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275
stage cancer (Stage I and II) and only 7 were stage III.The advanced stage patients
received adjuvant chemotherapy without radiation therapy. One rectal cancer
patient received adjuvant radiation therapy that was associated with pouch failure
and development of cancer recurrence. Only one of the rectal cancer patients died
during the average 6.1years of follow up. This group concluded that IPAA should
be considered in patients with coexisting colorectal cancer and UC.Surgery along
with chemotherapy, when needed, can provide good prognosis with very good
functional outcomes.
Finally, in a study that we did not include in our PICO analysis, McLeod [6]
compared IPAA to TPC, but included patients with Crohn’s disease and familial
adenomatous polyposis. A total of 27 patients had rectal cancer; as in the previous
studies, patients with advanced T4 tumors with poor differentiation did not receive
an IPAA.Use of radiation was much more common in the TPC group. Overall dis-
ease free survival was comparable between the 2 groups and median time to recur-
rence or death was 14months for both groups. The authors recommended IPAA as
a safe alternative to TPC with end ileostomy, but not in those with T
3
or T
4
lesions,
or those with threatened radial margins (Table30.2).
Although there are several studies comparing the IPAA versus TPC for UC for
health related quality of life measures, there are no studies on patients that also have
rectal cancer. Although most studies without rectal cancer patients demonstrate
comparable quality of life for both groups, in patients with rectal cancer there are
two distinct differences in management which can affect overall pouch function: the
increased use of handsewn anastomosis (especially for distal rectal tumors) and the
need for neoadjuvant chemoradiation or adjuvant chemotherapy.
IPAA with mucosectomy and handsewn anastomosis is a more demanding pro-
cedure that consists of stripping the anal transitional zone and suturing the anasto-
mosis. Alternatively, the stapled anastomosis retains the distal rectal mucosa
(possibly increasing the risk for local recurrence), but is superior in terms of post-
operative defecatory function. It has been shown extensively that the stapled tech-
nique has a superior functional outcome and better quality of life than hand-sewn
anastomosis with mucosectomy [9]. The oncologic advantage of the hand-sewn
technique is challenged in several articles that support the use of a stapled approach.
In 2009, Zmora [10] and Cohen [11] demonstrated that for most colorectal cancer
patients with ulcerative colitis, the stapled IPAA is a reasonable and safe option.
The use of radiation therapy before or after IPAA has not been analyzed exten-
sively. This is because in all the published studies, it is clearly stated that the
Table 30.2 Studies of IPAA and Rectal Cancer
Study
Patients with rectal
cancer
5Year-
recurrence
5Year—
survival
Quality of
evidence
Merchea [3] 28 TPC vs 11 IPAA 38% 62% Low
Ziv [4] 7 IPAA 0% 100% Low
Remzi [5] 26 IPAA 3.8% 96% Low
Hotta [7] 9 IPAA 0% 100% Low
Gorne [8] 14 IPAA N/A 79% Low
30 Management ofUlcerative Colitis inPatients withRectal Cancer
276
majority of the IPAAs were performed for early stage cancers and that most of the
patients with advanced rectal cancers declined radiation therapy. Wu [12] reported
the largest cohort of patients with rectal cancer with preoperative radiation therapy
that received an IPAA (n=9), and compared their outcomes with patients undergo-
ing IPAA without pelvic radiation. Chronic pouchitis was signicantly more com-
mon in patients with neoadjuvant chemoradiation. Furthermore, almost half of the
rectal cancer radiated patients (43%) lost their pouch during the follow up period,
while only 17% of the non-radiated pouches were excised over the same time
period. The average time for a radiated pouch to fail was 60 months. The study
concluded that pelvic radiation administered prior to IPAA creation appears to be
associated with worse pouch outcomes.
Several studies have demonstrated that postoperative radiation is linked to a high
chance for pouch failure (see Table30.3).
Recommendations Based onData
Patients with ulcerative colitis and early (T
1
or T
2
, N
0
) rectal cancer can undergo
IPAA instead of TPC with end ileostomy and expect comparable oncologic out-
comes (Weak Recommendation based on Low Quality Evidence).
Patients with ulcerative colitis requiring neoadjuvant or adjuvant chemoradiation
for locally advanced rectal cancer should not be offered IPAA, but rather undergo a
TPC with end ileostomy (Strong Recommendation based on Moderate Quality
Evidence).
