care. Palliative care services are provided by trained primary care providers in many countries across e252

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the world. In addition, palliative care services involve home health care, which is provided by primary care physicians in most health-care systems.70 Palliative and home health care are relatively new disciplines in the Gulf region.71 A few initiatives were published from the region to establish culturally acceptable guidance for end of life care.72 New training programmes in these fields are being established under the umbrella of primary care training programmes in several Gulf states.73,74 These training programmes will create a great opportunity to expand the role of primary care services in the care of cancer patients within the GCC region.75

Discussion The aggregate population of the GCC countries is estimated to be around 50 million and rising. Crucially, cancer incidence is expected to increase more in the GCC region than in any other region of the world over the next two decades. A striking proportion of patients with cancer present at late stage or occur at a young age with poor prognosis. Cancer thus places a sizeable burden on individuals, families, health systems, and economies. Cancer includes more than 100 diseases with different causal factors, preventive approaches, and treatment modalities. However, 40% of all cancers are preventable, another 40% are curable if diagnosed early and treated promptly, and the remaining 20% can be treated with palliative therapy to reduce disease burden. Therefore, the fight against cancer necessitates integration between primary, secondary, and tertiary medical care in any country. In addition, new approaches necessitate development of state of the art research facilities and programmes as well as active clinical trial networks to bring the most innovative therapeutic modalities to the affected population. Continuous training and education for practising oncologists is vital because this field is so complex and constantly evolving. Cancer registration remains a main pillar for effective cancer control and prevention strategies by providing evidence-based information on cancer burden and guiding both public health action and the planning of adequate cancer services. It helps to identify gaps and opportunities for cancer prevention, early detection, and screening of the most common cancers at the country and regional levels. National cancer registries in the GCC region reported unique presentation of cancer patterns among its people such as high incidences of lymphomas, leukaemia, and thyroid cancers and low incidence of lung, cervical, and prostate cancers compared with high income countries. Such information is important in setting up cancer care and prevention strategies at the country and regional levels. Thus, continuous support for the national population-based cancer registries as well as hospital-based registries is essential for provision of reliable data for cancer incidence, prevalence, trends, and survivals, and to providing necessary data for clinical trials and outcome research. Therefore, GCC states must e253

sustain their existing cancer registries and ensure maximum use of available data. Comprehensive strategies to improve cancer control in the GCC region are needed, focusing on improving access to health care, standards of care, and public awareness through school education and social networks, to provide a better quality of life. Early diagnosis of patients with cancer at the primary care level is a challenging task because most patients present with non-specific symptoms with wide differential diagnosis. To overcome such challenges, primary care services in GCC countries need to recruit skilled practitioners with access to the appropriate laboratory and radiological diagnostic facilities. In addition, primary care services require access to an efficient referral system to specialised health-care services, and the challenge of improving coordination between primary, secondary, and tertiary care systems must be addressed. A shift is needed to invest more resources in the GCC region in primary care services to improve the efficiency of health-care systems in the region. Effective cancer prevention and control calls for a multisectored and multi-disciplinary approach. We call upon other government departments, development partners, institutions of higher learning, civil society, private sector, and the region at large to work together to ensure success. In the GCC region, more than two thirds of all cancers respond to early detection and potential cure with appropriate treatment. Introduction of national screening and early detection programmes would require adequate resources for diagnosis and treatment in addition to total engagement of target populations to health-care system through efficient primary health care and an effective referral system. The most common cancers that are receptive to early detection and are of public health importance for GCC countries are breast cancer and colorectal cancer, and others including cervical cancer (in some countries) and oral cavity cancers (in the southern parts of Saudi Arabia) are also a priority. An important factor that contributes to improved cancer care is the access to innovative clinical trials and increased enrolment of patients in those trials. Access to this new data will have a major effect on patient survival, patient experience, and quality of clinical research. Partnership with tumour-specific international consortia will help establish a clinical trials network for the GCC states. Saudi Arabia has a well-developed clinical trials network, including a number of medical centres within the country and internationally. Graduate medical training and clinical fellowship training are reasonably well developed in some GCC countries, with trainees being offered opportunities in GCC medical centres and in medical centres in the USA and Europe—in particular in Germany and in the UK. Recently, most of the GCC countries have started investing substantial funds in building research capacity programmes, including the establishment of research www.thelancet.com/oncology Vol 16 May 2015

