Increasing incidence of Barrett’s oesophagus: a population-based study

GASTRO-INTESTINAL EPIDEMIOLOGY

Increasing incidence of Barrett’s oesophagus:a population-based study

Helen G. Coleman • Shivaram Bhat •

Liam J. Murray • Damian McManus •

Anna T. Gavin • Brian T. Johnston

Received: 7 April 2011 / Accepted: 1 June 2011 / Published online: 14 June 2011

� Springer Science+Business Media B.V. 2011

Abstract Oesophageal adenocarcinoma, a highly fatal

cancer, has risen in incidence in Western societies, but it is

unclear whether this is due to increasing incidence of its pre-

cursor condition, Barrett’s oesophagus (BO) or whether the

proportion of BO patients undergoing malignant progression

has increased in the face of unchanged BO incidence. Data

from population-based studies of BO incidence is limited,

with equivocal results to date difficult to distinguish from

changes in endoscopic practices. The aim of this study was to

assess population trends in Barrett’s oesophagus (BO) diag-

noses in relation to endoscopy and biopsy rates over a 13 year

period. The Northern Ireland Barrett’s oesophagus Register

(NIBR) is a population-based register of all 9,329 adults

diagnosed with columnar epithelium of the oesophagus in

Northern Ireland between 1993 and 2005, of whom 58.3%

were male. European age-standardised annual BO incidence

rates were calculated per 100,000 of the population, per 100

endoscopies and per 100 endoscopies including an oesopha-

geal biopsy. Average annual BO incidence rates rose by 159%

during the study period, increasing from 23.9/100,000 during

1993–1997 to 62.0/100,000 during 2002–2005. This elevation

far exceeded corresponding increases in rates of endoscopies

and oesophageal biopsies being conducted. BO incidence

increased most markedly in individuals aged\60 years, and

most notably amongst males aged \40 years. This study

points towards a true increase in the incidence of BO which

would appear to be most marked in young males. These

findings have significant implications for future rates of

oesophageal adenocarcinoma and surveillance programmes.

Keywords Barrett’s oesophagus � Epidemiology �Population-based � Trends

Abbreviations

BO Barrett’s oesophagus

NIBR Northern Ireland Barrett’s oesophagus Register

UK United Kingdom

US United States

Introduction

Oesophageal adenocarcinoma is relatively rare in the UK

[1], but is recognised as a growing public health problem.

H. G. Coleman (&)

Cancer Epidemiology & Health Services Research Group,

Centre for Public Health, Queen’s University Belfast,

Room 02:031 ICS-B Building, RVH Site, Grosvenor Road,

Belfast BT12 6BA, Northern Ireland, UK

e-mail: [email protected]

S. Bhat



Room 1:49 Mulhouse Building, RVH Site, Grosvenor Road,

Belfast BT12 6BJ, Northern Ireland, UK

L. J. Murray



ICS-B Building, RVH Site, Grosvenor Road,

Belfast BT12 6BA, Northern Ireland, UK

D. McManus

Belfast Health & Social Care Trust, BCH Site, Belfast BT9 7AB,

Northern Ireland, UK

A. T. Gavin

Northern Ireland Cancer Registry, Mulhouse Building, RVH

Site, Grosvenor Road, Belfast BT12 6BJ, Northern Ireland, UK

B. T. Johnston

Belfast Health & Social Care Trust, RVH Site, Grosvenor Road,

Belfast BT12 6BJ, Northern Ireland, UK

123

Eur J Epidemiol (2011) 26:739–745

DOI 10.1007/s10654-011-9596-z

Oesophageal adenocarcinoma incidence approximately

quadrupled in England and Wales between 1971 and 1998

[2] and rates have continued to rise in the past decade [3].

Similar striking increases in oesophageal adenocarcinoma

incidence have been observed across many Western soci-

eties [1, 4–7]. Such increases in incidence cannot be

entirely attributed to detection bias from improved diag-

nostic procedures [8], misclassification bias from reclassi-

fication of adjacent gastric cancers [8, 9], nor over-

diagnosis since mortality rates from this cancer have also

increased [9].

