ESPEN Guidelines on Enteral Nutrition: Surgery including ...espen.info/documents/ENSurgery.pdf ·...
Transcript of ESPEN Guidelines on Enteral Nutrition: Surgery including ...espen.info/documents/ENSurgery.pdf ·...
ARTICLE IN PRESS
Clinical Nutrition (2006) 25, 224–244
0261-5614/$ - sdoi:10.1016/j.c
Abbreviationfeeding; Norma
$For further�CorrespondE-mail addr
$$The authfor their contri
http://intl.elsevierhealth.com/journals/clnu
ESPEN GUIDELINES
ESPEN Guidelines on Enteral Nutrition:Surgery including Organ Transplantation$
A. Weimanna,�, M. Bragab, L. Harsanyic, A. Lavianod,O. Ljungqviste, P. Soetersf,DGEM:$$ K.W. Jauch, M. Kemen, J.M. Hiesmayr, T. Horbach,E.R. Kuse, K.H. Vestweber
aKlinik f. Allgemein- und Visceralchirurgie, Klinikum ‘‘St. Georg’’, Leipzig, GermanybDepartment of Surgery, San Raffaele University, Milan, Italyc1st Surgical Department, Semmelweis University, Budapest, HungarydDepartment of Clinical Medicine, Universita ‘‘La Sapienza’’ di Roma, ItalyeKarolinska Institutet, CLINTEC, Division of Surgery, Karolinska University Hospital Huddinge & Centre ofGastrointestinal Disease, Ersta Hospital, Stockholm, SwedenfDepartment of Surgery, Academic Hospital Maastricht, The Netherlands
Received 20 January 2006; accepted 20 January 2006
KEYWORDSGuideline;Clinical practice;Enteral nutrition;Tube feeding;Oral nutritionalsupplements;Surgery;Perioperativenutrition;Nutrition andtransplantation;Malnutrition;
ee front matter & 2006lnu.2006.01.015
s: EN, enteral nutritionl food/normal nutritioninformation on method
ing author. Tel.: +49 341ess: arved.weimann@saors of the DGEM (Germabution to this article.
Summary Enhanced recovery of patients after surgery (‘‘ERAS’’) has become animportant focus of perioperative management. From a metabolic and nutritionalpoint of view, the key aspects of perioperative care include:
� avoidance of long periods of pre-operative fasting;� re-establishment of oral feeding as early as possible after surgery;
� integration of nutrition into the overall management of the patient;
� metabolic control, e.g. of blood glucose;
� reduction of factors which exacerbate stress-related catabolism or impairgastrointestinal function;� early mobilisation
Eu
(o: nolo90nktn S
Enteral nutrition (EN) by means of oral nutritional supplements (ONS) and if
necessary tube feeding (TF) offers the possibility of increasing or ensuring nutrientropean Society for Clinical Nutrition and Metabolism. All rights reserved.
ral nutritional supplements and tube feeding); ONS, oral nutritional supplements; TF, tubeormal diet as offered by the catering system of a hospital including special dietsgy see Schutz et al.231 For further information on definition of terms see Lochs et al.232
92200; fax: +49 341 9092234.georg.de (A. Weimann).ociety for Nutritional Medicine) guidelines on enteral nutrition in surgery are acknowledged
ARTICLE IN PRESS
ESPEN Guidelines on Enteral Nutrition 225
Undernutrition;Complications
intake in cases where food intake is inadequate. These guidelines are intended togive evidence-based recommendations for the use of ONS and TF in surgical patients.They were developed by an interdisciplinary expert group in accordance withofficially accepted standards and are based on all relevant publications since 1980.The guideline was discussed and accepted in a consensus conference.
EN is indicated even in patients without obvious undernutrition, if it isanticipated that the patient will be unable to eat for more than 7 daysperioperatively. It is also indicated in patients who cannot maintain oral intakeabove 60% of recommended intake for more than 10 days. In these situationsnutritional support should be initiated without delay. Delay of surgery forpreoperative EN is recommended for patients at severe nutritional risk, defined bythe presence of at least one of the following criteria: weight loss 410–15% within 6months, BMIo18.5 kg/m2, Subjective Global Assessment Grade C, serum albumino30 g/l (with no evidence of hepatic or renal dysfunction).
Altogether, it is strongly recommended not to wait until severe undernutrition hasdeveloped, but to start EN therapy early, as soon as a nutritional risk becomesapparent.
The full version of this article is available at www.espen.org.& 2006 European Society for Clinical Nutrition and Metabolism. All rights reserved.
Summary of statements: Surgery
Subject
Recommendations Grade231 NumberGeneral
Preoperative fasting from midnight is unnecessaryin most patients.A
1Interruption of nutritional intake is unnecessaryafter surgery in most patients.
A
3Indications
Perioperative Use nutritional support in patients with severenutritional risk for 10–14 days prior to majorsurgery even if surgery has to be delayed.
A
4.1Severe nutritional risk refers to at least one:
4.1 – Weight loss 410–15% within 6 months– BMIo18.5 kg/m2– Subjective Global Assessment Grade C– Serum albumino30 g/l (with no evidence ofhepatic or renal dysfunction)
Initiate nutritional support (by the enteral routeif possible) without delay:
� even in patients without obviousundernutrition, if it is anticipated that thepatient will be unable to eat for more than 7 daysperioperativelyC
4� in patients who cannot maintain oral intakeabove 60% of recommended intake for more than10 days.
C
4Consider combination with parenteral nutrition inpatients in whom there is an indication fornutritional support and in whom energy needscannot be met (o60% of caloric requirement) viathe enteral route.
C
4ARTICLE IN PRESS
A. Weimann et al.226
Contraindications
Prefer the enteral route except for thefollowing contraindications: Intestinalobstructions or ileus, severe shock, intestinalischemia.C
4Application
Preoperative Encourage patients who do not meet theirenergy needs from normal food to take oralnutritional supplements during thepreoperative period.
C
4.1Administer preoperative enteral nutrition (EN)preferably before admission to the hospital.
C
4.1Patients undergoing surgery who are consideredto have no specific risk for aspiration, may drinkclear fluids until 2 h before anaesthesia. Solidsare allowed until 6 h before anaesthesia.
A
1Use preoperative carbohydrate loading (thenight before and 2 h before surgery) in mostpatients undergoing major surgery.
B
2Postoperative
Initiate normal food intake or enteral feedingearly after gastrointestinal surgery.A
4.2.1Oral intake, including clear liquids, can beinitiated within hours after surgery to mostpatients undergoing colon resections.
A
3Oral intake should, however, be adapted toindividual tolerance and to the type of surgerycarried out.
C
3Apply tube feeding in patients in whom earlyoral nutrition cannot be initiated, with specialregard to those
4.2.2
� undergoing major head and neck orgastrointestinal surgery for cancer
A
4.2.2� with severe trauma
A 4.2.2 � with obvious undernutrition at the time ofsurgeryA
4.2.2� in whom oral intake will be inadequate(o60%) for more than 10 days
C
4.2.2Initiate tube feeding for patients in need within24 h after surgery.
A
4.2.1,4.2.4Start tube feeding with a low flow rate (e.g.10–max. 20ml/h) due to limited intestinaltolerance.
C
4.2.4It may take 5 to 7 days to reach the targetintake and this is not considered harmful.
C
4.2.4Reassess nutritional status regularly during thestay in hospital and, if necessary, continuenutritional support after discharge, in patientswho have received nutritional supportperioperatively.
C
5Type of tube feeding
Placement of a needle catheter jejunostomy ornaso-jejunal tube is recommended for allcandidates for TF undergoing major abdominalsurgery.A
4.2.4When anastomoses of the proximalgastrointestinal tract have been performed,
B
4.2.1ARTICLE IN PRESS
ESPEN Guidelines on Enteral Nutrition 227
deliver EN via a tube placed distally to theanastomosis.Consider placement of a percutaneousendoscopic tube (e.g. PEG) if long term tubefeeding (44 weeks) is necessary, e.g. in severehead injury.
