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244
Initial studies date back to 1997 when Wu reported on 116 patients undergoing
laparoscopic and open surgery for primary as well as recurrent Crohn’s disease. Ten
patients underwent laparoscopic surgery for recurrent ileocolic disease with a con-
version rate of 20% to the open approach [10].
Following that initial experience, several studies have continued to show that
laparoscopic surgery for recurrent Crohn’s disease is both feasible and safe.
Specically, morbidity rates were comparable between primary and recurrent lapa-
roscopic resections and most studies did not report an increased conversion rate.
When conversion to the open approach did occur, it was typically associated with
the complexity of the disease, with rates widely ranging from 0% to 31% [11–15].
In 2010, Brouquet [16] conducted an elegant study where two groups with recur-
rent Crohn’s disease treated by laparoscopy or conventional open surgery were
compared. Overall, 33 procedures were performed in 28 patients. The study included
some patients who had previously undergone open surgery. Conversion rates were
as high as 31% and abandonment of a laparoscopic approach was mainly due to
intestinal injury, intraoperative ndings of entero-enteric stulas, or challenging
intraperitoneal adhesions. The complication and postoperative morbidity rates were
comparative between the laparoscopic and open approaches. In this study the lapa-
roscopic approach was recommended for selected patients with recurrent Crohn’s
disease recurrence who had less than three previous abdominal surgeries, no previ-
ous history of peritonitis, and non-stulizing disease.
However, it was still unclear whether previous open surgery increased the risk of
conversion from a laparoscopic to open approach when surgery was required for
recurrent disease [17, 18]. Huang [19] in 2012 commented on their experience with
the laparoscopic management of recurrent Crohn’s disease in 130 patients. Prior
Crohn’s disease-related abdominal surgery was recorded as well as operative times,
conversion rates, and complication rates. Thirty-seven percent of the patients who
were included in the study had undergone previous open abdominal surgery, which
resulted in no statistically signicant increase in the subsequent laparoscopic opera-
tive times, blood loss, or conversion rates. Postoperative morbidity was also compa-
rable between the two groups. It was concluded from this study that the laparoscopic
approach is safe and feasible for patients who had undergone previous open surgery,
and may in fact reduce further morbidity in this group of patients, as they might
require even more surgery in the future.
With improvements in the learning curves and more of this complex surgery
being done in specialty centers, the data has suggested improvement in clinical and
surgical outcomes.
Moftah in 2014 reported excellent outcomes using a single-port technique [20]
in a series of 33 patients of which 6 were recurrent cases. In a more recent study
from 2017 by Leo [21], sixteen patients underwent single-port laparoscopic surgery
for recurrent Crohn’s disease, 9 of whom had previous open surgery and 7 had lapa-
roscopic surgery. The morbidity was comparable, and the conversion rate was only
0.3%.
Another recently published study iterated the safety and feasibility message
about minimally invasive surgery for recurrent Crohn’s disease. Celentano [22]
N. A. Yassin and A. Spinelli
245
compared patients operated by laparoscopy for recurrent ileocolic Crohn’s dis-
ease and a history of two or more previous laparotomies, with 90 patients operated
for primary ileocolic Crohn’s disease and no history of previous abdominal sur-
gery. Morbidity and conversion rates were similar in the two groups, but operative
time was longer in recurrent patients with a history of previous abdominal
surgery.
Recommendations
Minimally invasive surgery represents a feasible and safe option for patients with
recurrent ileocolic Crohn’s disease leading to improved short-term outcomes.
(Evidence: Low; Recommendation: Moderate).
Personal View
Minimally invasive surgery for recurrent Crohn’s disease is feasible and can be
safely performed by experts. Although the evidence to support such a practice still
relies on cohort studies and case series, we approach most recurrent ileocolic
Crohn’s disease cases laparoscopically. Furthermore, we use single-port surgery
[28] to access the peritoneum in a safe, open technique. In cases with massive
entero-enteric adhesions where the operation may not be safely completed by lapa-
roscopy, proceeding with open surgery is made simple by enlarging the single
access site. This approach is combined with a low threshold for conversion that does
not introduce additional risk or loss of time.