It is possible that a rise in Barrett’s oesophagus (BO)

incidence, the pre-cursor for oesophageal adenocarcinoma,

could be accounting for the observed escalating oesopha-

geal adenocarcinoma rates. There is considerable debate

over whether there is a true rise in BO incidence in the UK

population, or if such an occurrence simply reflects chan-

ges in endoscopy practices and improvements in recogni-

tion of the disease [10]. One of the major difficulties in

accurately assessing BO incidence is a lack of robust

population-based data. Many of the studies published to

date that have identified increases in clinical BO diagnoses

exceeding those of concurrent increased rates of endoscopy

and biopsy included only relatively small numbers of BO

patients [10–13]. Nevertheless, a recent national study of

BO incidence originating from The Netherlands does

suggest an increased incidence of BO over an eleven year

period, particularly in younger males who are at a height-

ened risk of developing oesophageal adenocarcinoma [14].

By contrast two US studies have suggested that the

increase they found was largely accounted for by data

recording issues [15, 16]. The study conducted in The

Netherlands did not have available data on the numbers of

endoscopies performed [14]. Therefore, controversy

remains as to whether true changes in population BO trends

have occurred.

The aim of this investigation was to assess trends in BO

incidence in relation to endoscopy and biopsy rates over a

thirteen year period using data from the population-based

Northern Ireland Barrett’s oesophagus register.

Materials and methods

Data collection

The Northern Ireland Barrett’s oesophagus register (NIBR)

includes all patients diagnosed with BO (defined as

columnar-lined oesophagus) in Northern Ireland from

January 1993 until December 2005. The NIBR was con-

structed by performing a standardised review of pathology

reports from all oesophageal biopsies conducted in

Northern Ireland between 1993 and 2005 (corresponding to

SNOMED2 codes T62* and SNOMED3 codes T56*). Any

reports diagnosing histologically confirmed columnar epi-

thelium of the oesophagus, or synonymous terms, were

deemed to be BO and were eligible for inclusion. Reports

relating to the oesophagogastric junction or carcinoma of

either the oesophagus or oesophagogastric junction were

excluded, as were patients aged \16 years of age. Trained

staff extracted information on age, sex, date of BO diag-

nosis and, where possible, Barrett’s segment length from

the pathology reports. Data on Barrett’s segment length

were supplemented by a case note review of medical notes

conducted by three trained Tumour Verification Officers

from the Northern Ireland Cancer Registry. This case note

review was conducted for approximately one-third of

NIBR patients who were reported as having specialised

intestinal metaplasia. Finally, duplicate biopsies and

patients were removed so that only the index BO diagnosis

biopsy was retained in the NIBR.

Data on all upper gastrointestinal endoscopies and

oesophageal biopsies conducted in Northern Ireland within

the same time period were obtained from all public

healthcare providers. The largest private healthcare pro-

vider contributed endoscopy records from 1998 to 2005,

which amounted to only 2% of all endoscopies performed.

All electronic data from endoscopy to biopsy reports were

received to the Northern Ireland Cancer Registry. Infor-

mation on other conditions diagnosed at endoscopy,

including oesophagitis, gastritis, duodenitis and hiatus

hernia, were also recorded. Repeat endoscopies and

endoscopies including a biopsy that were performed after a

diagnosis of BO were removed from the endoscopy and

biopsy datasets. After rigorous electronic and manual res-

olution, 594 patients in the NIBR could not be matched to

any endoscopy records, probably due to name changes or

data entry differences, and these patients were added to the

endoscopy dataset for completion since they had to have

undergone an endoscopy to receive a BO diagnosis.

Ethical approval for the Northern Ireland Barrett’s reg-

ister and related research has been granted by the regional

ethics committee of Northern Ireland.