C
4.2.4Type of formula
In most patients a standard whole proteinformula is appropriate.C
4.2.3Use EN preferably with immuno-modulatingsubstrates (arginine, o-3 fatty acids andnucleotides) perioperatively independent of thenutritional risk for those patients
A
4.2.3� undergoing major neck surgery for cancer(laryngectomy, pharyngectomy)� undergoing major abdominal cancer surgery(oesophagectomy, gastrectomy, andpancreatoduodenectomy)� after severe trauma.
Whenever possible start these formulae 5–7days before surgery
C
4.2.3and continue postoperatively for 5 to 7 daysafter uncomplicated surgery.
C
4.2.3Grade: Grade of recommendation; Number: refers to statement number within the text.
Summary of statements: Organ transplantation
Subject
Recommendations Grade231 NumberIndication
Beforetransplantation
Undernutrition is a major factor influencingoutcome after transplantation so optimisingnutritional status is important.C
6In undernutrition, use additional ONS or even TF.
C 6 Assess nutritional status regularly whilemonitoring patients on the waiting list beforetransplantation.C
6Recommendations for the living donor andrecipient are not different from those for patientsundergoing major abdominal surgery.
C
6Aftertransplantation
Initiate early normal food or EN after heart, lung,liver, pancreas, and kidney transplantation.
C
7Even after transplantation of the small intestine,nutritional support can be initiated early, butshould be increased very carefully.
C
7Long-term nutritional monitoring and advice isrecommended for all transplants.
C
7Grade: Grade of recommendation; Number: refers to statement number within the text.
Preliminary remarks
To make proper plans for the nutritional support ofpatients undergoing surgery, it is essential tounderstand the basic changes in body metabolism
that occur as a result of injury. In addition, recentstudies have shown that not only does surgery itselfinfluence the response to nutritional support, butmany of the perioperative routines also have amajor impact on how well different nutritional
ARTICLE IN PRESS
A. Weimann et al.228
treatments are tolerated by the postoperativepatient.
Surgery, like any injury to the body elicits a seriesof reactions including release of stress hormonesand inflammatory mediators, i.e. cytokines. Thisrelease of mediators to the circulation has a majorimpact on body metabolism. They cause catabolismof glycogen, fat and protein with release ofglucose, free fatty acids and amino acids into thecirculation, so that substrates are diverted fromtheir normal purposes, e.g. physical activity, to thetask of healing and immune response. For optimalrehabilitation and wound healing, the body needsto be in an anabolic state. Recent studies haveshown that measures to reduce the stress of surgerycan minimize catabolism and support anabolismthroughout surgical treatment and allow patientsto recover substantially better and faster, evenafter major surgical operations. Such programs forenhanced recovery after surgery (ERAS)7 involve aseries of components that combine to minimizestress and to facilitate the return of function: theseinclude preoperative preparation and medication,fluid balance, anaesthesia and postoperative an-algesia, pre- and postoperative nutrition, andmobilization.
Severe undernutrition has long been known to bedetrimental to outcome1–3: it has also been shownthat even 12 h of preoperative fasting has beenassociated with prolonged recovery after uncom-plicated surgery.4,5 Furthermore, to improve pa-tients’ tolerance of normal food and to some extentof enteral feeding, a combination of treatments areneeded to facilitate earlier return of gastro-intestinal function.6,7
Insulin, one of the key factors regulating meta-bolism after surgery, was recently shown to be farmore important in the postoperative period thanpreviously recognized. A large randomized trial, inpostoperative patients in intensive care, showedthat when postoperative hyperglycemia was con-trolled by insulin infusion to maintain normoglyce-mia, morbidity and mortality was reduced byalmost half,8 showing that metabolic regulation isone of the key measures to reduce complicationsafter major surgery. This has implications fornutritional management since patients withmarked insulin resistance cannot tolerate feedingwithout developing hyperglycemia, necessitatingthe use of insulin to keep glucose levels withinnormal limits.
Some degree of insulin resistance develops afterall kinds of surgery, but its severity is related to thesize of the operation and any complications, e.g.sepsis. It lasts for about 2–3 weeks, even afteruncomplicated moderate surgery, and its develop-
ment is independent of the preoperative state ofthe patient. In one study9,228 the three mainvariables influencing length of stay were; the typeof operation, perioperative blood loss and thedegree of postoperative insulin resistance. Severalmeasures, with additive effects, may contribute toa reduction in insulin resistance, including painrelief,9 continuous epidural analgesia using localanaesthetics,10 and preparation of the patient withpreoperative carbohydrates (12 and 2–4 h preo-peratively) instead of overnight fasting.4 Using thisapproach of preoperative carbohydrate loading andcontinuous epidural analgesia, in patients under-going colorectal surgery, postoperative insulinresistance and nitrogen losses were reduced.11
Another factor that directly affects tolerance ofnormal food or EN is postoperative ileus, which maybe exacerbated and prolonged by opiates anderrors in fluid management. Experimental resultsdemonstrate the impact of intraoperative manip-ulation and subsequent panenteric inflammation asthe cause of dysmotility. This emphasizes theadvantages of minimal invasive and gentle surgicaltechnique.12
Traditionally, many patients undergoing majorgastrointestinal resections receive large volumes ofcrystalloids intravenously during and after surgery.Excess fluid administration would result in severalkilos in weight gain and even oedema. This wasrecently shown to be a major cause for post-operative ileus and delayed gastric emptying.13
When fluids were restricted to the amount neededto maintain salt and water balance, gastric empty-ing returned sooner and patients were capable oftolerating oral intake and had bowel movementsseveral days earlier than those in positive balance.The effect of opioids, used for pain relief, can beavoided or substantially minimized by the use ofepidural analgesia instead.6,7
In conclusion: Enhanced recovery of patientsafter surgery (ERAS) has become an important focusof perioperative management. After colorectalsurgery particularly, the so-called ‘‘fast track’’programs have been successful in promoting rapidrecovery and shortened length of hospital stay.7
From a metabolic and nutritional point of view,therefore, the key aspects of perioperative careinclude:
�
avoidance of long periods of pre-operativefasting, � re-establishment of oral feeding as early aspossible after surgery,
� integration of nutrition into the overall manage-ment of the patient,
� metabolic control, e.g. of blood glucose,ARTICLE IN PRESS
ESPEN Guidelines on Enteral Nutrition 229
�
reduction of factors which exacerbate stress-related catabolism or impair GI function, � early mobilisation.1. Is preoperative fasting necessary?
Preoperative fasting from midnight is unneces-sary in most patients. Patients undergoingsurgery, who are considered to have no specificrisk of aspiration, may drink clear fluids until 2 hbefore anaesthesia. Solids are allowed until 6 hbefore anaesthesia (A).
Comment: There is no evidence that patients givenfluids 2–3 h preoperatively are at any greater risk ofaspiration/regurgitation than those fasted for thetraditional 12 h (or even longer in some cases),since fluid clears the stomach rapidly in mostpatients14 (Ia). Many national anaesthesia societieshave changed their fasting guidelines15–17 (III) andnow recommend that patients may drink clearfluids up until 2 h before anaesthesia for electivesurgery. Exceptions to this recommendation arepatients ‘‘at special risk’’, undergoing emergencysurgery, and those with known delayed gastricemptying for any reason14 (Ia). Since the imple-mentation of these guidelines, there has been noreport of a dramatic rise in the incidence ofaspiration, regurgitation, or associated morbidityor mortality.14
2. Is preoperative metabolic preparation ofthe elective patient using carbohydratetreatment useful?
Instead of overnight fasting, preoperative car-bohydrate loading (the night before and 2hbefore surgery) is recommended in most patientsundergoing major surgery (B).
