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Am J Gastroenterol 2016; 111:228–239; doi:10.1038/ajg.2015.405; appear online 12 January 2016
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Mohammad H Derakhshan MD, FRSPH1, Melina Arnold PhD2, David H Brewster MD, FFPH3, James J Going PhD, FRCPath4, David R Mitchell MBCHB, MRCP1, David Forman PhD, FFPH2 and Kenneth E L McColl MD, FRSE1
Over the accomplished three decades, esophageal adenocarcinoma (EAC) has been one of the fastest accretion malignancies in abounding countries (1, 2). The blight is anticipation to be the aftereffect of gastroesophageal abatement damaging the distal esophagus and causing columnar metaplasia generally with abdominal phenotype. This Barrett’s film has an added accident of advanced to dysplasia and adenocarcinoma.
The ecology factors causing the contempo credible access in accident of EAC are unclear. Central blubber is associated with both abatement and EAC and the accretion prevalence of blubber is acceptable to explain some of the acceleration in accident of EAC (3, 4). Smoker is accession absolute accident agency for esophageal adenocarcinoma (5). However, the prevalence of smoker has decreased over added than six decades in best Western countries and appropriately this cannot anniversary for added contempo increases in accident of esophageal adenocarcinoma (6).
Another accessible annual is that Helicobacter pylori (H. pylori) infection has been attention adjoin acerbic reflux, and appropriately EAC, and this is actuality absent by the falling accident of the infection (7). There is a absolute abrogating affiliation amid H. pylori infection and both gastroesophageal abatement and EAC (8, 9). This abrogating affiliation amid H. pylori and EAC is absolute of the added accident factors of EAC including smoker and BMI (10). A proposed apparatus for the careful aftereffect of H. pylori is that the gastritis induced by it may annual abatement and bargain acerbic secretory accommodation of the belly mucosa. As the acidity of the belly abstract is its capital damaging component, abridgement of this by H. pylori would assure adjoin reflux-induced esophageal accident and associated adenocarcinoma (11).
H. pylori atrophic gastritis is the aloft accident agency for non-cardia belly blight (NCGC) (12). If H. pylori infection does assure adjoin EAC by inducing abatement and bargain acerbic secretion, there should be a abrogating affiliation amid NCGC and EAC at a citizenry akin as the belly mucosal changes predisposing to belly blight would be the aforementioned as those attention from EAC. Opposing accident trends for EAC and NCGC accept been appear in a abstraction of the citizenry of the East of England (13).
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This abstraction advised the accord amid the accepted incidences of the two cancers in altered bounded regions of the world. In addition, we advised the affiliation amid changes in accident of the two cancers over time.
Based on abstracts from Blight Accident in Five Continents Vol. X (CI5X) (14) and GLOBOCAN 2012 (15), age-specific and age-standardized (world population) accident ante (WASR) were estimated for EAC and belly blight by topographical subsite (cardia and non-cardia) in 2012. This adjustment has been declared in added detail by Arnold et al. (16) and Colquhoun et al. (17) In brief, sex- and age-specific (<65; ≥65 years) accommodation of EAC were computed for all countries included in CI5X except for those with no cases of EAC in one of four substrata (male, female; <65, ≥65 years; N=51). Similarly, the accommodation of cardia blight (C16.0) and NCGC (C16.1–6) cases out of all belly cancers with accepted cartography (C16.0–6) were affected for anniversary country included in CI5X and stratified by sex and the aforementioned ample age groups, provided there were two or added cases of cardia belly blight (CGC) and NCGC aural anniversary sex and age accumulation stratification. Area there were assorted abstracts sets (from altered bounded blight registries aural a country), cases and populations were affiliated to access estimated civic proportions. The histological types of esophageal blight and the topographical allocation of belly cancers were authentic according to the third copy of the All-embracing Allocation of Diseases for Oncology (ICD-O-3) presented in Blight Accident in Five Continents Vol. IX (CI5IX) (18, 19). For this analysis, the civic or bounded accommodation of CGC/NCGC and EAC cases bent in the antecedent accomplish were activated to the 2012 belly and EAC accident estimates in GLOBOCAN 2012. Age-standardized accident ante were computed application the apple accepted citizenry (Table 1).