Statistical analysis

Annual European age-standardised incidence rates of BO

were calculated per 100,000 of the Northern Ireland pop-

ulation using mid-year population estimates (Northern

Ireland Statistics and Research Agency). European age-

standardisation was conducted using standard methods as

outlined by the International Agency for Research on

Cancer [17]. For comparison purposes, incidence rates of

oesophagitis, gastritis, duodenitis and hiatus hernia per

100,000 of the population were also calculated. To deter-

mine BO incidence in relation to endoscopy rates, firstly

740 H. G. Coleman et al.

123

the annual number of endoscopies (excluding repeat

endoscopies after a BO diagnosis) in Northern Ireland were

calculated per 100,000 of the population and age-stand-

ardised according to European rates. Annual BO incidence

was then divided by endoscopy rates and multiplied by 100

to give BO incidence per 100 endoscopies performed. BO

incidence per 100 endoscopies that included oesophageal

biopsies (hereafter referred to as BO incidence per 100

biopsies) was calculated in a similar way. Incidence rates

are also presented in three time bands to maximise com-

parability with other published population-based estimates

of BO incidence [14]. Stratified analyses were conducted

according to gender, age groupings, deprivation quintiles

and BO segment length although results are not presented

for the latter as segment length was unknown for two-thirds

of patients. Comparisons between characteristics in BO

patients were performed using independent t-tests or chi-

squared tests, as appropriate. Poisson regression was

applied to assess trends in BO incidence over time. All data

cleaning and statistical analyses were conducted using

Microsoft Office Excel 2007 and Intercooled Stata version

11.0 (College Station, Texas, USA).

Results

Over the 13 year time period in Northern Ireland, 261,725

endoscopies of the upper gastrointestinal tract were con-

ducted and 24,876 of these included oesophageal biopsies

(excluding repeat endoscopies and biopsies performed after

a BO diagnosis). This corresponded to 197,635 unique

patients who underwent an endoscopy, and resulted in

9,329 individuals aged C16 years being diagnosed with

BO.

Males accounted for 58.3% of BO patients, and were

significantly younger than females at the time of BO

diagnosis (Table 1). Overall mean age of BO diagnosis

declined from 61.9 years in 1993–1997 to 60.4 years in

2002–2005. As shown in Table 1, BO segment length was

unknown for the majority of patients.

As shown in Fig. 1, European age-standardised BO

incidence rates increased steadily from 1993 to 2003, with

a sharp rise observed in 2000 followed by a slight down-

turn in the latter 2 years. These patterns of BO diagnoses

closely paralleled trends in endoscopy and, particularly,

oesophageal biopsy rates. Overall increases in BO inci-

dence were evident for both males and females, although

rates were consistently higher in males, and were universal

across categories of deprivation (data not shown). How-

ever, the simultaneous increase in endoscopy and biopsy

rates do not appear to explain all of the observed increase

in BO diagnoses. As shown in Table 2, average annual

BO incidence rates rose by 159%, increasing from 23.9/

100,000 during 1993–1997 to 62.0/100,000 during 2002–

2005. Over the same time period, there were only 35 and

45% corresponding increases in all endoscopies and in

endoscopies that included oesophageal biopsies, respec-

tively (Table 2). Even with somewhat increasing rates of

endoscopy and biopsy, BO was still diagnosed more fre-

quently per 100 endoscopies and per 100 biopsies in

2002–2005 compared with earlier time periods. The

marked elevation in BO incidence also far exceeds that of

other upper gastrointestinal disorders diagnosed per

100,000 of the population between 1993 and 2005, for

example oesophagitis rose by 33%, hiatus hernia increased

by 62%, and gastritis and duodenitis increased by 70%

(Fig. 2).

