Article

Impact of long-term enteral nutrition on clinical and endoscopic recurrence after resection for Crohn's disease: A prospective, non-randomized, parallel, controlled study

Inflammatory Bowel Disease Centre & Department of Surgery, Yokkaichi Social Insurance Hospital, Yokkaichi, Mie, Japan.
Alimentary Pharmacology & Therapeutics (Impact Factor: 5.73). 02/2007; 25(1):67-72. DOI: 10.1111/j.1365-2036.2006.03158.x
Source: PubMed

ABSTRACT

The impact of enteral nutrition on post-operative recurrence has not been properly examined.
To investigate the impact of enteral nutrition using an elemental diet on clinical and endoscopic recurrence after resection for Crohn's disease.
Forty consecutive patients who underwent resection for ileal or ileocolonic Crohn's disease were studied. After operation, 20 patients continuously received enteral nutritional therapy (EN group), and 20 had neither nutritional therapy nor food restriction (non-EN group). In the EN group, enteral formula (Elental) was infused through a nasogastric tube in the night-time, and low fat foods were taken in the daytime. All patients were followed up regularly for 1 year after operation. Ileocolonoscopy was performed at 6 and 12 months after operation.
One patient (5%) in the EN group and seven (35%) in the non-EN group developed clinical recurrence during 1-year follow-up (P = 0.048). Six months after operation, five patients (25%) in the EN group and eight (40%) in the non-EN group developed endoscopic recurrence (P = 0.50). Twelve months after operation, endoscopic recurrence was observed in six patients (30%) in the EN group and 14 (70%) in the non-EN group (P = 0.027).
Our long-term enteral nutritional therapy significantly reduced clinical and endoscopic recurrence after resection for Crohn's disease.

Full-text

Available from: Takayuki Yamamoto, May 28, 2014
Impact of long-term enteral nutrition on clinical and endoscopic
recurrence after resection for Crohn’s disease: a prospective,
non-randomized, parallel, controlled study
T.YAMAMOTO,M.NAKAHIGASHI,S.UMEGAE,T.KITAGAWA&K.MATSUMOTO
Inflammatory Bowel Disease Centre &
Department of Surgery, Yokkaichi
Social Insurance Hospital, Yokkaichi,
Mie, Japan
Correspondence to:
Dr T. Yamamoto, Inflammatory Bowel
Disease Centre & Department of
Surgery, Yokkaichi Social Insurance
Hospital, 10-8 Hazuyamacho,
Yokkaichi, Mie 510-0016, Japan.
E-mail: nao-taka@sannet.ne.jp
Publication data
Submitted 23 August 2006
First decision 11 September 2006
Resubmitted 14 September 2006
Accepted 14 September 2006
SUMMARY
Background
The impact of enteral nutrition on post-operative recurrence has not
been properly examined.
Aim
To investigate the impact of enteral nutrition using an elemental diet
on clinical and endoscopic recurrence after resection for Crohn’s
disease.
Methods
Forty consecutive patients who underwent resection for ileal or ileoco-
lonic Crohn’s disease were studied. After operation, 20 patients continu-
ously received enteral nutritional therapy (EN group), and 20 had
neither nutritional therapy nor food restriction (non-EN group). In the
EN group, enteral formula (Elental) was infused through a nasogastric
tube in the night-time, and low fat foods were taken in the daytime. All
patients were followed up regularly for 1 year after operation. Ileo-
colonoscopy was performed at 6 and 12 months after operation.
Results
One patient (5%) in the EN group and seven (35%) in the non-EN group
developed clinical recurrence during 1-year follow-up (P ¼ 0.048). Six
months after operation, five patients (25%) in the EN group and eight
(40%) in the non-EN group developed endoscopic recurrence (P ¼ 0.50).
Twelve months after operation, endoscopic recurrence was observed in
six patients (30%) in the EN group and 14 (70%) in the non-EN group
(P ¼ 0.027).
Conclusions
Our long-term enteral nutritional therapy significantly reduced clinical
and endoscopic recurrence after resection for Crohn’s disease.
Aliment Pharmacol Ther 25, 67–72
Alimentary Pharmacology & Therapeutics
ª 2007 The Authors 67
Journal compilation ª 2007 Blackwell Publishing Ltd
doi:10.1111/j.1365-2036.2006.03158.x
Page 1
INTRODUCTION
Crohn’s disease is a chronic inflammatory disorder of
unknown aetiology that may affect any level of the
gastrointestinal tract.
1, 2
Because many Crohn’s disease
patients are significantly at risk for protein-calorie
malnutrition, nutrition supp ort can be an important
adjunct to medical therapy.