References
1. Gomollón F, Dignass A, Annese V, Tilg H, Van Assche G, Lindsay JO, etal. 3rd European
evidence-based consensus on the diagnosis and management of Crohn’s disease 2016: Part 1:
Diagnosis and medical management. J Crohns Colitis. 2017;11(1):3–25.
2. Lapidus A, Bernell O, Hellers G, Löfberg R.Clinical course of colorectal Crohn’s disease: a
35-year follow-up study of 507 patients. Gastroenterology. 1998;114(6):1151–60.
3. Shaffer VO, Wexner SD.Surgical management of Crohn’s disease. Langenbecks Arch Surg.
2013;398(1):13–27.
4. Bernell O, Lapidus A, Hellers G.Risk factors for surgery and recurrence in 907 patients with
primary ileocaecal Crohn’s disease. Br J Surg. 2000;87(12):1697–701.
5. Bazzi P, Montorsi M, Spinelli A. Minimally invasive surgery in Crohn’s disease. Ann
Gastroenterol Q Publ Hell Soc Gastroenterol. 2011;24(4):276–9.
6. Bemelman WA, Warusavitarne J, Sampietro GM, Serclova Z, Zmora O, Luglio G, et al.
ECCO-ESCP consensus on surgery for Crohn’s Disease. J Crohns Colitis. 2017;12(1):1–16.
7. Kirat HT, Pokala N, Vogel JD, Fazio VW, Kiran RP.Can laparoscopic ileocolic resection be
performed with comparable safety to open surgery for regional enteritis: data from National
Surgical Quality Improvement Program. Am Surg. 2010;76(12):1393–6.
8. Maggiori L, Panis Y.Surgical management of IBD—from an open to a laparoscopic approach.
Nat Rev Gastroenterol Hepatol. 2013;10(5):297–306.
26 Role ofMinimally Invasive Reoperative Surgery
246
9. Lee Y, Fleming FJ, Deeb A-P, Gunzler D, Messing S, Monson JRT.A laparoscopic approach
reduces short-term complications and length of stay following ileocolic resection in Crohn’s
disease: an analysis of outcomes from the NSQIP database. Colorectal Dis. 2012;14(5):572–7.
10. Wu JS, Birnbaum EH, Kodner IJ, Fry RD, Read TE, Fleshman JW. Laparoscopic-assisted
ileocolic resections in patients with Crohn’s disease: are abscesses, phlegmons, or recurrent
disease contraindications? Surgery. 1997;122(4):682–8.
11. Hasegawa H, Watanabe M, Nishibori H, Okabayashi K, Hibi T, Kitajima M.Laparoscopic
surgery for recurrent Crohn’s disease. Br J Surg. 2003;90(8):970–3.
12. Moorthy K, Shaul T, Foley RJ.Factors that predict conversion in patients undergoing laparo-
scopic surgery for Crohn’s disease. Am J Surg. 2004;187(1):47–51.
13. Uchikoshi F, Ito T, Nezu R, Tanemura M, Kai Y, Mizushima T, etal. Advantages of laparoscope-
assisted surgery for recurrent Crohn disease. Surg Endosc. 2004;18(11):1675–9.
14. Lawes DA, Motson RW.Avoidance of laparotomy for recurrent disease is a long-term benet
of laparoscopic resection for Crohn’s disease. Br J Surg. 2006;93(5):607–8.
15. Edden Y, Ciardullo J, Sherafgan K, Harris MT, Bub DS, Gorne SR, et al. Laparoscopic-
assisted ileocolic resection for Crohn’s disease. JSLS. 2008;12(2):139–42.
16. Brouquet A, Bretagnol F, Soprani A, Valleur P, Bouhnik Y, Panis Y.A laparoscopic approach
to iterative ileocolonic resection for the recurrence of Crohn’s disease. Surg Endosc.
2010;24(4):879–87.
17. Maggiori L, Cook MC, Bretagnol F, Ferron M, Alves A, Panis Y.Prior abdominal open sur-
gery does not impair outcomes of laparoscopic colorectal surgery: a case-control study in 367
patients. Colorectal Dis. 2013;15(2):236–43.
18. Aytac E, Stocchi L, Remzi FH, Kiran RP.Is laparoscopic surgery for recurrent Crohn’s disease
benecial in patients with previous primary resection through midline laparotomy? A case-
matched study. Surg Endosc. 2012;26(12):3552–6.
