Review Article

Worldwide Incidence of Colorectal Cancer, Leukemia, and Lymphoma in Inflammatory Bowel Disease: An Updated Systematic Review and Meta-Analysis

Table 1

Characteristics of included studies of CRC in IBD.
(a)

AuthorJournalPublication yearStudy designStudy populationRegion of originNumber of sitesStudy duration (yrs)Person-yearsNumber of patientsDiagnosisMean age (yrs)Female (%)Mean disease duration (yrs)Surgery (%)

Askling  et  al.  [25]    Gastroenterology 2001 Cohort National registry Europe (Western) Countrywide 54 169,332 
91,833  
77,499
19,459 
8,810
10,649
IBD
CD
UC
48.6
53.0
45.0

Bernstein  et  al.  [24]Cancer2001Case-controlAdministrative claimsCanadaRegionwide1441,005 
21,340
19,665
5,529 
2,857
2,672
IBD
CD
UC
39.0
36.3
41.7
54.5
59.0
50.0

Farrell  et  al.  [26]Gut2000CohortReferral centerEurope (Western)19 6,256 782 IBD44.152.010.0

Fraser  et  al.  [18]Aliment Pharmacol Ther2002CohortReferral centerEurope (Western)Countywide35 55,388 
20,494
34,894
1,578 
584
994
IBD
CD
UC
35.053.0

Gillen  et  al.  [27]    Gut 1994 Cohort Referral center Europe (Western) Countrywide 30 12,324 
2,320
10,004
611 
125
486
IBD
CD
UC

Herrinton  et  al.  [28]Gastroenterology2012CohortAdministrative claimsUnited StatesCountywide1261,793 
28,469
33,324
14,875 
5,053
9,822
IBD
CD
UC
61.8
62.4
61.1

Hou  et  al. [29]Inflamm Bowel Dis2012CohortNational registryUnited StatesCountrywide11 112,243 20,949 UC61.65.05.0

Jess  et  al. [7]Gastroenterology2012CohortNational registryEurope (Western)Countywide29385,608 
130,391
255,217
47,374 
14,463
32,911
IBD
CD
UC
40.3
35.7
44.9
55.0
57.0
53.0

Jess  et  al. [39]Aliment Pharmacol Ther2004CohortRegional registryEurope (Western)Regionwide356,569374CD58.0

Jussila  et  al. [10]    Scand J Gastroenterol 2013 Cohort National registry Europe (Western) Countrywide 23 232,536 
51,876
180,660
20,970 
4,983
15,987
IBD
CD
UC

Lakatos  et  al. [38]Inflamm Bowel Dis2006CohortProvincial registryEurope (Eastern)711 8,564 723 UC49.047.010.0

Lakatos  et  al. [30]J Crohn’s Colitis2011CohortProvincial registryEurope (Eastern)731 5,758 506 CD31.550.431.0

Lennard-Jones  et  al. [31]Gut1990CohortSurveillanceEurope (Western)121 4,048 401 UC42.6

Lovasz  et  al.  [32]J Gastroenterol Liver Dis2013CohortProvincial registryEurope (Eastern)Regionwide34 7,759 640 CD28.049.811.038.4

Manninen  et  al.  [11]J Crohn’s Colitis2013CohortReferral centerEurope (Western)12122,900 
7,265
15,635
1,804 
551
1,253
IBD
CD
UC
33.0
30.0
34.0
47.0
51.0
45.0
13.5
13.0
13.1
46.0

Mellemkjær  et  al.  [33]Cancer Causes Control2000CohortNational registryEurope (Western)Countrywide16 22,875 2,645 CD50.0

Mizushima  et  al.  [21]Digestion2010CohortReferral centerAsia120 4,248 294 CD39.030.6

Palli  et  al.  [22]Gastroenterology2000CohortRegional registryEurope (Western)11910,592 
2,716
7,877
920 
231
689
IBD
CD
UC

Pasternak  et  al.    [34]Am J Epidemiology2013CohortNational registryEurope (Western)Countrywide11 304,992 38,772 IBD47.055.04.0

Selinger  et  al. [13]Clin Gastroenterol Hepatol2014CohortReferral centerAustralia/New Zealand21513,423 
5,417
8,006
881 
377
504
IBD
CD
UC
31.5
29.0
34.0
53.1
59.1
47.1

van  Schaik    et  al. [35]Gut2012CohortNational registryEurope (Western)Countrywide8 4,864 835 IBD43.057.02.9

Venkataraman  et  al.    [36]Australian J Gastroenterol Hepatol2005CohortReferral centerAsia1254,901532UC36.86.08.8