Comment: Preoperative intake of a carbohydratedrink (CHO) with 800ml the night before and 400mlbefore surgery does not increase the risk ofaspiration.14,16–18,23,24
In colorectal patients, and those with hipreplacement the intake of an hypo-osmolar 12.5%carbohydrate rich drink has been shown to reducepostoperative insulin resistance19–21 (Ib) and pre-serve skeletal muscle mass18 (Ib). Muscle strengthwas improved up at 1 month after surgery22 (Ib).Oral carbohydrates have also been reported toimprove preoperative well being23 (Ib).24
Two studies have investigated the effect of apreoperative carbohydrate drink (CHO) on post-operative nausea and vomiting (PONV) in patients
undergoing laparoscopic cholecystectomy.25,26 Oneshowed a reduction in PONV with CHO compared tofasting, while neither showed a clear differencebetween CHO and placebo25,26 (Ib).
After major upper gastrointestinal surgery, noeffect of this treatment was found on complicationrate, and length of hospital stay: further studiesare needed in this group of patients18 (Ib).
3. Is postoperative interruption of oralnutritional intake generally necessary aftersurgery?
In general, interruption of nutritional intake isunnecessary after surgery (A). Oral intakeshould, however, be adapted to individualtolerance and to the type of surgery carriedout (C).
Oral intake, including clear liquids, can beinitiated within hours after surgery in mostpatients undergoing colon resections (A).
Comment: Oral nutrition (normal food and/or ONS)can be initiated, in most cases, immediately aftersurgery, since neither oesophago-gastric decom-pression nor delayed oral intake, after cholecys-tectomy or colorectal resection have provenbeneficial27–30 (Ib), especially in using ERAS proto-col for colorectal surgery. However, the situationwith regard to major upper GI surgery is less clear.Early normal food or EN, including clear liquids onthe first or second postoperative day, did not causeimpairment of healing of anastomoses in the colonor rectum6,28,29,31,32 (Ib),33 (Ia). In comparison toconventional open surgery, early oral intake is evenbetter tolerated after laparoscopic colonic resec-tion, due to earlier onset of peristalsis and bowelmovement with this technique34 (Ib),35,36 (IIa).However, no differences were found betweenlaparoscopic and conventional open colonic surgerywhen the full ERAS protocol was employed37 (Ib).
The amount of initial oral intake should beadapted to the state of gastrointestinal functionand to individual tolerance33 (Ia),28,31,32 (Ib),35,38,39
(IIa),40 (IIb).
4. When is perioperative nutritional supportindicated?
Inadequate oral intake for more than 14 days isassociated with a higher mortality (Ib). EN istherefore indicated even in patients withoutobvious undernutrition, if it is anticipated that
ARTICLE IN PRESS
A. Weimann et al.230
the patient will be unable to eat for more than 7days perioperatively. It is also indicated inpatients who cannot maintain oral intake above60% of recommended intake for more than 10days. In these situations nutritional support (bythe enteral route if possible) should be initiatedwithout delay (C).
The enteral route should always be preferredexcept for the following contraindications:
�
intestinal obstructions or ileus, � severe shock, � intestinal ischemia.Combination with parenteral nutrition should beconsidered in patients in whom there is anindication for nutritional support and in whomenergy needs cannot be met (o60% of caloricrequirement) via the enteral route, e.g. in upperGI fistulae (C).
Comment: The influence of nutritional status onpostoperative morbidity and mortality has beenwell documented in both retrospective41–46 andprospective studies.1,47–58 Inadequate oral intakefor more than 14 days is associated with a highermortality59 (Ib).
Two multivariate analyses have shown, forhospitalised patients in general and for thoseundergoing surgery for cancer in particular, thatundernutrition is an independent risk factorfor the incidence of complications, as well asincreased mortality, length of hospital stay, andcosts.60,61
Undernutrition frequently occurs in associationwith underlying disease (e.g. cancer) or withchronic organ failure2,60,62–69 (see respectiveguidelines). In a recent prospective multicenterobservational study of patients with gastric can-cer70 dysphagia and gastric outlet syndrome due tostenosis have been shown independent factors forthe risk of anastomotic leakage after total gas-trectomy. It also influences outcome after trans-plantation3,71–77 as well as increasing the morbidityand mortality of geriatric patients undergoingsurgery.78
The general indications for nutritional supportin surgery are in the prevention and treatment ofundernutrition, i.e. the correction of undernu-trition before surgery and the maintenance ofnutritional status after surgery, when periods ofprolonged fasting and/or severe catabolism areexpected. Morbidity, length of hospital stay, andmortality are considered principal outcome para-meters when evaluating the benefits of nutri-tional support.
After discharge from hospital or when pallia-tion is the main aim of nutritional support,improvement in nutritional status and in qualityof life are the main evaluation criteria.79–91
The current American Society for Parenteral andEnteral Nutrition guidelines (ASPEN) recommendpostoperative nutritional support for patients whocannot meet their caloric requirements within 7–10days.92
The effect of EN on the outcome after surgeryhas not been assessed in a consistent manner93–127
(Ib) (see Table 1).The current ESPEN working group reviewed 35
prospective randomized controlled trials, focusing onendpoints of outcome, and including patients aftergastrointestinal surgery (without transplantation),trauma, and hip fracture. EN was defined as the useof ONS and TFs. Early EN was compared to normalfood, administration of crystalloids and total par-enteral nutrition (TPN). Twenty-four of these 35 trialsreported significant advantages of EN with particularregard to the reduction of infectious complications,length of hospital stay and costs (Ib).
In eight of these 35 studies no benefits wereobserved98,109,113,115,119,120,125,126 (Ib). Some authorshave pointed out possible disadvantages of EN whichhave not been observed by others. These areincreased length of stay97 (Ib), reduced lungfunction after oesophageal or pancreatic resectionthrough abdominal distension112 (Ib) or delayedgastric emptying with increased length of stayfollowing pancreatic surgery128 (IIa). These problemsmay have been related to too rapid administrationof feed in the early stages. In patients with severetrauma tolerance of enteral intake has to be care-fully monitored107 (Ib) (see guidelines ‘‘Intensivecare’’). Compared to TPN, early EN decreasedpostoperative infection rate in undernourished GIcancer patients, but not in those who were wellnourished121 (Ib).
In seven out of 11 randomised controlledtrials129–139 (Table 2) only surrogate measures ofoutcome were used, e.g. positive effects of EN onnitrogen balance and substrate tolerance. In fourout of 11 studies no significant differences wereshown between early EN and standard hospitalfeeding practice131,132,137,138 (Ib).
Two meta analyses of studies, in which EN wascompared with PN in both surgery and internalmedicine, showed a significantly reduced rate ofinfections140 (Ia) and a shortened length of hospitalstay141 (Ia) in the enterally fed patients.
It was claimed by the authors of the lattermetaanalysis that no significant influence onmortality was shown.
ARTICLE IN PRESS
Table
1En
teralnu
tritionin
thesurgical
patient:Re
view
oftheliterature
rega
rdingprospec
tive
rand
omized
controlled
trials
withen
dpointsof
outcom
e.