19. Huang R, Valerian BT, Lee EC.Laparoscopic approach in patients with recurrent Crohn’s
disease. Am Surg. 2012;78(5):595–9.
20. Moftah M, Nazour F, Cunningham M, Cahill RA.Single port laparoscopic surgery for patients
with complex and recurrent Crohn’s disease. J Crohns Colitis. 2014;8(9):1055–61.
21. Leo CA, Samaranayake SF, Chandrasinghe PC, Shaikh IA, Hodgkinson JD, Warusavitarne
JH.Single port laparoscopic surgery for complex Crohn’s disease is safe with a lower conver-
sion rate. J Laparoendosc Adv Surg Tech A. 2017;27(11):1095–100.
22. Celentano V, Sagias F, Flashman KG, Conti J, Khan J.Laparoscopic redo ileocolic resec-
tion for Crohn’s disease in patients with previous multiple laparotomies. Scand J Surg. 2018;
https://doi.org/10.1177/1457496918772370.
23. Holubar SD, Dozois EJ, Privitera A, Cima RR, Pemberton JH, Young-Fadok T, Larson
DW. Laparoscopic surgery for recurrent ileocolic Crohnʼs disease. Inamm Bowel Dis.
2010;16(8):1382–6.
24. Chaudhary B, Glancy D, Dixon AR.Laparoscopic surgery for recurrent ileocolic Crohn’s dis-
ease is as safe and effective as primary resection. Colorectal Dis. 2011;13(12):1413–6.
25. Pinto RA, Shawki S, Narita K, Weiss EG, Wexner SD.Laparoscopy for recurrent Crohn’s
disease: how do the results compare with the results for primary Crohn’s disease? Colorectal
Dis. 2011;13(3):302–7.
26. Bandyopadhyay D, Sagar PM, Mirnezami A, Lengyel J, Morrison C, Gatt M.Laparoscopic
resection for recurrent Crohn’s disease: safety, feasibility and short-term outcomes. Colorectal
Dis. 2011;13(2):161–5.
27. Panteleimonitis S, Ahmed J, Parker T, Qureshi T, Parvaiz A.Laparoscopic resection for pri-
mary and recurrent Crohn’s disease: A case series of over 100 consecutive cases. Int J Surg.
2017;47:69–76.
28. Carvello M, de Groof EJ, de Buck van Overstraeten A, Sacchi M, Wolthuis AM, Buskens CJ,
etal. Single port laparoscopic ileocaecal resection for Crohn’s disease: a multicentre compari-
son with multi-port laparoscopy. Colorectal Dis. 2018;20(1):53–8.
N. A. Yassin and A. Spinelli
247
© Springer Nature Switzerland AG 2019
N. Hyman et al. (eds.), Mastery of IBD Surgery,
https://doi.org/10.1007/978-3-030-16755-4_27
M. G. Kiernan
Graduate Entry Medical School, University of Limerick, Limerick, Ireland
4i Centre for Interventions in Infection, Inammation and Immunity, University of Limerick,
Limerick, Ireland
J. C. Coffey (
*)
Graduate Entry Medical School, University of Limerick, Limerick, Ireland
4i Centre for Interventions in Infection, Inammation and Immunity, University of Limerick,
Limerick, Ireland
Department of Surgery, University Hospital Group Limerick, Limerick, Ireland
e-mail: Calvin.Coffey@ul.ie
27
Extent ofMesenteric Resection
MirandaG.Kiernan andJ.CalvinCoffey
Introduction
Rates of surgery in Crohn’s disease have remained largely unchanged [1]. Indeed, a
rather substantial proportion of patients with Crohn’s disease continue to require
one of more operations. In addition, the proportion requiring re-operation is also
signicant with rates varying between 4% and 60% [2–19].
Recent clarications of mesenteric anatomy have identied and claried the fas-
cial and peritoneal landscape associated with the small and large intestine [20]. In
addition, data increasingly points to a pathobiological role for the mesentery in
Crohn’s disease [2, 21]. Mesenteric-based surgical treatment strategies have become
the gold standard in colorectal surgical practice in the management of colon and
rectal cancer, but not in management of Crohn’s disease [22].