Personal View
Patients with rectal cancer in the setting of ulcerative colitis need to undergo a
sound oncologic operation and at the same time, attempt to have a curative resection
for their ulcerative colitis. The sequence from dysplasia to cancer in the background
of inammation from ulcerative colitis patients is less predictable, and may occur at
a rate faster than what is seen with the traditional adenoma to carcinoma sequence
[15]. Thus, patients with ulcerative colitis and colorectal cancer are at higher risk of
developing another cancer in the remaining inamed colon or rectum. This can
occur in the remaining rectum when total abdominal colectomy is performed for
Table 30.3 Studies of the consequence of radiation therapy and IPAA
Study
Rectal cancer Postoperative radiation IPAA failure
Quality of evidence
Radice [13] 21 5 3 Low
Remzi [5] 26 1 1 Low
Gorne [8] 14 2 1 Low
Inoue [14] 1 1 0 Low
E. Messaris and W. Koltun
277
either initial colon cancer treatment or severe colitis, and there is a subsequent delay
in removing the retained rectum. In those patients undergoing TAC for dysplasia or
cancer, close surveillance of the rectum is necessary to avoid the development of a
second rectal malignancy, prior to either completion proctectomy or IPAA
reconstruction.
Thus, UC patients with a rectal cancer have two options; either an IPAA or a TPC
with end ileostomy. The current data is insufcient to support a rm recommenda-
tion. While all available data suggests that oncologic outcomes for both procedures
are equivalent, it is clear that in all the studies, there was a very strict pre-selection
of patients. IPAA can be safely performed as a primary or secondary procedure in
conjunction with radical resection of the tumor bearing rectum in most early (T
1,
T
2
,
N
0
) rectal cancer patients. As in patients who do not have ulcerative colitis, if the
tumor is invading sphincter muscles or reaches the level of the dentate line, radical
resection without reconstruction is recommended. In a similar fashion, for symp-
tomatic patients (i.e. bleeding or obstructing tumor) or with metastatic disease, a
TPC with an end ileostomy would be the lowest risk procedure to get the patient to
chemotherapy as soon as possible.
A signicant challenge remains for patients with more advanced rectal cancer
who require neoadjuvant chemoradiation or adjuvant chemoradiation. Patients
with locally advanced rectal malignancies who undergo IPAA are at greater risk
of pouch excision, diversion and death. Preoperative combined chemoradiation
for Stage II or III rectal lesions followed by IPAA is theoretically possible; how-
ever with the small amount of data presently available, these patients are at sig-
nicantly increased risk for pouch failure and subsequent pouch excision. In
addition, a signicant number of colorectal cancers may be found only after the
surgical excision is done ostensibly for dysplasia and adjuvant chemoradiation
therapy may then be required. Patients with rectal lesions who already received an
IPAA and now require postoperative chemoradiation are probably best treated by
deferring the radiation and utilizing just chemotherapy. Postoperative adjuvant
chemotherapy is compatible with this approach, and does not appear to increase
the risk for pouch failure or any other complications. The use of preoperative
chemotherapy has recently emerged as an option in the care of patients with
locally advanced rectal cancers but has not been studied in IPAA patients.
In conclusion, early stage (T
1
, T
2
, N
0
) upper and mid rectal tumors in the setting
of ulcerative colitis can be safely treated with restorative proctocolectomy (IPAA)
with acceptable oncologic and functional outcomes when compared to TPC with
end ileostomy. Adjuvant chemotherapy if needed is safe. Distal rectal tumors in
patients should be considered for TPC with end ileostomy.
Neoadjuvant or adjuvant chemoradiation is associated with high incidence of
pouch failure and complications. Thus, IPAA is not recommended in patients with
locally advanced tumors that need neoadjuvant radiation therapy. No data exists on
the role of neoadjuvant chemotherapy for locally advanced rectal tumors in the set-
ting of ulcerative colitis with subsequent IPAA.
30 Management ofUlcerative Colitis inPatients withRectal Cancer
278
References
1. Kornbluth A, Sachar DB, Practice Parameters Committee of the American College of
Gastroenterology. Ulcerative colitis practice guidelines in adults: American College Of
Gastroenterology, Practice Parameters Committee. Am J Gastroenterol. 2010;105(3):501–23.
2. Pohl C, Hombach A, Kruis W. Chronic inammatory bowel disease and cancer. Hepato-
Gastroenterology. 2000;47(31):57–70.