Author
Year
NSu
rgery
Nutritional
regimen
Start
Resu
lts
Rating
Saga
ret
al.9
319
7930
Abdom
inal
TFvs.crystalloids+dex
trose
POD1,
nasojejuna
l,25
ml/hl
Less
weigh
tloss,reduc
edne
g.Nbalan
ce,
shortene
dLO
S+
Rya
net
al.9
419
8114
Abdom
inal
TFvs.crystalloids
POD1,
NCJ,
50ml/h
Less
weigh
tloss
+Bastow
etal.9
519
8312
2Mod
eratelyan
dseve
rely
underno
urishe
dwom
enwith
frac
ture
ofthefemoral
neck
TFvs.no
rmal
food
Within5day
s,na
soga
stric
Inparticu
larin
seve
reMN:shorterreha
bilitation,
reduc
edLO
S,im
prove
men
tof
anthropom
etric
param
etersan
dserum
protein
+
Shuk
laet
al.9
619
8411
0Abdom
inal
andorolaryn
geal
Preo
pTFvs.no
rmal
food
Preo
p.hy
perca
loricfor10
day
sLe
ssco
mplica
tion
s,reduc
edmortality,reduc
edLO
S+
Smithet
al.9
719
8550
Abdom
inal
TFvs.crystalloids
POD3,
NCJ
Nodifferenc
ein
nutritiona
lparam
eters,
increa
sedLO
S–
Mug
gia-Su
llam
etal.9
819
8519
Abdom
inal
TFvs.TPN
POD1–
10,NCJ
Nodifferenc
e7
Adam
set
al.9
919
8646
Trau
ma
TFvs.TPN
POD1–
14,jejuno
stom
yNodifferenc
ein
rate
ofco
mplica
tion
san
dN
balan
ce+
Bow
eret
al.1
00
1986
20Abdom
inal
TFvs.TPN
POD1–
7,NCJ
Reduc
edco
st+
Moo
reet
al.1
01
1989
59Trau
ma
TFvs.TPN
12h,
NCJ
Less
seve
reinfections,no
differenc
ein
Nbalan
ce+
Delmiet
al.1
02
1990
59Hip
frac
ture
(age
460
yr)
ONSvs.no
rmal
food
After
rand
omisation,
for
mea
n32
day
s,1�daily
254kcal
Sign
ifica
ntly
less
complica
tion
san
dmortality
inho
spital
andafter6mon
ths,
sign
ifica
ntly
reduc
edLO
S
+
Schroe
der
etal.1
03
1991
32Abdom
inal
TFvs.crystalloids+dex
trose
Day
ofsurgery,
nasojejuna
l,50
ml/h
Improve
dwou
ndhe
aling,
noothe
rdifferenc
e+
Kudsk
etal.1
04
1992
98Trau
ma
TFvs.TPN
POD1,
NCJ
Sign
ifica
ntly
less
infections
+Vo
nMey
enfeldtet
al.1
05
1992
101
Abdom
inal
Preo
pTFor
ONSvs.TPN
Atleast10
day
sin
case
ofun
dernu
trition,
nasoga
stric
ororal,15
0%BEE
afterHarris
Ben
edict
Lower
rate
ofintraa
bdom
inal
abscessin
underno
urishe
dpatientsco
mpared
toun
derno
urishe
dco
ntrols
+
Iovine
lliet
al.1
06
1993
48La
ryng
ectomy
TFvs.TPN
After
24h,
PEG
,en
ergy:
HarrisBen
edict+40
%Nodifferenc
ein
weigh
t,tricep
sskin
folds,
mid-
arm
circum
ferenc
e,Alb,TFN
,reduc
edLO
S+
Dun
ham
etal.1
07
1994
37Se
vere
trau
ma(ISS
415
)TFvs.TPNvs.PN/T
Fca
.24
hNodifferenc
ein
mortality,high
ermortality
inintestinal
dysfunc
tion
�
Beier-H
olge
rsen
and
Boe
sby1
08
1996
30Abdom
inal
TFvs.place
bo
Day
ofsurgery,
nasoduo
den
alLe
ssinfections
+
Baigrie
etal.1
09
1996
97Abdom
inal
TFvs.TPN
POD3,
NCJ
Tren
dtowardsless
infections.
7Safe
Carret
al.1
10
1996
30Abdom
inal
TFvs.crystalloids
Day
ofsurgery,
NCJ
Sign
ifica
ntly
improve
dN-balan
ceon
day
1,no
differenc
ein
intestinal
permea
bilityin
the
interven
tion
grou
p,but
increa
sein
control
grou
p,less
complica
tion
s
+Safe
Keeleet
al.1
11
1997
100
Abdom
inal
Normal
food
+ONS(in-
and
outpatients)
ONS(1.5
kcal/m
l)ad
lib
—startwithoral
nutrition
Supplemen
tedgrou
p:
�inpatient
period:less
weigh
tloss,
mainten
ance
ofha
ndgrip
streng
th,less
fatigu
e,less
complica
tion
s
�ou
tpatient
period:no
sign
ifica
ntdifferenc
e
+
Watters
etal.1
12
1997
28Oesop
hage
al+p
ancrea
tic
resection
TFvs.crystalloids
Day
ofsurgery,
NCJ
Reduc
ed,resp.func
tion
,less
mob
ility
�
Reyn
oldset
al.1
13
1997
67Abdom
inal
TFvs.TPN
POD1,
NCJ
Nodifferenc
ein
complica
tion
s7
ESPEN Guidelines on Enteral Nutrition 231
ARTICLE IN PRESS
Table
1(con
tinu
ed)
Author
Year
NSu
rgery
Nutritional
regimen
Start
Resu
lts
Rating
Sand
etal.1
14
1997
29Gastrec
tomy
TFvs.TPN
POD1,
NCJ
Less
expen
sive
+Sh
irab
eet
al.1
15
1997
26Live
rresection
TFvs.TPN
POD2,
nasojejuna
lNosign
ifica
ntdifferenc
ein
outcom
e7
Sing
het
al.1
16
1998
43Pe
rforation-periton
itis
TFvs.crystalloids
NCJ,
12hpostop.
Less
complica
tion
s+
Sullivan
etal.1
17
1998
17Frac
ture
offemoral
neck
Noc
turnal
TFvs.no
rmal
food
Not
consistent
Nosign
ifica
ntdifferenc
ein
‘‘in-hospital
Outco
me’’,
but
in6-mon
thsmortality
+
Bea
ttie
etal.1
18
2000
101
Abdom
inal
Normal
food
+ONS
Inparallelto
startof
oral
nutrition
Improve
dnu
tritiona
lstatus,QOL,
reduc
edmortality
+
Mac
Fieet
al.1
19
2000
100
Abdom
inal
Normal
food
+ONS(periop;
preop
;postop)vs.no
rmal
food
alon
e
Approx.
2wee
kspreop
.,from
POD1foraminim
umof
7day
s
Nodifferenc
ein
outcom
eNoroutine7
Espau
lellaet
al.1
20
2000
171
Frac
ture
offemoral
neck
Normal
food
+ONSvs.no
rmal
food
+place
bo
Within48
hfor60
day
s:ONS:15
0kcal/d
,20
gprotein,
Ca,
Vit
D,alon
gwithothe
rmineralsan
dvitamins
Place
bo;
155kcal/d
;mainly
carboh
ydrates
Noad
vantag
esin
rega
rdto
reha
bilitationan
dmortality,sign
ifica
ntly
less
complica
tion
sov
er6
mon
ths
Noroutine7
Pace
lliet
al.1
26
2001
241
Und
ernu
trition
—ab
dom
inal
TFvs.PN
POD1,
NCJor
nasojejuna
l,30
ml/h
Nodifferenc
ein
rate
ofco
mplica
tion
san
dmortality
Noben
efits7
Bozze
ttiet
al.1
27
2001
317
Und
ernu
trition
—ab
dom
inal
TFvs.PN
POD1,
NCJor
nasojejuna
l,isoc
aloric
EN:sign
ifica
ntly
less
complica
tion
san
dreduc
edLO
S+
Braga
etal.1
21
2001
257
Abdom
inal
—up
per
GIca
ncer
TFvs.PN
6hpostop.,
NCJor
nasojejuna
l,nu
tritiona
lgo
al25
kcal/k
g/d,EN
andTPN
wereisoc
aloric
and
continue
dun
tilad
equa
teoral
intake
of80
0kcal/d
EN:sign
ifica
ntly
less
(fou
r-fold)ex
pen
sive
tend
ency
toless
infections
andshorterleng
thof
hospital
stay
+
Malho
traet
al.1
22
2004
200
Peritonitisfollow
inggu
tperforation
TFvs.PN(dex
troseon
ly)
POD2,
nasoga
stric,
TF:
50ml/h,
600kcal/d
plus
300kcal
i.v.ve
rsus
PN:
600kcal/d
i.v.
