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Oesophageal cancer in Golestan Province, a high-incidence area in northern Iran - A review Article in European journal of cancer (Oxford, England: 1990) · October 2009 DOI: 10.1016/j.ejca.2009.09.018 · Source: PubMed
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Review
Oesophageal cancer in Golestan Province, a high-incidence area in northern Iran – A review Farhad Islami a,b,c, Farin Kamangar a,d,e, Dariush Nasrollahzadeh Paolo Boffetta b, Reza Malekzadeh a,*
a,f
, Henrik Møller c,
a
Digestive Disease Research Center, Shariati Hospital, Tehran University of Medical Sciences, Kargar Shomali Avenue, 14117 Tehran, Iran International Agency for Research on Cancer, 69008 Lyon, France c King’s College London, Thames Cancer Registry, London SE1 3QD, UK d Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD 20892-7232, USA e Department of Public Health Analysis, School of Community Health and Policy, Morgan State University, Baltimore, MD 21251, USA f Department of Medical Epidemiology and Biostatistics, Karolinska Institute, SE-171 77 Stockholm, Sweden b
A R T I C L E I N F O
A B S T R A C T
Article history:
Golestan Province, located in the south-east littoral of the Caspian Sea in northern Iran, has
Received 26 July 2009
one of the highest rates of oesophageal cancer (OC) in the world. We review the epidemi-
Received in revised form 11
ologic studies that have investigated the epidemiologic patterns and causes of OC in this
September 2009
area and provide some suggestions for further studies.
Accepted 15 September 2009 Available online xxxx
Oesophageal squamous cell carcinoma (OSCC) constitutes over 90% of all OC cases in Golestan. In retrospective studies, cigarettes and hookah smoking, nass use (a chewing tobacco product), opium consumption, hot tea drinking, poor oral health, low intake of
Keywords:
fresh fruit and vegetables, and low socioeconomic status have been associated with higher
Oesophageal neoplasms
risk of OSCC in Golestan. However, the association of tobacco with OSCC in this area is not
Carcinoma, squamous cell
as strong as that seen in Western countries. Alcohol is consumed by a very small percent-
Adenocarcinoma
age of the population and is not a risk factor for OSCC in this area.
Epidemiology
Other factors, such as polycyclic aromatic hydrocarbons, N-nitroso compounds, drinking
Risk factors
water contaminants, infections, food contamination with mycotoxins, and genetic factors
Review
merit further investigation as risk factors for OSCC in Golestan. An ongoing cohort study in
Iran
this area is an important resource for studying some of these factors and also for confirming the previously found associations. Ó 2009 Elsevier Ltd. All rights reserved.
1.
Introduction
Oesophageal cancer (OC) is the eighth most common cancer and the sixth most common cause of death from cancer worldwide.1 International variation in the incidence of OC is striking, with over 20-fold differences between high-risk and
low-risk areas of the world (Table 1). Golestan Province, located in the south-east littoral of the Caspian Sea in northern Iran (Fig. 1), has some of the highest rates of OC in the world.2 A series of etiological and mechanistic studies of OC in Golestan Province began in the 1970s, but these studies were discontinued after the sociopolitical changes in Iran in
* Corresponding author: Tel.: +98 21 82415300; fax: +98 21 82415400. E-mail address:
[email protected] (R. Malekzadeh). 0959-8049/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.ejca.2009.09.018
Please cite this article in press as: Islami F et al., Oesophageal cancer in Golestan Province, a high-incidence area in northern Iran – A review, Eur J Cancer (2009), doi:10.1016/j.ejca.2009.09.018
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Table 1 – Age adjusted incidence rates (per 105 World Standard Population/year) of oesophageal cancer in selected areas of the world. Area 2
Iran, Caspian littoral other than Golestan-1970s Iran, Golestan (western parts of province)-1970s2 Iran, Golestan (eastern parts of province)-1970s2 Iran, Golestan (western parts of province)-1990sa77 Iran, Golestan (whole province)-1990sb5 Iran (north-west), Ardabil Province78 Iran (central), Semnan Province80 China, Linxian81 China, Beijing1 Osaka, Japan1 Sweden1 UK, England1 Uruguay, Montevideo1
Male
Female
% SCC
13 to 28 54 to 84 81 to 166 144 43 15 12 109c 10 10 3 8 11
2 to 20 39 to 77 60 to 195 49 36 14 9 109c 4 2 1 4 3
Not reported Not reported 916 Not reported Not reported 8579 Not reported 10082 90 90 69 41 84
a A screening study between 1995 and 1997, using exfoliative balloon cytology on 4192 asymptomatic adults in western parts of Golestan Province. b A retrospective cancer surveillance. c The ASR was adjusted for gender and was not reported for males and females separately.
Fig. 1 – Geographic location of Golestan Province in the Caspian littoral of Iran.
1979. A new series of studies, collectively known as the GastroEsophageal Malignancies in Northern Iran (GEMINI), including Golestan Case–Control Study, Golestan Cohort Study, and a series of ancillary studies started from 2001. In this review, we summarise the available data on the epidemiologic features and etiology of OC in Golestan, with particular focus on the recently published results that were not included in earlier reviews. We also compare the results to those found in other areas of the world, especially Linxian, China, where incidence rates of >100/105 have been reported. Our aim is to review the current status of knowledge and to provide suggestions for further research.
2.