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Panel: Summary of the proposed recommendation from the Riyadh document Recommendation 1: alleviating cancer burden at Gulf Cooperation Council Health Ministers’ institutional level • Calling upon the council states to exert their utmost efforts to reduce cancer mortality rates by 25% within a 10 year period (2015–2025) according to the directions of WHO • Updating the Gulf executive plan for cancer control (2010–2020) to cope with the world recent trends and according to the updated Gulf plan for control of noncommunicable diseases (2014–2025)

Recommendation 6: strengthening the role of private sector and national investment • Empowering leaders, policy, and legislation makers as well as the national health strategies in all ministries, governmental and non-governmental establishments, and related civil society organisations to collaborate positively with the private sector and encourage national investment, with provision of information related to cancer economics and burden within the platform of health promotion

Recommendation 2: alleviating the cancer burden at the level of health sectors Urging the health ministries in the Gulf Cooperation Council states, the Gulf Centre for Cancer Control and Prevention, International Agency for Research on Cancer, and WHO to understand the importance of establishing a reference body with the following responsibilities:

Recommendation 7: promotion of palliative care • Give more support to palliative care centres • Inclusion of palliative care as a specialty with more encouragement and motivation • Inclusion of religious and spiritual principles about health promotion in all educational curricula at all health and medical educational institutes • Directing health promotion programmes to acquire necessary skills to change unhealthy behaviours, and integration of such programmes within the scholastic curricula, coupled with monitoring the results

• Setting a database about the current and future economic burden of cancer on the health system at the regional and country level • Provide advice and consultation to the member states in efforts to plan national programs for the optimal use of resources • Assistance in preparing policies which promote healthy life styles and deal with other risk factors • Strengthening joint national, regional, and international efforts to minimise burden of cancer Recommendation 3: promotion of scientific research • Dissemination of research outcomes as well as the international and regional activities in the field of cancer economics and burden of disease • Conduct and support of cancer research and studies • Support of monitoring, surveillance, follow-up, and evaluation methods (based on a specific information system) of cancer Recommendation 4: strengthening national plans, policies, and programmes • Member states are requested to finalise and activate national cancer control programs Recommendation 5: raising awareness and health education • Effecting regional and international platforms of health promotion, healthy lifestyles, and control of various types of cancer • Dissemination of information of cancer burden to the public to increase awareness, community education, and to minimise risk factors of such diseases

centres of excellence in Saudi Arabia (eg, King Faisal Special Hospital and Research Centre, King Abdulaziz Medical City) Qatar (eg, Qatar Biomedical Research Institute) and the UAE. Qatar, for example, has allocated 2·8% of its GDP to support research and development www.thelancet.com/oncology Vol 16 May 2015

Recommendation 8: maximising the role of primary health care • Shift more resources to primary care services to improve the efficiency of health-care systems Recommendation 9: strengthening the role of civil society and support of community participation • Promote women and civil society empowerment policies in control and care in an integrated form within all health systems frameworks, and national health promotion strategic plans in various specialties: community, education, religious, and economic Recommendation 10: effective empowerment of patients with cancer and their families • Through promotion of patient rights from health, social, human, and psychological perspective • Provision of an outstanding advanced health-care system with the most up-to-date curative, diagnostic, rehabilitative and palliative techniques • Ensure high quality and timely service • Ensure equity in access to health service appropriate to all community individuals Recommendation 11: encourage exchange of information and participation at regional and international meetings for GCC member states

with a special focus on heath and biomedical research, primarily through the Qatar Foundation. Research is also another pillar for a sound cancer strategy. One important area of cancer research that has not been thoroughly addressed in the GCC region is the e254

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Search strategy and selection criteria We have used the following keywords in our search for appropriate and timely references by using PubMed, journals, books, and cancer incidence reports: Gulf Countries Council (GCC), GCC countries and cancer, breast cancer, Arab countries, colorectal cancer, prostate cancer, cancer incidence, cancer screening, cancer awareness, leukaemia, lymphoma, lung cancer, thyroid cancer, skin cancer, liver cancer, viral oncology, cancer education, cancer and Gulf countries, as well other keywords including different types of cancer. All these cancer search keywords were combined during the search with either Arab countries and/or Gulf countries. We have also consulted and used WHO and International Agency for Research on Cancer websites as well as GCC Health Ministers Council Executive Board documents as reference information. Articles in English and Arabic from 1995 to present were considered.

