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Endoscopic management of patients with familial adenomatous polyposis after prophylactic colectomy or restorative proctocolectomy – systematic review of the literature

Aleksandar Gavric
Aleksandar Gavric
, 
Liseth Rivero Sanchez
Liseth Rivero Sanchez
, 
Angelo Brunori
Angelo Brunori
, 
Raquel Bravo
Raquel Bravo
, 
Francesc Balaguer
Francesc Balaguer
 und 
Maria Pellisé
Maria Pellisé
   | 11. Juni 2024
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Article Category: Review
Online veröffentlicht: 11. Juni 2024
Seitenbereich: 153 - 169
Eingereicht: 06. März 2024
Akzeptiert: 16. Apr. 2024
DOI: https://doi.org/10.2478/raon-2024-0029
Schlüsselwörter
© 2024 Aleksandar Gavric et al., published by Sciendo
This work is licensed under the Creative Commons Attribution 4.0 International License.

FIGURE 1.

Flowchart of the systematic review according to the Preferred Reporting Items for Systematic Reviews (PRISMA) schema.
Flowchart of the systematic review according to the Preferred Reporting Items for Systematic Reviews (PRISMA) schema.

FIGURE 2.

Surveillance endoscopy in a 48-year old patient with FAP after colectomy with IRA revealed 18 m LST-G (A). After submucosal injection with gelofusine, indigo carmine and adrenaline, piecemeal endoscopic mucosal resection (pEMR) (B) was performed.
Surveillance endoscopy in a 48-year old patient with FAP after colectomy with IRA revealed 18 m LST-G (A). After submucosal injection with gelofusine, indigo carmine and adrenaline, piecemeal endoscopic mucosal resection (pEMR) (B) was performed.

FIGURE 3.

Surveillance endoscopy in a 49-year old patient with FAP after proctocolectomy with IPAA revealed 25 mm LST-G mixed type lesion in the rectal cuff. Lesion was spreading from the anastomosis to the dentate line. Patient had undergone surgery five years earlier and did not show up for endoscopy follow-up since then (A). Lesion was removed with pEMR (B).
Surveillance endoscopy in a 49-year old patient with FAP after proctocolectomy with IPAA revealed 25 mm LST-G mixed type lesion in the rectal cuff. Lesion was spreading from the anastomosis to the dentate line. Patient had undergone surgery five years earlier and did not show up for endoscopy follow-up since then (A). Lesion was removed with pEMR (B).

Cancer rate after primary ileal pouch anal anastomosis (IPAA)

First author and publication date (ref.) No of patients Age at cancer diagnosis (years) Time to cancer (years) Interval since last surveillance endoscopy and findings Endoscopic findings at diagnosis Location Staging of cancer and status
Aelvoet et al., 202355 3/111 (2.7%) / / / / / Pouch excision
Pasquer et al., 202158 1/92 (1.1) 30 / 1 month Pouch body Endoscopic resection
Ganschow et al., 201861 1 / 27 / / Pouch body Resection and reconstruction of a new pouch - alive
Walsh et al., 201663 1 54 / Regular annual surveillance New endoscopy due to anemia and rectal blood loos Anastomosis T3N2Mx, resection and ileostomy, alive during last FUP.
Wasmuth et al., 201367 1 / 11 / / Rectal cuff Resection and ileostomy - alive
Boostrom et al., 201366 1 / 23.7 / / Pouch body Transanal resection - alive
Ozdemir et al., 201338 4 /

Mucosectomy group; median 11.3 years (8.3–22)

Without mucosecomy; 8 years

 		Regular annual surveillance / All ATZ

?

3 underwent APR - alive

1 transanal resection – died 4 years later dissemination
Makni et al., 201269 1 26 10 8 months Polyps, LGD? Pouch body? Pouch excision – died 12 months later dissemination
Tonelli et al., 201251 2

29

58

 10

12 months, normal

6 months, normal

?