3–5
While the mechanism is
uncertain, nutrition support also has a primary role in
inducing remission in patients with active Crohn’s dis-
ease.
3–5
Elemental diet is a liquid diet, made up of free
amino acids, carbohydrates and fats. These can be
absorbed without further digestion, and can cause a
remission of the disease. In our previous study,
6
we
confirmed that elemental diet therapy induced clinical
remission along with a reduction in mucosal inflam-
mation and mucosal healing in the majority of
patients with active Crohn’s disease. However, it has
not been fully examined whether enteral nutrition is
useful in maintaining remission and reducing recur-
rence after operation for Crohn’s disease.
Prior to this study, we had started a randomized-
controlled trial comparing post-operative recurrence
rates between patients treated with and without long-
term enteral nutrition. However, in the enteral nutri-
tion group, many patients could not continue the
treatment because of lack of compliance. We had to
stop the randomized trial and change the study design.
Thus, a significant problem with enteral nutritional
therapy is patient compliance. In our institution, all
patients were treated with the enteral nutrition at least
one time before operation, and treatment compliance
was preoperatively assessed in each patient. In this
study, only patients with high compliance were treated
with post-operative enteral nutrition, while for patients
with low compliance enteral nutrition was not given.
The purpose of this prospective study was to examine
whether long-term enteral nutrition (elemental diet
infusion in the night-time and a low fat diet in the
daytime) is useful in reducing clinical and endoscopic
recurrence rates after resection for Crohn’s disease.
METHODS
Patients
This study was a prospective, non-randomized parallel,
controlled trial. The study was conducted in accord-
ance with the principle of good clinical practice, the
Declaration of Helsinki and the study protocol was
approved by our Institutional Review Board. Inclusion
criteria were: (i) age between 15 and 75 years; (ii)
patient who had endoscopic and histological diagnosis
of Cr ohn’s disease; (iii) those who required resection
for ileal and ileocolonic (including ileocaecal) Crohn’s
disease; (iv) those who received enteral nutritional
therapy including elemental diet infusion at least one
time before operation; (v) those who agreed to con-
tinue assigned treatment (with or without enteral
nutrition) for more than 1 year after operation and (vi)
those who agreed to have ileocolonoscopy after opera-
tion even if they did not have any clinical symptoms.
Patients with colonic Crohn’s disease alone or with
diffuse small bowel Crohn’s disease were excluded
from the study.
Forty consecutive patients (26 males; mean age
32 years) who required resection for ileal or ileocolon-
ic Crohn’s disease were studied. The mea n duration
from diagnosis of Crohn’s disease to operation was
38 months. Four patients were smokers at the time of
operation. Eight patients had had previous ileocaecal
resection for Crohn’s disease. All except three patients
were treated with corticosteroids (prednisolone,
5–40 mg/day) for more than 1 month immediately
before operation. Thirty-one patients were also receiv-
ing mesalazine (Pentasa, 750–3000 mg/d ay). In all
patients, the main indication for surgery was bowel
obstruction. Four patients had a concomitant enteric
fistula or abscess. Twelve patients underwent ileal
resection for term inal ileal disease, 20 patients under-
went ileocolonic resection for primary ileocolonic dis-
ease and eight patie nts underwent ileocolonic resection
for anastomotic recurrence after primary ileocaecal
resection. In all patients, after bowel resection, a stapled
functional end-to-end anastomosis
7
was performed
without a covering ileostomy. We confirmed that
macroscopic disease was not remaining at the site of an-
astomosis, and that there was no macroscopic involve-
ment at the resection margins in the resected specimen.
Post-operative treatment
The purpose of this study was to investigate the effic-
acy of long-term enteral nutrition; nocturnal elemental
diet infusion and a low fat diet in the daytime. Before
operation, all patients had experienced elemental diet
infusion through a self-intubated nasogastric tube
using an infusion pump. Treatment compliance was
assessed in each patient; half of the patients (with low
compliance) could not afford to continue the treatment
68 T. YAMAMOTO et al.
ª 2007 The Authors, Aliment Pharmacol Ther 25, 67–72
Journal compilation ª 2007 Blackwell Publishing Ltd
Page 2
because they could not insert a nasogastric tube, or
because they often developed severe diarrhoea, or
abdominal distension or colic during the treatment. In
contrast, the remaining half of the patients (with high
compliance) had no serious problems during the ele-
mental diet infus ion, but actually the majority of them
did not continue the treatment merely because they
did not like it, or because the treatment was tiresome.
After giving informed consent, 20 patients with high
compliance were assigned to enteral nutrition group
(EN group), and the remaining 20 pa tients with low
compliance were assigned to non-enteral nutrition
group (non-EN group). All patients agreed to continue
the assigned treatment for more than 1 year after
operation.