3. Merchea A, Wolff BG, Dozois EJ, Abdelsattar ZM, Harmsen WS, Larson DW.Clinical fea-
tures and oncologic outcomes in patients with rectal cancer and ulcerative colitis: a single-
institution experience. Dis Colon Rectum. 2012;55(8):881–5.
4. Ziv Y, Fazio VW, Strong SA, Oakley JR, Milsom JW, Lavery IC.Ulcerative colitis and coex-
isting colorectal cancer: recurrence rate after restorative proctocolectomy. Ann Surg Oncol.
1994;1(6):512–5.
5. Remzi FH, Preen M. Rectal cancer and ulcerative colitis: does it change the therapeutic
approach? Color Dis. 2003;5(5):483–5.
6. Snelgrove R, Brown CJ, O'Connor BI, Huang H, Victor JC, Gryfe R, MacRae H, Cohen Z,
McLeod RS.Proctocolectomy for colorectal cancer--is the ileal pouch anal anastomosis a safe
alternative to permanent ileostomy? Int J Color Dis. 2014;29(12):1485–91.
7. Hotta S, Shimada Y, Nakano M, Yamada S, Abe K, Oyanagi H, Yagi R, Tajima Y, Nakano M,
Kameyama H, Nagahashi M, Sakata J, Kobayashi T, Wakai T.Feasibility of restorative proc-
tocolectomy in patients with ulcerative colitis-associated lower rectal cancer: a retrospective
study. Asian J Surg. 2019;42:267–73.
8. Gorne SR, Harris MT, Bub DS, Bauer JJ.Restorative proctocolectomy for ulcerative colitis
complicated by colorectal cancer. Dis Colon Rectum. 2004;47(8):1377–85.
9. Lovegrove RE, Constantinides VA, Heriot AG, Athanasiou T, Darzi A, Remzi FH, Nicholls
RJ, Fazio VW, Tekkis PP.A comparison of hand-sewn versus stapled ileal pouch anal anas-
tomosis (IPAA) following proctocolectomy: a meta-analysis of 4183 patients. Ann Surg.
2006;244(1):18–26.
10. Zmora O, Spector D, Dotan I, Klausner JM, Rabau M, Tulchinsky H.Is stapled ileal pouch
anal anastomosis a safe option in ulcerative colitis patients with dysplasia or cancer? Int J
Color Dis. 2009;24(10):1181–6.
11. Al-Sukhni W, McLeod RS, MacRae H, O'Connor B, Huang H, Cohen Z.Oncologic outcome
in patients with ulcerative colitis associated with dyplasia or cancer who underwent stapled or
handsewn ileal pouch-anal anastomosis. Dis Colon Rectum. 2010;53(11):1495–500.
12. Wu XR, Kiran RP, Remzi FH, Katz S, Mukewar S, Shen B. Preoperative pelvic radiation
increases the risk for ileal pouch failure in patients with colitis-associated colorectal cancer. J
Crohns Colitis. 2013;7(10):e419–26.
13. Radice E, Nelson H, Devine RM, Dozois RR, Nivatvongs S, Pemberton JH, Wolff BG, Fozard
BJ, Ilstrup D.Ileal pouch-anal anastomosis in patients with colorectal cancer: long-term func-
tional and oncologic outcomes. Dis Colon Rectum. 1998;41(1):11–7.
14. Inoue Y, Araki T, Okugawa Y, Kawamoto A, Hiro J, Toiyama Y, Tanaka K, Uchida K, Mohri Y,
Kusunoki M.Chemoradiotherapy followed by restorative proctocolectomy with partial inter-
sphincteric resection for advanced rectal cancer associated with ulcerative colitis: report of a
case. Surg Today. 2014;44(2):387–90.
15. Robles AI, Traverso G, Zhang M, Roberts NJ, Khan MA, Joseph C, Lauwers GY, Selaru FM,
Popoli M, Pittman ME, Ke X, Hruban RH, Meltzer SJ, Kinzler KW, Vogelstein B, Harris
CC, Papadopoulos N. Whole-exome sequencing analyses of inammatory bowel disease-
associated colorectal cancers. Gastroenterology. 2016;150(4):931–43.