TF:
safe,sign
ifica
ntly
less
weigh
tloss,tend
ency
toless
complica
tion
san
dshorterLO
Sin
ICUan
din
hospital,tend
ency
tohigh
errate
ofvo
miting,
diarrho
ea,ab
dom
inal
distension
+safe
Smed
leyet
al.1
23
2004
179
Abdom
inal
—lower
gastrointestinal
Periop
ONSvs.no
ONSvs.
preop
only
vs.postopon
lyMinim
um7day
spreop
,up
to4wee
ksafterdisch
arge
,1.5kcal/m
lad
libitum
resultingin
mea
nad
ditiona
lintake
sof
300–
540kcal/d
Periop
.ONS.:postop.sign
ifica
ntly
less
weigh
tloss,fewer
minor
complica
tion
s,co
st-effec
tive
+
Mac
ket
al.1
24
2004
36Pa
ncreatod
uoden
ectom
yTFviadou
ble-
gastrojejuno
stom
ytubevs.
stan
dardca
re
POD1or
2,startwith20
ml/
h,increa
sewith20
ml/hea
chday
astolerated,go
alrate:
25kcal/k
g/d
TF:
sign
ifica
ntly
less
gastro-paresis,sign
ifica
ntly
shorterLO
San
dho
spital
charge
s+
Sullivan
etal.1
25
2004
57Geriatric
patientswithhip
frac
ture
TF/
ONSvs.stan
dardca
reTe
stgrou
p:up
to1.37
5kcal
viana
soen
teralTFov
ernigh
tTF:
grea
tertotaldaily
nutrient
intake
duringthe
firstwee
k,high
rate
ofintoleranc
eto
-TF,
nodifferenc
ein
therate
ofpostoperative
life
–threaten
ingco
mplica
tion
sor
mortality
within6mon
ths
7
Abb
reviations:(T)EN¼
enteraln
utrition
;TF¼
tubefeed
ing;
ONS¼
oral
nutritiona
lsup
plemen
ts;(T)PN¼
totalp
aren
teraln
utrition
;NCJ¼
need
leca
theter
jejuno
stom
y;LO
S¼
leng
thof
stay
;QOL¼
qua
lity
oflife;NKce
ll¼
naturalkiller
cells;
N¼
nitrog
en;POD¼
postoperativeday.
A. Weimann et al.232
ARTICLE IN PRESS
ESPEN Guidelines on Enteral Nutrition 233
In one trial of overnight nasogastric feeding95
(Ib), in which the patients were first stratified bynutritional status before randomisation, there wasa significant reduction in rehabilitation time andpostoperative stay in the undernourished groups. Inanother study of TF, there was no influence onhospital outcome, although 6-month mortality wasreduced117 (Ib). In the study by Delmi et al.102 (Ib)ONS once daily significantly improved outcome at 6months with a lower rate of complications andmortality.
There are no controlled data with regard tocombined EN and PN after elective surgery. Forcritically ill patients, a recently published systema-tic review142 (Ib) including five controlled trialsrevealed no advantages of combined EN and PN onmortality or infections, or on length of hospitalstay. However, the quality of the data is not goodenough to draw further conclusions for patientsafter elective surgery.
4.1. When is preoperative EN indicated?
Patients with severe nutritional risk benefitfrom nutritional support for 10–14 days priorto major surgery even if surgery has to bedelayed (A). Whenever feasible, the enteralroute should be preferred (A).
In cancer patients undergoing upper majorabdominal surgery preoperative EN preferablywith immune modulating substrates (arginine, x-3 fatty acids and nucleotides) is recommendedfor 5–7 days independently of their nutritionalrisk (A).
Many patients do not meet their energy needsfrom normal food and therefore they should beencouraged to take ONS during the preoperativeperiod (C).
Preoperative EN should preferably be adminis-tered before admission to the hospital (C).
Comment: For surgical patients the benefits ofnutritional support were shown in cases of se-vere undernutrition96,105,143 (Ib),144 (Ia), particu-larly with regard to the rate of complications96,105
(Ib). These patients were fed preoperatively for atleast 10 days.
‘‘Severe’’ nutritional risk is defined by the ESPENworking group as the presence of at least one of thefollowing criteria:
�
weight loss 410–15% within 6 months, � BMIo18.5 kg/m2, � Subjective Global Assessment (SGA) Grade C229, � serum albumino30 g/l (with no evidence ofhepatic or renal dysfunction).
as disease associated catabolism.Preoperative ONS, using a standard whole protein
These parameters reflect undernutrition as well
formula, was studied in general surgical patients intwo PRCTs145,123 (Ib). Although one study showed nosignificant impact on outcome, Smedley et al.123
found a significant reduction in minor complications.Furthermore, preoperative ONS continued postopera-tively, minimized postoperative weight loss.
Preoperative intake of ONS (3� 250ml) enrichedwith immune modulating substrates (arginine, o-3fatty acids and nucleotides) for 5–7 days reducedpostoperative morbidity and length of stay aftermajor abdominal cancer surgery146–149 (Ib). Under-nourished patients, in particular, appear to bene-fit150 (Ib).
The prospective controlled trial by Gianottiet al.151 (Ib) randomised 305 gastrointestinalcancer patients without severe undernutrition toreceive either preoperative or perioperative im-mune modulating formulae. A reduction in infec-tious complications and length of hospital stay wereobserved in both groups. These authors also showedthe cost-effectiveness of preoperative immunemodulating formulae in this group of patients152
(IIb). However, this study did not include a groupwith standard formula. Therefore, It can beargued, that the observed effects would have beenalso obtained with standard formulae.
4.2. Postoperative EN
4.2.1. Is early normal food intake or EN (o24h)following gastrointestinal surgery beneficial?
Early initiation of normal food intake or enteralfeeding is recommended after gastrointestinalsurgery (A). When anastomoses of the proximalgastrointestinal tract have been performed, ENcan be delivered via a tube whose tip is placeddistal to the anastomosis (B).
Comment: In several prospective studies, bene-ficial effects of early normal food or EN were shownwith regard to the rate of infectious complicationsand the length of hospital stay33,153 (Ia),154,155
(Ib),156 (IIa). Early TF was not a risk factor forgastric intolerance and pneumonia157 (Ib).
Limited data are available regarding immediateoral nutrition in patients with anastomoses in theproximal gastrointestinal tract, e.g. followinggastrectomy, pancreatoduodenectomy or oesopha-geal resection230. Many studies have shown thebenefits and feasibility of feeding via a tube eitherinserted distal to the anastomosis, e.g. jejunost-omy, or inserted via the nose with its tip passeddistally at the time of operation, e.g. nasojejunaltube126,127,158–160 (IIb).
ARTICLE IN PRESS
Table
2En
teralnu
tritionin
thesurgical
patient:Re
view
oftheliterature
rega
rdingprospec
tive
rand
omized
controlled
trials
withsurrog
ateen
dpoints.