The conventional surgical approach in Crohn’s disease is to divide the mesentery
ush with the intestine [2]. Alternatively, surgeons divide the mesentery at the rst
level they regard as safe to divide. The result is that the mesentery is retained. This
conservative approach arose mainly from concerns regarding the possibility of
intraoperative hemorrhage. In Crohn’s disease, the diseased mesentery is often
friable and inamed and bleeds readily on division. This means that in simple
248
separation of components of a phlegmon, which generally include broad areas of
mesentery, bleeding can be extensive [2, 20, 21, 23–26].
Emerging data indicates that pathobiological events primarily occur along two
major axes in Crohn’s disease. These are the circumferential (i.e., submucosal) and
radial (i.e., mesenteric) axes. Whilst disease appears to arise in these locations,
spread from here ultimately involves the mucosa whilst also generating the trans-
mural appearance characteristic of Crohn’s disease. Where the radial and circumfer-
ential axes intersect, inammation is most intense and results in ulceration. Several
observations support this model. For example, mucosal ulceration always com-
mences at the intersection of the mesentery and mucosa (i.e., where axes meet) [21,
27–32]. A detailed review of the data supporting this model is beyond the scope of
this chapter, but the concept of circumferential and radial axes of pathobiology is
surgically relevant and is the basis for mesenteric resection (Table27.1).
Search Strategy
A comprehensive literature search of Cochrane Database of Collected Research,
EMBASE, MEDLINE, and PubMed was performed to identify all the English-
language publications related to wide and limited mesenteric resection, Crohn’s
disease and outcomes from 1911 to 2018. Key search terms included the following:
“mesentery,” “Crohn’s disease,” “convention”, “ileocolic”, “resection.” The refer-
ences of the included studies were reviewed to identify additional studies that were
incorporated as appropriate.
Results
Only two studies were identied that compare different forms of mesenteric
resection in Crohn’s disease [2, 33]. These, including limitations, will be described
in the following:
Our group compared conventional (mesenteric sparing) with extensive (mesen-
tery included) mesenteric resection [2]. In the test arm, the mesentery was mobi-
lized and detached back to the central/root region at the head of the pancreas, and
the mesentery was hemostatically divided at a level that approximately corre-
sponded to D2 resection (i.e., at the takeoff of the ileocolic vessel from the superior
mesenteric artery). There was a signicant reduction in the proportion of patients
who progressed to require reoperation in the group in which the mesentery was
Table 27.1 PICO table
General IBD
Patient Population Intervention Comparator
Outcomes Studied
Extent of
mesenteric
resection
Crohn's patients
requiring
resectional surgery
Wide
mesenteric
excision
Limited
mesenteric
excision
Recurrence rate,
post-op
complications
M. G. Kiernan and J. C. Coey
249
resected. On multivariate analysis this remained signicant, as did smoking status at
the time of surgery and disease phenotype.
A preliminary analysis of short-term outcomes demonstrated that inclusion of
the mesentery as part of the resection was at least as safe as conventional resection
(see Table27.2) and some complications trended towards being reduced in patients
in which the mesentery was resected.
We applied the mesenteric-based approach in the setting of ileal disease, ileoco-
lic disease, Crohn’s colitis, and in patients requiring ileal pouch resection or proc-
tectomy. This indicates that the approach may be used for a broad range of indications
in Crohn’s disease. However, the procedure was not always possible at the index
procedure. To date, six patients with ileocolic disease were unsuitable for resection
at the index operation. These patients underwent defunctioning ileostomy and reop-
eration after several months. At reoperation it was possible to resect both diseased
intestine and mesentery and restore intestinal continuity in ve patients. This sug-
gests that a staged approach may be safely adopted in patients in whom extensive
disease precludes safe resection at the rst operation.
Our study was limited in so far as a single institute was involved, and a prospec-
tive group was compared against an historic group. Notwithstanding this, the dif-
ferential between both control and test groups supports a comprehensive head to
head challenge of both approaches in the setting of a randomized, multicenter, con-
trolled, and blinded study. Several such studies are currently in progress [34, 35].
