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The Geographical Clusters of Gastrointestinal Tract Cancer in , Southern

Mehrdad Askarian, Ali Goli1, Mahbobeh Oroei, Hossein Faramarzi2

Department of Community Medicine, ABSTRACT Anesthesiology and Critical Care Research Center, Shiraz University of Medical Sciences, Background: Gastrointestinal tract cancer (GI.C) is one of the 1 Shiraz, Islamic Republic of Iran, Department common cancers in world-wide. The incidence rate of it is different in of Social Science, College of Human Sciences, Shiraz University, Shiraz, Islamic Republic of Iran, various geographical regions. This study was performed to assess spatial 2Department of Non-Communicable Diseases, clusters of the occurrence of GI.C in Fars Province. Deputy of Health, Shiraz University of Medical Sciences, Shiraz, Islamic Republic of Iran Methods: In this cross-sectional study, the new cases were 4569 cases from 2001 to 2009. The crude incidence rates were standardized based Correspondence to: on world population for both sexes. The spatial analysis was conducted Prof. Mehrdad Askarian, using the geographical information systems. We used the local Indicators Department of Community Medicine, Shiraz University of Medical Sciences, of spatial association measure, in order to identify local spatial clusters. P. O. Box: 71345-1737, Shiraz, Islamic Results: From a total of the new cases, 62.8% cases were male. The most Republic of Iran. E-mail: [email protected] common GI.Cs were stomach and colorectal cancer in men and women respectively. The significant cluster patterns were discovered from 2002 to 2007. The common type of spatial clustering was a high-high cluster, Date of Submission: Mar 13, 2013 that to indicate from North-west to South-east of Fars Province. Date of Acceptance: Dec 19, 2013 Conclusions: Analysis of the geographical distribution of GI.C will provide opportunities for policymakers for applying preventive How to cite this article: Askarian , oli A, Original Article roei , aramar i . The eographical ls ters o measures. Furthermore, it could be helpful for researchers for future astrointestinal Tract ancer in ars roi nce, ot hern epidemiological studies for investigation of etiological agents in regions ran. nt re e : . with significant spatial clustering of high incidence of cancer. Keywords: Gastrointestinal neoplasm, Iran, spatial clustering

INTRODUCTION Cancer has affected increasingly the human population Archiveduring the past decades.of In theSID less developed and economically transitioning countries burden of cancer is increased due to adoption of unhealthy western life-styles such as smoking, physical inactivity and caloriedense food.[1] Cancer is the third most common cause of death in Iran after cardiovascular diseases and car accidents.[2-4] In the Eastern Mediterranean region of World Health Organization, Iran is the second country in cancer mortality rate.[5] Gastrointestinal tract cancer (GI.C) is one of the common cancers in the world-wide.[6] The burden of GI.C is heavy for patients with gastrointestinal disease, because it is the major cause of mortality and hospital admissions. Furthermore, increase in the incidence of