Epidemiologic features
The incidence rates of OC are highly variable across geographic areas. Whereas rates are relatively low in many
parts of the world, exceptionally high-incidence rates have been reported from some parts of China. Moderate to high incidence rates have been reported from other areas or populations, including parts of Central Asia, South Africa, South America, northern France, and among African-Americans in the United States.3,4 A cancer registry, conducted between 1969 and 1971, reported age-adjusted rates over 100 per 105/year for OC in eastern parts of Golestan Province (Table 1), comparable to rates found in high-risk areas of China. Moving approximately 500 km to the west, the rates in Gilan Province, in the western part of the Caspian littoral, fell to 10 per 105/year, which resembled those seen in low-incidence areas of the world. A marked change in the male to female ratio of age-adjusted incidence rates was also observed; the male to female ratio was approximately 3:1 in Gilan Province but approximately 1:1 in Golestan.2 This pattern resembled what had been observed in
Please cite this article in press as: Islami F et al., Oesophageal cancer in Golestan Province, a high-incidence area in northern Iran – A review, Eur J Cancer (2009), doi:10.1016/j.ejca.2009.09.018
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other parts of the world: in low-incidence areas men are more likely to be diagnosed with OC but in high-incidence areas of China and Africa the sex ratio is close to unity.1 Turkmen are the main ethnic group residing in the highrisk areas of the Caspian littoral. In contrast, there are very few Turkmen in the low-risk areas of the Caspian littoral.3 However, within the high-risk areas, it is unclear whether Turkmen have a higher risk than other ethnic groups. More recent studies (Table 2) have shown that although the incidence rates have approximately halved compared to the 1970s, they are still high. A retrospective cancer surveillance between 1996 and 2000 in Golestan demonstrated that OC was the most common cancer (excluding skin cancers) among both sexes; the reported ASR (per 105/year) in the whole province was 43 for males and 36 for females.5 It should be noted that misclassification of other types of upper gastrointestinal cancers, including gastric cardia cancers, as OC might have contributed to the very high incidence measured in the early 1970s, since many cases were diagnosed only on clinical or radiological examination,2 whereas in recent surveys most cases were diagnosed on the basis of histologic examination of endoscopy-based biopsies.5,6 Squamous cell carcinoma is the predominant histologic type of OC in the world.4 Nevertheless, a shift in proportion of OC from squamous cell carcinoma to adenocarcinoma has been reported in Western countries, notably from the 1970s in the United States and from the 1980s and early 1990s in some European countries.7–9 The reason for this shift is not clear, but it may be related to several factors, including transitions in lifestyle and diet, overweight, and declining rates of helicobacter pylori infection in the Western world.8,10 In Europe, while incidence of oesophageal squamous cell carcinoma (OSCC) has remained stable or declined during the past few decades, the incidence of oesophageal adenocarcinoma has been rising.8,9 This increase has been more prominent in Northern Europe, notably in the United Kingdom and Ireland, but smaller increases have also been reported from other parts of the continent.8,9 In Northern Europe and among
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Southern European women, oesophageal adenocarcinoma has outnumbered OSCC. The only exception to the recent trend was observed among women in Western European countries, including France, the Netherlands, and Switzerland, among whom the ratio of OSCC to oesophageal adenocarcinoma seems to have increased in recent decades.9 In other parts of the world, particularly in high-incidence areas, OSCC is much more common than oesophageal adenocarcinoma (Table 1).4 In Golestan, OSCC and oesophageal adenocarcinoma constitute 91% and 9% of oesophageal malignancies, respectively; other oesophageal tumours are rare.6 Earlier OC studies in Golestan provided little information on histological subtypes. Therefore, it is not clear whether the ratio of OSCC to oesophageal adenocarcinoma in Golestan has changed during the past few decades, when the incidence of OC declined considerably there. Since the majority of oesophageal malignancies in Golestan are of squamous cell type, the results reported in this review mainly apply to OSCC.
3.
Environmental risk factors
Tobacco use: Risk of OSCC is increased 3- to 7-fold among current smokers in many parts of the world,4,11 and the International Agency for Research on Cancer (IARC) has classified tobacco smoking as a known cause of OSCC.12 Smokeless tobacco use has also shown an association with risk of OSCC in Swedish studies.13 In the pilot phase of the Golestan Cohort Study, which was conducted on 1057 randomly selected inhabitants in both rural and urban areas, 30% of rural men, 39% of urban men, 1% of rural women, and 3% of urban women had ever smoked cigarettes.14 The corresponding percentages for ever use of nass (a chewing tobacco product containing a mixture of tobacco, lime, and ash) were 19%, 2%, 1%, and 0%, respectively. In Golestan, although all forms of tobacco use (cigarettes, hookah, and nass) have been associated with higher risk of OSCC,15 the strength of association (relative risk of 1.7) is less than what is seen in low-incidence
Table 2 – Prevalence of polymorphic alleles in three Iranian populations and Japanese or other Asian populations with low oesophageal cancer incidence. Polymorphism CYP1A1 (T3801C) (m1) CYP1A1 (A1506G) (m2) CYP1A1 (T3205C) (m3) CYP2A6*9 (T–48G) CYP2E1 c2 (G–1293C)(RasI) GSTM1*0/*0 (Homo deletion) GSTT1*0/*0 (Homo deletion) GSTP1 (A313G) ADH2*2 ADH3*2 (A350G) ALDH2*2 O6-MGMT (C290T) (Codon 84)
Turkmen % 29 11 0 14 4 41 22 23 51 20 1 24
Turks % 19 2 0 5 6 57 20 26 46 22 2 16
Zoroastrians % 9 1 0 4 6 66 19 20 68 13 5 11
P value