Wandall  et  al.   [37]Scand J Gastroenterol2000CohortRegional registryEurope (Western)Regionwide258,101801UC41.044.810.115.9

Winther  et  al.    [19]Clin Gastroenterol Hepatol2004CohortRegional registryEurope (Western)Regionwide3522,2901,160UC53.4

Yano  et  al.  [14]J Gastroenterol Hepatol2013CohortReferral centerAsia12510,552770CD25.131.313.1

Did not report separate incidence estimates for CD and UC.
(b)

AuthorJournalPublication yearPSC (%)Pancolitis (%)Immunomodulator use (%)Biologic use (%)Observed number of CRCsIncidence rate (per 100,000 persons)Standard error95% CI lower bound95% CI upper boundBias rating

Askling et al. [25] Gastroenterology 2001 10.3
17.0
4.8
143
40
103
84.4
43.6
132.9
7.1
6.9
13.1
70.6
30.1
107.2
98.2
57.1
158.6
Moderate

Bernstein et al. [24]Cancer20010.0
0.0
0.0
0.0
0.0
0.0
60
24
36
146.3
112.5
183.1
18.9
23.0
30.5
109.3
67.5
123.3
183.3
157.5
242.9
Moderate

Farrell et al. [26]Gut200026.030.0348.027.7−6.3102.3Moderate

Fraser et al. [18]Aliment Pharmacol Ther200230.00.0
0.0
0.0
0.0
0.0
0.0
23
4
19
41.5
19.5
54.5
8.7
9.8
12.5
24.5
0.4
30.0
58.5
38.6
79.0
Moderate

Gillen et al. [27] Gut 1994 37
8
29
300.2
344.9
289.9
49.4
121.9
53.8
203.5
105.9
184.4
396.9
583.9
395.4
Moderate

Herrinton et al. [28]Gastroenterology201282
29
53
132.7
101.9
159.0
14.7
18.9
21.8
104.0
64.8
116.2
161.4
139.0
201.8
Moderate

Hou et al. [29]Inflamm Bowel Dis2012183163.012.0139.4186.6Moderate

Jess et al. [7]Gastroenterology2012338
70
268
87.7
53.7
105.0
4.8
6.4
6.4
78.4
41.1
92.4
97.0
66.3
117.6
Moderate

Jess et al. [39]Aliment Pharmacol Ther2004460.930.41.2120.6Moderate

Jussila et al. [10] Scand J Gastroenterol 2013 189
32
157
81.3
61.7
86.9
5.9
10.9
6.9
69.7
40.3
73.3
92.9
83.1
100.5
Moderate

Lakatos et al. [38]Inflamm Bowel Dis20062.925.813151.842.169.3234.3Moderate

Lakatos et al. [30]J Crohn’s Colitis20111.8586.838.810.7162.9Moderate

Lennard-Jones et al. [31]Gut199022543.5115.9316.4770.6Moderate

Lovasz et al. [32]J Gastroenterol Liver Dis20130.934.547.27.7677.331.615.4139.2Moderate

Manninen et al. [11]J Crohn’s Colitis20132.5
1.1
3.2
43.2
37.7
49.4
21
5
16
91.7
68.8
102.3
20.0
30.8
25.6
52.5
8.5
52.2
130.9
129.1
152.4
Moderate

Mellemkjær et al. [33]Cancer Causes Control20001565.616.932.498.8Moderate

Mizushima et al. [21]Digestion201012.46141.257.628.2254.2Moderate

Palli et al. [22]Gastroenterology200012
2
10
113.0
73.6
127.0
32.6
52.0
40.2
49.1
−28.4
48.3
176.9
175.6
205.7
Moderate

Pasternak et al. [34]Am J Epidemiology20130.00.0380124.66.4112.1137.1Moderate

Selinger et al. [13]Clin Gastroenterol Hepatol201438.4
37.4
39.1
29
5
24
216.0
92.3
299.8
40.1
41.3
61.2
137.4
11.4
179.9
294.6
173.2
419.7
Moderate

van Schaik et al. [35]Gut201229.00.00.09185.061.764.1305.9Moderate

Venkataraman et al. [36]Australian J Gastroenterol Hepatol200544.05102.045.612.6191.4Moderate

Wandall et al. [37]Scand J Gastroenterol200018.0674.130.314.8133.4Moderate

Winther et al. [19]Clin Gastroenterol Hepatol200454.01358.316.226.690.0Moderate

Yano et al. [14]J Gastroenterol Hepatol201314.7985.328.429.6141.0Moderate