nternational or nal o ree ntie ei cine, ol , o , l , www.SID.ir Askarian, et al.: The mapping gastrointestinal tract cancer most gastrointestinal diseases has major implications University of Medical Sciences, which covers the for health care systems and health communities.[7] population of Fars. The cancer data were reports The incidence rate of GI.C is high in Iran as well from hospitals and diagnostic departments based as the less developed countries.[8] Annually about on histopathological findings from 2001 to 2009. 50,000 new cases of cancer are reported in the GI.C is a term that encompasses a group of cancers country and hence that in almost 38% of the cases, that affect the gastrointestinal tract. Types of GI.Cs the GI.C is partially affected.[6,9] GI.C have been include esophagus, stomach, small intestine, colon observed as one of the most common fatal cancer in and rectum, anus, liver, bile ducts, gall bladder and Iran.[9] It is related to diagnosis at advanced stages pancreas.[18] and inequality in access to effective therapies. So The data sheet included 33,398 patient names, sex, early detection may increase the chance of successful age at the time of diagnosis, place of residence and treatment and decrease the burden of cancer.[9,10] cancer diagnose and was based on the international GI.C incidence is different in the various classification of disease for oncology.[19] The data . The northern part of the were checked and any duplicates cases with the country is well-recognized to be the region with the same information, cases from other provinces, highest incidence of the GI.C.[11] The geographical diagnosis other than GI.C and uncertain addresses distribution of cancer especially GI.C suggests were excluded. The final data were summarized a relationship between its occurrence and the in another sheet and included 4569 new cases and environment such as ecological cultural, genetic and consisted of sex, place of residence and an eight socioeconomic factors.[4,5,10,12] age-group classification. The spatial analysis of cancer rate is effectively The crude incidence rates were calculated in communicated among policymakers and public various age groups and for both genders in each health researchers. The mapping of health statistics county of the province Fars every year. In order to can show occurrence rates in certain areas, control age as a confounding variable, we computed geographic trends and allow comparison of disease age-standardized incidence rates (ASRs) per 100,000 patterns with patterns of risk factors.[13] persons using the direct method of standardization In Iran, most of the existing literature in this to world population.[20] context is on epidemiological studies that have not The calculated ASRs were transferred to the GIS used spatial statistics by a geographical information software (Arc GIS 9.3) and the mapping tools of system (GIS).[2,4,11,14] GIS were used for visualizing ASR for each year. Despite variations in incidence, however, a few In GIS, various types of maps could commonly be studies have documented evaluation of geographical used for health statistics. We applied a graduated variation of GI.C incidence by applying GIS.[9,15] scale referred to in the software (graduated symbol) The purpose of the present paper is to describe in percentage of total ASR of each year. The the incidence of GI.C and geographical differences classification was manually constructed in five in its incidence in the various parts of Fars Province using GIS during the yearsArchive 2001-2009. of SID METHODS This study was carried out in Fars Province, which is located in southern Iran and has an area of about 122,400 km2 and is located at 27°31-31°42′ longitude North and 50°37′-55°38′ latitude East.[16] The total population of Fars is about 4.6 million and male to female ratio is 1.03.[17] The administrative divisions in 2010 included 24 counties. The capital city is Shiraz, one of the metropolises in Iran [Figure 1]. In this cross-sectional study, the major sources of data collection related to cancer were derived from the Cancer Registry Center of Shiraz Figure 1: ap o cont ies o ars

nternational or nal o ree ntie ei cine, ol , www.SID.ir o , l , Askarian, et al.: The mapping gastrointestinal tract cancer classes and then applied to maps in each series. Table 2 and Table 3 show the principle Furthermore, we used exploratory spatial data GI.C sites in each sex. According to ASR, analysis (ESDA) to determine the distribution the most common cancer in men was stomach pattern of cancer for each year. Moran’s index cancer (85.04) and among women it was colorectal was applied as a useful measure of spatial cancer (48.15). For mapping of GI.C, total ASR autocorrelation for detecting spatial clusters. This distribution of regions is plotted in Figure 3. In the index shows the degree of association of a variable most of the counties, ASR for men was observed in relation to its location, to refer similarity between more than women. The distribution pattern of neighboring observations in a pattern. The null cancer was dispersed, but in the last few years in hypothesis is that there is no spatial autocorrelation the period, scattering was less and the proportion or significant clustering among ASR in the counties. of each county was increased. Approximately, it Whereas the alternative hypothesis suggests that was up to 0.5% in 2008 and 2009. High incidences a significant clustering exists. Moran’s index is occurred in the most of the northern counties and tested by computing standard normal deviate some of the southern counties (Larestan, (Z score) and to take values in the range (−1, 1). and ) [Figure 3]. A significant positive autocorrelation coefficient, By using ESDA, clustering patterns were indicates clustering i.e. when nearby regions are discovered from 2002 to 2007 and hence that Moran’s similar in ASR. Clustering pattern for counties can index was significant in these years [Table 4]. be high-high, low-low, high-low or low-high level Geoda Software was utilized to determine in comparison to their neighboring counties. The spatial clusters in certain years. Figure 4 is a LISA first two categories indicate the expected spatial map that shows the four spatial clustering types. The clustering, where regions with similar features tend red counties represent high ASR are surrounded to be closer to each other. High-low or low-high by those which also have high ASR. The high-high level, however are considered as spatial outliers. If cluster is concentrated on Shiraz, Sepidan, Moran’s index is a significant negative value, that Mamasani, Nayriz, Estahban, Fasa, Firuzabad counties are dissimilar and there is no clustering. and . The high-low cluster (Larestan) A Moran’s index of approximately zero shows that indicates that it has a high ASR in contrast with its the distribution pattern is randomly.[21,22] neighboring counties [Figure 4]. In the first 5 years, We used the local indicators of spatial occurrence of cancer in men was dispersed in the association (LISA) measure to identify local spatial counties and then gradually, ASR became less clusters. LISA analysis was generally mapped scattered and proportion of counties in 2007-2009 to indicate counties with high Moran’s index period increased in the smoothed maps [Figure 5]. coefficient, which suggested clusters of similar The spatial dependency of cancer was clustered values among various regions.[21] ASR calculation in 2003-2006 and 2009 at the significance level was performed in Microsoft Excel and spatial and of 0.05 for men [Table 4]. The distribution map temporal analyses were performed using Arc GIS of ASR of women was approximately scattered 9.3™ and Geoda 1.0.1™.Archive of SID RESULTS A total of 4569 new GI.C cases were diagnosed during 2001-2009 in Fars Province, that 2870 (62.81%) cases were male. The mean ages were approximately 69.93 ± 1.3 years and 64.95 ± 1.5 years for men and women, respectively. ASR of GI.C as shown in Figure 2 that the highest ASR was due to 2007. The average ASRs were 19.15 and 11.67/100,000 persons in men and women, respectively. Table 1 shows the population of each county during Fars in 2001-2009 and the values of ASR Figure 2: The age stana ri e rate in ars roi nce, ran, for each year of the study period.

