Review Article

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

Table 3

Characteristics of included studies of lymphoma 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 (%)

Abbas et al. [40]Am J Gastroenterol2012CohortNational registryUnited StatesCountrywide11.0 352,429 32,039 UC60.07.0

Beaugerie et al. [41]Lancet2009CohortNational registryEurope (Western)Countrywide3.0 22,706  
10,899
11,807
10,810  
5,153
5,657
IBD 
CD
UC
53.0

Bernstein et al. [24]Cancer2001Case-controlAdministrative claimsCanadaRegionwide14.0 41,005  
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

Chiorean et al. [42]Dig Dis Sci2011Case-controlReferral centerUnited States18.4 30,121  
19,127
10,994
3,585  
2,277
1,308
IBD 
CD
UC

Farrell et al. [26]Gut2000CohortReferral centerEurope (Western)19.0 6,256 782 IBD44.152.010.0

Fraser et al. [18]Aliment Pharmacol Ther2002CohortReferral centerEurope (Western)Countrywide35.0 55,388  
20,494
34,894
1,578  
584
994
IBD 
CD
UC
35.053.0

Herrinton et al. [43]Am J Gastroenterol2011CohortAdministrative claimsUnited StatesRegionwide13.0 67,867 16,023 IBD53.0

Jess et al. [8]Am J Gastroenterol2013CohortRegional registryEurope (Western)132.0 33,843  
11,261
22,582
2,211  
774
1,437
IBD 
CD
UC
53.0 
57.0
49.0

Jess et al. [39]Aliment Pharmacol Ther2004CohortRegional registryEurope (Western)Regionwide35.06,569374CD58.0

Jussila et al. [10]Scand J Gastroenterol2013CohortNational registryEurope (Western)Countrywide23.0232,536 
51,876
180,660
20,970  
4,983
15,987
IBD 
CD
UC

Khan et al. [44]Gastroenterology2013CohortNational registryUnited StatesCountrywide10.0 199,046 36,891 UC60.07.0

Lakatos et al. [45]J Crohn’s Colitis 2012CohortProvincial registryEurope (Eastern)731.0 19,293  
7,093
12,830
1,420  
506
914
IBD 
CD
UC
32.5 
28.5
36.5
48.8 
50.0
47.6
22.8 
41.3
4.2

Lewis et al. [46]Gastroenterology2001CohortNational registryEurope (Western)Countrywide9.0 64,239  
24,221
40,018
16,996  
6,605
10,391
IBD 
CD
UC
47.3 
44.3
50.3
54.0 
58.0
50.0

Loftus Jr. et al. [47]Am J Gastroenterol2000CohortRegional registryUnited States253.0 6,662  
3,150
3,512
454  
216
238
IBD 
CD
UC
24.014.9

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

Mizushima et al. [21]Digestion2010CohortReferral centerAsia120.0 4,248 294 CD39.030.6

Palli et al. [22]Gastroenterology2000CohortRegional registryEurope (Western)119.0 10,592  
2,716
7,877
920  
231
689
IBD 
CD
UC

Pasternak et al. [34]Am J Epidemiology2013CohortNational registryEurope (Western)Countrywide11.0 304,992 38,772 IBD47.055.04.0

Van Domselaar et al. [48]J Gastroenterol Hepatol2010CohortReferral centerEurope (Western)1 8,563 911 IBD53.028.64.8

Winther et al. [19]Clin Gastroenterol Hepatol2004CohortRegional registryEurope (Western)Regionwide35.0 22,290 1,160 UC53.4

Yano et al. [14]J Gastroenterol Hepatol2013CohortReferral centerAsia125.0 10,552 770 CD25.131.313.1

(b)

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

Abbas et al. [40]Am J Gastroenterol20120.00.028280.04.870.789.3Moderate

Beaugerie et al. [41]Lancet200929.6 
13.0
16.0
0.0 
0.0
0.0
0.0 
0.0
0.0
6 
3
3
26.4 
27.5
25.4
10.8 
15.9
14.7
5.3 
−3.6
−3.3
47.5 
58.6
54.1
Moderate

Bernstein et al. [24]Cancer20010.0 
0.0
0.0
0.0 
0.0
0.0
16 
9
7
39.0 
42.2
35.6
9.8 
14.1
13.5
19.9 
14.6
9.2
58.1 
69.8
62.0
Moderate

Chiorean et al. [42]Dig Dis Sci20118 
5
3
26.6 
26.1
27.3
9.4 
11.7
15.8
8.2 
3.2
−3.6
45.0 
49.0
58.2
Moderate

Farrell et al. [26]Gut200026.030.0464.032.01.3126.7Moderate

Fraser et al. [18]Aliment Pharmacol Ther200230.00.0 
0.0
0.0
0.0 
0.0
0.0
5 
1
4
9.0 
4.87
11.5
4.0 
4.9
5.8
1.1 
−4.7
0.2
16.9 
14.4
22.8
Moderate

Herrinton et al. [43]Am J Gastroenterol20110.00.03348.68.532.065.2Moderate

Jess et al. [8]Am J Gastroenterol201326.7 
41.0
19.0
27.2 
45.0
18.0
15 
7
8
44.3 
62.2
35.4
11.4 
23.5
12.5
21.9 
16.1
10.9
66.7 
108.3
59.9
Moderate

Jess et al. [39]Aliment Pharmacol Ther200400.00.03.7Moderate

Jussila et al. [10]Scand J Gastroenterol201372 
14
58
31.0 
27.0
32.1
3.7 
7.2
4.2
23.8 
12.9
23.8
38.2 
41.1
40.4
Moderate

Khan et al. [44]Gastroenterology20130.00.011960.05.549.270.8Moderate

Lakatos et al. [45]J Crohn’s Colitis20122.3 
1.8
2.7
30.2 
35.9
24.4
0.0 
0.0
0.0
0.0 
0.0
0.0
3 
1
2
15.5 
14.1
15.6
8.9 
14.1
11.0
−2.0 
−13.5
−6.0
33.0 
41.7
37.2
Moderate

Lewis et al. [46]Gastroenterology20019.5 
13.0
6.0
18 
7
11
28.0 
28.9
27.5
6.6 
10.9
8.3
15.1 
7.5
11.2
40.9 
50.3
43.8
Moderate

Loftus Jr. et al. [47]Am J Gastroenterol20001 
1
0
15.0 
32.0
0.0
15.0 
32.0
−14.4 
−30.7
0.0
44.4 
94.7
3.7
Moderate

Mellemkjær et al. [33]Cancer Causes Control2000417.58.80.434.7Moderate

Mizushima et al. [21]Digestion201012.400.00.03.7Moderate

Palli et al. [22]Gastroenterology20007 
1
6
66.0 
36.8
76.2
24.9 
36.8
31.1
17.1 
−35.3
15.2
114.9 
108.9
137.2
Moderate

Pasternak et al. [34]Am J Epidemiology20130.00.04615.12.210.719.5Moderate

Van Domselaar et al. [48]J Gastroenterol Hepatol2010781.730.921.2142.2Moderate

Winther et al. [19]Clin Gastroenterol Hepatol200454.0217.912.7−6.942.8Moderate

Yano et al. [14]J Gastroenterol Hepatol201314.700.00.03.7Moderate

Did not report separate incidence estimates for CD and UC.