Cancer Epidemiology and Control in The Arab World - Past, Present and Future. Elsayed Salim Tanta

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Cancer Epidemiology in the Arab Region

REVIEW

Cancer Epidemiology and Control in the Arab World - Past,


Present and Future
Elsayed I Salim1, Malcolm A Moore*1,2, Jawad A Al-Lawati3, Jamal Al-Sayyad4,
Amin Bawazir5, Shouki Bazarbashi6, Abdulbari Bener7, Marilys Corbex8, Nagi
El-Saghir9, Omran S Habib10, Wasim Maziak11, Ibrahim Abdel-Barr Seif-Eldin12,
Tomotaka Sobue2
Abstract
The Arab world, stretching from Lebanon and Syria in the north, through to Morocco in the west, Yemen in
the south and Iraq in the east, is the home of more than 300 million people. Cancer is already a major problem
and the lifestyle changes underlying the markedly increasing rates for diabetes suggest that the burden of
neoplasia will only become heavier over time, especially with increasing obesity and aging of what are now still
youthful populations. The age-distributions of the affected patients in fact might also indicate cohort effects in
many cases. There are a number of active registries in the region and population-based data are now available
for a considerable number of countries. A body of Arab scientists are also contributing to epidemiological
research into the causes of cancer and how to develop effective control programs. The present review covers the
relevant PubMed literature and cancer incidence data from various sources, highlighting similarities and variation
in the different cancer types, with attempts to explain disparities with reference to possible environmental factors.
In males, the predominant cancers vary, with lung, urinary bladder or liver in first place, while for females
throughout the region breast cancer is the greatest problem. In both sexes, non-Hodgkins lymphomas and
leukemias are relatively frequent, along with thyroid cancer in certain female populations. Adenocarcinomas of
the breast, prostate and colorectum appear to be increasing. Coordination of activities within the Arab world
could bring major benefits to cancer control in the eastern Mediterranean region.
Asian Pacific J Cancer Prev, 10, 3-16
Introduction Algeria, Morocco and Maruitania) as well as Saudi Arabia,
Yemen, the Sultanate of Oman, the United Arab Emirates,
The countries of the Arab Middle-east share a great Qatar, Bahrain, Kuwait and Iraq. Although population-
deal in terms of culture while markedly differing in their based cancer incidence rates in Jordan, with and without
levels of economic development. The variation between Egypt, have been published (Freedman et al., 2003;
and within populations is reflected in different disease Freedman et al., 2007), a more general coverage has not
profiles, although in all cases the burden of cancer is been hitherto been available. All sources available to the
already appreciable. The available data indicate that authors were therefore accessed to give as comprehensive
incidence rates are rising and with aging as well as a picture as possible regarding the cancer burden, risk
continued population growth this means that the problem factors and preventive approaches. Representative relevant
will loom larger in the future. papers in PubMed were cited with the focus on individual
Since the literature regarding cancer registration data organ sites, in an attempt to explain variation in incidence
and associated epidemiological findings are scattered, the rates in terms of accepted risk and beneficial factors.
present research was undertaken to provide an overview.
The countries/populations included are the Lebanon, Syria, Cancer Registration in the Arab World
Palestine (the West Bank and Gaza and Israeli -
Palestinians), Jordan, Egypt, Sudan, Djibouti and Eritrea The established cancer registries within the Arab world
and the Maghreb countries of North Africa (Libya, Tunisia, are shown in Figure 1. The oldest population-based

1
UICC Asian Regional Office for Cancer Control, [email protected], 2Cancer Information Services and Surveillance Division,
Center for Cancer Control and Information Services, National Cancer Center, Tokyo, Japan, 3National Cancer Registry, NCD
Surveillance & Control Department, Ministry of Health, Muscat, Sultanate of Oman, 4Bahrain Cancer Registry, Ministry of Health,
Manama, Bahrain, 5Aden Cancer Center, Aden University, Yemen, 6National Cancer Registry, King Faisal Specialist Hospital and
Research Center, Riyadh, Saudi Arabia, 7Dept. of Epidemiology and Medical Statistics, Hamad Medical Corporation, Doha, Qatar,
8
WHO Eastern Mediterranean Regional Office, Cairo, 9Department of Internal Medicine, American University of Beirut, Lebanon,
10
Dept of Community Medicine, Al-Sadr Teaching Hospital, Basrah, Iraq, 11Syrian Center for Tobacco Studies, School of Public
Health, University of Memphis, USA, 12Gharbia Population-based Cancer Registry, Tanta Cancer Centre, Tanta, Egypt
Asian Pacific Journal of Cancer Prevention, Vol 10, 2009 3
Elsayed I Salim et al
al., 2007) and for Lebanon, Saudi Arabia and Qatar, from
Shamseddine et al (2004), Bazarbashi et al (2001) and
Bener et al (2008), respectively.
Percentages of all neoplasms for the five most frequent
cancers for these and other countries illustrated graphically
in Figure 2 were from Globocan 2002 or from hospital-
IACR Voting CIV based registries in Libya (El Mistiri et al., 2007), Yemen
/
IACR Voting Non-CIV
(Al-Thobhani et al., 2001), Bahrain (Alsayyad and
IACR Non -Voting
Non IACR
Hamadeh, 2007) and Iraq (Habib et al., 2006; 2007).
In males, while lung cancer featured in the most
Figure 1. Cancer Registries in the Arab Countries of frequent neoplasms in the latest data in all but the Yemen
Asia and the North African Region case, urinary bladder tumours were more prevalent in three
countries and liver and oral cavity lesions occupied the
Table 1. Numbers of Middle Eastern Countries and
first position in Saudi Arabia and the Yemen, respectively.
Registries in the Series of Nine Volumes of CIV
Mauritania was also exceptional in having prostate cancer
Volume I II III IV V VI VII VIII IX as number one. For countries not included in Figure 2,
Kuwait* 1 1 1 1 1 Syrian males in Aleppo demonstrated age-adjusted
Oman* 1 1 incidence rates highest for bladder, leukaemia and lung
Algeria: Setif 1 cancers, in that order (Mzayek et al., 2002), while in Libya
Bahrain* 1 the most frequently diagnosed malignancies were lung
Egypt: Gharbia 1 cancer (19%) and colorectal cancer (10%), followed by
Tunisia: Sousse 1 cancers of the head and neck (9%) and bladder (9%) (El
*: National Cancer Registry Mistiri et al., 2007). In the Moroccan National Oncology
Institute, for 1986 and 1987 in males, nasopharyngeal
registry is that of Kuwait, which has been reporting to cancer accounted for 12.3%, lymphoma 10.1%, laryngeal
Cancer Incidence in Five Continents since 1987 (see Table cancer 8.2% and lung cancer 6.5% of the total (Chaouki
1), with Algeria, Bahrain, Egypt and Tunisia being included and el Gueddari, 1991). In the Al Jouf region of Saudi
in the last issue, in 2007. The population-based age- Arabia, lymphomas and leukemias combined, colorectal
standardized cancer incidence data for the major body sites and skin cancers have been reported to be the most
in Volume IX were examined for the present paper (see common (El Hag et al., 2002). In Gaza, lung cancer, and
Tables 2 and 3 for females and males respectively). In again leukaemia and lymphoma appear to be the most
addition, findings for Jordan and the Palestinian Authority frequent (Kahan et al., 1997).
were obtained from http://mecc.cancer.gov (Freedman et Breast cancer, almost without exception, is the most

Table 2. Population-based Cancer Registry Data for Arab Countries - Females


Jordan# Palestine* Egypt* Saudi** Algeria* Tunisia* Oman* Qatar## Bahrain* Kuwait*
Buccal 2.3 0.7 0.1 1.3 0.2 0.7 1.0 0.7 1.6 1.5
Pharynx 0.2 0.4 1.8 0.3 0.6 0.3 0.5 - 1.5 0.2
Nasopharynx 0.5 0.4 1.8 0.7 1.7 1.9 0.3 - 0.3 0.8
Oesophagus 0.7 0.4 0.9 0.9 0.2 0.2 2.7 1.1 1.8 1.6
Stomach 3.5 3.5 2.0 1.7 3.1 2.5 6.2 2.5 5.4 2.6
Colon 7.2 10.8 2.7 3.1 2.8 6.1 2.2 2.2 5.1 7.6
Rectum 3.0 3.7 1.7 1.8 3.8 2.9 1.4 6.1 2.2 4.2
Liver 1.3 0.7 4.5 2.2 0.8 0.7 3.2 1.8 3.1 3.6
Gallbladder 0.3 2.8 1.0 1.1 10.0 3.1 1.1 0.7 0.9 1.7
Pancreas 1.0 2.4 2.3 0.6 0.3 1,9 1.6 1.1 2.8 3.0
Larynx 0.4 0.6 0.3 0.1 0.1 0.2 0.3 - 0.7 0.5
Trachea, lung 3.1 5.1 3.6 1.4 1.7 1.7 2.3 2.5 11.8 4.6
Breast 38.0 38.5 42.5 11.8 18.8 29.8 14.6 30.1 46.8 41.3
Ovary 4.6 3.7 5.1 2.3 2.1 3.3 6.2 - 7.4 5.4
Corpus uteri 5.8 9.0 2.6 2.0 1.1 3.4 0.9 - 5.2 3.6
Cervix uteri 2.6 2.4 2.1 2.2 11.6 7.1 6.5 - 6.0 4.5
Kidney 1.9 1.6 1.5 1.2 1.2 1.6 1.6 1.8 3.5 2.0
Bladder 1.8 1.7 3.1 1.2 0.5 2.2 2.2 0.7 3.8 2.9
Brain 3.6 3.3 6.2 1.3 1.6 1.8 2.6 1.4 0.9 3.1
Thyroid 4.5 7.0 2.6 4.4 3.6 3.1 5.9 5.7 7.7 7.3
Non-Hodgkin 5.4 9.1 9.9 4.1 3.8 3.7 4.4 6.8 5.6 6.5
Leukemia 4.9 3.9 4.1 2.7 2.4 3.6 3.3 - 3.3 3.8
Total 112 134 122 58 85 106 91 87 143 129
# ##
From: *Curado et al., 2007; **Bazarbashi et al., 2001; Freedman et al., 2007; Bener et al., 2008