E. Messaris and W. Koltun
279
© Springer Nature Switzerland AG 2019
N. Hyman et al. (eds.), Mastery of IBD Surgery,
https://doi.org/10.1007/978-3-030-16755-4_31
H. Kunitake, MD, MPH (*) · L. Bordeianou, MD, MPH
Department of General and Gastrointestinal Surgery, Massachusetts General Hospital,
Boston, MA, USA
e-mail: hkunitake@partners.org
31
Surgical Approach totheOlder
Ulcerative Colitis Patient
HirokoKunitake andLilianaBordeianou
Introduction
Ulcerative colitis has a bimodal age distribution; between 10% and 15% of patients
are diagnosed with ulcerative colitis after the age of 60years [1]. A signicant pro-
portion of these patients require surgery and the choice between proctocolectomy
with end ileostomy or proctocolectomy with ileal pouch-anal anastomosis (IPAA)
can be difcult.
Previously, patients over age 50 undergoing surgery for ulcerative colitis were
assumed to be poor candidates for IPAA and were more likely to undergo end ileos-
tomy. A study of 3635 patients with ulcerative colitis between 2005 and 2012 using
the American College of Surgeons NSQIP database found that the odds of having an
end ileostomy decreased by 12% per year in patients 61–70years compared with
patients under age 50 as IPAA became a more acceptable option for older patients
[2]. However older patients generally have more comorbidities and may have
decreased functional capacity; the risk of complications and their anticipated qual-
ity of life should be factored into which procedure is offered and ultimately per-
formed for older ulcerative colitis patients [3] (Table31.1).
Table 31.1 PICO table
Patients
Intervention Comparator
Outcome
Surgical approach to the older
ulcerative colitis patient
IPAA Ileostomy Complication rate, quality
of life
280
Search Strategy
A comprehensive literature search of Cochrane Database of Collected Research,
EMBASE, MEDLINE, and PubMed was performed to identify all of the English-
language publications related to ulcerative colitis, colectomy and ileal pouch-anal
anastomosis, older patient and complication rate and quality of life (QOL) out-
comes from 1985 to 2018. Key search terms included the following: “colectomy,”
“colitis,” “ileal pouch-anal anastomosis,” “inammatory bowel disease,” “elderly,”
“older,” “proctocolectomy,” and “ulcerative colitis.” Studies were excluded if they
did not directly address older patients with ileal pouch-anal anastomosis or failed to
measure complication rates or any component of health-related quality of life. Due
to the small cohorts of older patients undergoing IPAA for ulcerative colitis, studies
which included familial adenomatous polyposis patients along with ulcerative coli-
tis patients undergoing IPAA were included. Only the most recent study was
included if similar studies from the same institution were encountered. The refer-
ences of the included studies were reviewed to identify additional studies that were
incorporated as appropriate.
Results
The denition of older patient differed among studies. Some studies dened older
patient as ≥50 or 55years and several studies used ≥70years. There were no studies
which specically compared complications or quality of life between IPAA and
ileostomy in older ulcerative colitis patients. However, several studies evaluated
complications and quality of life of IPAA patients stratied by age group or focused
on a cohort of older IPAA patients. The cohorts of older IPAA patients in published
studies are small.
As expected, older patients had more comorbidities and higher ASA scores
[4–8]. Complication rates were generally comparable between older patients
and younger patients undergoing IPAA (Table 31.2) [5, 6, 9, 10]. However,
older patients suffered more from dehydration than younger patients [4, 6, 11].
Small bowel obstruction was more common in younger patients [4, 11]. One
study noted that pouch-anal stenosis was signicantly more common in older
patients with ulcerative colitis compared with younger patients (37% vs. 17%,
p=0.02) [10].