An earlier study by Ewe etal. [33] found that increased surgical radicality was
associated with increased rates of surgical recurrence and they recommended that a
non-radical approach be adopted in patients undergoing surgery for Crohn’s dis-
ease. The follow-up was limited to 3 years. It is not possible, based on the publica-
tion, to determine the technical basis of their approach (i.e. how much mesentery
was resected and how). It is also unclear as to whether the approach was standard-
ized between units involved. Finally, surgeons adopted the conventional model of
Table 27.2 Post-operative complication rates in CD patients undergoing ileocolic resection
Post-op complication/parameter
Cohort A Cohort B
P-value
Total 19 (63%) 15 (44%) 0.124 (Chi
2
test)
Surgical site infection
(including wound infection and wound
breakdown/dehiscence)
14 (47%) 9 (27%) 0.093 (Chi
2
test)
Sepsis 3 (10%) 0 (0%) 0.059 (Chi
2
test)
Intra-abdominal/pelvic collection 5 (17%) 3 (9%) 0.344 (Chi
2
test)
Anastomotic leak 3 (10%) 0 (0%) 0.059 (Chi
2
test)
Death 0 (0%) 0 (0%) N/A
Re-operation 2 (7%) 0 (0%) 0.126 (Chi
2
test)
Drainage of collection 3 (10%) 0 (0%) 0.059 (Chi
2
test)
Revision of abdominal wound 2 (7%) 0 (0%) 0.126 (Chi
2
test)
Washout 0 (0%) 1 (3%) 0.344 (Chi
2
test)
Cohort A = mesentery not included during resection (n=30), Cohort B = mesentery included dur-
ing resection (n = 34). MW-U = Mann Whitney-U test
27 Extent ofMesenteric Resection
250
mesenteric anatomy during that era. This model has been shown to be erroneous.
The importance of mesenteric-based surgery emerged during the 1990’s and mesen-
teric anatomy was updated in tandem. Thus it is unclear as to how radical Ewe etal.
were in terms of the mesenteric component of their resection.
Recommendations
The ndings regarding inclusion of the mesentery as part of a resection in ileocolic
Crohn’s disease should be considered as preliminary.
They require further investigation in the setting of trials as discussed above. In
view of our ndings we continue to include the mesentery, where safe to do so, in
ileocolic disease and in Crohn’s colitis. In the absence of data other than that from
our institute, we make the following recommendations if one is including the mes-
entery as part of the resection in Crohn’s disease.
The intestine and mesentery should be detached (but not disconnected) along
planes established during embryological development. This should be conducted as
far proximally as the head of the pancreas to allow hemostatic division of the mes-
entery and provide unimpeded access to the mesentery should difculties with
hemostasis arise.
Placement of the proximal intestinal division should be guided by mesenteric
rather than intestinal manifestations of disease. The mesenteric transition zone (see
below) should be identied and the proximal intestinal division made immediately
proximal to this. The distal intestinal and mesenteric margin should be placed at the
rst level at which both are found to be normal.
The mesentery is best divided between Kocher clamps, and suture ligated by
creating an overlapping series of ligature loops using a heavy (0.0) suture.
Overlapping suture loops ensures that all mesentery is included in the ligation (i.e.,
with no gaps in mesentery outside the ligature that could bleed or ooze after).
During mesenteric division it is important not to directly encroach on the central
region of the mesentery that contains the superior mesenteric artery and vein because
damage to either is potentially fatal. If there is a phlegmon and the components of
this cannot be separated without extensive hemorrhage, then resection should be
abandoned. It is unlikely that a Kono-S strictureplasty will be possible in this set-
ting. Options at that point include defunctioning loop ileostomy (with a staged
resection at a later point) or bypass. Our experience (albeit in a limited cohort) is
that following loop ileostomy formation, resection with restoration of intestinal
continuity usually becomes possible at a later stage.
Personal View
Mesenteric-based surgical strategies in Crohn’s disease require further exploration.
As part of this it has been suggested that they be introduced early in the treatment
paradigm of Crohn’s disease, and not just reserved for when complications arise, or
when symptoms are refractory to medical treatment [36].