4 Asian Pacific Journal of Cancer Prevention, Vol 10, 2009


Cancer Epidemiology in the Arab Region
Lebanon

Syria

Jordan

Palestine

Egypt

Libya

Tunisia

Algeria

Morocco

Mauritania

Sudan

Saudi Arabia Saudi Arabia

Yemen

Oman

UAE

Qatar

Oral Stomach Colon Rectum Liver Gallbladder Larynx Lung Bladder Prostate Breast Ovary Cervix Thyroid NHL Leukemia Brain Other

Figure 2. Percentage Data for the Five Most Prevalent Cancers in Countries of the Middle East
Table 3. Age-standardized Cancer Incidence Data for Arab Countries - Males
Jordan# Palestine* Egypt* Saudi** Algeria* Tunisia* Oman* Qatar## Bahrain* Kuwait*
Buccal 2.6 2.7 0.5 1.0 1.4 2.6 2.3 - 3.3 1.8
Pharynx 2.3 0.5 1.8 0.3 4.5 0.7 0.4 - 0.8 0.3
Nasopharynx 2.3 1.1 1.8 2.5 5.4 4.6 1.0 0.7 2.9 1.7
Oesophagus 1.5 1.1 1.7 1.3 0.2 0.5 2.6 0.4 4.2 2.2
Stomach 6.0 6.7 3.3 2.4 7.1 5.1 13.4 2.0 8.5 3.4
Colon 7.6 10.6 4.2 2.4 3.0 6.5 2.5 3.4 7.9 8.4
Rectum 3.9 8.3 2.1 2.4 3.6 5.1 2.1 3.0 4.4 5.2
Liver 1.9 2.6 21.9 5.9 1.1 2.2 7.4 3.4 5.3 8.1
Gallbladder 0.8 2.0 1.2 0.8 2.1 1.8 0.7 - 0.8 1.8
Pancreas 1.8 5.0 4.0 1.1 0.5 2.5 2.1 0.7 4.9 3.7
Larynx 4.8 6.1 4.2 1.4 2.8 5.7 1.4 0.9 4.7 2.7
Trachea, lung 16.4 40.4 14.0 4.1 19.9 37.1 9.8 5.9 34.2 15.6
Prostate 11.2 20.0 8.5 3.4 7.5 14.1 10.5 3.0 14.3 10.5
Kidney 3.4 4.4 2.5 1.7 0.7 2.6 1.7 1.6 4.7 5.8
Bladder 13.2 18.1 27.9 2.9 4.5 19.0 5.1 1.8 14.7 6.3
Brain 4.4 4.9 4.0 1.9 0.7 3.7 3.5 2.0 3.0 5.1
Thyroid 1.7 2.0 1.1 1.5 1.4 1.3 1.7 - 1.1 3.5
Non-Hodgkin 7.3 10.0 16.9 4.4 5.3 6.7 8.2 5.9 7.1 10.4
Leukemia 7.3 7.3 5.4 3.9 3.1 5.1 4.8 - 7.7 4.9
Total 115 183 162 59 94 160 105 51 160 121
# ##
From: *Curado et al., 2007; **Bazarbashi et al., 2005; Freedman et al., 2007; Bener et al., 2008

Asian Pacific Journal of Cancer Prevention, Vol 10, 2009 5


Elsayed I Salim et al

0-2.5 5.0-7.5 10.0-15.0 0-2.5 5.0-7.5 10.0-20.0

2.5-5.0 7.5-10.0 >15.0 2.5-5.0 7.5-10.0 >20.0

Figure 3. Male Melanoma Incidences/100,000 Figure 5. Male Oesophageal Cancer Incidences/100,000


((Globocan, 2002: Ferlay et al., 2004) (Globocan, 2002: Ferlay et al., 2004)

frequent tumour type in females, followed by colon in five commonly affected site followed by the tongue in Iraq
populations and cervix in three. In Syrian females age- (Al-Rawi and Talabani, 2008). In Jordan, the floor of the
adjusted incidence rates were highest for breast, uterus (+ mouth is the most common site, then again the tongue
cervix) and leukaemia (Mzayek et al., 2002). In Gaza, (Ma’aita, 2000). Of the cases of cancer recorded in the
leukaemia and lymphoma occupy second and third place Kuwait Cancer Registry in the 10 years 1979-1988, 7.4%
(Kahan et al., 1997). Cervical cancer was earlier found to involved the lip, oral cavity or pharynx (Morris et al.,
be number one in Morroco (Chaouki and el Gueddari, 2000).
1991), but it is conceivable that the situation has now
changed. Oesophageal Cancer
In clear contrast to Iran, the Arabic world has generally
Organ Specific Epidemiology very low incidences of oesophageal cancer (see Figure
5). CIV data for relative incidence of the squamous cell
Skin Cancer carcinoma and adenocarcinoma types are listed in Table
Skin cancer, including melanoma, is rare in the region, 4.
with the exception of Sudan (see Figure 3). The most The reason for the variation between countries and
common skin cancers seen, at least in Saudi Arabia, are sexes remains unclear. In Bahrain, in direct opposition to
the basal cell carcinoma (BCC) and squamous cell the CIV data, SCC (males) and adenocarcinomas (females)
carcinoma (SCC), with site distributions similar to studies were reported to be the main histological types, with the
in Caucasians pointing to sun as the risk factor, followed lower and upper third of the oesophagus as the most and
by Kaposi’s sarcoma (Al-Maghrabi et al., 2004). In Qatar, least frequently involved sites, respectively (Al-Hilli and
BCC is the commonest skin cancer but expatriates account Malik, 2003). The reason why the CIV data are not in
for a large proportion, especially Europeans (Mahmoud agreement is unclear. In the Yemen✎✄ a preponderance of
and Azadeh, 1996). women with carcinoma of the mid-oesophagus was noted,
previously only recorded in areas of high prevalence, with
Oral Cancer a high frequency of Qat chewing and water-pipe smoking
Cancer of the buccal cavity is relatively rare across found for both men and women (Gunaid et al., 1995). A
the Arab countries, with the exception of parts of the Yemen slight preponderance of female cases was also earlier found
where it may be number one (see Figure 4), thought to be for Qataris, in this case with nutrition and social status
related to the habits of chewing tobacco and qat (Sawair reported to be probable etiologic factors (Ejeckam et al.,
et al., 2007). Qat chewing can provoke the development 1993).
of oral keratotic white lesions which become more severe
with duration (Ali et al., 2004; Scheifele et al., 2007). Stomach Cancer
Furthermore, in Saudi Arabia there are very wide With the exception of males in Oman, gastric cancer
regional disparities in incidence, with an almost thirty- incidences are low (Figure 6). The fact that Omani females
fold difference between the lowest and highest rates also have a relatively high value suggests a specific factor
(Brown et al., 2006). The lower lip may be the most in this country. The marked difference from Iran is not

Table 4. Oesophageal Cancer Histopathology: SCC-


AC Percentages (Curado et al., 2007)
Male Female
SCC AC Ratio SCC AC Ratio
Egypt 60 25 2.4:1 80 14 5.7:1
0-2.5 5.0-7.5 10.0-15.0 Palestine 28 27 1.0:1 18 37 0.5:1
Algeria 33 0 --- 33 33 1.0:1
2.5-5.0 7.5-10.0 >15.0 Tunisia 100 0 --- 50 50 1.0:1
Bahrain 52 52 1.0:1 80 0 ---
Figure 4. Male Oral Cancer Incidences/100,000 Kuwait 38 38 1.0:1 67 33 2.0:1
Oman 28 26 1.0:1 25 31 0.8:1
(Globocan, 2002: Ferlay et al., 2004)