IIa + IIc polyp

Pouch body

Pouch body

 Excision with ileostomy, T3N0M0, died 6 months later dissemination/Excision with ileostomy, T2N0M0, alive after 56 month FUP
voon Roon et al., 201170 1 / 13 / / Pouch body Excision of a pouch – died 2 years of disseminated disease
Banasiewicz et al., 201133 5 / / / / Pouch body /
Ault et al., 200971 2

61

50

11

10

6, normal

/

 Pain and blood per rectum, 3 cm mass/Sacral pain, bleeding ulcer Pouch body / Pouch body T2N1Mx, died of AMI prior treatment / Metastatic disease, chemotherapy
Tajika et al., 200983 2

55

68

8.6

20

9 months, normal

No FUP

 30×25 mm cancer / Polyposis and 25 × 25 mm polyp Pouch body/Kock’s pouch body

T4N2M0 – died 1 year later

T3N?M? – died (MDS)
Lee et al., 200871 1 / 7 / Ulcerating tumor Pouch body T4N1M0, APR ileostomy. Developed metastases 2 years later.
Friederich et al., 200832 4

35

37

32

36

14

10.2

16.4

6.2

4.4 years, normal

2.1 years, normal

No control (symptoms)

0.6 years, Tubullovilous

HGD

 / All pouch body

Dukes C

Dukes B

Dukes B

Dukes B
Linehan et al., 200772 1 40 10 / Pelvic pain, discharge Pouch body (patient had ileostomy but pouch was left in situ) Excision. At last FUP patient was well.
Ulas et al., 200674 1 / 9 / / Anastomosis Dukes B, APR, metachronous cancer after 1 year
Campos et al., 200519 1 / 12 No FUP Presented with rectal bleeding Pouch body T2N0Mx, APR and ileostomy, patient well at 6 years FUP.
Vroueraets et al., 200475 2

48

36

9

10

 5 years normal, then 2 and 1 years (both multiple LGD adenomas refused surgery) / Regular FUP every 2 years Presented after 1 year with rectal bleeding /Normal. Routine biopsies at subsequent FUP revealed adenoca.

Anastomosis

Anastomosis

 T2N0M0, APR, alive 1 year later / T4N0M0, APR, alive 8 months later
Cherki et al., 200376 1 35 3.5 1.5 years / Pouch body T3N1M1, resection with ileostomy, died 1 month later
Ooi et al., 200336 2

36

/

2 years 3 months

8 years

/

/

Symptoms of anal bleeding/

/

Anastomosis

Anastomosis

 T3NOMO, APR, ileostomy, died 2.5 years later dissemination / T2N0M0, transanal excision with ileostomy (refused APR), died 4 years later, dissemination
Brown et al., 200178 1 44 7 years 4 months Under FUP every 6 months / Anastomosis /
Vuilleumier et al., 200079 1 38 7 No FUP / Anastomosis Resection with ileostomy – died 12 months later dissemination
Palkar et al., 199715 1 39 4.7 3 months ? Pouch body T4NOM? - alive
Kim et al., 199715 1 / / / / Pouch body? /
Bassuini et al., 199680 1 31 3 No FUP / Pouch body /
Von Herbay et al., 199614 1 33 8 Anastomosis T1N0M0
Hoehner et al., 19947 1 34 20 / / Anastomosis /

Rate of adenoma development in the neoterminal ileum in patients after ileorectal anastomosis (IRA) and ileal pouch anal anastomosis (IPAA)