In the EN group, the elemental diet infusion was
started approximately 1 week after operation if there
were no anastomotic complications. The enteral for-
mula was a commercially available Elental (Ajinomoto,
Tokyo, Japan), which is composed of amino acids,
very little fat, vitamins, trace elements and a major
energy source, dextrin. A summary of the composition
of Elental was shown in the previous study.
6
The cal-
orie density was 1 kcal/mL with an osmolarity of
760 mOsm/L. In the night-time, the elemental formula
was infused continuously through a silicone-elastomer
nasogastric tube using an infusion pump. The nasogas -
tric tube was self-intubated every night. The concen-
tration of the elemental diet was gradually increased
from one-third to the full strength over 10 days (adap-
tation phase) to reduce side effects , such as diarrhoea
and abdominal colic. The infusion speed was also
increased stepwise from 20 mL/h to the full-dose
(100–150 mL/h) over 10 days (adaptation phase). After
the adaptation phase, a maintenance dose at the full
strength was administered in the nig ht-time (for
6–10 h). The volume of the elemental diet infused per
night was 1200–1800 mL. In the daytime, low fat
foods (20–30 g/day) were taken according to the
instructions of their dieticians. The daily calorie intake
was approximately 35–40 kcal/kg body weight;
approximately half of the calorie was obt ained from
the elemental diet therapy. This enteral nutritional
therapy was continued at their home for more than
1 year after operation. The majority of the patients
experienced diarrhoea, or abdominal distension or
colic during the elemental infusion. These symptoms
were treated with temporary decreases in the infusion
speed. The diarrhoea sometimes required antidiarrhoeal
drugs (loperamide or codeine). However, these abdom-
inal symptoms were not serious and could be con-
trolled without an interruption of the treatment in all
patients. Our nutritional support team and dieticians
regularly interviewed patients to check whether their
enteral nutritional therapy was being performed
appropriately. In contrast, in the non-EN group,
patients had neither any nutritional therapy nor any
food restriction during the entire study.
After operation, all patients in both groups received
mesalazine (Pentasa, 3000 mg/day) during the entire
study. No patients received corticosteroids, immuno-
suppressive drugs or infliximab before recurrent symp-
toms occurred.
Follow-up
All patients were reviewed monthly in our clinic after
discharge. At clinic, peripheral venous blood samples
were collected for measurements of white cell count,
haemoglobin, platelet count, erythrocyte sedimentation
rate, C-reactive protein and albumin. The disease
activity was assessed according to a Crohn’s disease
activity index (CDAI).
8
Clinical recurrence was defined
as the CDAI score of 150. Ileocolonoscopy was per-
formed for all patients at 6 and 12 months after
operation, and endoscopic recurrence was defined as
the Rutgeerts score 2.
9
Endoscopic investigators were
blind to patient status.
Statistical analysis
Comparisons of frequencies were analysed using the
chi-square test with Yates’ correction. The mean values
between two groups were compared using the
unpaired Student’s t-test. P-values of <0.05 was con-
sidered to be statistically significant.
RESULTS
Patients within each treatment group were well
matched in terms of age, sex, duration of Crohn’s dis-
ease before operation, smoking history, previous
operation, disease location, indication for resection,
and preoperative and post-operative medication
(
Table 1).
All patients in the EN group could continue their
enteral nutrition therapy for more than 1 year after
operation. Clinical and endoscopic recurrence rates in
each group are shown in
Table 2. During the 1-year
follow-up, one patient (5%) in the EN group and sev en
ENTERAL NUTRITION FOR CROHN’S DISEASE 69
ª 2007 The Authors, Aliment Pharmacol Ther 25, 67–72
Journal compilation ª 2007 Blackwell Publishing Ltd
Page 3
(35%) in the non-EN group developed clinical recur-
rence (odds ratio, 10.2; P ¼ 0.048). The mean duration
from operation to clinical recurrence was 10 (range:
7–11) months. All of eight patients who developed
clinical recurrence were treated with oral corticoster-
oids (prednisolone, 20–30 mg/da y). After 1-month
treatment, their clinical symptoms were relieved, and
all patients achieved clinical remission.
Six months after operation, five patients (25%) in
the EN group and eight (40%) in the non-EN group
developed endoscopic recurrence (odds ratio, 2.0; P ¼
0.50). Twelve months after operation, endoscopic
recurrence was observed in six patients (30%) in the
EN group and 14 (70%) in the non-EN group (odds
ratio, 5.4; P ¼ 0.027). Endoscopic recurrence was
observed in the ileum proximal to the anastomosis in
all patients. In both groups, all patients who had endo-
scopic recurrence at 6 months after operation had
recurrence at 12 months as well. All patients who
developed clinical recurrence had endoscopic recur-
rence at 6 months after operation.