6 Asian Pacific Journal of Cancer Prevention, Vol 10, 2009


Cancer Epidemiology in the Arab Region
Zeid et al., 2002), and in Qatar the descending and sigmoid
colon is the most common anatomical site affected (Rasul
et al., 2001). Cases in Saudi Arabia also tend to be
relatively young (Mansoor et al., 2002). The profound
rightward shift of colorectal carcinoma described in Saudi
Arabia, compounded with a rising incidence of advanced
0-10 20-30 40-60
lesions in younger age group, is also of interest (Guraya
10-20 30-40 >60.0 and Eltinay, 2006). Arab patients appear to be relatively
young in Palestine with a high percentage of poorly-
differentiated and mucinous, advanced stage cancers
Figure 6. Male Gastric Cancer Incidences/100,000 (Shpitz et al., 2006). A high proportion of familial MSI
(Globocan, 2002: Ferlay et al., 2004)
cases and a lowincidence of TP53 mutations were recently
due to a lower frequency of the more virulent H. pylori reported to be hallmarks of Saudi colorectal carcinomas
strains, at least from data for Iraq (Hussein et al., 2008). (Bavi et al., 2008).
Furthermore, in the Gulf, there was no difference found The low incidence of colorectal cancer in the Arab
between farmers with a lower standard of living and non- countries could be due to the dietary factors, with high
farmers in respect of their H. pylori profiles (Bener et al., intake of fruit and vegetables (Al-Shamsi et al., 2003).
2006). The prevalence of infection with the bacteria in One environmental factor might be pesticides. Thus
dyspeptic patients in Yemen appears high (Gunaid et al., farming in Egypt is associated positively with high serum
2003). organochlorines and serum levels in colorectal cancer
patients may be higher than in appropriate controls
Colorectal Cancer (Soliman et al., 1997).
The incidences of colon and rectum cancer in the Arab
world are relatively low, although in some of the more Liver Cancer
affluent countries it is number two after breast (see Figure Liver cancer, while much less frequent than in high-
7). There is only limited variation in incidence rates incidence countries, is nevertheless a major problem in
between sexes and the colon-rectum ratio varies from males in Egypt and Saudi Arabia and to a lesser extent in
approximately 1:1 to 3:1 (see Table 5), with the one the other countries of the Gulf (see Figure 8). The
exception of Algeria where rectal cancers are in the hepatocellular carcinoma accounts for the majority of
majority. tumours although there some variation between the sexes
In Yemen there is a relatively high proportion of early- in the relative incidence of cholangiocellular carcinomas
onset tumors (19.3% of cases were <40 years), with a left (CCC) (see Table 6). The hepatitis B virus✄(HBV) is the
sided subsite distribution (49.4% of cases in the rectum leading cause of HCC in Lebanon (Yaghi et al., 2006)
and rectosigmoid junction) (Basaleem and Al-Sakkaf, and in Egypt (Anwar et al., 2008), but in the latter HCV
2004). Similarly, in Egypt 38% of patients are younger has now become the predominant factor associated with
than 40 and 75% of lesions are on the left side (Abou- the more recent epidemic. It has been well documented

0-5 10-15 20-40

0-5 10-15 20-30


5-10 15-20 >40.0

5-10 15-20 >30

Figure 7. Male Colorectal Cancer Incidences/100,000 Figure 8. Male Liver Cancer Incidences/100,000
(Globocan, 2002: Ferlay et al., 2004) (Globocan, 2002: Ferlay et al., 2004)
Table 5. Colorectal Cancers: Colon and Rectal Table 6. Liver Cancer Histopathology: HCC-CCC
Carcinoma Incidences and Ratios(Curado et al., 2007) Percentages (Curado et al., 2007)
Male Female Male Female
Colon Rectum Ratio Colon Rectum Ratio HCC CC Ratio HCC CC Ratio
Egypt 4.2 1.2 3.5:1 2.7 1.7 1.6:1 Egypt 88 4 22.0:1 80 6 13.3:1
Palestine 10.6 8.3 1.3:1 10.8 3.7 2.9:1 Palestine 69 3 23.0:1 42 14 3.0:1
Algeria 3.0 3.6 0.8:1 2.8 3.8 0.7:1 Algeria 39 31 1.3:1 0 60 ---
Tunisia 6.5 5.1 1.3:1 6.1 2.9 2.1:1 Tunisia 65 18 3.6:1 60 20 3.0:1
Bahrain 7.9 4.4 1.8:1 5.1 2.2 2.3:1 Bahrain 75 15 5.0:1 54 27 2.0:1
Kuwait 8.4 5.2 1.5:1 7.6 4.2 1.8:1 Kuwait 77 8 9.6:1 89 11 8.1:1
Oman 2.5 2.1 1.2:1 2.2 1.4 1.6:1 Oman 77 16 7.7:1 67 27 2.5:1

Asian Pacific Journal of Cancer Prevention, Vol 10, 2009 7


Elsayed I Salim et al
that Egypt has one of the highest prevalence rates of HCV
infection in the world with different strains involved
(Abdel-Hamid et al., 2007), but there may also be an
etiological role for aflatoxin B1 (Hifnawy et al., 2004).
There is significant geographic variation in incidence
among districts (Lehman et al., 2008). Prevalence of HCC
is high in the Nile Delta area, and is more common in 0-2 4-6 8-10
males, rural residents and farmers so that pollution due to
insecticides might be a risk factor (Abdel-Wahab et al., 2-4 6-8 >10.0

2007).
Figure 10. Male Laryngeal Cancer Incidences/100,000
Gallbladder Cancer
(Globocan, 2002: Ferlay et al., 2004)
Algerian females appear to be exceptional in having a
relatively high proportion of gallbladder cancer cases (see
Figure 2), the tumour elsewhere in the region being thirteen have lung cancer as number one, and all but one
generally rare. include the site in the most frequent five. In a recent survey,
the highest ASR was in Bahrain (34.3 for males, 12.1 for
Pancreatic Cancer females) followed by Qatar (18.5 and 5.5 ) and Kuwait
Except in the Lebanon and Syria, rates for pancreatic (13.8 and 4.0); the lowest rates were in Saudi Arabia (4.8
cancer are generally low (see Figure 9), the reported and 1.3 for females) (Al-Hamdan et al., 2006). From CIV
clustering of cases in the northeast Nile delta region data, squamous cell carcinomas and adenocarcinomas
possibly being related to water pollution (Soliman et al., account for approximately the same proportions in males,
2006), very probably linked to cadmium and farming while adenocarcinomas (AC) tend to predominate in
(Kriegel et al., 2006). In general, multiple tobacco females (see Table 7). In Tunisia, the AC incidence was
consumption methods, passive smoking, pesticide relatively low in 1990 when compared to western
exposures, and diabetes are associated with an increased countries, but this has been shown to increase to become
risk for pancreatic cancer, with prolonged lactation and more common than the SCC type (B’chir et al., 2007).
increased parity associated with a reduced risk (Lo et al., This was not evident in the CIV data, however.
2007). The marked increase in the incidence of lung cancer
among Palestinain Arab men during the last decade,
Nasopharyngeal Cancer without any evidence of increased smoking prevalence,
Nasopharyngeal cancer is relatively common in might reflect a gradual loss of some apparent protection
Western North African males but otherwise rare. in this subpopulation (Tarabeia et al., 2008). In Egypt there
Characteristics of NPC patients in Lebanon and their has been a report that pleural mesothelioma is increasing,
parameters of outcome are comparable to those reported survival being linked to genetic alteration (Gaafar and
in Western series (Geara et al., 2005). Early onset suggests Eldin, 2005).
a possible underlying genetic susceptibility in Saudi
Arabians (Andejani et al., 2004).

Laryngeal Cancer
Iraq, the Lebanon and to a lesser extent the Yemen,
Egypt and relatively developed North Africa, have high
incidences of laryngeal cancer, it elsewhere appearing of
relatively minor importance (see Figure 10). 0-10 20-30 40-50

10-20 30-40 >50


Lung Cancer
Although incidences are lower than in the West (see
Figure 11) , of the countries included in Figure 2, seven of Figure 11. Male Lung Cancer Incidences/100,000
(Globocan, 2002: Ferlay et al., 2004)

Table 7. Lung Cancer Histopathology: SCC-


Adenocarcinoma Ratios (Curado et al., 2007)
Male Female
SCC AC Ratio SCC AC Ratio
Egypt 22.4 24.2 0.9:1 9.1 50.0 0.2:1
0-1.5 3.0-4.5 6.0-7.5 Palestine 28.0 26.6 1.1:1 7.4 50.0 0.1:1
Algeria 63.0 6.4 9.8:1 43.8 28.1 1.6:1
1.5-3.0 4.5-6.0 >7.5
Tunisia 46.6 18.5 2.5:1 23.5 29.4 0.8:1
Bahrain 34.5 21.6 1.6:1 26.9 30.8 0.9:1
Figure 9. Male Pancreatic Cancer Incidences/100,000 Kuwait 17.1 18.9 0.9:1 18.8 37.5 0.5:1
(Globocan, 2002: Ferlay et al., 2004) Oman 28.5 26.0 1.1:1 25.0 31.3 0.8:1

8 Asian Pacific Journal of Cancer Prevention, Vol 10, 2009


Cancer Epidemiology in the Arab Region
Alexandria (Bedwani et al., 1997). This is in line with the
fact that polymorphisms in glutathione S-transferase genes
are associated with increased risk of bladder cancer (Saad
et al., 2005). Interestingly, odds ratios were 15.8 for male
ever-smokers with a history of urinary schistosomiasis,
compared with never-smokers without such a history, and
0-2 4-6 8-10
3.2 for men ever-infected with urinary Schistosoma
2-4 6-8 >10
haematobium and ever-employed in high-risk occupations,
compared with those never-infected and with no high-risk
occupational history (Bedwani et al., 1998).
Figure 12. Male Kidney Cancer Incidences/100,000
Despite the high prevalence, there are no population-
(Globocan, 2002: Ferlay et al., 2004)
based bladder screening programs in place. Combining
Kidney Cancer NMP22 with malignant or suspicious cytological result
With the exception of males in Syria, Lebanon and improved sensitivity for the detection of bladder cancer
Palestine, renal cancer incidences are low in the Arab world but with a major decrease in specificity, suggesting a
(see Figure 12). potential role in screening rather than diagnosis (Kapila
et al., 2008).
Urinary Bladder Cancer
While urinary bladder cancers are well known to be Prostate Cancer
the predominant neoplasm in Egyptian males (see Table In many of the countries of the Middle-east, prostate
2), high rates are also present in Iraq, Jordan Tunisia and cancer is already a problem (see Figure 14) and in
Bahrain, but not in Qatar and elsewhere in the Gulf, Mauritanian males it is the most frequent neoplasm (see
pointing to considerable variation in risk factors across Figure 2). A Egyptian case-control study pointed to
the Arab world (see Figure 13). Data for the sausages, butter and natural ghee as risk factors, while
histopathological distribution are summarized in Table 8. vegetables were protective (Kamel et al., 2006).
Traditionally, Schistosoma haematobium has been Screening is opportunistic. However, data should be
considered the most important etiological agent (Bedwani interpreted with caution because public awareness
et al., 1998), but transitional cell carcinoma has recently campaigns have led to large numbers of individuals being
become the most frequent type in Egypt, replacing lesions found positive. Arab Kuwaiti and Omani men were
with squamous features generally associated with reported to have lower serum PSA levels and prostate
parasites, corroborating findings from small-scale hospital- volumes than those reported for Caucasians, but similar
based studies indicating that the etiology of bladder cancer to those reported for Asians (Japanese and Chinese)
has changed significantly over the past 26 years (Felix et (Kehinde et al., 2005). Mean PSA values for Saudi men
al., 2008). A remarkably strong association with various are also low (Kamal et al., 2003). Although raised serum
measures of cigarette smoking has been found that could PSA is commonly associated with prostate cancer,
explain 75% of bladder cancer cases among males from subclinical prostatitis is a significant source of high serum
PSA in over 40% of men in Kuwait, suggesting the need
for a locally applicable paradigm to identify prostate cancer
(Anim et al., 2007).