role of environmental exposures such as chemicals, air pollutants, and radiation. Moreover, assessment of modifiable risk factors such as tobacco use, unhealthy diet, physical inactivity, and obesity, which account for more than 65% of cancer cases worldwide, offers important opportunities for prevention. Although there are various cancer research centres in the GCC region, most of these lack sufficient and continuous access to research funding. Dedicated funds for cancer research can help set up competitive and sustainable research programmes that will benefit the entire GCC population and beyond. Cancer care, clinical trials, and cancer research are costly activities, and there should be no compromise in high quality standards in accomplishing these goals and delivering these needed services to GCC populations and globally. 2014 saw the organisation of a major conference dedicated to bridging the gaps of the burden of cancer in the GCC countries with the participation of scientists, clinicians, decision makers, and other experts from the GCC countries and internationally. The conference, which took place on Oct 20–21, 2014, under the auspices of the health minister’s council for cooperation council states in Riyadh, Saudi Arabia, has led to the development of the Riyadh document, a set of recommendations that was submitted to GCC health ministers for their endorsement (panel). Following endorsement of the Riyadh document, an implementation plan with measurable milestones and timeline will be developed and shared among representatives of GCC Health Ministers Council. These conference recommendations stem from the realisation that there are important obstacles to the improvement of cancer care in the GCC countries separately. At least half of GCC countries have a relatively young health-care system and cancer care is still developing. Substantial infrastructure development challenges are evident in a number of the GCC countries, and health research, including cancer research, needs to be improved. More positively, most of the GCC countries have made major investment in health-care infrastructure development. More collaborative research programmes e255

and educational exchanges are taking place among these countries. Additionally, GCC countries not only share geographical, historical, and cultural ties, but also form a political union with the GCC Executive Board of the GCC Health Ministers Council as an ideal mechanism through which these planned collaborative activities stated in the recommendations could be channelled. Overall, these recommendations are feasible and can potentially be achieved in a realistic timeframe. The ability to implement these recommendations will largely depend on how rigorous and well-planned implementation and follow-up proves. A major factor in favour of these recommendations is that a structure already exists, the GCC Health Minister’s Council and its executive board, which may be well-suited to facilitate and manage the implementation of these recommendations. A potential challenge could be the fact that health-care systems are at different phases of development in different GCC countries. Saudi Arabia and Qatar are the only two GCC countries with cancer care strategies, and Qatar is the only GCC country with a cancer research strategy. However, only the future integration and collaboration of these organisations can ensure effective cancer care across the GCC region. Contributors SA-O was responsible for the conduct, management, and final approval of the report. SA and AH did the scientific literature search. SA-O, AH, SA, AA, TK, and AA-Z all participated in writing and editing the Review. Declaration of interests We declare no competing interests. Acknowledgments We thank Amal N Al-Madouj, for her support in data collection, and Baralah Muharab Almurshed, for her support in data management. References 1 WHO. All cancers (excluding non-melanoma skin cancer) estimated incidence, mortality and prevalence worldwide in 2012. http://globocan.iarc.fr/Pages/fact_sheets_cancer.aspx (accessed May 12, 2014). 2 Salim EI, Moore MA, Al-Lawati JA, et al. Cancer epidemiology and control in the Arab world—past, present and future. Asian Pac J Cancer Prev 2009; 10: 3–16. 3 WHO. WHO recognizes progress of Gulf states for adopting regional strategy to address noncommunicable diseases 2012. http://www.who.int/mediacentre/news/statements/2012/ ncds_20120106/en/ (accessed Jan 11, 2014). 4 Al-Madouj AN, Al-Zahrani AS, SF. A-O. Cancer incidence among nationals of the GCC states, 1998–2009. Riyadh, Saudi Arabia: King Faisal Specialist Hospital and Research Center, 2013. 5 Kasteng F, Wilking N, Jönsson. B. Patient access to cancer drugs in nine countries in the Middle East http://www.comparatorreports. se/Middle%20East%20oncology%20drug%20uptake%20Final%20 report%20Sept%2015%202008.pdf (accessed Feb 5, 2014). 6 Al-Eid HS, Garcia AD, Cancer incidence report, Saudi Arabia 2010. 2014. http://www.scr.org.sa/ (accessed April 10, 2015) 7 Al Diab A, Qureshi S, Al Saleh KA, et al. Review on breast cancer in the kingdom of Saudi Arabia. Middle East J Sci Res 2013; 14: 532–43. 8 Alghamdi IG, Hussain II, Alghamdi MS, Dohal AA, Alghamdi MM, El-Sheemy MA. Incidence rate of non-Hodgkin’s lymphomas among males in Saudi Arabia: an observational descriptive epidemiological analysis of data from the Saudi Cancer Registry, 2001–2008. Int J Gen Med 2014; 7: 311–17. 9 WHO. 2008–2013 Action plan for the global strategy for the prevention and control of noncommunicable diseases. http://www. who.int/nmh/publications/ncd_action_plan_en.pdf (accessed Dec 13, 2013).

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