Pouch function including stool frequency and incontinence episodes were com-
parable between older and younger patients in the majority of studies (Table31.2)
[4–6, 10] Pellino [4] found that older patients took signicantly more antidiarrheals
than the younger group at 1-year follow-up; however, this observation was not con-
rmed at 3-year follow-up. In a retrospective review of 2002 patients, Chapman [9]
reported higher number of stools at night, more frequent day time incontinence for
patients ≥55years compared with patients <45years (15.2% vs. 4.1% at 1 year,
p=.004) and more frequent night time incontinence in patients ≥55years compared
with patients <45years (26.1% vs. 9.4% at 1 year, p= .001; 19.6% vs. 9.3% at
H. Kunitake and L. Bordeianou
281
Table 31.2 Complications and pouch function for older patients undergoing IPAA
Study
Patients
(N) IPAA
Complication
rate QOL measure QOL results
Quality of
evidence
(Newcastle-
Ottawa
quality
assessment)
Pellino
(2013)
[4]
27 Patients
over age
70 vs. 81
younger
controls
Comparable
major
complications;
older group had
more
dehydration,
younger group
more SBO
Pouch
function at
1year/3years
IBDQ at
1year/3years
Comparable;
older patients
took more
antidiarrheals at
1year
Comparable
Good
Delaney
(2002)
[13]
17 Patients
≥ age 70
4 Patients with
major
complications, 1
death at
6months
post-op
Pouch
function
CGQL
SF-36
Complete
continence in
38%
Good QOL and
health
Comparable to
healthy
individuals ≥65
Fair
Ho
(2005)
[5]
17 Patients
≥ age 70
vs. 313
patients in
younger
age groups
Comparable
between age
groups
Pouch
function
No difference
in major or
minor
incontinence.
Older patients
had more
frequent bowel
movements
Good
Pinto
(2010)
[6]
33 Patients
≥ age 65
vs. 33
matched
younger
patients
Comparable
major
complications;
older group had
more
dehydration
Pouch
function
Comparable Good
Chapman
(2005)
[9]
65 Patients
≥ age 55
vs. 1937
patients in
younger
age groups
Comparable
between age
groups
Pouch
function
QOL
Daytime and
nighttime
incontinence
more frequent
in patients
≥55years
Comparable
Good
Dayton
(1996)
[11]
32 Patients
≥55years
vs. 423
patients
<55years
Comparable;
older group had
more
dehydration
Pouch
function
Stool frequency,
daytime and
nighttime
incontinence
higher in
patients
≥55years
Good
(continued)
31 Surgical Approach totheOlder Ulcerative Colitis Patient
282
3years, p=.03). Delaney, in a study of 1895 patients, also found that incontinence
and night time seepage were more common in older patients [12].
Older patients and younger patients with IPAA reported similar restrictions in
travel, sports activity, social activity, family relations and work. Severe sexual
restrictions were more common in patients ≥55 years compared with patients
<45years at 5year and 10year follow-up [9]. Delaney used the Cleveland Global
Quality of Life (CGQL) score which encompasses quality of life, health and current
energy level. IPAA patients ≥70years in this study reported good CGQL scores.
This study also compared Short Form-36 results between the IPAA patients
≥70 years and the U.S. population norm for healthy individuals ≥65 years and
found no signicant difference. Importantly, 82% of these patients stated that they
would undergo IPAA again and 89% would recommend it to others.
In a separate retrospective review by Pellino of ten IPAA patients >80 years old
compared with 30 randomly selected younger controls, older patients had signicantly
more nocturnal seepage and used antidiarrheal medications more frequently. By 1 year,
only nocturnal seepage remained signicantly higher in the elderly group. All patients
retained their pouch at a median follow up of 7 (range 2–13) years. All patients reported
they would undergo surgery again and recommend IPAA to other patients.
Recommendations
1. Ileal pouch-anal anastomosis can be safely performed in older patients who have
well-managed comorbidities, adequate anal sphincter function and the ability to
understand and manage their pouch function. (Evidence: moderate;
Recommendation: strong)
2. Older patients with IPAA are at higher risk of dehydration than younger patients
and should be monitored carefully for dehydration. (Evidence: moderate:
Recommendation: strong)
3. Older patients with IPAA may have more frequent stools and an increased rate
of incontinence, but they are generally satised with their pouch function and
quality of life.
Table 31.2 (continued)
Study
Patients
(N) IPAA
Complication
rate QOL measure QOL results
Quality of
evidence
(Newcastle-
Ottawa
quality
assessment)
Tan
(1997)
[10]
28 Patients
> age 50
vs. 199
patients in
younger
age groups
Comparable
major
complications;
pouch-anal
stenosis more
common in older
group
Pouch
function
Comparable Good
H. Kunitake and L. Bordeianou
283
Personal View
In our view, IPAA is an acceptable and safe option for selected older ulcerative
colitis patients. We agree with the American Society of Colon and Rectal
Surgeons Practice Parameters for the Surgical Treatment of Ulcerative Colitis
and the European Crohn’s and Colitis Organisation Consensus guidelines which
both state that IPAA can be offered to selected older patients as long as the
patient retains good anal sphincter function and has adequate mental and physi-
cal function [14, 15].