Breast Cancer
Breast cancer now occupies the number one position
in all countries of the Arab world, even if absolute rates
0-5 10-15 20-25 are relatively low (see Figure 15). Cases tend to be young
and almost half of patients are below 50, with a median
5-10 15-20 >25 age of 49-52 years as compared to 63 in industrialized
nations (El Saghir et al., 2007). A preponderance in
Figure 13. Male Urinary Bladder Cancer Incidences/
100,000 (Globocan, 2002: Ferlay et al., 2004)

Table 8. Urinary Bladder Cancer Histopathology:


TCC-SCC Ratios (Curado et al., 2007)
Male Female
SCC TCC Ratio SCC AC Ratio
0-5 10-15 20-30
Egypt 19.9 69.0 0.29:1 40.1 47.4 0.85:1
Palestine 0.0 96.4 INF:1 0.0 96.2 INF:1
5-10 15-20 >30
Algeria 11.4 58.6 0.19:1 0.0 60.0 INF:1
Tunisia 1.1 94.3 0.01:1 4.5 90.9 0.05:1
Bahrain 2.7 79.5 0.04:1 10.0 75.0 0.13:1
Kuwait 4.3 91.3 0.04:1 4.8 81.0 0.06:1 Figure 14. Prostate Cancer Incidences/100,000
Oman 12.0 80.7 0.15:1 8.6 68.6 0.13:1 (Globocan, 2002: Ferlay et al., 2004)

Asian Pacific Journal of Cancer Prevention, Vol 10, 2009 9


Elsayed I Salim et al
examination leading to more early diagnosis and breast-
conserving surgery, so that population-based screening in
those countries with affluent resources and accessible care
should be implemented (El Saghir et al., 2007).
Knowledge of breast cancer risk-factors and screening
awareness are high among women nurses and teachers in
0-10 20-30 40-50
Amman, Jordan (Madanat and Merrill, 2002) but health
workers infrequently offered screening examinations and
10-20 30-40 >50
women were found to lack adequate knowledge about
Figure 15. Female Breast Cancer Incidences/100,000 breast cancer screeningin Qatar (Bener et al., 2001). Health
(Globocan, 2002: Ferlay et al., 2004) planners and healthcare providers must capitalize on
encouraging factors and minimize deterring factors to
relatively young individuals has been reported for the optimize breast cancer screening practices (Bener et al.,
Lebanon (El Saghir et al., 2002), Alexandria in Egypt 2002). Screening campaigns should aslo target husbands
(Hosny and Elkaffas, 2002a), and Aden in the Yemen to encourage their wives to enrol (El Saghir, 2007).
(Abdul Hamid et al., 2001). Positive correlations were found between nursing
Epidemiological findings point to the same risk factors students BSE practice and their academic experience in
as in the Western world. A positive family history of breast nursing college in Saudi Arabia (Alsaif, 2004). Female
cancer, young age at menarche, late age at last full-term secondary-school students in Jeddah demonstrated only
pregnancy and wide inter-birth interval were significant low knowledge of risk factors and presentation in those
predictors for occurrence in Egypt (Kishk, 1999). not having familial experience (Milaat, 2000), although
Postmenopausal obesity is a significant risk factor in the vast majority demonstrated a positive attitude towards
Jordan, along with number of pregnancies (more than 4) learning breast self-examination (Altaf et al., 2004). There
(Atoum and Al-Hourani, 2004a). On the other hand, longer is a significant association between failure to practise
period of breast feeding (more than 24 months) decreases breast self-examination and diagnostic delay in Egypt
the risk (Atoum and Al-Hourani, 2004b). Risk factors in (Abdel-Fattah et al., 2000). Guidelines are clearly needed
Kuwait include high BMI, lack of regular exercise, early (Altaf, 2004). Husbands whose wives have breast cancer
age at menarche, late age at first pregnancy, hormonal may also need a network of support to address their specific
therapy, and frequent consumption of carbohydrate, issues and concerns (Woloski-Wruble and Kadmon, 2002)
sweets, animal fat, and vegetable oil (margarine) with low
intake of fresh vegetables and olive oil (Saleh et al., 2008). Ovarian Cancer
In Iraq, family history and oral contraceptives use were Ovarian cancer is moderately frequent in the Middle-
found to be associated (Fakri et al., 2006). Parental east (see Figure 16). The majority of lesions are seroud,
consanguinity in Arabs, even when a marriage is between followed by mucinour and adeocarcinoma types (Curado
first cousins or double first cousins, was not associated et al., 2007). It has been suggested that substitution of non-
with an altered risk of breast cancer (Denic et al., 2005). animal for animal fat during adult life might reduce the
Infertility and usage of infertility drugs in general are not risk of ovarian cancer (Lubin et al., 2006).
associated with increased risk for breast cancer (Lerner-
Geva et al., 2004). One analysis yielded an estimated 73% Endometrial Cancer
higher breast cancer incidence in the highest compared to Endometrial cancer of the corpus uterus is relatively
the light at night exposed communities (Kloog et al., 2008). infrequent, with a picture similar to that for the ovary (see
High-risk HPV infections are associated with human breast Figure 17). Research has indicated elevated risk with
cancer progression in Syrian women (Akil et al., 2008). increased number of abortions, ovarian cycles and live
Locally advanced disease is very common in Egypt, births, and decreased risk with increased parity as
Tunisia, the Yemen, Saudi Arabia, Kuwait, Syria, Palestine compared to the nulliparous case (El-Khwsky et al., 2006).
and others, and total mastectomy is the most commonly In another study, endometrial thickness >5mm, diabetes,
performed surgery (Abdul Hamid et al., 2001; Chiedozi hypertension and obesity were not found to be among the
et al., 2003; El Saghir et al., 2007; Saleh et al., 2007; risk factors, in contrast to age and occurrence of post
Tarabeia et al., 2007). Metastases were reproted to be
relatively low in one study (Abuzallouf et al., 2007), but
this appears exceptional. Overall 5 year survival rates
available from the literature are 59.6% in Saudi Arabia
(Ravichandran et al., 2005) and 68.8% in Bahrain (Fakhro
et al., 1999) while in Oman 5-year relapse-free and overall
survival rates were reported to be 62% and 64%,
respectively (Al-Moundhri et al., 2004). Prevalence of 0-2 ✤ 4-6 ✤8-10

HER2/neu overexpression in a small sample of Qatari


2-4 6-8 >10
female cases was found to be 26%, linked to an elevated
relapse rate and mortality (Rasul et al., 2003).
Results from recent studies like the Cairo Breast Cancer Figure 16. Ovarian Cancer Incidences/100,000
Screening Trial show a positive impact of clinical breast (Globocan, 2002: Ferlay et al., 2004)

10 Asian Pacific Journal of Cancer Prevention, Vol 10, 2009


Cancer Epidemiology in the Arab Region

0-2 4-6 8-10 0-1 2-3 4-5

1-2 3-4 >5


2-4 6-8 >10

Figure 17. Endometrial Cancer Incidences/100,000 Figure 19. Male Brain and Nervous Cancer Incidences/
(Globocan, 2002: Ferlay et al., 2004) 100,000(Globocan, 2002: Ferlay et al., 2004)
menopausal bleeding (Al-Kadri et al., 2004). neoplastic devekopment (Maaita and Barakat, 2002).