First author and publication date (ref.) Adenomas in the neoterminal ileum – after primary IPAA; n (%) Cumulative risk for development of neoterminal adenomas Years since surgery Risk factor for adenomas in neoterminal ileum Rate of adenomas in the neoterminal ileum – after primary IRA; n (%) Years since surgery
Tajika et al., 201916 4/24 (16.7) 4.4% at 20 years and 36% at 30 years after primary surgery 23.1 ± 5.8 0/14 (0.0)
Boostrom et al., 201366 4/33 polyps (12.0)
Pommaretet et al., 201335 9/118 (6.5) Presence of pouch adenomas (OR, 2.16, P = 0.007)
Booij et al., 201018 5/34 (14.7) 2 patients had resection of neo-terminal ileum, one due to LGD and other due to HGD adenoma.
Gleeson et al., 200830 3/13 (23.1) Median 6.5 (0–15) 4/16 (25.0) Median 12 (1–29)
Moussata et al., 200717 Mean 17.6 +-7.8(6–35) Mean from colectomy to diagnosis: 16.4+-8.5 (5–30) 10/21 (47.6) of which 2 were advanced adenomas.
Groves et al., 200534 2/20 (10.0) 6 (1–14) 1/47 (2.0%) 12 (0–39)
Thompson-Fawcett et al., 200177 1/24 (4.2) Median 7 (1–19)

Patient characteristics and rate of rectal remnant cancer rate in patients after ileorectal anastomosis (IRA)

First author and publication date Proportion of man; n / (%) APC mutation Underwent n/(%); Positive in; n/(%) Follow-up (years/months) since surgery Years since surgery to cancer diagnosis Age at surgery Age at cancer diagnosis Rectal remnant cancer rate; n/(%) Cumulative risk for rectal cancer Rectal cancer mortality
Colletti et al., 202258 57.4% 93.6% / / Median of 13 years / / 47 / 715 (6.57) / 14/47 (29.8%) at median follow up of 13 years.
Pasquer et al., 202159 95 (48.2) / / / / / 12 / (6.1); 1 was metastatic, 2 were resected endoscopically, 10 surgically / /
Maehata et al., 201520 16 (59.3)

21 (77.8)

14 (66.7)

 21.1 (3–35) / Median 27 years (9–66) / 10/27 (37.0); 6/10 cancers were TisN0M0 8% at 10 years; 19% at 20 years; 57% at 30 years 3/27 (11.1)
Koskenvuo et al., 201322 59 (42.1) / Median 15 years (0–44) / Mean 36 years (18–71) Cumulative risk 2% at 40 years age; 7% at 50; 13% at 60 years age and 16 % at 70 years age. 18/140 (13%) 3% at 5 years; 4% at 10 years; 11% at 20 years; 24% at 30 years after IRA 10/140 (7%); 5-year survival 55%. Cumulative risk for death due to rectal cancer after IRA: 2% at 5 years, 3% at 10 years and 9% at 30 years.
Booij et al., 201018 19 (44.2) / / / Median 16 (7–25) / 3/34 (8.8) / 2/34 (5.8)
Sinha et al., 201026 232 (54.3)

/

311/427 (72.8)

 Median 15 years (7–25) / Median 21 years (11–67) / 48/427 (11.2%) / /
Yamaguchi et al., 200925 35 (59.3) / Median 8.9 years / Median 30 years (13–65) / 17/59 (30%) / 5-year survival 94%; 10-year survival 94%.
Nieuwenhuis et al., 200927 / / / / / / / 3.7% for group 1; 9.3% for group 2; 8.3% for group 3.% /
Campos et al., 200819 / / 91.1 (3–557) / Mean 45.8 years Mean 50.6 years 6/36 (16.7) 17.2% at 5 years; 24.1% at 10 years; 43.1% after 15 years /
Gleeson et al., 200830 / / FUP initiated median 12 (1–29) years after surgery / / 40 and 59 years. 2/16 (12.5) / /
Bullow et al., 200824 401 (51.7) / Median 7 years (0–13). Patients were operated between 1950–2006 Median 27 (7–75) / 60/776 (7.7%) (56/576; 10% and 4/200; 2%) 10-year cumulative risk 4.4% [95% CI 2.6–6.2] in pre-pouch era; 10-year cumulative risk 2.5% [95% CI 0–5.5] in pouch era; /
Moussata et al., 200717 They only watched ileal muocas above the IRA 10 (47.6)