When examining endoscopy patterns in Northern Ire-

land, across all three time bands females underwent more

endoscopies than males (Table 2). However, BO incidence

per 100 endoscopies was almost twice as high in males

compared with females. In contrast, males were more

Table 1 Descriptive

characteristics of Barrett’s

oesophagus patients in Northern

Ireland 1993–2005

a Significance testing between

males and females

All Males Females P-valuea

n = 9,329 (%) n = 5,432 (%) n = 3,897 (%)

Age (years, mean ± SD) 60.8 ± 15.5 58.5 ± 15.2 64.0 ± 15.4 \0.001

Age group (years)

16 to \40 938 (10.0) 658 (12.1) 280 (7.2) \0.001

40 to \50 1,405 (15.0) 951 (17.5) 454 (11.6)

50 to \60 1,973 (21.2) 1,233 (22.7) 740 (19.0)

60 to \70 2,070 (22.2) 1,213 (22.3) 857 (22.0)

70 to \80 1,908 (20.5) 946 (17.5) 962 (24.7)

C80 1,035 (11.1) 431 (7.9) 604 (15.5)

Barrett’s segment length

Long (C 3 cm) 2,219 (23.8) 1,333 (24.5) 886 (22.7) 0.13

Short (\ 3 cm) 856 (9.2) 494 (9.1) 362 (9.3)

Unknown 6,254 (67.0) 3,605 (66.4) 2,649 (68.0)

Increasing incidence of Barrett’s oesophagus 741

123

likely to have had oesophageal biopsies conducted than

females. While BO incidence per 100 biopsies remains

consistently higher in males compared with females, the

actual difference between sexes is less striking than that

seen for BO incidence per 100 endoscopies. The overall

1.9 and 1.8 fold increases evident for BO incidence per

100 endoscopies and biopsies, respectively, between

1993–1997 and 2002–2005 mask some disparities between

sexes. Compared with females, males have experienced a

greater increase in BO incidence per 100 endoscopies

(92.2% v. 69.8%) yet a smaller increase in BO incidence

per 100 biopsies (64.4% v. 71.9%).

Figure 3 illustrates the percentage change in BO inci-

dence per 100,000 population by age categories in

2002–2005 compared with 1993–1997. Increases in BO

incidence were observed universally across age categories

and between sexes, but were more marked in\60 year age

categories. A particularly large 236% increase in BO

incidence was noted amongst males aged\40 years, which

was not apparent in females of that age group. However,

there were relatively few male BO patients in this age

group (as shown in Table 1) meaning that this percentage

increase equated to an absolute increase of 19 extra BO

cases diagnosed in 2002–2005 compared with 1993–1997.

Discussion

This study demonstrates that BO incidence rates have risen

in the Northern Ireland population, and although diagnosis

rates reflect changes in endoscopy and oesophageal biopsy

rates, the latter do not fully account for the larger increase

in BO incidence. Furthermore, rising BO incidence rates

were particularly striking amongst younger males.