Author
Year
NSu
rgery
Nutritional
regimene
Resu
lts
Rating
Lim
etal.1
29
1981
19Oesop
hagu
sTF(gastrostomy)
vs.TPNfor
4wks
TPN:quicker
pos.N-balan
cea.
weigh
tloss
+
McA
rdle
etal.1
30
1986
20(nostrict
rand
omisation)
Cystectom
yTF(jejun
al)vs.TPNor
norm
alfood
Improve
men
tof
intestinal
func
tion
+
Fletch
eran
dLittle
131
1986
28Aorticreplace
men
tTFvs.PNvs.cristalloids
Nodifferenc
ein
N-balan
ce7
Nissila
etal.1
32
1989
22Abdom
inal
TFvs.TPN
Nodifferenc
ein
NK-cell-func
tion
7Mag
nusson
etal.1
33
1989
20Colorec
tal
TFwithgluc
oseon
lyvs.
gluc
osei.v.
Improve
men
tof
gluc
osetoleranc
e+
Hwan
get
al.1
34
1991
24Bileduc
tTF(nasod
uoden
al)vs.
crystalloids
Improve
dN-balan
ce+
Such
neret
al.1
35
1995
34Neu
rosurgery
TFvs.TPN
Improve
men
tof
visc.protein
synthe
sis,
ofnu
tr.index
,toleranc
eof
substratesan
dof
intestinal
func
tion
+
Hoc
hwaldet
al.1
36
1997
29Abdom
inal
TFvs.crystalloids
Dec
reaseof
fatox
idationan
dca
tabolism,im
prove
men
tof
N-
balan
ce
+
Beier-H
olge
rsen
and
Brand
strup137
1999
60Abdom
inal
TFvs.place
bo
Noim
pac
ton
cell-m
ediated
immun
ity
7
Brook
set
al.1
38
1999
19Abdom
inal
TFvs.crystalloids
Noim
pac
ton
intestinal
permea
bility
7Huan
dZh
eng1
39
2003
135
Abdom
inal-impaired
live
rfunc
tion
TFvs.TPNvs.co
ntrol
EN:ea
rlierreac
hing
positiveN-
balan
ce,lower
loss
ofbod
yweigh
t,postop.no
chan
gein
intestinal
permea
bility(significa
ntin
TPN)
+
Abb
reviations:
(T)EN¼
enteralnu
trition;
TF¼
tube
feed
ing;
ONS¼
oral
nutritiona
lsupp
lemen
ts;
(T)PN¼
totalparen
teralnu
trition;
NCJ¼
need
leca
theter
jejuno
stom
y;LO
S¼
leng
thof
stay
;QOL¼
qua
lity
oflife;NKce
ll¼
naturalkiller
cells;
N¼
nitrog
en,POD¼
postoperativeday.
A. Weimann et al.234
ARTICLE IN PRESS
ESPEN Guidelines on Enteral Nutrition 235
A recent study in patients undergoing totallaryngectomy with primary pharyngeal closureshowed that initiation of oral feeding on the firstpostoperative day was safe161 (Ib).
4.2.2. Which patients benefit from early post-operative TF?
Early TF (within 24 h) is indicated in patients inwhom early oral nutrition cannot be initiated(see Table 1), in case of patients:
�
undergoing major head and neck or gastro-intestinal surgery for cancer(A), � with severe trauma (A), � with obvious undernutrition at the time ofsurgery (A),
�yThe ESPEN-working group agrees that hypoalbuminia is aclear surgical risk factor, however, it reflects disease associatedinflammation and disease severity rather than undernutrition. Itis also influenced by the dilutional effect of intravenouscrystalloids.
in whom oral intake will be inadequate(o60%) for more than 10 days (C).
Comment: Patients undergoing major surgery forhead and neck, and abdominal cancer (larynx,pharynx or oesophageal resection, gastrectomy,partial pancreatoduodenectomy) often exhibit nu-tritional depletion before surgery1,50,53–55,62,65,67,68
(see guidelines ‘‘Oncology’’) and run a higher riskof developing septic complications.1,50,53–55,61,68
Postoperatively, oral intake is often delayed dueto swelling, obstruction or impaired gastric empty-ing, or in order to prevent straining the anasto-mosis, making it difficult to meet nutritionalrequirements. Nutritional support reduces morbid-ity with an increasing protective effect of TPN, EN,and immune-modulating formulae61 (IIb).
Trauma patients with normal nutritional statushave a high risk of developing septic complicationsand multiple organ failure. Early EN has beenclaimed to reduce septic complications44 (Ia),101,104
(Ib) and, has been suggested to reduce the rateof multiple organ failure when initiated within24 h162 (Ib).
4.2.3. Which formulae should be used?
In most patients a standard whole proteinformula is appropriate (C).
With special regard to patients with obvioussevere nutritional risk, those undergoing majorcancer surgery of the neck (laryngectomy,pharyngectomy) and of the abdomen (oesopha-gectomy, gastrectomy, and pancreatoduode-nectomy) as well as after severe traumabenefit from the use of immune modulatingformulae (enriched with arginine, omega-3 fattyacids and nucleotides) (A). Whenever possibleadministration of these supplemented formulaeshould be started before surgery (A) and con-
tinued postoperatively for 5–7 days after un-complicated surgery (C).
Comment: Data are available from several rando-mised controlled trials on the use of immunemodulating ONS and TF formulae, including argi-nine, o-3-fatty acids and ribonucleotides, with orwithout glutamine146,147,163–175 (Ib). In some ofthese trials there is no clear distinction madebetween critically ill and elective surgical patientsundergoing major surgery (see guidelines ‘‘inten-sive care’’). Four meta analyses of trials, ingeneral surgical and trauma patients, suggest thatimmune modulating nutritional formulae havecontributed to a decreased rate of postoperativecomplications and consequently to a decreasedlength of stay in the hospital175–178 (Ia).
Three randomised controlled trials showed thatpostoperative immune modulating formulae areeffective in both undernourished150 and wellnourished gastrointestinal cancer patients149,151
(Ib). In patients undergoing gastrectomy for gastriccancer, early EN with immune modulating formulawas associated with significantly less wound-heal-ing problems, suture failure, and infectious as wellas global complications179 (Ib).
A National US-Database evaluation also sup-ported the cost-effectiveness of nutritional formu-lae modulating immune-function. In order toreduce resource consumption and total cost, abreakeven infection rate was also calculated forwell nourished as well as undernourished surgicalpatients180 (IIb).
The US experts summit181 issued consensusrecommendations concerning undernourished pa-tients. Their indications for nutritional supportwere:
Patients undergoing elective gastrointestinalsurgery
�
Moderately or severely undernourished patients(serum albumin o35 g/ly) undergoing majorelective upper gastrointestinal tract procedures. � Severely malnourished patients (albumino28 g/l(see footnote y)) undergoing lower gastrointest-inal surgery.
Although benefits of enteral formulae enrichedwith glutamine alone have been found in several
randomised controlled trials in critically ill pa-tients, particularly those suffering from severetrauma or burns182–185 (Ib), no strong data forARTICLE IN PRESS
A. Weimann et al.236
patients after major neck or abdominal cancersurgery are available.
For formulae containing synbiotics with fibre andLactobacillus, a significantly lower incidence ofinfections was shown after major abdominal sur-gery, particularly that involving gastric and pan-creatic resections. No difference was observedbetween the effects of living or heat-killedlactobacilli186 (Ib).
A recent study in brain injured patients187
showed significant advantages of a formula contain-ing glutamine and probiotics with regard to infec-tion rate and length of stay in the intensive careunit (Ib).
4.2.4. How should patients be tube fed aftersurgery?
Placement of a needle catheter jejunostomy ornaso-jejunal tube is recommended for all candi-dates for TF undergoing major abdominal sur-gery (A).
TF should be initiated within 24h after surgery (A).
TF should start with a low flow rate (e.g.10—max. 20ml/h) due to limited intestinaltolerance (C). It may take 5–7 days to reachthe target intake and this is not consideredharmful (C).
If long-term TF (44 weeks) is necessary, e.g. insevere head injury, placement of a percutaneoustube (e.g. percutaneous endoscopic gastrosto-my—PEG) should be considered (C).