M. G. Kiernan and J. C. Coey
251
If a surgeon is to conduct a mesenteric resection it is important to fully mobilize
the mesentery back to the central region at the level of the pancreas. This mobilizes
the mesentery enough to provide unimpeded access should difculties arise in rela-
tion to hemostasis [37]. An understanding of mesenteric anatomy, and how this
dictates the peritoneal landscape is essential and requires the surgeon to depart from
the classic model of mesenteric anatomy. The classic model erroneously holds that
the small intestinal region of mesentery, transverse mesocolon, and mesosigmoid,
all attach directly to the posterior abdominal wall. With recognition of mesenteric
continuity from duodenojejunal exure to anorectal junction it was recognized that
no such attachments occur [38–42]. Instead, broad regions of the mesentery (e.g.,
right and left mesocolon) atten out against and are anchored to the posterior
abdominal wall.
The importance of this anatomical property extends beyond the mesentery.
According to the classic model of anatomy, the peritoneal landscape is complex and
unpredictable as it is determined by a multiplicity of mesenteries. Mesenteric conti-
nuity means this is far from the case and the mesenteric landscape determines the
peritoneal blueprint in all cases. The peritoneal landscape is entirely predicated on
the anatomy of the mesentery and contiguous organs. Whilst it might seem that we
are laboring an anatomical point, one cannot overestimate the importance of these
concepts in a disease setting that is anatomically complex and challenging.
We do not recommend the mesentery be divided between arterial clamps or using
currently available vessel sealing devices. Whilst there may still be some oozing
even with our approach, it is readily controlled provided the mesentery has been
fully mobilized. We have rarely encountered a mesenteric hematoma using the
approaches mentioned above. When this did occur, it was controlled by mesenteric
compression, between two 10×10 swabs, placed at on either side of the mesentery
and gently compressed. It is important that the entire operative team have all equip-
ment available prior to division of the mesentery. Mesenteric hemostatic division
can be rendered challenging if adequate numbers of Kocher clamps or heavy sutures
are not immediately available throughout the process. Anesthesia staff should be
alerted to the fact that the mesentery is about to be divided.
The proximal resection margin should be placed just proximal to the transition
zone (i.e., zone where the mesentery changes from normal to abnormal) [2]. As
such, mesenteric, rather than intestinal, features of disease should be used to guide
positioning of the proximal intestinal division. Mesenteric features include thicken-
ing, swelling, fat wrapping (also called creeping fat) and loss of the angle between
the mesentery and contiguous intestine.
We do not recommend that one aims to resect all diseased mesentery. As men-
tioned above it is important not to encroach directly on the central region of the
mesentery. The benets of complete mesocolic excision (CME) are clear-cut in
terms of oncological outcome, but they do come at the price of increased short-term
complications [43, 44]. A “D3” or “CME-type” exploration of diseased mesentery
is not recommended in the setting of Crohn’s disease.
If the mesentery is severely diseased, alternative strategies may be adopted.
Accordingly, the diseased region may be taken out of circuit, using a loop ileos-
tomy. After a period of no less than three months, a repeat laparotomy can be
27 Extent ofMesenteric Resection
252
performed, and our experience is that resection with restoration of continuity is
often feasible. This should not be considered a surgical failure but rather a strategic
option. It is important that patients are aware of that possibility before both index
and subsequent operations. We recommend consultation with gastroenterological
services to determine whether patients should be placed on adjuvant medical treat-
ment during the interval between operations.
Selected cases may be completed using the laparoscopic approach. The surgeon
should not take the technical short-cuts that sometimes are adopted when using
minimally invasive techniques (i.e., incomplete mesenteric mobilization). The com-
plications that could arise due to avoidable trauma on damaged mesentery are
unforgiving. It is also likely that any case that can be laparoscopically completed
can also be achieved using the robotic approach, although this is an area for future
investigation.
The question commonly arises as to how one reconciles the excellent results
associated with the Kono-S anastomosis or strictureplasty (in which the mesentery
is retained) with the results of our series, in which the mesentery was resected [45–
50]. In the Kono-S procedure, an intestinal anastomosis is created that is circumfer-
entially free of mesenteric inputs. It is more difcult to reconcile ndings associated
with strictureplasty (in which the mesentery is retained). As mentioned above,
pathobiological events in Crohn’s disease occur along two axes. These are the cir-
cumferential submucosal axis, and the radial mesenteric axis. Following stricture-
plasty, the circumferential axis is altered and lengthened. It is likely this alters
submucosal inputs, as well as the intensity of inammatory inputs at the junction
between mesentery and intestine.
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27 Extent ofMesenteric Resection