For the longitudinal study, WASR of EAC and absolute belly blight (TGC) were extracted from Blight Accident in Five Continents-Plus (CI5-plus) (1). Cardia and non-cardia subsite abstracts were not acclimated because there were few longitudinal abstracts for the specific subsite and additionally because there accept been connected changes in the subsite affair practices for belly blight in histopathology laboratories. A absolute of 38 populations about the apple were called for this abstraction based on (a) availability of abstracts of esophageal blight recorded by histology, (b) a time aeon of at atomic 19 years catastrophe in 2007, (c) if abstracted abstracts sets were accessible for indigenous groups, at atomic one abstracts set per indigenous accumulation was selected. The accident (WASR) of EAC and TGC at the alpha year (different for anniversary registry), year 1989 (earliest time accepted for all populations) and year 2007 (end year) were appear in Table 2, for men and women separately.
For the cross-sectional study, Spearman’s rho correlations were acclimated to analyze the accord amid WASR of the two cancers. In the longitudinal study, in accession to Spearman’s rho correlations for pairwise alternation of EAC and TGC time trends for alone registries, corruption clay was acclimated to appraisal the amount of accident changes over time as declared by Kim et al. (20). Briefly, application Joinpoint Programme adaptation 4.1.0 (National Blight Institute) we analyzed the time trend abstracts for anniversary cancer, in anniversary registry, in men and women alone (38 × 2 × 2=152 abstracts sets). The programme adapted the simplest Joinpoint archetypal that the abstracts allowed. The models acclimated the log of the WASR for artful the boilerplate anniversary percent change (AAPC) in ante and their agnate 95% aplomb intervals (CIs). Back any comparisons were fabricated amid altered populations, the AAPC was consistently bound to the aforementioned 19-year aeon (1989–2007). Back correlations were fabricated amid the change of blight accident amid the two cancers aural the aforementioned population, we present this in two altered forms, firstly for the abounding breadth of accessible longitudinal abstracts for anniversary citizenry and secondly, attached it to the aforementioned accepted ascertainment aeon (1989–2007).
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As EAC is abundant added accepted in men, we accept focused mainly on after-effects for men aural the capital argument but accept provided commensurable analyses for women in the supplement.
Incidence amount estimates were accessible for 51 countries (Table 1). There was a advanced ambit in the ante of both belly blight and EAC beyond these altered countries. The accident of EAC assorted from 0.23 per 100,000 person-years (py) to 7.24. The accident of TGC assorted from 2.84 to 62.26 and that of NCGC from 1.75 to 58.64. In accepted terms, belly blight accident was accomplished in East Asia and everyman in Western Europe and North America admitting EAC showed the adverse trend. In all 51 countries except the UK, EAC accident ante were lower than the TGC ante and in 43 of 51 countries additionally lower than the NCGC accident rate.
Statistically cogent abrogating correlations amid the accident ante of EAC and both TGC (men (correlation accessory (CC)=−0.38, P=0.006), women (CC=−0.41, P=0.003)) and NCGC accident (men (CC=−0.41, P=0.003) and women (CC=−0.43, P=0.005)) were observed.
The advanced ambit in accident of both EAC and TGC calm with their afflicted alternation resulted in a added than 200-fold ambit in the ratios of TGC to EAC beyond the altered countries (more than 200:1 for the Republic of Korea to below than 1:1 for the United Kingdom).
Despite the able abrogating alternation amid the accident ante of the two cancers, assay of the abstracts credibility adumbrated that in two respects the alternation was not beeline (Figure 1a, b). First, the accident of EAC seemed to be at a agnate low akin for all countries with abstinent or aerial belly blight accident and with a accelerating acceleration in accident at lower belly blight levels. The accident of TGC below which the acceleration in EAC was credible was ~15 per 100,000 py in men (Figure 1) and 7.5 per 100,000 py in women (Supplementary Amount S1a,b online). Second, back the accident of TGC was low, the akin of EAC accident assorted appreciably amid countries with some assuming credible elevation, some abstinent and some no elevation. The agnate abstracts for women showed a agnate arrangement admitting this was below bright due to abundant lower accident ante (see Supplementary Amount S1a,b in supplement).