21/21 (100.0)

14/21 (66.7)

 		Mean 8.4 years ± 5 since colectomy / / / 0/21 (0.0) / /
Church et al., 200338 92 / (46.7) / Pre-pouch era: 212 months (IQR 148 months); Pouch era: 60 months (IQR 80 months) / Median age 23 years (IQR 15.5 years pre-pouch and 17 years pouch) / 8 (12.9%) in the pre-pouch era and 0 in pouch era. / /
Bertario et al., 200023 206/371 (55.5)

297/371 (80.1)

200/297 (67.3)

 Median 81 months Median 102 months (1–26 years) Mean 32 years / 27/371 (7.3)

10 years – 7.7%

15 years – 13.1 %

20 years – 23.0%

 6/371 (1.6)
Jenner et al., 199821 25/55 (45.0) 55/(100.0) Median 10 (1–31) / Mean age 30 (13–62) Median 41 7/55 (12.7) / /

Patient characteristics and rate of adenomas in patients after primary ileal pouch anal anastomosis (IPAA)

First author and publication date Sex (man); n (%) APC mutation Underwent; n (%); Positive in; n (%) Distinguish between pouch body and rectal cuff Follow-up (months/years) Time from surgery to first adenomas (years) Age at surgery (years) Rate of adenomas (≥ 1 polyp) Size of adenomas, mm Histology of adenomas; n (%) Number of Adenomas
Aelvoet AS et al., 202355 81 (56)

101 (91)

96 (86)

 		Yes Median 152 (77–240) 15% at 5 years; 48% at 10 years; 85% at 20 years. Median 24 (18–32) Median 5 (3–15) Tubular adenomas 31 (28%), Tubulovillous 26 (23%), Villous 5 (5%) Prepouch ileum 4(2–13), Pouch body 20 (5–50), rectal cuff 6 (3–10)
Tajika et al., 201926 16 (47.1) / Yes Median 21.6 (3.7–8.8) 32 (35.9) of patients showed progression of pouch adenomas during FUP Median 34.6 (17–52) 24/34 (70.6) 2–40 mm 6 advanced adenomas (25.0) 1–300
Ganschow et al., 201861 100 (52.1)

133 (69.3))

? / 133

 		No Median 12.8 (9–17) for patients with pouch adenomas and (2.5–12.2) for patients without pouch adenomas; 32 (35.9) of patients showed progression of pouch adenomas during FUP 27.5 years (10.2–58.5) 90/192 (46.9) at a median of 8.5 years (0.9–25.1) after IPAA. 5 years after IPAA 84.9% patients free of adenoma; 15 years after 40.4% and 20 years after 21.9% patients were free of adenomas. 53/192 (58.9) ≤ 4 mm; 24/192 (26.7) 5 – 10 mm; 13/192 (14.4) ≥ 10 mm Tubular adenomas in 69/192 (76.7); tubulovillous adenomas in 16/192 (17.8); villous in 5/192 (5.6) 46/192 (51.1) had < 4; 14/192 (15.6) 5–10; 30/192 (33.3) > 10 adenomas
Goldstein et al., 201563 24 (41.0) Yes Mean 11.6 years +-14.6 years Median adenoma free time interval since surgery; Cuff 10.8 years Pouch 16.9 years Mean 30.8 years +-10.8 years 35/59 (59.0);

- 20 isolated in cuff

- 4 isolated in pouch body

- 11 in pouch and body

 		/ All LGD /
Zahid et al., 201519 14 (51.8) No Mean 9.2 years Median; 72 months (18–249) Median 31 years (14–65) 12/27 (44.0) / Only 1 polyp HGD (< 99%) /
Kennedy et al., 201466 43 (45.0) Watched only anastomosis Mean 7.6 (0 – 24) Mean 15.4 (4–20) 9/95 (9.4)
Pommaretet et al., 201336

110 / 139

92 / 110 (Cohort included IRA, ileostomy and IPAA patients but did not distinguish between).