Between 1993–1997 and 2002–2005 there was a 159%

increase in BO incidence, corresponding to an increase in

the frequency of BO detection per 100,000 of the popula-

tion from 1/51 individuals to 1/21 individuals over the

13 year period. A similar population-based study from the

Netherlands also noted an increase in BO of 41% in males

and 23% in females over a 12 year period [14]. That study

was based on histology and could not comment on whether

Fig. 1 European age-standardised Barrett’s oesophagus incidence in

relation to endoscopy and oesophageal biopsy rates in Northern

Ireland. EASR BO European age-standardised rate of Barrett’s

oesophagus

Table 2 Average annual Barrett’s oesophagus incidence rates in Northern Ireland

Time period BO incidencea/

100,000 population

Endoscopies/100,000

population

BO incidencea/100

endoscopies

Oesophageal biopsies/

100,000 population

BO incidencea/100

oesophageal biopsies

All

1993–1997 23.9 1314.6 1.8 120.0 19.8

1998–2001 46.3 1690.9 2.7 160.6 28.4

2002–2005 62.0 1777.1 3.5 174.7 35.4

% changeb 159.5 35.2 93.3 45.5 78.8

Males

1993–1997 30.3 1278.1 2.4 137.0 22.1

1998–2001 60.3 1634.9 3.7 192.2 30.9

2002–2005 75.9 1676.8 4.5 209.0 36.3

% changeb 150.4 31.2 92.2 52.5 64.2

Females

1993–1997 19.0 1348.3 1.4 104.3 18.2

1998–2001 33.5 1742.6 1.9 131.5 25.0

2002–2005 44.6 1870.5 2.4 142.7 31.2

% changeb 134.7 38.7 69.8 36.8 71.9

a European age-standardised Barrett’s oesophagus (BO) incidence ratesb % change relates to 2002–2005 compared to 1993–1997 time period


123

or not rising endoscopy rates could be the sole explanation

for the rise in BO. A small study of 260 cases of BO, also

from the Netherlands, suggested that the rise was real and

not solely explained by endoscopy rates [13], although

other International data have not supported this [15, 16].

Both of the latter studies were based in the USA, one of

which found that overall BO incidence did not significantly

alter between 1996 and 2002 [15], while another also

observed largely unchanged BO incidence rates from 1998

until 2004 and attributed increases in incidence in 2005 and

2006 to data collection biases, even when accounting for

endoscopy volumes in the study region [16]. Unlike the

current analysis, none of the above studies were able to

explore population-based BO incidence rates in relation to

both endoscopy and oesophageal biopsy rates [13–16].

Our data, based on over 9,000 cases, do indicate an

increase in BO diagnosis significantly greater than the 35%

increase in endoscopy rates over the same period. We were

also able to demonstrate that the increase in incidence of

other diagnoses made at endoscopy, for example

oesophagitis, corresponded to similar changes in endos-

copy rate and were considerably less than the observed rate

of BO incidence increase. This suggests that the BO

increase is not part of a general diagnosis inflation, where

all oesophageal conditions would be expected to be diag-

nosed more frequently and reported to a similar degree.

The slight downturn in BO and endoscopy rates in

2004–2005 is difficult to explain, although updated

guidelines for the diagnosis of BO were published in 2005

by the British Society of Gastroenterology [18] and may

have altered the behaviour of endoscopists and histopa-

thologists, although it is unlikely this would have impacted

on incidence rates so quickly. Until further data is available

for later years we can only currently interpret this downturn

as an anomaly, although it may represent a plateau in

clinical BO diagnoses. A similar plateau has been also been

observed in recent data from Olmsted County, USA, [19]

suggesting that the increase in BO incidence may have

peaked.

One of the key pieces of data from our study is the rate

of BO diagnosis per endoscopic biopsy. Between

1993–1997 and 2002–2005, overall BO incidence

increased from being detected in a fifth of oesophageal

biopsies to a third of biopsies. There are several potential

explanations for this finding. Firstly, there could be a true

increase in BO (which is being biopsied) associated with a

smaller decline in non-BO oesophageal biopsies. Secondly,

endoscopists could be targeting the oesophagus differently

and choosing to biopsy short segments of BO that they

previously would have ignored and are no longer biopsying

normal oesophagus. This is supported by an Australian

study that showed a very large increase in short segment

BO and an actual decrease in long segment BO [12]. Due

to the large number of unknown BO length in our cohort,

this cannot be stated with absolute certainty, however our

limited data showed an increase in both long and short

segment BO cases suggesting that the overall increase is at

least partially reflecting a true rise in BO diagnoses in the

population. Thirdly, it is plausible that endoscopists and

histopathologists may have reduced their threshold for

making a diagnosis of BO or are looking more carefully for

it due to increased awareness of the disease in recent years

[10].

The age and gender specific data are important and may

point towards a true increase of BO being the correct

interpretation. It could be interpreted that this study pro-

vides some evidence that physicians appear to be better

targeting females since the elevation in BO diagnosed per

biopsy was twice that of the increase in biopsy rates.