Correlations amid accident ante (WASR) of EAC and belly blight in cross-sectional abstraction in men. Note: anniversary dot represents a abstracts set from a country. (a) EAC vs. absolute belly cancer, (b) EAC vs. non-cardia belly cancers, (c) beheld absorption of countries disconnected into groups A–D. CC, alternation coefficient.
In adjustment to investigate added the bounded administration of the countries according to their TGC and EAC accident rates, we sub-divided them into four groups (Figure 1c). In men, the aboriginal three groups consisted of countries with low TGC accident (<15 per 100,000 py) and EAC accident aerial (>5)—Group A, average (1.5–5)—Group B, and low (<1.5)—Group C. The fourth accumulation (D) consisted of countries with aerial ante of belly blight (>15) and low EAC (<1.5).
The countries in these altered groupings are credible in Amount 2. Accumulation A with the accomplished amount of EAC and low (<15) TGC was bound to the United Kingdom, the Netherlands, and Ireland. Accumulation B with abstinent EAC and low TGC (<15) comprised Northern America, Australia, New Zealand, Germany, Belgium, Denmark, Finland, Norway, France, Brazil, and Uruguay. Accumulation C with low EAC and low TGC (<15) was a actual amalgamate accumulation from about the apple (Thailand, Phiippines, India, Bulgaria, Croatia, Egypt, Israel, Italy, Spain, Poland, Serbia, Slovakia, and Singapore). Accumulation D with low EAC and abstinent to aerial TGC includes South American countries, Eastern Europe, Korea, China, Japan, Russia, Iran, and Turkey.
Maps of countries blush coded with beheld absorption of populations with altered combinations of EAC and belly blight incidences in cross-sectional abstraction in men. Note: the blush coding is based on groupings A–D as declared beforehand in Amount 1c. Accumulation A (red): TGC<15 and EAC≥5, accumulation B (yellow): TGC<15 and 1.5≤EAC<5, accumulation C (green): TGC<15 and EAC<1.5, and accumulation D (blue): TGC≥15 and EAC<1.5. The blah cipher indicates no abstracts available.
In women, sub-dividing all countries into groups based on their ante of esophageal and belly blight accident approved agnate bounded patterns (Supplementary Amount S2 in supplement).
To analyze the amount of change in accident of EAC and TGC during the aeon of 1989–2007 in males, we affected AAPC for anniversary of the 38 populations individually, and presented these in Amount 3, ordered by bottomward AAPC of EAC. During this time period, best populations (34/38, 89%) had accomplished a cogent abatement in the accident of TGC, with these 34 assuming a ambit of AAPC from −1.4% (95% CI: −2.1, −0.6) in Miyagi, Japan to −5.1% (95% CI: −5.8, −4.3) in Tyrol, Austria. Twenty-five of 38 (66%) populations showed a cogent access in accident of EAC during the aeon of ascertainment and no citizenry showed a cogent abatement in accident (Figure 3). Anniversary increases in EAC accident ranged from 1.5% (95% CI: 0.8, 2.3) in Victoria, Australia to 11.7% (95% CI: 3.7, 20.2) in Estonia.
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We advised any differences amid the 13 populations assuming no cogent acceleration in EAC and the 25 citizenry assuming a rise. The populations which showed no cogent change in EAC showed a amount of abatement in TGC (AAPC ambit −4.9% to 0.7%) agnate to those that showed access in EAC (AAPC range=−5.1% to −1.4%; P=0.504). Likewise, the registries assuming no acceleration in EAC did not alter from those assuming an access in that the two groups had a agnate best contempo (2007) TGC accident (9.5 vs. 9.6/1,000,000 py; P=0.584).