 / Median 15 years 25 years (9−61 years) 57/118 (48.3) > 10 mm:12 94% LGD; 6% HGD

1−4: 22

5−20: 18

> 20: 17
Boostrom et al., 201366 52 (44.5) Yes 125 months (25–423 months) 12.4 years (15–405 months) 26 years (4–60 years) 30/117 (25.6) 5.9 mm (2 mm to 20 mm) 22 LGD, 8 tubulovillous /
Wasmuth et al., 201367 34 (55.7) / Yes (body and anastomosis) Cumulative rate of adenomas at 28 years 17% for mucosectomy group and 75% at 15 years in a group without mucosectomy (P < 0.0001) 20 (10–49)

Anastomosis: 4/39 (10.0) vs. 14/22 (64.0) (P < 0.0001)

Pouch body: 8/39 vs. 6/22 (P 0.57)
Tonelli et al., 201251 / 45 (65%) No Median 133 months (12–288 months) Mean 7 years (1–15 years) 33 years (17–63 years) 25 (36.0) Mean 3 mm (1–40) Adenomas, dysplasia not specified Mean 8 (1–47)
Yan et al., 201268 30 (71.5) / Yes Median 7.2 (2.2–20) 29 (16–65) At the anastomosis 6/33 (18.2) / / /
Banasiewicz et al., 201133 79 (47.9) / / Endoscopies performed 2–19 years since surgery.

Mean 14 months to LGD; Mean 16 months to HGD.

Estimated frequency LGD 15 years later 50% and for HGD 17.5 years later 50%.

 21/165 (12.7) LGD - 21/32 (65.6); HGD - 11/32 (34.4)
Gleeson et al., 200831 / / Yes / FUP began median 6.5 (0–15) after surgery / 13/13 (100): 10/13 pouch body; 2/13 anastomosis; 3/13 ileum above anastomosis < 5 mm / 5–30
Friederich et al., 200832 119 (56.0) / / Mean 7.9 (0.4–20.3 years)

Cumulative risk of 16% at 5-years and 42.4% at 10 years for adenoma development.

Cumulative risk of 12.8% at 10 years for advanced adenoma development.

 Mean 30.0 years (10–62.6 years) 47/212 (35%) / / /
Campos et al., 200817 / / No 50.8 (5–228) 3/26 (11.5)
Moussata et al., 200725 12 (57.1)

23/23 (100.0)

22/23 (95.7)

 		Yes (only polyps in the ileal mucosa of the pouch body are described) Mean 5.4 +- 2.6 (1–11) Mean 4.7+-3.3 years (1–14) 17/23 (74.0) Mean size 5.2 mm +-3.4 mm; 3 polyps were > 10 mm. LGD 16/17 (94.1); HGD 1/17 (5.9) /
Groves et al., 200535 35 (58.3) / Between pouch and above anastomosis ileum 6 years (1–17 years) / 32.5 years (13–66 years) 34/60 (57%) of which 5 were > 10 mm / 11 were advance adenomas Mean size 5 mm (1–40 mm) / Median number 4
Thompson-Fawcett et al., 200177 /

20/33 (60.6)

18/20 (90.0)

 		Only pouch body / / / 20/33 (60.0) adenomas 1–3 mm / Median 10 (1–100) Also lymphoid hyperplasia included

Summary of recommendations from the international guidelines

First author and publication date (ref.) Endoscopic surveillance – patients with IRA Indications for secondary proctectomy patients with IRA Endoscopic surveillance – patients with IPAA
Vasen et al., 20087 Every 3 to 6 months Multiple large adenomas (> 5 mm) Adenomas with dysplasia Every 6 to 12 months
Balmaña et al., 2013, ESMO8 Every 12 months No recommendations Every 12 months
Stoffel et al., 2015, ASCO9 Every 6 to 12 months No recommendations Every 6 months to 5 years (Intervals should be determined on a case-by-case basis and may be even shorter than 1 year for some individuals)
Sygnal et al., 2015, ACG10 Every 12 months No recommendations Every 12 months
Herzig et al., 2017, ASCRS4 Every 12 months No recommendations Every 12 months
Van Leerdam ME et al., 2019, ESGE53 Every 12 to 24 months No recommendations Every 12 to 24 months
Yang J et al., 2020, ASGE54 6 months after surgery with 6 to 12 months further surveillance interval 12 months after surgery with 12 to 24 months further surveillance interval. 6 months if advance adenoma