DISCUSSION
In Crohn’s disease, ileal or ileocaecal disease is the
most common presentation.
1, 2
After resection for Cro-
hn’s disease, post-operative recurrence is common,
and the disease recurs at the site of anastomosis in
most patients.
1, 2
In our literature review,
10
there are
several factors affecting recurrence after operation for
Crohn’s disease. The most significant factor was smo-
king. Several randomized-controlled trials offered
evidence of the efficacy of mesalazine and immuno-
suppressive drugs [azathioprine and mercaptopurine
(6-mercaptopurine)] in reducing post-operative recur-
rence. Several retrospective studies
11, 12
reported that
enteral nutritional therapy reduced recurrence after
surgery for Crohn’s disease. However, the impact of
enteral nutrition on post-operative recurrence has not
been prospectively examined in well-designed studies.
Prior to this study, the randomized-controlled trial
was not practical because patients with low compli-
ance could not continue our enteral nutritional ther-
apy. In this study, according to patient compliance
assessed preoperatively, we assigned patients with high
compliance to the enteral nutrition group, and those
with low compliance to the non-enteral nutrition
group. As a result, all patients in the enteral nutrition
group could complete the 1-year treatment in this
study, and they are now continuing the treatment
without any problems.
In this study, patients within each treatment group
were well matched in terms of patient demography,
smoking habit, disease location, indication for surgery
Table 1. Demographic characteristics and disease history
EN group
(n ¼ 20)
Non-EN
group
(n ¼ 20) P-value
Age (mean S.E.; years) 31 3.7 33 3.9 0.10
Male:female 12:8 14:6 0.74
Duration of Crohn’s disease
before operation
(mean S.E.; months)
37 7.1 39 8.2 0.41
Smoker (n) 2 2 >0.99
Previous operation (n) 4 4 >0.99
Disease location (n) 0.77
Terminal ileum 5 7
Terminal ileum and colon 11 9
Ileocolonic anastomosis 4 4
Indication for resection (n)
Bowel obstruction 20 20
Concomitant abscess
or fistula
2 2 >0.99
Preoperative medication (n)
Corticosteroids 18 19 >0.99
Mesalazine 14 17 0.45
Immunosuppressive drugs
or infliximab
00
Post-operative
medication* (n)
Corticosteroids 0 0
Mesalazine 20 20
Immunosuppressive drugs
or infliximab
00
* Before clinical recurrence occurred.
Table 2. Clinical and endoscopic recurrence rates after
operation
EN group
[n ¼ 20;
n (%)]
Non-EN group
[n ¼ 20;
n (%)] P-value
Clinical recurrence during
1-year follow-up
1 (5) 7 (35) 0.048
Endoscopic recurrence
6 months after
operation
5 (25) 8 (40) 0.50
12 months after
operation
6 (30) 14 (70) 0.027
70 T. YAMAMOTO et al.
ª 2007 The Authors, Aliment Pharmacol Ther 25, 67–72
Journal compilation ª 2007 Blackwell Publishing Ltd
Page 4
and medication. Further, after operation, all patients
received mesalazine (Pentasa, 3000 mg/day) during the
entire study. No patients received prophylactic admin-
istration of corticosteroids, immunosuppressive drugs
or infliximab before recurrent symptoms occurred.
We assessed both clinical and endoscopic disease
activities because clinical symptoms were not always
related to recurrent Crohn’s disease. In this study, we
confirmed that macroscopic disease was curatively
resected at operation. Endoscopic recurrence increased
with time (overall, 33% at 6 months vs. 50% at
12 months after operation), and occurred in the ileum
proximal to the anastomosis in all patients. Endo-
scopic recurrence rate was much higher than clinical
recurrence rate (overall, 20%). Clinical recurrence
occurred from 7 to 11 months after operation. Further,
all patients developing clinical recurrence had endo-
scopic recurrence at 6 months after operation.
Our enteral nutritional therapy significantly reduced
both clinical and endoscopic recurrence rates after
resection for Crohn’s disease. In the enteral nutrition
group, only one patient developed endoscopic recur-
rence between 6 and 12 months after operation,
whereas six patients in the non-enteral nutrition group
developed endoscopic recurrence during the same per-
iod. Thus, our enteral nutritional therapy was useful in
maintaining endoscopic remission after operation. With
a longer follow-up, reoperation rate for recurrence may
also be reduced in the enteral nutrition group.