Comment: In several PRCTs the feasibility of needlecatheter jejunostomy for EN after major abdominalsurgery has been well documented.147,158,160
Open or even laparoscopic placement of theneedle catheter jejunostomy according to standar-dized techniques is associated with lowrisk160,188–196 (IIb,III),197 (IIa). Insertion of a dou-ble-gastrojejunostomy tube during pancreaticoduo-denectomy has also been shown to be safe124 (Ib).
In anecdotal reports a too rapid administration offeed may lead to the development of small bowelischemia.198–205 Tolerance of TF has to be mon-itored closely in patients with impaired gastro-intestinal function107 (Ib). It may therefore take5–7 days before nutritional requirements can beachieved by the enteral route.100,108,159
Percutaneous endoscopic gastrostomy should beconsidered where there is an indication for long-termenteral feeding when abdominal surgery is notindicated, e.g. after severe head injury or neurosur-gery. For patients with upper GI stenosis due toesophageal cancer and scheduled surgery afterneoadjuvant radio-chemotherapy, a preoperative
PEG should be only placed according to the discre-tion of the surgeon. The guidelines for PEG place-ment206 recommend the intervention for enteralfeeding of more than 2–3 weeks duration. However,recent results from the FOOD Trial in dysphagicstroke patients207 do not support early PEG feeding.
5. Which patients will benefit from EN afterdischarge from the hospital?
Regular reassessment of nutritional status dur-ing the stay in hospital and, if necessary,continuation of nutritional support after dis-charge, is advised for patients who have re-ceived nutritional support perioperatively (C).
Comment: In six randomised controlled trialspostoperative and post hospital administration ofONS have been investigated102,111,118,120,123 (Ib).The available data do not show with certainty thatroutine administration improves outcome but theydo show benefit in terms of nutritional status, rateof minor complications and well-being in patientswho cannot meet their nutritional requirements athome from normal food. This applies mainly tomajor gastrointestinal surgery, e.g. colorectalresections,208 gastrectomy209 and to geriatric pa-tients with fractures.45,52 Among geriatric patients,compliance with nutritional intake was low, in-dependently of nutritional status. However, totalenergy intake was still significantly higher in thetreatment compared to the control group52 (IIa).
Organ transplantation
6. When is EN necessary before solid organtransplantation?
Undernutrition is a major factor influencingoutcome after transplantation, so optimisingnutritional status is important (C).
In undernutrition, additional ONS or even TF isadvised (C).
Regular assessment of nutritional status isnecessary while monitoring patients on thewaiting list before transplantation (C).
Recommendations for the living donor and reci-pient are no different from those for patientsundergoing major abdominal surgery (C).
Comment: Undernutrition is likely to lead to afaster progression of the underlying disease,
ARTICLE IN PRESS
ESPEN Guidelines on Enteral Nutrition 237
especially in cardiac and respiratory insufficiency,and leads to impaired functional status (seerespective guidelines). Particular issues regardingthe influence of EN on the course/progression ofliver disease are discussed in the hepatologysection. Nutritional parameters have been shownto correlate with outcome after transplanta-tion74,210,211 (IIa+b). During the, often long, pre-operative waiting period, there is time to try toreplete patients nutritionally. Four interventionstudies (two randomised) of preoperative nutritionin patients waiting for organ transplantation havebeen performed212,213 (Ib),214,215 (IIa). Improve-ment in parameters of nutritional status was shownin all four studies. There was no difference inmortality for the patients with nutritional supple-mentation on the waiting list and patients aftertransplantation213 (Ib). This was however onlyinvestigated in one study. In case of nutritionalintervention no association was found betweenmortality and nutritional status211 (IIb). In onerandomised study the improved parameters ofnutritional status pretransplant did not affectoutcome and mortality213 (Ib).
Early results concerning the benefits of immunemodulating formulae during the waiting period and 5days after liver transplantation show favourable long-term impact on total body protein and a possiblereduction of infectious complications215 (IIa).
At present, there are no data available with regardto metabolic preconditioning of the (living) donorand recipient. Experimental results216 showing theimpact of nutritional status on liver preservationinjury also favour the concept of metabolic prepara-tion by preoperative carbohydrate drink.
7. When is EN indicated after organtransplantation?
After heart, lung, liver, pancreas, and kidneytransplantation, early normal food or EN shouldbe initiated (C).
Even after transplantation of the small intes-tine, nutritional support can be initiated early,but should be increased very carefully (C).
No recommendation can be given with regard tothe use of immune modulating formulae.
Long-term nutritional monitoring and advice isrecommended for all transplants (C).
Comment: It is generally agreed that early normalfood or EN should be administered in transplantpatients.217,218 In cases of undernutrition it shouldbe combined with PN.
Absorption and blood levels of tacrolimus are notaffected by EN219 (IIb).
EN is at least equal to PN in patients after livertransplantation220 (Ib) and has been shown toreduce the incidence of viral infections221 (Ib).Compared to standard formulae, combined withselective decontamination of the small intestine,the use of a high fibre formula with probioticbacteria (lactobacillus plantarum) has been shownto reduce significantly the rate of infections222 (Ib).Early EN enriched with a mixture of probioticbacteria and fibre significantly reduced bacterialinfection rate compared with a supplement con-taining only fibre223 (Ib).
Insertion of a needle catheter jejunostomy isfeasible in liver transplant patients224 (IIb).
EN is possible despite increased intestinal secre-tion in small bowel transplantation and can beperformed at low rates in the first week.225–227
Experience with the use of immune modulatingformulae is still only small. The first controlled dataon the use of an immune modulating formulae afterliver transplantation suggest that unfavourableeffects on immunosuppression are unlikely215 (IIa).
References
1. van Bokhorst-de van der Schueren MA, van Leeuwen PA,Sauerwein HP, Kuik DJ, Snow GB, Quak JJ. Assessment ofmalnutrition parameters in head and neck cancer and theirrelation to postoperative complications. Head Neck1997;19(5):419–25.
2. Durkin MT, Mercer KG, McNulty MF, et al. Vascular surgicalsociety of great britain and ireland: contribution ofmalnutrition to postoperative morbidity in vascular surgicalpatients. Br J Surg 1999;86(5):702.
3. Pikul J, Sharpe MD, Lowndes R, Ghent CN. Degree ofpreoperative malnutrition is predictive of postoperativemorbidity and mortality in liver transplant recipients.Transplantation 1994;57(3):469–72.
4. Ljungqvist O, Nygren J, Thorell A. Modulation of post-operative insulin resistance by pre-operative carbohydrateloading. Proc Nutr Soc 2002;61(3):329–36.
5. Ljungqvist O, Nygren J, Thorell A, Brodin U, Efendic S.Preoperative nutrition—elective surgery in the fed or theovernight fasted state. Clin Nutr 2001;20(Suppl. 1):167–71.
6. Kehlet H. Multimodal approach to control postoperativepathophysiology and rehabilitation. Br J Anaesth 1997;78(5):606–17.
7. Fearon KC, Ljungqvist O, Von Meyenfeldt M, et al.Enhanced recovery after surgery: a consensus review ofclinical care for patients undergoing colonic resection. ClinNutr 2005;24(3):466–77.
8. van den BG, Wouters P, Weekers F, et al. Intensive insulintherapy in the critically ill patients. N Engl J Med2001;345(19):1359–67.
9. Greisen J, Juhl CB, Grofte T, Vilstrup H, Jensen TS, SchmitzO. Acute pain induces insulin resistance in humans.Anesthesiology 2001;95(3):578–84.
ARTICLE IN PRESS
A. Weimann et al.238
10. Uchida I, Asoh T, Shirasaka C, Tsuji H. Effect of epiduralanalgesia on postoperative insulin resistance as evaluatedby insulin clamp technique. Br J Surg 1988;75(6):557–62.