The abstracts for women afresh showed a agnate arrangement and are credible in Supplementary Amount S3. In addition, added analyses application best but capricious periods of ascertainment (19–50 years) were conducted with agnate allegation and are presented in the supplement as Supplementary Amount S4 for men only.
We looked for any alternation amid the accident trends for both cancers for those 38 populations with acceptable longitudinal abstracts and included the abounding ascertainment aeon of commutual abstracts (i.e., not bound to 1989–2007) (Table 3). In men, cogent abrogating correlations amid accident amount trends of EAC and TGC over time were present in 27 of the 38 populations back compared over above-mentioned 19–50 years and evaluated in pairs (Table 3). Absolute correlations were not empiric for any population.
When the adding of correlations amid EAC and TGC accident trends was bound to the accepted but below ascertainment aeon (last 19 years of 1989–2007), the consequence of correlations was weaker in some of the populations. Alone 19 of 38 populations showed cogent abrogating correlations for men and 7 of 38 for women (see Supplementary Table S1 in supplement).
We advised the accord amid the cross-sectional abstracts of best contempo incidences of the two cancers and the longitudinal accident trends. On the cross-sectional besprinkle artifice amount assuming the alternation amid accepted accident of EAC and TGC beyond altered countries we superimposed a band advertence the accident trend over above-mentioned years accessible from the longitudinal data. This accustomed us to appraise the changes in accident of both TGC and EAC blight over time and how it accompanying to their accepted incidences in altered countries. To facilitate beheld assay we did this alone for anniversary of the four categories of countries i.e., groups A, B, C, and D based on accident arrangement of the two cancers (Figure 4). For the longitudinal abstracts we called the three populations from anniversary of the groups A, B, C, and D with the longest ascertainment periods.
Longitudinal abstracts superimposed on cross-sectional blight incidences in men. In anniversary console (a–d), the dots announce the cross-sectional abstracts of the best contempo esophageal and belly adenocarcinoma incidences for the altered countries as credible beforehand in Amount 1. The superimposed blush curve represent longitudinal abstracts for populations from groups A–D (as declared beforehand in Amount 1c) in panels a–d, respectively. In anniversary group, we accept called the longitudinal abstracts for the three populations in that accumulation with the longest accessible abstracts set. The citizenry represented by the longitudinal abstracts band and the date of the alpha and end of the band is credible in the box below anniversary console (color-coded). The time band of the longitudinal abstracts is consistently from appropriate to left.
The constant plots adumbrated that the countries with accepted low accident of TGC and accepted high, medium, or low accident of EAC had ahead resembled countries with a accepted aerial accident of TGC and accepted low accident of EAC. As the accident of TGC has collapsed this has been accompanied by capricious degrees of access in EAC with some populations assuming a credible increase, some abstinent increase, and some no increase.
Our abstraction has approved an afflicted affiliation amid the accident of EAC and belly cancer. This is credible with annual to both the accepted incidences of these two cancers beyond altered countries and with annual to alteration accident of the two cancers aural the aforementioned populations over time. The afflicted affiliation is arresting in actualization of the actuality that the two cancers are biologically actual similar. Both EAC and TGC appear from epithelia of carefully adjacent, absolutely abutting regions of the aerial gastrointestinal tract, both are the aftereffect of abiding accident and deepening exerted by their luminal ambiance and both usually actualization actual agnate and generally duplicate histological appearance.
Our cross-sectional abstraction showed that both cancers were agnate in accepting a advanced ambit in accepted accident ante (20–30-fold in males) beyond the altered countries but altered in accepting allegory bounded patterns. The longitudinal studies showed that the incidences of both TGC and EAC had afflicted clearly over contempo decades but these changes were in adverse admonition and there was a statistically cogent afflicted affiliation amid the alteration accident ante of the two cancers in 71% of the registries.
Combining the cross-sectional and longitudinal abstracts provided an all-embracing annual of what has been accident to these two cancers over time and in altered regions of the world. Previously, best countries had a aerial accident of belly blight and a low accident of EAC. Since then, the accident of belly blight has collapsed in all countries and as it has accomplished low levels it has been accompanied by capricious degrees of access in EAC with some regions assuming credible increase, some abstinent and others no increase.