However, the greatest increase in BO diagnosis was in the

under-60 year age categories for both sexes, which is

consistent with the findings of Post et al. in the Netherlands

[14]. Moreover, BO incidence was consistently higher in

Fig. 2 Bar chart comparing % change in incidence of Barrett’s

oesophagus and other endoscopically diagnosed disorders in Northern

Ireland

0

50

100

150

200

250

16-<40 40-<50 50-<60 60-<70 70-<80

% c

han

ge

fro

m 1

993-

1997

to

200

2-20

05

Age category (years)

AllMales

Females

Fig. 3 Percentage change in age-specific BO incidence in Northern

Ireland


123

males, which could possibly be attributed to patterns of

obesity and central adiposity in the population [20, 21].

Indeed, there is a gender discrepancy in the under-40 year

age group with a large increase in BO diagnosis among

males and less so among females. This would be consistent

with the known older presentation of BO in females that is

demonstrated in both the current study and other smaller

published studies [13, 22]. These age and gender differ-

ences make altered endoscopic behaviour or altered histo-

pathology reporting less likely explanations for the

increase, as neither of these would be expected to apply

differentially across age groups or gender. If our data do

represent a true increase, this has implications for a

potentially increasing pool of individuals at risk of OAC in

the coming decades especially as the largest percentage

increase in BO diagnosis was in the youngest group of

males. Moreover, results from this study also indicate that

mean age of BO diagnosis is declining, which is consistent

with other reports from the UK [23], fuelling concerns over

possible future rises in oesophageal adenocarcinoma inci-

dence in a younger population.

Two important strengths of this study are its size and the

fact that it is a comprehensive, population-based analysis of

a relatively stable community. Through the NIBR we have

been able to capture all diagnoses of BO within a single

geographic location, allowing accurate comments to be

made regarding the emerging pattern of BO incidence.

Another major strength of this study is the accountability of

both endoscopy and oesophageal biopsy rates in our cal-

culations of BO incidence. One issue which needs to be

taken into account when comparing BO incidence in our

study with others is that Northern Ireland has a higher rate

of endoscopy compared with the rest of the UK (12.5 v.

8/1,000 population per year) (R. Hulatt, personal commu-

nication). Therefore, the generalisability of our findings

with BO incidence in other populations may be limited. We

were also unable to match 594 BO patients to their initial

endoscopy records, and so added them into the endoscopy

dataset, which may have artificially inflated the number of

endoscopies performed over this time period slightly,

however these patients only accounted for 6% of all BO

patients, and therefore any potential dilution effect on BO

rates per endoscopy is minimal. In addition, despite the

thorough analysis of endoscopy and biopsy data we are

unable to account for any changes in BO detection due to

increased awareness of the condition amongst practitioners.

We were also unable to obtain information on BO segment

length for a substantial proportion of patients therefore

analysis into increases in short v. long segment BO was

limited.

In conclusion, this large population-based study pro-

vides evidence pointing towards a true increase in the

incidence of BO which would appear to be most marked in

young males. These findings have significant implications

for future rates of oesophageal adenocarcinoma and

increased demand on surveillance programmes. Future

research should be directed towards identifying factors that

may reduce BO incidence in the population and minimise

the proportion of these patients that will undergo malignant

progression.

Acknowledgments We would like to acknowledge the contribution

of the tumour verification officers in the Northern Ireland Cancer

Registry and all staff in the Centre for Public Health who contributed

to the development of the Northern Ireland Barrett’s register. This

work was supported by funding from the Ulster Cancer Foundation

and the Health and Social Care Research and Development Office,

Northern Ireland. The Northern Ireland Cancer Registry is funded by

the Public Health Agency for Northern Ireland. The funding bodies

had no role in the study design and all researchers involved in this

study are independent of the funding bodies. All authors had full

access to all of the data (including statistical reports and tables) in the

study and can take full responsibility for the integrity of the data and

the accuracy of the data analysis.

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Increasing incidence of Barrett’s oesophagus: a population-based study

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