nternational or nal o ree ntie ei cine, ol , o , l , www.SID.ir Askarian, et al.: The mapping gastrointestinal tract cancer

Table 1: A o . in cont ies o ars roi nce, ran, r ing County Mean of Total ASR population (2001‑2009) 2001 2002 2003 2004 2005 2006 2007 2008 2009 Aa e h . . . . . . . . . Arsan an . . . . . . . . . aa nat . . . . . . . . . ara . . . . . . . . . l i . . . . . . . . . staha n . . . . . . . . . arasha n . . . . . . . . . asa . . . . . . . . . ir aa . . . . . . . . . ahrom . . . . . . . . . a ern . . . . . . . . . hon . . . . . . . . . horrami . . . . . . . . . amer . . . . . . . . . arestan . . . . . . . . . amasani . . . . . . . . . ara sht . . . . . . . . . ohr . . . . . . . . . ar i . . . . . . . . . asarga . . . . . . . . . ir an ar in . . . . . . . . . epia n . . . . . . . . . hira . . . . . . . . . arrin asht . . . . . . . . . A Age stana ri e i ncie nce rate . astrointestinal tract cancer

Table 2: Age‑specific incidence rates, crude incidence rate and ASR of GI.C (2001‑2009) in men, Fars Province of Iran Sites No. 0‑20 21‑34 35‑44 45‑54 55‑64 65‑74 75‑84 ≥85 Crude ASR sophags tomach olon an r ectm ie r alll ae r, etc ancreas ther . Total Archive of SID A Age stana ri e i ncie nce rate . astrointestinal tract cancer in the period of study. Most of northern counties DISCUSSION of Fars had a regular and increasing trend, but Whereas epidemiology of cancer incidence using southern counties did not and to move revealed GIS has been well-studied in developed countries, it and increasing pattern of ASR in the final has not received adequate attention in developing years (2007-2009). The geographical distribution countries. was random in most years and showed significant As, there are not enough study about mapping spatial autocorrelations and clustering only in the GI.C in different parts of Iran, especially from 2003, 2004 and 2007 [Figure 6]. southern Provinces, we compared findings based

nternational or nal o ree ntie ei cine, ol , www.SID.ir o , l , Askarian, et al.: The mapping gastrointestinal tract cancer

Figure 3: patial istrit ion o gastrointestinal cancer in the cont ies o ars, r ing

Figure 4: patial cls ters o total o age stana ri e i ncie nce rate in ars roi nce,

Table 3: Age‑specific incidence rates, crude incidence rate and ASR of GI.C (2001‑2009) in women, Fars Province of Iran Sites No.Archive 0‑20 21‑34 35‑44 45‑54 55‑64 of 65‑74 SID 75‑84 ≥85 Crude ASR sophags tomach olon an r ectm ie r alll ae r, etc., ancreas ther . Total A Age stana ri e i ncie nce rate . astrointestinal tract cancer on epidemiologic aspects of GI.C in our study. The and women respectively. In contrast of the findings total ASRs were 240.96 and 149.57 among men of Mehrabani et al., (9.14, 5.9) and Masoompour

nternational or nal o ree ntie ei cine, ol , o , l , www.SID.ir Askarian, et al.: The mapping gastrointestinal tract cancer