Cervical Cancer Brian and Nervous Tissue Cancer


While cervical cancer is generally low in the Arab Relative to world levels, incidence rates for brain and
world (see Figure 18) and does not appear to be increasing, nervous cancer in the region are relatively high (see Figure
it still occupies second place for frequency in Algeria, 19). The incidence of acoustic neuroma in Qatar is slightly
Tunisia and Oman. Furthermore, there may be some under- higher than that in other countries, with a possible link to
reporting and in a prospective study in Saudi Arabia the frequent cellular phone use (Salahaldin and Bener, 2006).
percentage of abnormal pap smears was 4.7%, much higher
than the 1.6% reported in the compounded literature (Altaf, Thyroid Cancer
2006).✄ Adeocarcinomas account for approximately 10% Thyroid cancer is of medium importance (see Figure
of the lesins (Curado et al., 2007). 21), but occupies the number two position in females in
Clearly the human papilloma virus is the prime risk Saudi Arabia and is prevalent in other coutries of the Gulf
factor and the Muslim religious background is naturally as well as Jordan. The dramatic decline in the incidence
of great significance in this regard. It should be mentioned of follicular thyroid carcinoma combined with the increase
in this context that penile cancer is also extremely rare, as in the advanced forms in Central Jordan may suggest a
for example documented in Saudi Arabia (Abomelha, possible environmental factor (Shomaf et al., 2006). In
2004). Regarding risk factors, early marriage, frequent contrast, papillary carcinomas form the bulk of cases in
coitus started early in life and increasing number of the Yemen, where the salt iodization program might have
pregnancies are predisposing factors, while abortions and an effect on the incidence (Abdulmughni et al., 2004).
age at menarche are without influence (Ejeckam et al.,
1994). Polygamy, smoking and hormonal contraception Leukemias and Lymphomas
were not identified as risk factors in one study, whereas In both sexes, Non-Hodgkins lymphomas and to a
positive women again showed higher parity (Hajjaj et al., lesser extent leukemias, are relatively important neoplasms
2006). In Egypt, HPV 16/18 is the major risk factor, across the region (see Figures 21 and 22). However,
frequently with mixed infections and bilharzial infestation research findings are limited, especially as to risk factors.
(el-All et al., 2007). There is some support for the hypothesis that NHL is a
Screening programs are not in place and one problem malignant outcome of chronic HCV infection (Cowgill et
is with attitudes. Of 98 physicians who participated in a al., 2004). It is possible that the tumour type is increasing,
study in the UAE. only 40% reported ever having from data for Alexandria, particularly in the elderly
performed a Pap smear, so that a training programme on population (Abdel-Fattah and Yassine, 2007).
cervical screening was considered necessary (Badrinath
et al., 2004). In Jordan, about a third of women were found Childhood cancers
to be unaware of the significance of a positive cervical There are only limited research data for cancers of
smear and three-quarters did not know the causes of childhood in the Middle-East. However, it is likely that

0-5 10-15 20-25 0-2 4-6 8-10

5-10 15-20 >25 2-4 6-8 >10

Figure 18. Cervical Cancer Incidences/100,000 Figure 21. Male Thyroid Cancer Incidences/100,000
(Globocan, 2002: Ferlay et al., 2004) (Globocan, 2002: Ferlay et al., 2004)

Asian Pacific Journal of Cancer Prevention, Vol 10, 2009 11


Elsayed I Salim et al
Table 9. ASR Cancer Incidence Over Time - CIV
Volume IV* V** VI# VII## VIII## IX+
Kuwait
Oesophagus --- 1.7 3.7 1.7 1.7 2.2
Stomach --- 5.6 4.1 4.1 5.6 3.4
0-2 4-6 8-10
Colon --- 6.3 1.9 3.5 6.3 8.4
Rectum --- 4.0 2.4 3.9 4.0 5.2
2-4 6-8 >10
Liver --- 4.4 7.2 7.3 8.4 8.1
Prostate --- 11.4 4.4 6.5 11.4 10.5
Breast --- 15.9 17.2 32.8 32.8 41.3
Figure 22. Male Non-Hodgkins Lymphoma Incidences/ Ovary --- 3.3 3.7 4.7 5.7 5.4
100,000 (Globocan, 2002: Ferlay et al., 2004) Endometrium --- 1.8 2.4 2.4 3.8 3.6
Cervix --- 3.9 4.1 7.6 4.2 4.5
Thyroid --- 6.3 1.4 6.1 7.6 7.3
Larynx --- 3.5 2.4 2.5 3.5 0.5
Lung --- 21.5 14.5 20.3 21.5 15.6
Kidney --- 3.8 2.4 2.1 3.8 5.8
Bladder --- 4.6 5.7 7.0 4.6 6.3
NHL --- 8.6 7.3 5.5 8.6 10.4
Leukemia --- 5.5 7.4 5.1 5.5 4.9
0-2 4-6 8-10
Palestine
Oesophagus 1.0 1.0 1.1 0.5 0.7 1.1
2-4 6-8 >10
Stomach 7.2 7.9 6.9 6.8 6.7 6.7
Colon 3.3 4.7 4.6 6.2 9.6 10.6
Figure 23. Male Leukemia Incidences/100,000 Rectum 3.1 3.0 3.6 3.1 3.8 8.3
(Globocan, 2002: Ferlay et al., 2004) Liver 2.4 2.9 3.0 2.6 3.2 2.6
Prostate 4.9 6.5 7.7 10.4 14.8 20.0
lymphatic and haemopoietic cancer incidences are Breast 11.0 14.0 17.0 21.3 27.7 41.3
increasing (Hosny and Elkaffas , 2002b). Ovary 3.8 3.4 2.4 3.0 4.0 5.4
Endometrium 1.2 3.1 2.8 4.9 5.7 3.6
Cervix 2.1 3.0 2.6 3.0 2.5 4.5
Future Perspectives Thyroid 1.8 2.5 2.6 4.1 4.8 7.3
Larynx 6.4 4.9 4.1 3.7 5.4 6.1
It should be stressed that cancer registry data in the Lung 28.8 23.4 26.2 29.1 35.1 40.4
regionare scanty, especially for those countries with large Kidney 8.6 2.5 3.3 3.3 3.3 4.4
populations, so that emphasis should be palced on better Bladder 1.8 12.5 9.1 13.1 15.5 18.1
development of regional and national registries. There may NHL 7.5 6.7 5.4 8.3 9.7 10.0
be too much reliance on pathology reports and luekemias, Leukemia 5.9 5.1 6.2 6.0 7.8 7.3
for example are likely to be under-reported. Optimally, *
Waterhouse et al., 1982; **Muir et al., 1987; #;##;###
Parkin et al.,
governments would make registration mandatory, with 1992;1997;2002; +Curado et al., 2007
roles for WHO/UICC/OARC in assuring quality and
reliability. To create an environment conducive to more Kepler, 2001).
allocation of resources and personnel, Arab scientists need It is well known from migrant studies that Arab
to report their data in peer-reviewed journals (El-Saghir populations were earlier characterized by generally low
et al., 2007). rates for cancers of colon and rectum, lung, ovary and
Although most of the registries in the Middle east have prostate (McCredie et al., 1994). Cancers which tended to
not been operating for a sufficient length of time to give be more common in migrants were stomach, liver, and
information on time trends, data are available over 30 years bladder. These still are important but the future will see
for Palestinians and for 25 years for Kuwaitis (see Table the main burden in diabetes-associated tumours, as in the
9). Common to both are relatively consistent increases in developed world. To what extent these are affluence-
cancers of the colon, prostate, endometrium and breast, related needs to now be determined by epidemiological
as well as Non-Hodgkins lymphomas and perhaps ovarian research into psychosocial factors. The Arab countires are
and thyroid cancers. All of the adenocarcinomas are particulary interesting in this regard, given the wide
considered linked to a Westernized lifestyle. A nutrition variation in Gross National Product. Hopefully, such
transition, as well documented for Egypt (Galal, 2002) enigmas as the decreasing lung rates in Kuwait and very
has occurred in the context of abundant dietary energy low incidences in some of the Arab countries, despite clear
availability, urbanisation and moderate fat intakes. The increase in Palestinians, will thereby also be explained.
prevalence of obesity in adults in the region is very high, Given the recent increase in ‘hubble bubble’ (Arkila,
particularly among women. The prevalences of diabetes Narkila) smoking by youth across the region, more stress
mellitus and of hypertension parallel that of obesity. needs to be placed on anti-smoking efforts. Advertising is
Smoking, physical inactivity, and obesity contribute rampant and uncontrolled in many countries and more
substantially to the burden of chronic disease (Centers protection is clearly required for adolescents. Other areas
for Disease Control and Prevention, 2002; Kulwicki and which need particular attention aresmoking nutrition