What is the annual for the opposing incidences and time trends of these two cancers? Could differences amid countries in allocation of junctional cancers into esophageal vs. belly locations and/or changes in allocation of these cancers over time explain some of the observations? In the cross-sectional study, we begin that the afflicted affiliation remained able and absolutely became hardly stronger by excluding cancers occurring at the belly cardia and appropriately added acceptable to be misclassified. The longitudinal abstracts alone provided advice on TGC. Spurious afflicted affiliation amid accident trends of the two cancers due to alteration allocation of cardia junctional cancers would alone be acceptable to be a cogent affair in countries with a actual aerial accident of belly blight and low accident of EAC as misclassification of a baby admeasurement of the aloft could essentially access the closing (21). Such misclassification, however, could not explain the able afflicted accident trends as they were best credible in countries with lower belly blight accident (22).
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The credible changes in accident of TGC and EAC over a abbreviate time calibration announce the access of a alteration ecology factor. In addition, the afflicted affiliation amid the alteration incidences indicates that the ambiance agency is advance adverse furnishings on these two cancers. The ecology factors that are anticipation to explain the falling accident of TGC accommodate a falling accident of H. pylori atrophic gastritis, comestible changes and bargain smoker (23, 24). Could the falling accident of any of these be associated with an access in EAC and appropriately explain the afflicted affiliation in the accident trends of the two cancers? Smoker is not a applicant as it is a agnate accident agency for both cancers (5, 25). Comestible changes adeptness be important. There is some affirmation that added assimilation of vitamins and bargain alkali burning may accept contributed to the falling accident of belly blight (26, 27). These specific comestible factors would not in themselves explain the access in EAC and absolutely added vitamin burning may assure from EAC (28). However, added caloric assimilation and associated blubber is a absolute accident agency for EAC (28). It is accordingly accessible that changes in the diet absolute both a abatement in alkali agreeable and added caloric agreeable could aftermath a abatement in absolute TGC and acceleration in EAC. However, a contempo assay adumbrated that accretion blubber may alone anniversary for 6.5% of the access in accident of EAC and suggesting the role of added ecology factors (3).
Another ecology agency that adeptness apply adverse furnishings on the accident of the two cancers is H. pylori atrophic gastritis which is the best important etiological agency for NCGC (29). In countries with a aerial accident of belly blight there is additionally a aerial accident of atrophic gastritis and associated broken belly acerbic beard (30). In contrast, in capacity afterwards H. pylori, belly acerbic is maintained and shows no abatement with accretion age (31). In countries with a aerial accident of belly blight the aerial prevalence of H. pylori atrophic gastritis will assure from EAC as any gastroesophageal refluxate will accept bargain adeptness to accident the esophagus due to its bargain acidity. Epidemiological studies accept credible constant associations amid H. pylori and both TGC and EAC actuality absolute with annual to the aloft and abrogating with annual to the closing (10). As the prevalence of H. pylori atrophic gastritis falls, it will be accompanied by a abatement in belly blight but potentially additionally a acceleration in EAC due to accretion belly acidity. The prevalence of H. pylori infection has collapsed over contempo decades in affiliation with bigger active altitude (32).
Interactions amid H. pylori and comestible factors adeptness additionally be important. There is some affirmation that a high-vitamin, low-salt diet may assure from the development of atrophic gastritis in H. pylori-infected capacity (33). Bigger active conditions, with accompanying abatement in H. pylori prevalence as able-bodied as added vitamin and bargain alkali assimilation could calm clearly abate atrophic gastritis with resultant abatement in TGC and access in EAC.
In the antecedent abstraction by Anderson et al. (8) assuming a able abrogating affiliation amid H. pylori and esophageal adenocarcinoma, the affiliation persisted alike afterwards acclimation for atrophic gastritis detected by serum pepsinogens. However, it is accustomed that serum pepsinogens are aloof markers of abatement (34). In addition, H. pylori body-predominant gastritis is associated with bargain belly acerbic beard absolute of abatement (35). Furthermore, body-predominant gastritis is an important accident agency for belly blight (36), so alike afterwards cogent abatement it adeptness both advance belly blight and assure from esophageal adenocarcinoma.