Figure 5: patial i strit ion o gastrointestinal cancer in men, r ing

Archive of SID

Figure 6: Spatial distribution of gastrointestinal cancer in women, during 2001‑2009 et al., (20.1 and 12.4), our results showed an et al. have reported ASR 40.4 and 26.1 in men and increased incidence.[4,14] This increasing trend of women respectively in East Azerbaijan. Furthermore GI.C in may be due to improvements in cancer the mean age at the time of first diagnosis was registry, diagnostic facilities, aging of the population lower than our study.[11] The study has conducted and non-correct westernized lifestyle.[23] by Mohebbi et al. in 2001-2005 in Mazandaran The Northern Provinces of Iran are well known and Golestan provinces of Iran found very high of with high GI.C ASR in the world. Hossein Somi ASRs (51.8 for men, 33.4 for women).[9]

nternational or nal o ree ntie ei cine, ol , www.SID.ir o , l , Askarian, et al.: The mapping gastrointestinal tract cancer

Table 4: ni ces o spatial at ocorrelation . r ing low-fiber diet and high body mass index especially in women.[14] Year Sex Moran’s Z score P value Type of ASR The assessment of spatial distribution of GI.C index spatial by ESDA, the obtained Moran index shows that pattern geographical clusters in the men were similar to −0.065 −0.180 . anom . total ASR. But the Moran’s index of ASR in women −0.076 −0.275 . anom . were less clustering patterns in the time of the −0.066 −0.197 . anom . study. It may be loss of regularity incidence and not . . . ls tere . completing correct address of residence. . . . anom . From the four types of spatial clustering, the −0.085 −0.356 . anom . high-high clusters were important and to be observed . . . ls tere . on the Shiraz, Sepidan, Kazerun, Mamasani, . . . ls tere . Estahban, Fasa, Firuzabad, Nayriz and . . . . ls tere . Probably, there are common risk factors that to . . . ls tere . induce high incidence of GI.C in these counties. . . . ls tere . This study showed a presentation of the . . . ls tere . distribution of GI.C on the maps using GIS. GIS . . . ls tere . is utilized as effective technology to determine the . . . ls tere . health maps and significant clusters, that it can help . . . anom . to policymakers and researchers in order to decision . . . ls tere . making for the further studies in geographic areas . . . ls tere . with clusters of high cancer incidence.[25] The . . . anom . researchers should consider not only maps help . . . ls tere . . . . anom . to visually evaluate geographical pattern, also . . . ls tere . the significant clusters were the golden points . . . anom . for epidemiological studies. Therefore the cancer −0.035 . . anom . registry should be accurate, clear and residence . . . anom . address for GIS researchers. . . . anom . . . . ls tere . CONCLUSIONS . . . anom . The GIS analysis is a method that is feasible and A Age stan ar i e inci ence rate . astrointestinal helpful in generating hypothesis and identifying tract cancer oth ale emale. P=. areas for intervention. It could be necessary and important to help researchers to assess risk factors. In our study, the most common of GI.C in men Therefore, knowledge of geographical distribution and women was stomach and colorectal cancer of cancer is expected to provide accurate and easily respectively, as well as other provinces of Iran and accessible information for implementation of Archive[2,11,15] preventive of activities SID in community health. less developed countries, in contrast East Azerbaijan, Mazandaran and Golestan provinces, Further studies are needed on the efficiency of the esophagus cancer was common in women.[11,9] GIS, not only to determine etiological agents of According to the findings of Mehrabani et al. in cancer but also to help policy makers in management Fars, ASR of stomach cancer in men was 3.82 and of health promotion and preventive strategies. colorectal cancer in women was 2.41, whereas we found higher significantly [Tables 2 and 3].[4] The ACKNOWLEDGMENTS stomach cancer may be related to high prevalence This article is the result of a research project (2781). of Helicobacter pylori infection, genetic factors, The Vice-Chancellor for research at Shiraz University change of diet and smoking.[5,24] The colorectal of Medical Sciences funded this project. This research cancer was the most frequencies in women, that was performed by Mahbobeh Oroei in partial fulfillment may be associated with consuming high calories, of the requirements for certification as a specialist in