12 Asian Pacific Journal of Cancer Prevention, Vol 10, 2009


Cancer Epidemiology in the Arab Region
including the role played by local vegetables and herbs Al-Lawati JA, al-Shaqsi B, al-Siyabi N (2001). Cancer
(Abu-Rabia, 2005). The importance of environmental registration in the Sultanate of Oman. Asian Pacific J Cancer
exposure to pesticides and other contaminants has also Prev, 2 (IACR Suppl), 71-4.
be highlighted (Safi, 2002). Given the clear variation in Al-Lawati JA, Santhosh-Kumar CR, Mohammed AJ, Jaffer MA
(1999). Cancer incidence in Oman, 1993-1997. East Mediterr
cancer burden within the Arab world, despite a shared
Health J, 5, 1035-41.
culture, collaboration across individual registries across Al-Maghrabi JA, Al-Ghamdi AS, Elhakeem HA. Pattern of skin
the region should lead to a far better understanding of the cancer in Southwestern Saudi Arabia. Saudi Med J, 25, 776-
status and the evidence base which is essential for effective 9.
cancer control programs. Almog R, Hagoel L, Tamir A, Barnett O, Rennert G
(2008).Quality control in a National Program for the Early
References Detection of Breast Cancer: women’s satisfaction with the
mammography process. Womens Health Issues, 18, 110-7.
Al-Moundhri M, Al-Bahrani B, Pervez I, et al (2004). The
Abdel Aziz MT, Abdel Aziz MZ, Atta HM, et al (2006). Screening outcome of treatment of breast cancer in a developing
for human papillomavirus (HPV) in Egyptian women by the country--Oman. Breast, 13, 139-45.
second-generation hybrid capture (HC II) test. Med Sci Monit, Al-Rawi NH, Talabani NG (2008). Squamous cell carcinoma of
12, MT43-9. the oral cavity: a case series analysis of clinical presentation
Abdel-Fattah MM, Yassine OG (2007). Non-Hodgkin’s and histological grading of 1,425 cases from Iraq. Clin Oral
lymphomas in Alexandria, Egypt; incidence rates and trend Investig, 12, 15-8.
study (1995-2004). Eur J Cancer Prev, 16, 479-85. Alsaif AA (2004). Breast self-examination among Saudi female
Abdel-Fattah M, Zaki A, Bassili A, el-Shazly M, Tognoni G nursing students in Saudi Arabia. Saudi Med J, 25, 1574-8.
(2000). Breast self-examination practice and its impact on Alsayyad J, Hamadeh R (2007). Cancer incidence among the
breast cancer diagnosis in Alexandria, Egypt. East Mediterr Bahraini population: a five-year (1998-2002) experience. Ann
Health J, 6, 34-40. Saudi Med, 27, 251-8.
Abdel-Hady ES, Emam M, Al-Gohary A, et al (2006). Screening Al-Shamsi SR, Bener A, Al-Sharhan M, et al (2003).
for cervical carcinoma using visual inspection with acetic Clinicopathological pattern of colorectal cancer in the United
acid. Int J Gynaecol Obstet, 93, 118-22. Arab Emirates. Saudi Med J, 24, 518-22.
Abdel-Hamid M, El-Daly M, Molnegren V, et al (2007). Genetic Altaf FJ (2004). Breast cancer screening. Saudi Med J, 25, 991-
diversity in hepatitis C virus in Egypt and possible association 7.
with hepatocellular carcinoma. J Gen Virol, 88, 1526-31. Altaf FJ (2006). Cervical cancer screening with pattern of pap
Abdel-Wahab M, El-Ghawalby N, Mostafa M, et al (2007). smear. Review of multicenter studies. Saudi Med J, 27, 1498-
Epidemiology of hepatocellular carcinoma in lower Egypt, 502.
Mansoura Gastroenterology Center. Hepato- Altaf FJ, Abdullah LS, Jamal AA (2004). Frequency of benign
gastroenterology, 54, 157-62. and preinvasive breast diseases. Saudi Med J, 25, 493-7.
Abdul Hamid G, Tayeb MS, Bawazir AA (2001). Breast cancer Al-Thobhani AK, Raja’a YA, Noman TA (2001). The pattern
in south-east Republic of Yemen. East Mediterr Health J, 7, and distribution of malignant neoplasms among Yemeni
1012-6. patients. Saudi Med J. Oct;22(10):910-3.
Abdulmughni YA, Al-Hureibi MA, Al-Hureibi KA, et al (2004). Andejani AA, Kundapur V, Malaker K (2004). Age distribution
Thyroid cancer in Yemen. Saudi Med J, 25, 55-9. of nasopharyngeal cancer in Saudi Arabia. Saudi Med J, 25,
Abomelha MS (2004). Genito-urinary cancer in Saudi Arabia. 1579-82.
Saudi Med J, 25, 552-6. Anim JT, Kehinde EO, Sheikh MA, et al (2007). Serum prostate-
Abou-Zeid AA, Khafagy W, Marzouk DM, et al (2002). specific antigen levels in Middle Eastern men with subclinical
Colorectal cancer in Egypt. Dis Colon Rectum, 45, 1255-60 prostatitis. Med Princ Pract, 16, 53-8.
Abu-Rabia A (2005). Herbs as a food and medicine source in Anwar WA, Khaled HM, Amra HA, et al (2008). Changing
Palestine. Asian Pac J Cancer Prev, 6, 404-7. pattern of hepatocellular carcinoma (HCC) and its risk factors
Abuzallouf S, Motawy M, Thotathil Z (2007). Baseline staging in Egypt: possibilities for prevention. Mutat Res, 659, 176-
of newly diagnosed breast cancer--Kuwait cancer control 84.
center experience. Med Princ Pract, 16, 22-4. Atoum MF, Al-Hourani HM. Lifestyle related risk factors for
Akil N, Yasmeen A, Kassab A, et al (2008). High-risk human breast cancer in Jordanian females. Saudi Med J, 2004
papillomavirus infections in breast cancer in Syrian women Sep;25(9):1245-8.
and their association with Id-1 expression: a tissue microarray Atoum MF, Al-Hourani HM. Comparison of some risk factors
study. Br J Cancer, 99, 404-7. between non-familial and familial breast cancer females in
Al-Hamdan N, Al-Jarallah M, Al-Jarallah M, et al (2006). The Jordan. Saudi Med J. 2004 Feb;25(2):168-71.
incidence of lung cancer in the Gulf Cooperation Council Azaiza F, Cohen M (2008a). Between traditional and modern
countries. Ann Saudi Med, 26, 433-8. perceptions of breast and cervical cancer screenings: a
Al Hamdan N, Bazarbashi S, Ajarim D, et al (2001). History of qualitative study of Arab women in Israel. Psychooncology,
cancer registration in the country of Saudi Arabia. Asian 17, 34-41.
Pacific J Cancer Prev, 2 (IACR Suppl), 61-4. Azaiza F, Cohen M (2008b). Colorectal cancer screening,
Al-Hilli F, Malik AK (2003). Oesophageal cancer in Bahrain. intentions, and predictors in Jewish and Arab Israelis: a
East Mediterr Health J, 9, 372-6. population-based study. Health Educ Behav, 35, 478-93.
Ali AA, Al-Sharabi AK, Aguirre JM, Nahas R (2004). A study Badrinath P, Ghazal-Aswad S, Osman N, Deemas E, McIlvenny
of 342 oral keratotic white lesions induced by qat chewing S (2004). A study of knowledge, attitude, and practice of
among 2500 Yemeni. J Oral Pathol Med, 33, 368-72. cervical screening among female primary care physicians in
Al-Kadri HM, Al-Awami SH, Madkhali AM. Assessment of risk the United Arab Emirates. Health Care Women Int, 25, 663-
factors of uterine cancer in Saudi patients with 70.
postmenopausal bleeding. Saudi Med J, 25, 857-61. Bahnassy AA, Zekri AR, Abdallah S, El-Shehaby AM, Sherif