For our older patients, particularly those with a history of fecal leakage, we rec-
ommend anal manometry testing prior to consideration of IPAA.Patients with very
low resting anal sphincter pressures should not proceed to IPAA.
We nd that many of our older ulcerative colitis patients prefer to have their
disease addressed in a single operation with a total proctocolectomy and end ileos-
tomy rather than undergo two or potentially three operations. Still, IPAA is a pos-
sibility for patients who wish to avoid permanent ileostomy.
References
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disease and ulcerative colitis in Olmsted county, Minnesota from 1970 through 2010. Clin
Gastroenterol Hepatol. 2017;15:857–63.
2. Cohan JN, Bacchetti P, Varma MG. Impact of patient age on procedure type for ulcerative
colitis: a national study. Dis Colon Rectum. 2015;58:769–74.
3. Bollegala N, Jackson TD, Nguyen GC.Increased postoperative mortality and complications
among elderly patients with inammatory bowel diseases: an analysis of the national surgical
quality improvement program cohort. Clin Gastroenterol Hepatol. 2016;14:1274–81.
4. Pellino G, Sciaudone G, Candilio G, Camerlingo A, Marcellinaro R, Rocco F, De Fatico S,
Canonico S, Selvaggi F.Complications and functional outcomes of restorative proctocolec-
tomy for ulcerative colitis in the elderly. BMC Surg. 2013;13:S9.
5. Ho KS, Chang CC, Baig MK, Borjesson L, Nogueras JJ, Efron J, Weiss EG, Sands D, Vernava
AM, Wexner SD.Ileal pouch anal anastomosis for ulcerative colitis is feasible for septuagenar-
ians. Color Dis. 2005;8:235–8.
6. Pinto RA, Canedo J, Murad-Regadas S, Regadas SF, Weiss EG, Wexner SD.Ileal pouch–anal
anastomosis in elderly patients: is there a difference in morbidity compared with younger
patients? Color Dis. 2010;13:177–83.
7. Pellino G, Sciaudone G, Candilio G, De Fatico GS, Landino I, Canonico S, Selvaggi
F. Restorative proctocolectomy with ileal pouch-anal anastomosis is safe and effective in
selected very elderly patients suffering from ulcerative colitis. Int J Surg. 2014;12:S56–9.
8. Ananthakrishnan AN, McGinley EL, Binion DG.Inammatory bowel disease in the elderly
is associated with worse outcomes: a national study of hospitalizations. Inamm Bowel Dis.
2009;15(2):182–9.
9. Chapman JR, Larson DW, Wolff BG, Dozois EJ, Cima RR, Pemberton JH, Crownhart BS,
Larson DR. Ileal pouch-anal anastomosis, does age at the time of surgery affect outcome?
Arch Surg. 2005;140:534–40.
10. Tan HT, Connolly AB, Morton D, Keighley MR.Results of restorative proctocolectomy in the
elderly. Int J Color Dis. 1997;12:319–22.
11. Dayton MT, Larsen KR.Should older patients undergo ileal pouch-anal anastomosis? Am J
Surg. 1996;172:444–8.
31 Surgical Approach totheOlder Ulcerative Colitis Patient
284
12. Delaney CP, Fazio VW, Remzi FH, Hammel J, Church JM, Hull TL, Senagore AJ, Strong SA,
Lavery IC.Prospective, age-related analysis of surgical results, functional outcome, and qual-
ity of life after ileal pouch-anal anastomosis. Ann Surg. 2003;238:221–8.
13. Delaney CP, Dadvand B, Remzi FH, Church JM, Fazio VW. Functional outcome, quality of
life, and complications after ileal pouch-anal anastomosis in selected septuagenarians. Dis
Colon Rectum. 2002;45:890–4.
14. Ross H, Steele SR, Varma M, Dykes S, Cima R, Buie WD, Rafferty J.Practice parameters for
the surgical treatment of ulcerative colitis. Dis Colon Rectum. 2014;57:5–22.
15. Magro F, Gionchetti P, Eliakim R, et al. for the European Crohn’s and Colitis Organisation
(ECCO). Third European evidence-based consensus on diagnosis and management of ulcer-
ative colitis. Part 1: Denitions, diagnosis, extra-intestinal manifestations, pregnancy, cancer
surveillance, surgery, and ileo-anal pouch disorders. J Crohns Colitis. 2017;11:649–70.
H. Kunitake and L. Bordeianou