In our previous study,
6
28 patients with active Cro-
hn’s di sease were treated with the same elemental diet
therapy for 4 weeks. After treatment, clinical remission
was ac hieved in 71% of patients. Endoscopic healing
and improvement rates were 44% and 76% in the ter-
minal ileum and 39% and 78% in the large bowel,
respectively. Histological healing and improvement
rates were 19% and 54% in the terminal ileum and
20% and 55% in the large bowel, respectively. The
mucosal concentrations of interleukin (IL)-1b, IL-6,
IL-8 and tumour necrosis factor (TNF)-a in both the
ileum and the large bowel significantly decreased after
treatment. We found that the endoscopic and histo-
logical healing of the mucosal inflammation was asso-
ciated with a decline of the mucosal cytokines.
The mechanism of action of enteral nutrition using
elemental diet remains unclear. Elemental diet has
minimal fat content, <2% of total calories. The restric-
tion of fat associated with the use of elementa l diet
might alter the ratio of eicosanoids (leukotriene B
4
,
thromboxane A
2
, prostaglandin E
2
) with subsequent
downregulation of the inflammatory cascade.
13
Ele-
mental diet may inhibit intestinal immune responses
by reducing the number of cytokine-producing cells.
The efficacy of enteral nutri tion includes improvement
in intestinal permeability leading to decreased antigen
uptake and less stimulation of gut-associated immune
system, improved cell-mediated immu nity and altered
bowel flora.
14–16
However, the detailed mechanism by
which entera l nutrition exerts the therapeutic and
immunological effects in Crohn’s disease remains
unknown. Further investigations are necessary.
In conclusion, our long-term enteral nutritional ther-
apy significantly reduced clinical and endoscopic recur-
rence after resection for Crohn’s disease. In other words,
patients who could continue our treatment had a
reduced recurrence rate after operation. As stated
before, a significant problem with enteral nutrition is
patient compliance. Poor palatability of the elemental
diet often limits the patient’s ability to continue the
treatment; however, this could be circumvented by the
usage of a nasogastric feeding tube. The nasogastric
tube was intubated without any difficulties because the
tube is thin and soft. We recommend that patients with
Crohn’s disease have our enteral nutritional therapy to
reduce recurrence and maintain remission after opera-
tion. However, this is a small, non-randomized and
non-blinded study. To assess a definite efficacy of our
enteral nutritional therapy, a randomized-controlled
trial with a larger number of patients is necessary.
ACKNOWLEDGEMENT
No externa l funding was received for this study.
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Page 6
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    [Show abstract] [Hide abstract] ABSTRACT: Each of the medical and surgical therapies for Crohn’s disease has inherent advantages and disadvantages that must be balanced for patients with moderate to severe disease. Most patients with Crohn’s disease require surgery at some point during the lifelong illness, but surgical therapy is not curative for most patients, as postoperative recurrence of Crohn’s disease is common and can pose diagnostic and therapeutic challenges. Disease monitoring and appropriate prophylaxis are necessary in patients at high risk.
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    [Show abstract] [Hide abstract] ABSTRACT: Long-term enteral nutrition may maintain clinical and endoscopic remission in patients with Crohn's disease (CD). The aim of this prospective study was to investigate the impacts of long-term enteral nutrition on clinical and endoscopic disease activities and mucosal tissue cytokines in patients with quiescent CD. Forty patients with CD who achieved clinical remission were included. Of these, 20 received continuous elemental diet (Elental) infusion during the nighttime and a low-fat diet during the daytime (EN group) and 20 received neither nutritional therapy nor food restriction (non-EN group). With these regimens, all 40 patients were monitored for 1 year. Further, ileocolonoscopy was performed at entry, at 6 and 12 months, and mucosal biopsies were taken for cytokine assays. On an intention-to-treat basis, 5 patients (25%) in the EN group and 13 (65%) in the non-EN group had a clinical relapse during the 1-year observation (P = 0.03). The mean endoscopic inflammation (EI) scores were not significantly different between the groups at both entry and 6 months, but at 12 months EI scores were significantly higher in the non-EN group than in the EN group (P = 0.04). Additionally, the mucosal tissue interleukin (IL)-1beta, IL-6, and tumor necrosis factor (TNF)-alpha levels significantly increased with time in the non-EN group (entry versus 12 months, IL-1beta, P = 0.02; IL-6, P = 0.002; TNF-alpha, P = 0.001). In the EN group these cytokines did not show a significant increase. Long-term enteral nutrition in patients with quiescent CD has a clear suppressive effect on clinical and endoscopic disease activities and the mucosal inflammatory cytokine levels.
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