Asian Pacific Journal of Cancer Prevention, Vol 10, 2009 13


Elsayed I Salim et al
GM (2005). Human papillomavirus infection in Egyptian Curado MP, Edwards B, Shin HR, et al (eds) (2007). Cancer
esophageal carcinoma: correlation with p53, p21, mdm2, C- Incidence in Five Continents, Vol.IX, IARC Scientific
erbB2 and impact on survival. Pathol Int, 55, 53-62. Publications No. 160, Lyon IARC.
Basaleem HO, Al-Sakkaf KA (2004). Colorectal cancer among Darwish H, Trejo IE, Shapira I, et al (2002). Fighting colorectal
Yemeni patients. Characteristics and trends. Saudi Med J, cancer: molecular epidemiology differences among
25, 1002-5. Ashkenazi and Sephardic Jews and Palestinians. Ann Oncol,
Bazarbashi S, de Vol EB, Ravichandran K, Young SE (2005). 13, 1497-501.
Cancer Incidence Report Saudi Arabia, 2001. National Denic S, Bener A, Sabri S, Khatib F, Milenkovic J (2005).
Cancer Registry, Ministry of Health. www.kfshrc.edu.sa/ Parental consanguinity and risk of breast cancer: a
oncology/files/ncr01 population-based case-control study. Med Sci Monit, 11,
Bavi PP, Abubaker JA, Jehan ZD, et al (2008). Colorectal CR415-9.
carcinomas from Middle East. Molecular and tissue Ejeckam GC, Abdulla F, el-Sakka M, Dauleh W, Haseeb F (1994).
microarray analysis of genomic instability pathways. Saudi Gynaecological malignancies in Qatar. East Afr Med J, 71,
Med J, 29, 75-80. 777-81.
Bawazir A, Basalem A, Suwailah M (2003). Cancer incidence. Ejeckam GC, Ahmed FA, Azadeh B (1993). Esophageal cancer
Five-year report, Aden, Lahej, Abyana dn Aldhale’e. Aden in Qatar. Trop Geogr Med, 45, 25-7.
Cancer Center. el-All HS, Refaat A, Dandash K (2007). Prevalence of cervical
B’chir F, Laouani A, Ksibi S, Arnaud MJ, Saguem S (2007). neoplastic lesions and Human Papilloma Virus infection in
Cigarette filter and the incidence of lung adenocarcinoma Egypt: National Cervical Cancer Screening Project. Infect
among Tunisian population. Lung Cancer, 57, 26-33. Agent Cancer, 2, 12.
Bedwani R, el-Khwsky F, Renganathan E, et al (1997). El Hag IA, Katchabeswaran R, Chiedozi LC, Kollur SM (2002).
Epidemiology of bladder cancer in Alexandria, Egypt: Pattern and incidence of cancer in Northern Saudi Arabia.
tobacco smoking. Int J Cancer, 73, 64-7. Saudi Med J, 23, 1210-3.
Bedwani R, Renganathan E, El Kwhsky F, et al (1998). El-Helal TA, Bener A, Galadari I (1997). Pattern of cancer in
Schistosomiasis and the risk of bladder cancer in Alexandria, the United Arab Emirates referred to Al-Ain Hospital. Ann
Egypt. Br J Cancer, 77, 1186-9. Saudi Med, 17, 506-9.
Bener A, Adeyemi EO, Almehdi AM, et al (2006). Helicobacter el-Houseini ME, Mohammed MS, Elshemey WM, et al (2005).
pylori profile in asymptomatic farmers and non-farmers. Int Enhanced detection of hepatocellular carcinoma. Cancer
J Environ Health Res, 16, 449-54. Control, 12, 248-53.
Bener A, Alwash R, Miller CJ, Denic S, Dunn EV (2001). El-Khwsky FS, Maghraby HK, Rostom YA, Abd El-Rahman
Knowledge, attitudes, and practices related to breast cancer AH (2006). Multivariate analysis of reproductive risk factors
screening: a survey of Arabic women. J Cancer Educ, 16, for ovarian cancer in Alexandria, Egypt. J Egypt Natl Canc
215-20. Inst, 18, 30-4.
Bener A, Ayub H, Kakil R, Ibrahim W (2008). Patterns of cancer El Mistiri M, Verdecchia A, Rashid I, et al (2007). Cancer
incidence among the population of Qatar : a worldwide incidence in eastern Libya: the first report from the Benghazi
comparative study. Asian Pacific J Cancer Prev, 9, 19-24. Cancer Registry, 2003. Int J Cancer, 120, 392-7.
Bener A, Denic S, Al-Mazrouei M (2001). Consanguinity and El Saghir NS, Adib S, Mufarrij A, et al (1998). Cancer in
family history of cancer in children with leukemia and Lebanon: analysis of 10,220 cases from the American
lymphomas. Cancer, 92, 1-6. University of Beirut Medical Center. J Med Liban, 46, 4-11.
Bener A, Honein G, Carter AO, et al (2002). The determinants El Saghir NS, Khalil MK, Eid T, et al (2007). Trends in
of breast cancer screening behavior: a focus group study of epidemiology and management of breast cancer in
women in the United Arab Emirates. Oncol Nurs Forum, developing Arab countries: a literature and registry analysis.
29, E91-8. Int J Surg, 5, 225-33.
Bener A, Hussain R, Teebi AS (2007). Consanguineous marriages El Saghir NS, Shamseddine AI, Geara F, et al (2002). Age
and their effects on common adult diseases: studies from an distribution of breast cancer in Lebanon: increased
endogamous population. Med Princ Pract, 16, 262-7. percentages and age adjusted incidence rates of younger-
Birkenfeld S, Niv Y. Survey of primary physicians’ knowledge aged groups at presentation. J Med Liban, 50, 3-9.
of colorectal cancer screening. J Clin Gastroenterol, 40, 64- El-Shalakany AH, Saeed MM, Abdel-Aal MR, et al (2008). Direct
7. visual inspection of the cervix with Lugol iodine for the
Brown A, Ravichandran K, Warnakulasuriya S (2006). The detection of premalignant lesions. J Low Genit Tract Dis,
unequal burden related to the risk of oral cancer in the 12, 193-8.
different regions of the Kingdom of Saudi Arabia. Community El-Shalakany A, Hassan SS, Ammar E, Ibrahim MA, Salam MA,
Dent Health, 23, 101-6. Farid M. Direct visual inspection of the cervix for the
Centers for Disease Control and Prevention (CDC). Prevalence detection of premalignant lesions. J Low Genit Tract Dis, 8,
of selected risk factors for chronic disease--Jordan, 2002. 16-20.
MMWR Morb Mortal Wkly Rep. 2003 Oct 31;52(43):1042- Fakhro AE, Fateha BE, al-Asheeri N, al-Ekri SA (1999). Breast
4. cancer: patient characteristics and survival analysis at
Chaouki N, el Gueddari B (1991). Epidemiological descriptive Salmaniya medical complex, Bahrain. East Mediterr Health
approach of cancer in Morocco through the activity of the J, 5, 430-9.
National Institute of Oncology. 1986-7. Bull Cancer, 78, Fakri S, Al-Azzawi A, Al-Tawil N (2006). Antiperspirant use as
603-9. a risk factor for breast cancer in Iraq. East Mediterr Health
Chiedozi LC, El-Hag IA, Kollur SM (2003). Breast diseases in J, 12, 478-82.
the Northern region of Saudi Arabia. Saudi Med J, 24, 623- Felix AS, Soliman AS, Khaled H, et al (2008). The changing
7. patterns of bladder cancer in Egypt over the past 26 years.
Cowgill KD, Loffredo CA, Eissa SA, et al (2004). Case-control Cancer Causes Control, 19, 421-9.
study of non-Hodgkin's lymphoma and hepatitis C virus Ferlay J, Bray F, Pisani P, Parkin DM (2004). GLOBOCAN 2002:
infection in Egypt. Int J Epidemiol, 33, 1034-9. Cancer Incidence, Mortality and Prevalence Worldwide.

14 Asian Pacific Journal of Cancer Prevention, Vol 10, 2009


Cancer Epidemiology in the Arab Region
IARC CancerBase No. 5, version 2.0, IARCPress, Lyon. Kamal BA, Ali GA, Taha SA (2003). Prostate specific antigen
Freedman LS, Barchana M, Al-Kayed S, et al (2003). A reference ranges in Saudi men. Saudi Med J, 24, 665-8.
comparison of population-based cancer incidence rates in Kamel NM, Tayel ES, El Abbady AA, Khashab SS. Risk factors
Israel and Jordan. Eur J Cancer Prev, 12, 359-65. of cancer prostate. A case control study. J Egypt Public
Freedman LS, Edwards B, Ries LAG, Young JL (Eds) (2007). Health Assoc, 81, 143-63.
Cancer Incidence in Four Member Countries (Cyprus, Egypt, Kapila K, Kehinde EO, Anim JT, et al (2008). Could nuclear
Israel, and Jordan) of the Middle East Cancer Consortium matrix protein 22 (NMP22) play a role with urine cytology
(MECC) Compared with US SEER. National Cancer in screening for bladder cancer? - experience at Kuwait
Institute. NIH Pub. No. 06-5873. Bethesda, MD. University. Cytopathology (in press).
Gaafar RM, Eldin NH (2005). Epidemic of mesothelioma in Kehinde EO, Mojiminiyi OA, Sheikh M, et al (2005). Age-
Egypt. Lung Cancer, 49 Suppl 1, S17-20. specific reference levels of serum prostate-specific antigen
Galal OM (2002). The nutrition transition in Egypt: obesity, and prostate volume in healthy Arab men. BJU Int, 96, 308-
undernutrition and the food consumption context. Public 12.
Health Nutr, 5, 141-8. Khalil KA, Salama OE, El Zeiny NA, El din Khalil S, Esmail
Geara FB, Nasr E, Tucker SL, et al (2005). Nasopharyngeal NF (1999). A study of pattern of gastrointestinal malignant
cancer in the Middle East: experience of the American neoplasms in the last decade (1987-1996) in Alexandria. J
University of Beirut Medical Center. Int J Radiat Oncol Biol Egypt Public Health Assoc, 74, 503-27.
Phys, 61, 1408-15. Kishk NA. Breast cancer in relation to some reproductive factors.
Ghafoor M, Schuyten R, Bener A. (2003). Epidemiology of J Egypt Public Health Assoc, 74, 547-66.
prostate cancer in United Arab Emirates. Med J Malaysia, Kriegel AM, Soliman AS, Zhang Q, et al (2006). Serum cadmium
58, 712-6. levels in pancreatic cancer patients from the East Nile Delta
Gunaid AA, Hassan NA, Murray-Lyon I. (2003). Prevalence and region of Egypt. Environ Health Perspect, 114, 113-9.
risk factors for Helicobacter pylori infection among Yemeni Kulwicki AD, Kepler C. Assessment of cardiovascular risk
dyspeptic patients. Saudi Med J, 24, 512-7. factors among residents of a city in Jordan. J Cult Divers.
Gunaid AA, Sumairi AA, Shidrawi RG, et al (1995). Oesophageal 2001 Summer;8(2):34-40.
and gastric carcinoma in the Republic of Yemen. Br J Cancer, Lehman EM, Soliman AS, Ismail K, et al (2008). Patterns of
71, 409-10. hepatocellular carcinoma incidence in Egypt from a
Guraya SY, Eltinay OE (2006). Higher prevalence in young population-based cancer registry. Hepatol Res, 38, 465-73.
population and rightward shift of colorectal carcinoma. Saudi Lo AC, Soliman AS, El-Ghawalby N, et al (2007). Lifestyle,
Med J, 27, 1391-3. occupational, and reproductive factors in relation to
Habib OS, Al-Ali JK, Al-Wiswasi MK, Ajeel NAH (2006). The pancreatic cancer risk. Pancreas, 35, 120-9.
burden of cancer in Basrah: The state of the art - first report. Maaita M, Barakat M. Jordanian women’s attitudes towards
Available on: www.basmedcol.com. cervical screening and cervical cancer. J Obstet Gynaecol.
Habib OS, Al-Ali JK, Al-Wiswasi MK, et al (2007). Cancer 2002 Jul;22(4):421-2.
registration in Basrah 2005: preliminary results. Asian Pac Maalej M, Hentati D, Messai T, et al (2008). Breast cancer in
J Cancer Prev, 8, 187-90. Tunisia in 2004: a comparative clinical and epidemiological
Hajjaj AA, Senok AC, Al-Mahmeed AE, et al (2006). Human study. Bull Cancer, 95, E5-9.
papillomavirus infection among women attending health Madanat H, Merrill RM. Breast cancer risk-factor and screening
facilities in the Kingdom of Bahrain. Saudi Med J, 27, 487- awareness among women nurses and teachers in Amman,
91. Jordan. Cancer Nurs. 2002 Aug;25(4):276-82.
Hifnawy MS, Mangoud AM, Eissa MH, et al (2004). The role of Madbouly KM, Senagore AJ, Mukerjee A, et al (2007). Colorectal
aflatoxin-contaminated food materials and HCV in cancer in a population with endemic Schistosoma mansoni:
developing hepatocellular carcinoma in Al-Sharkia is this an at-risk population? Int J Colorectal Dis, 22, 175-
Governorate, Egypt. J Egypt Soc Parasitol, 34, 479-88. 81.
Hosny G, Elkaffas SM (2002a). A prediction model for the Mahmoud SF, Azadeh B (1996). Basal cell carcinoma in Qatar.
incidence patterns of female breast cancers in Alexandria, Int J Dermatol, 35, 704-6.
Egypt. J Egypt Public Health Assoc, 77, 329-45. Mansoor I, Zahrani IH, Abdul Aziz S (2002). Colorectal cancers
Hosny G, Elkaffas SM (2002b). Patterns in the incidence of in Saudi Arabia. Saudi Med J, 23, 322-7.
pediatric cancer in Alexandria, Egypt, from 1972 to 2001. J McCredie M, Coates M, Grulich A (1994). Cancer incidence in
Egypt Public Health Assoc, 77, 451-68. migrants to New South Wales (Australia) from the Middle
Hussein MR, Ismael HH (2004). Alterations of p53, Bcl-2, and East, 1972-91. Cancer Causes Control, 5, 414-21.
hMSH2 protein expression in the normal breast, benign Memon A, Varghese A, Suresh A (2002). Benign thyroid disease
proliferative breast disease, in situ and infiltrating ductal and dietary factors in thyroid cancer: a case-control study in
breast carcinomas in the upper Egypt. Cancer Biol Ther, 3, Kuwait. Br J Cancer, 86, 1745-50.
983-8. Menczer J, Liphshitz I, Barchana M (2006). A decreasing
Hussein NR, Mohammadi M, Talebkhan Y, et al (2008). incidence of ovarian carcinoma in Israel. Int J Gynecol
Differences in virulence markers between Helicobacter Cancer, 16, 41-4.
pylori strains from Iraq and those from Iran: potential Milaat WA (2000). Knowledge of secondary-school female
importance of regional differences in H. pylori-associated students on breast cancer and breast self-examination in
disease. J Clin Microbiol, 46, 1774-9. Jeddah, Saudi Arabia. East Mediterr Health J, 6, 338-44.
Jahan S, Al-Saigul AM, Abdelgadir MH (2006). Breast cancer. Morris RE, Mahmeed BE, Gjorgov AN, Jazzaf HG, Rashid BA
Knowledge, attitudes and practices of breast self examination (2000). The epidemiology of lip, oral cavity and pharyngeal
among women in Qassim region of Saudi Arabia. Saudi Med cancers in Kuwait 1979-1988. Br J Oral Maxillofac Surg,
J, 27, 1737-41. 38, 316-9.
Kahan E, Ibrahim AS, El Najjar K, et al (1997). Cancer patterns Mosli HA (2003). Prostate cancer in Saudi Arabia in 2002. Saudi
in the Middle East--special report from the Middle East Med J, 24, 573-81.
Cancer Society. Acta Oncol, 36, 631-6. Muir CS, Waterhouse J, Mack T, Powell J, Whelan SL (Eds)