Though there were able afflicted associations amid the two cancers with annual to both accepted incidences and time trends, there was a accumulation of countries with a low accident of both cancers. This was a amalgamate accumulation consisting of Thailand, Philippines, Singapore, India, Egypt, Israel, Bulgaria, Croatia, Italy, Spain, Poland, Serbia, and Slovenia. Due to the bound availability of longitudinal abstracts for abounding of these populations, it was difficult to actuate whether their low accident of both cancers was due to the absence of a acceleration in EAC as their accident of TGC fell, or whether they had never had a aerial accident of TGC and were somehow adequate from both cancers. It is accessible that abiogenetic and/or ecology factors present in some of these populations adeptness arrest the progression from deepening to neoplasia which is a accepted final footfall in the pathways arch to both TGC and EAC. A abridgement of access in EAC admitting TGC falling to a low akin adeptness be due to the abiogenetic and/or ecology factors attention from gastroesophageal reflux, which is an capital aboriginal footfall in the alleyway to EAC. Comparative studies of countries with low vs. aerial accident of EAC admitting low accident of TGC may afford new ablaze on the assay and pathogenesis of EAC.
An important catechism is whether countries area belly blight accident is still aerial but falling such as Japan and South East Asia will appointment a acceleration in EAC agnate to that afresh accomplished in Western countries. A abatement in the accident of belly blight to a low akin is not necessarily accompanied by a acceleration in esophageal adenocarcinoma as accent above. However, the accepted accident of belly blight in Japan and South East Asia is still at a akin which back present in Western countries was not yet associated with any acceleration in EAC and it will be absorbing to beam what happens back this point is reached.
Strengths of our abstraction accommodate the use of high-quality all-around surveillance data. Limitations additionally charge about to be recognized. Accident ante acclimated in the cross-sectional assay were based on country-, age-, and sex-specific accommodation of EAC from CI5X, which were again activated to GLOBOCAN 2012 data. Hence, they represent estimates of the accurate accident ante aural anniversary country and should be interpreted with caution. Our admittance belief for the cross-sectional abstraction along resulted in a alternative of 51 mostly advantageous countries, which may not be absolutely adumbrative on the all-around level. Pathological practices and classifications of histological subtypes accept afflicted over time, which should be kept in apperception back interpreting the results, abnormally from the longitudinal analyses. Also, registries accoutrement altered time periods (19–50 years) were included in some of the longitudinal analysis, authoritative them not anon comparable. Finally, best of the countries included in the cross-sectional studies accept added than one aboriginal blight anthology and alike admitting we called the better anthology accessible from anniversary country, it may not represent the abounding civic picture.
In conclusion, this abstraction demonstrates a able afflicted affiliation amid belly blight and EAC with annual to both their accepted incidences and time trends, suggesting a alteration accepted ecology access advance adverse furnishings on these two cancers. Admitting ecological studies do not authorize causality, one biologically believable ecology agency that could explain this abnormal afflicted affiliation is H. pylori atrophic gastritis. However, changes in ache accident are usually the aftereffect of several interacting ecology factors and changes in affairs predisposing to blubber as able-bodied as comestible interactions with H. pylori to abet abatement are additionally acceptable to be important.
Guarantor of the article: Kenneth E.L. McColl, MD, FRSE.
Specific columnist contributions: Mohammad H. Derakhshan: design, analysis, and bookish input; Melina Arnold: analyses and bookish input; David H. Brewster: architecture and bookish input; James J. Going: bookish input; David R. Mitchell: bookish input; David Forman: architecture and bookish input; Kenneth E.L. McColl: abstraction of abstraction and all-embracing supervision.
Financial support: This abstraction was adjourned by an NHS Greater Glasgow Endowment Fund, UK.
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Potential aggressive interests: None.
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