nternational or nal o ree ntie ei cine, ol , o , l , www.SID.ir Askarian, et al.: The mapping gastrointestinal tract cancer community medicine at Shiraz University of Medical rom orth estern ran. Asian ac ancer re Sciences in Shiraz, Iran. : . The authors thank Deputy of Health at Shiraz 12. Wu KS, Huo X, Zhu GH. Relationships between University of Medical Sciences particularly Mohsen esophageal cancer an spatial eni ronment actors Moghadami and Mahin Farahmand for Collaboration sing eographic n ormation stem. ci Total n iron of the Cancer Registry Center and also Research : . Counseling Center of Shiraz Medical School for editing . ell , oskins , ickle , arten erg . rrent of this article. practices in spatial anal sis o cancer ata: apping health statistics to in orm policm akers an the pl ic. REFERENCES nt ealth eogr : . . asoompor , armohammai , e aian ae h A, . emal A, ra , enter , erla , ar , ankarani . ancer inci ence in so thern ran, orman . loa l cancer statistics. A ancer lin : esl ts o popl ation a se cancer registr . : . ancer pie miol : e . . aa ei , os ai , alek , Tosi , asom eh , . a ai A, ahei , or aie , Alimohammai an , anaei , et al. ancer occr rence in emnan roi nce, hor ani A, ahman ar , et al. The first population‑based ran: es lts o a pop lation ase cancer registr . cancer sr e in erman roi nce o ran. ran l ic Asian ac ancer re : . ealth : . . os ai , oa , ama ani , aa nlo , 16. Wikipedia. Fars Province. Available from: http://www. a sa eghi , e ighi . ancer inci ence an en.wikipedia. Org/wiki/Fars_Province. [Last cited on mortalit i n ran. Ann ncol : . Apr . . ehra ani , Ta ei , e ari T, hamsina , . tatistical enter o ran. electe ini ngs o ational hokrpo r , Amini , et al. ancer occ rrence in opl ation an o sing enss , . Aa ilal e rom: ars roi nce, ot hern ran. ran e rescent e http://www.amar.org.ir/Portals/1/Iran/data.pdf. [Last : . cite on an . . a a i A, o raie , ohagheghi A, . igesti e stem: ancer Agenc . A aila le o sa i arrahi A, aleke a eh , arkin . ancer from: http://www.bccancer.bc.ca/PPI/TypesofCancer/ occr rence in ran in , an international perspectie . DigestiveSystem/default.htm. [Last cited on 2013 Mar 11]. Asian ac ancer re : . . rit A, erc , ack A, hanmga ratnam , oi n , . hai mi , ahmooi , ohamma , eraati , arkin , et al. International Classification of Diseases aso li , heikh athollahi . amil histor or ncolog . r e. enea : . of the cancer on the survival of the patients with . Ahma , oschi into , ope A, rra , gastrointestinal cancer in northern ran, sing railt Lozano R, Inoue M. Age standardization of rates: A new moe ls. astroenterol : . stana r. iscs sion aper eries: o. . . illiams , o erts , Ali , he ng , ohen , WHO; 2000. Available from: http://www.who.int/ emer , et al. astroenterolog seri ces in the . healthinfo/paper31.pdf. [Last cited on 2013 Jan 27]. The r e n o i sease, an the organisation an e lie r . mith , oo chil , ongle A. eospatial o ser ices or gastrointestinal an li er isor ers: Anals is. n e. eicester: ataor . A review of the evidence. Gut 2007;56 Suppl 1:1‑113. . hamis . eas ring the spatial correlation o . olah oo an , a a i A, a mar A , ha emi . i e ne mplom ent in ra . o Appl ci : . common cancers in ran.Archive Arch ran e : . of SID 23. Yoo KY. Mini review: Cancer prevention in the Asia . ohei , ahmooi , ol e , or i ela ni , pacific region. Asian Pac J Cancer Prev 2010;11:836‑44. ohamma , eraati , et al. eographical sprea o . ia oshi , alek a eh , aneshman , Ashktora . gastrointestinal tract cancer inci ence in the aspian ea Helicobacter pylori en emic an gastric isease. ig is region o ran: patial anals is o cancer registr a ta. ci : . ancer : . . le ea , ami A, ilmi , alal . apping cancer . erletti , alassi , pa ea T. The socioeconomic disease using geographical information system (GIS) in eterminants o cancer. n iron ealth e ira tate an. omm nit ealth : . ppl : . . ossein omi , irine ha , arhang , a ae ri , ani A, ei arshai , et al. astrointestinal cancer Source of Support: il, Conflict of Interest: one e clare. occ rrence in ast A ar ai an: A i e ear st

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