Asian Pacific Journal of Cancer Prevention, Vol 10, 2009 15


Elsayed I Salim et al
Cancer Incidence in Five Continents Vol. V. IARC Scientific Shamseddine A, Sibai AM, Gehchan N, et al, for The Lebanese
Publications No 88. 1987 IARC, Lyon. Cancer Epidemiology Group (2004). Cancer incidence in
Musaiger AO (1990). Nutritional disorders associated with postwar Lebanon: findings from the first national population-
affluence in Bahrain. Fam Pract, 7, 9-13. based registry, 1998. Ann Epidemiol, 14, 663-8.
Mzayek F, Asfar T, Rastam S, Maziak W (2002) Neoplastic Shema L, Ore L, Ben-Shachar M, Haj M, Linn S (2007). The
diseases in Aleppo, Syria. Eur J Cancer Prev, 11, 503-7. association between breastfeeding and breast cancer
Nasr AH, Khatri ML (2000). Head and neck squamous cell occurrence among Israeli Jewish women: a case control
carcinoma in Hajjah, Yemen. Saudi Med J, 21, 565-8. study. J Cancer Res Clin Oncol, 133, 539-46.
Omar S, Khaled H, Gaafar R, et al (2003). Breast cancer in Egypt: Shpitz B, Millman M, Ziv Y, et al (2006). Predominance of
a review of disease presentation and detection strategies. East younger age, advanced stage, poorly-differentiated and
Mediterr Health J, 9, 448-63. mucinous histology in Israeli Arab patients with colorectal
Parkin DM, Muir CS, Whelan SL, Gao YT, Ferlay J, Powell J cancer. Anticancer Res, 26, 533-7.
(Eds). Cancer Incidence in Five Continents Vol. VI. IARC Sion-Vardy N, Priel-Cohen Z, Mermershtain W, Neulander E,
Scientific Publications No 120. 1992 IARC, Lyon. Benharroch D (2008). Ethnicity and its significance in the
Parkin DM, Vatanasapt V. (Eds) (2001).Cancer registration in pathobiology of prostatic carcinoma in Southern Israel. Urol
Asia in the year 2000: Past present and future. Asian Pacific Oncol, 26, 31-6.
J Cancer Prev, 2, S1-89. Soliman AS, Smith MA, Cooper SP, et al (1997). Serum
Parkin DM, Whelan SL, Ferlay J, Raymond L, Young J. (Eds) organochlorine pesticide levels in patients with colorectal
Cancer Incidence in Five Continents Vol. VII. IARC cancer in Egypt. Arch Environ Health, 52, 409-15.
Scientific Publications No 143, 1997 IARC, Lyon. Soliman AS, Wang X, Stanley JD, et al (2006). Geographical
Parkin, DM, Whelan SL, Ferlay J, Teppo L,Thomas DB. (Eds). clustering of pancreatic cancers in the Northeast Nile Delta
Cancer Incidence in Five Continents Vol. VIII. IARC region of Egypt. Arch Environ Contam Toxicol, 51, 142-8.
Scientific Publications No 155, 2002 IARC, Lyon. Soskolne V, Marie S, Manor O. Beliefs, recommendations and
Parvez T, Gumgumji AA, Anwar MS, Al-Ahmadi SS (2004). intentions are important explanatory factors of
Awareness about causes of gastrointestinal tract (GIT) mammography screening behavior among Muslim Arab
malignancies. J Coll Physicians Surg Pak, 14, 98-101. women in Israel. Health Educ Res, 22, 665-76.
Qasem BM (2001). History of cancer registration in the country Tarabeia J, Baron-Epel O, Barchana M, et al (2007). A
of Jordan. Asian Pacific J Cancer Prev, 2 (IACR Suppl), comparison of trends in incidence and mortality rates of
25-29. breast cancer, incidence to mortality ratio and stage at
Qari FA (2004). Pattern of thyroid malignancy at a University diagnosis between Arab and Jewish women in Israel, 1979-
Hospital in Western Saudi Arabia. Saudi Med J, 25, 866-70. 2002. Eur J Cancer Prev, 16, 36-42.
Rasul KI, Awidi AS, Mubarak AA, Al-Homsi UM (2001). Study Tarabeia J, Green MS, Barchana M, et al (2008). Increasing lung
of colorectal cancer in Qatar. Saudi Med J, 22, 705-7. cancer incidence among Israeli Arab men reflects a change
Rasul KI, Mohammaed K, Abdalla AS, et al (2003). Study of in the earlier paradox of low incidence and high smoking
HER2/neu status in Qatari women with breast carcinoma. prevalence. Eur J Cancer Prev, 17, 291-6.
Saudi Med J, 24, 832-6. Waterhouse J, Muir C, Shanmugaratnam K, Powell J (Eds).
Ravichandran K, Hamdan NA, Dyab AR (2005). Population Cancer Incidence in Five Continents Vol. IV. IARC Scientific
based survival of female breast cancer cases in Riyadh Publications No 42. 1982 IARC, Lyon.
Region, Saudi Arabia. Asian Pac J Cancer Prev, 6, 72-6. Yaghi C, Sharara AI, Rassam P, et al (2006). Hepatocellular
Saad AA, O’Connor PJ, Mostafa MH, et al (2005). Glutathione carcinoma in Lebanon: Etiology and prognostic factors
S-transferase M1, T1 and P1 polymorphisms and bladder associated with short-term survival. World J Gastroenterol,
cancer risk in Egyptians. Int J Biol Markers, 20, 69-72. 12, 3575-80.
Safi JM (2002). Association between chronic exposure to
pesticides and recorded cases of human malignancy in Gaza
Governorates (1990-1999). Sci Total Environ, 284, 75-84.
Saidel-Odes L, Odes HS (2005). Strategy for colorectal cancer
screening. Isr Med Assoc J, 7, 248-51.
Salahaldin AH, Bener A (2006). Long-term and frequent cellular
phone use and risk of acoustic neuroma. Int Tinnitus J, 12,
145-8.
Saleh F, Abdeen S (2007). Pathobiological features of breast
tumours in the State of Kuwait: a comprehensive analysis. J
Carcinog, 6, 12.
Saleh F, Reno W, Ibrahim G, et al (2008). The first pilot study
on characteristics and practice patterns of Kuwaiti breast
cancer patients. J Environ Pathol Toxicol Oncol, 27, 61-75.
Sawair FA, Al-Mutwakel A, Al-Eryani K, et al (2007). High
relative frequency of oral squamous cell carcinoma in Yemen:
qat and tobacco chewing as its aetiological background. Int
J Environ Health Res, 17, 185-95.
Scheifele C, Nassar A, Reichart PA (2007). Prevalence of oral
cancer and potentially malignant lesions among shammah
users in Yemen. Oral Oncol, 43, 42-50.
Shaham D, Breuer R, Copel L, et al (2006). Computed
tomography screening for lung cancer: applicability of an
international protocol in a single-institution environment.
Clin Lung Cancer, 7, 262-7.

16 Asian Pacific Journal of Cancer Prevention, Vol 10, 2009

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