Characteristics of included studies

First author and publication date (ref.) No. of patients Country Setting Study design Surgery performed (period) Study population
Aelvoet et al., 202355 144 (111 IPAA, 33 ileostomy) The Netherlands Single Cohort/Retrospective / IPAA, ileostomy
Tatsuta et al., 202356 65 (22 IRA, 20 IPAA) Japan Single Cohort/Retrospective 1976–2022 IRA, IPAA
Anele et al., 202257 199 (199 IRA) United Kingdom Single Cohort/Retrospective 1990–2017 IRA
Colletti et al., 202258 715 (715 IRA) Italy Multicentre Retrospective analysis of the Registry 1977–2021 IRA
Pasquer et al., 202159 289 (197 IRA, 92 IPAA) France Multicentre Retrospective analysis of the Registry 1965–2015 IRA, IPAA
Ardoino et al., 202060 925 (585 IRA, 340 IPAA) Italy Multicenter Retrospective analysis of the Registry 1947–2015 IRA, IPAA
Tajika et al., 201916 47 (14 IRA, 25 IPAA, 8 ileostomy) Japan Single Cohort/Retrospective 1965–2017 IRA, IPAA and ileostomy
Ganschow et al., 201861 192 Germany Singe Cohort/Prospective and retrospective analysis of Polyposis Registry Endoscopy data collected during 2010–2013 IPAA
Kariv et al., 201762 45 Israel Single Cohort/Retrospective 1986–2013 IPAA
Patel et al., 201642 21 (6 IRA, 5 IPAA, 10 intact colon) Indianapolis, USA Single Cohort/Retrospective Endoscopies performed between 2004–2016 IRA, IPAA and intact colon
Walsh et al., 201663 1 Ireland Single Case report 1987 IPAA - cancer
Maehata et al., 201520 27 Japan Single Cohort/Retrospective 1990–2004 IRA
Ganschow et al., 201550 100; 50 hand-sewn and 50 stapled anastomoses Germany Single Cohort/Prospective ? Hand-sewn vs. stapled anastomosis
Goldstein et al., 201563 59 Israel Single Cohort/Retrospective 1986–2013 IPAA
Zahid et al., 201564 27 Australia Single Cohort/Retrospective 1984–2011 IPAA
Kennedy et al., 201465 95; 85 hand-sewn and 1 stapled anastomosis Rochester, Mayo Clinic, USA Single Cohort/Retrospective 1987–2011 IPAA
Koskenvuo et al., 201322 140 Finland Single Cohort/Retrospective 1963–2012 IRA
Pommaret et al., 201335 118 France Single Cohort/Retrospective / IPAA and IRA
Boostrom et al., 201366 117 Rochester, Mayo Clinic, USA Single Cohort/Retrospective 1972–2007 IPAA
Ozdemir et al., 201337 260; 86 hand-sewn and 175 stapled anastomoses Cleveland, USA Single Analysis of polyposis registry 1983–2010 Hand-sewn vs. stapled anastomosis
Wasmuth et al., 201367 61; 39 hand-sewn with mucosectomy and 22 without of which 15 were stapled and 7 hand-sewn anastomoses Norway Multicenter Analysis of polyposis registry 1986–2008 IPAA (mucosectomy vs. no-mucosectomy)
Yan et al., 201268 42 (33 IPAA; 6 IRA ?) China Single Cohort/Retrospective 1988–2008 IPAA and IRA
Makni et al., 201269 1 Tunisia Single Case report 1996 IPAA - cancer
Tonelli et al., 201251 69 Italy Single Cohort/Prospective data collection 1984–2008 IPAA
von Roon et al., 201170 140; 44 hand-sewn and 76 stapled anastomoses UK Single Retrospective analysis of St. Mark’s Hospital Polyposis Registry 1978–2007 Hand-sewn vs. stapled anastomosis
Banasiewicz et al., 201132 165 Poland Bicenter Bicenter/Retrospective analysis 1985–2009 operated, Clinical data from endoscopy FUP between 2004–2009 IPAA
Booij et al., 201018 43 (34 IRA) The Netherlands Single Cohort/Retrospective 1977–2005 IRA and IPAA
Sinha et al., 201026 427 UK Single Retrospective analysis of St. Mark’s Hospital Polyposis Registry 1990–2008 IRA
Ault et al., 200971 2 Los Angeles, USA Single Case series 1990, 1993 IPAA - cancer
Nieuwenhuis et al., 200927 475 Denmark, Finland, Sweden, Netherlands Multicenter Analysis of polyposis registry / IRA
Yamaguchi et al., 200925 59 Japan Single Cohort/Retrospective 1962–2007 IRA
Friederich et al., 200831 212; 71 hand-sewn with mucosectomy and 115 stapled anastomoses The Netherlands Single Analysis of National Polyposis Registry 1985–2005 IPAA
Campos et al., 200819 36 Brasil Single Cohort/Retrospective 1977–2006 IRA and IPAA
Bullow et al., 200824 776; 576 operated in pre-pouch period and 200 in pouch period starting in 1990 Denmark, Finland, Sweden, Netherlands Multicenter Analysis of polyposis registry 1950–2006 IRA
Gleeson et al., 200830 16 Rochester, Mayo Clinic, USA Single Cohort/Retrospective analysis 1964–2003(Analysis of endoscopies between 1992–2006) IPAA and IRA
Lee et al., 200872 1 Korea Single Case report 1998 IPAA - cancer
Linehan et al., 200773 1 Ireland Single Case report 1997 IPAA - cancer
Valanzano et al., 200728 25 Italy Single Cohort/Prospective 1986–2004 IRA
Moussata et al., 200717 21 France Single Cohort/Retrospective / IPAA and IRA
Ulas et al., 200674 1 Turkey Single Case report 1993 IPAA - cancer
Campos et al., 200519 1 Brazil Single Case report / IPAA - cancer
Groves et al., 200534 60 UK Single Retrospective analysis of St. Mark’s Hospital Polyposis Registry / IPAA
Vroueraets et al., 200475 2 The Netherlands Single Case report 1990, 1991 IPAA – cancer
Ooi et al., 200336 2 Cleveland, USA Single Case report / IPAA – cancer
Church et al., 200338 197; 62 operated in pre-pouch period and 135 in pouch period starting in 1983 Cleveland, USA Single Analysis of polyposis registry 1950–1999 IRA
Cherki et al., 200376 1 France Single Case report / IPAA - cancer
Thompson-Fawcett et al., 200177 33 Canada Single Cohort/Prospective / IPAA
Church et al., 200115 213 (165 IRA) Cleveland, USA Single Analysis of polyposis registry / IRA and IPAA
Brown et al., 200178 1 Singapore Single Case report / IPAA - cancer
Bertario et al., 200023 371 Italy Multicenter Retrospective analysis of Hereditary tumor registry 1955–1997 IRA
Vuilleumier et al., 200079 1 UK Single Case report 1990 IPAA - cancer
Jenner et al., 199821 55 Australia Single Analysis of polyposis registry ?–1994 IRA
Bassuini et al., 199680 1 UK Single Case report 1991 IPAA - cancer
Hoehner et al., 19946 1 Iowa, USA Single Case report / IPAA - cancer
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