11. Soop M, Carlson GL, Hopkinson J, et al. Randomized clinicaltrial of the effects of immediate enteral nutrition onmetabolic responses to major colorectal surgery in anenhanced recovery protocol. Br J Surg 2004;91(9):1138–45.
12. Schwarz NT, Kalff JC, Turler A, et al. Selective jejunalmanipulation causes postoperative pan-enteric inflamma-tion and dysmotility. Gastroenterology 2004;126(1):159–69.
13. Lobo DN, Bostock KA, Neal KR, Perkins AC, Rowlands BJ,Allison SP. Effect of salt and water balance on recovery ofgastrointestinal function after elective colonic resection: arandomised controlled trial. Lancet 2002;359(9320):1812–8.
14. Brady M, Kinn S, Stuart P. Preoperative fasting for adults toprevent perioperative complications. Cochrane DatabaseSyst Rev 2003(4):CD004423.
15. Practice guidelines for preoperative fasting and the use ofpharmacologic agents to reduce the risk of pulmonaryaspiration: application to healthy patients undergoingelective procedures: a report by the American Society ofAnesthesiologist Task Force on Preoperative Fasting.Anesthesiology 1999;90(3):896–905.
16. Soreide E, Fasting S, Raeder J. New preoperative fastingguidelines in Norway. Acta Anaesthesiol Scand 1997;41(6):799.
17. Spies CD, Breuer JP, Gust R, et al. Preoperative fasting, anupdate. Anaesthesist 2003;52(11):1039–45.
18. Yuill KA, Richardson RA, Davidson HI, Garden OJ, Parks RW.The administration of an oral carbohydrate-containing fluidprior to major elective upper-gastrointestinal surgerypreserves skeletal muscle mass postoperatively—a rando-mised clinical trial. Clin Nutr 2005;24(1):32–7.
19. Nygren J, Soop M, Thorell A, Efendic S, Nair KS, LjungqvistO. Preoperative oral carbohydrate administration reducespostoperative insulin resistance. Clin Nutr 1998;17(2):65–71.
20. Soop M, Myrenfors P, Nygren J, Thorell A, Ljungqvist O.Preoperative oral carbohydrate intake attenuates meta-bolic changes immediately after hip replacement. ClinNutr 1998;17(Suppl. 1):3–4.
21. Soop M, Nygren J, Thorell A, et al. Preoperative oralcarbohydrate treatment attenuates endogenous glucoserelease 3 days after surgery. Clin Nutr 2004;23(4):733–41.
22. Henriksen MG, Hessov I, Dela F, Hansen HV, Haraldsted V,Rodt SA. Effects of preoperative oral carbohydrates andpeptides on postoperative endocrine response, mobiliza-tion, nutrition and muscle function in abdominal surgery.Acta Anaesthesiol Scand 2003;47(2):191–9.
23. Hausel J, Nygren J, Lagerkranser M, et al. A carbohydrate-rich drink reduces preoperative discomfort in electivesurgery patients. Anesth Analg 2001;93(5):1344–50.
24. Hofman Z, Van Drunen J, Yuill K, Richardson R, Davidson I,Cecil T. Tolerance and efficacy of immediate pre-operativecarbohydrate feeding in uncomplicated elective surgicalpatients. Clin Nutr 2001;20(Suppl. 3):32.
25. Hausel J, Nygren J, Thorell A, Lagerkranser M, LjungqvistO. Randomized clinical trial of the effects of oralpreoperative carbohydrates on postoperative nausea andvomiting after laparoscopic cholecystectomy. Br J Surg2005;92(4):415–21.
26. Bisgaard T, Kristiansen VB, Hjortso NC, Jacobsen LS,Rosenberg J, Kehlet H. Randomized clinical trial comparing
an oral carbohydrate beverage with placebo beforelaparoscopic cholecystectomy. Br J Surg 2004;91(2):151–8.
27. Bickel A, Shtamler B, Mizrahi S. Early oral feeding followingremoval of nasogastric tube in gastrointestinal operations.A randomized prospective study. Arch Surg 1992;127(3):287–9.
28. Elmore MF, Gallagher SC, Jones JG, Koons KK, Schmalhau-sen AW, Strange PS. Esophagogastric decompression andenteral feeding following cholecystectomy: a controlled,randomized prospective trial. J Parenter Enteral Nutr1989;13(4):377–81.
29. Feo CV, Romanini B, Sortini D, et al. Early oral feeding aftercolorectal resection: a randomized controlled study. ANZ JSurg 2004;74(5):298–301.
30. Petrelli NJ, Stulc JP, Rodriguez-Bigas M, Blumenson L.Nasogastric decompression following elective colorectalsurgery: a prospective randomized study. Am Surg1993;59(10):632–5.
31. Jeffery KM, Harkins B, Cresci GA, Martindale RG. The clearliquid diet is no longer a necessity in the routinepostoperative management of surgical patients. Am Surg1996;62(3):167–70.
32. Reissman P, Teoh TA, Cohen SM, Weiss EG, Nogueras JJ,Wexner SD. Is early oral feeding safe after electivecolorectal surgery? A prospective randomized trial. AnnSurg 1995;222(1):73–7.
33. Lewis SJ, Egger M, Sylvester PA, Thomas S. Early enteralfeeding versus ‘‘nil by mouth’’ after gastrointestinalsurgery: systematic review and meta-analysis of controlledtrials. BMJ 2001;323(7316):773–6.
34. Schwenk W, Bohm B, Haase O, Junghans T, Muller JM.Laparoscopic versus conventional colorectal resection: aprospective randomised study of postoperative ileus andearly postoperative feeding. Langenbecks Arch Surg1998;383(1):49–55.
35. Chen HH, Wexner SD, Iroatulam AJ, et al. Laparoscopiccolectomy compares favorably with colectomy by lapar-otomy for reduction of postoperative ileus. Dis ColonRectum 2000;43(1):61–5.
36. Bardram L, Funch-Jensen P, Kehlet H. Rapid rehabilitationin elderly patients after laparoscopic colonic resection. BrJ Surg 2000;87(11):1540–5.
37. Basse L, Jakobsen DH, Bardram L, et al. Functional recoveryafter open versus laparoscopic colonic resection: a rando-mized, blinded study. Ann Surg 2005;241(3):416–23.
38. Choi J, O’Connell TX. Safe and effective early post-operative feeding and hospital discharge after open colonresection. Am Surg 1996;62(10):853–6.
39. Detry R, Ciccarelli O, Komlan A, Claeys N. Early feedingafter colorectal surgery. Preliminary results. Acta Chir Belg1999;99(6):292–4.
40. Bronnimann S, Studer M, Wagner HE. Early postoperativenutrition after elective colonic surgery. Langenbecks ArchChir Suppl Kongressbd 1998;115:1094–5.
41. Velanovich V. The value of routine preoperative laboratorytesting in predicting postoperative complications: a multi-variate analysis. Surgery 1991;109(3 Part 1):236–43.
42. Engelman DT, Adams DH, Byrne JG, et al. Impact of bodymass index and albumin on morbidity and mortality aftercardiac surgery. J Thorac Cardiovasc Surg 1999;118(5):866–73.
43. Kama NA, Coskun T, Yuksek YN, Yazgan A. Factors affectingpost-operative mortality in malignant biliary tract obstruc-tion. Hepatogastroenterology 1999;46(25):103–7.
44. Takagi K, Yamamori H, Toyoda Y, Nakajima N, Tashiro T.Modulating effects of the feeding route on stress response
ARTICLE IN PRESS
ESPEN Guidelines on Enteral Nutrition 239
and endotoxin translocation in severely stressed patientsreceiving thoracic esophagectomy. Nutrition 2000;16(5):355–60.
45. Koval KJ, Maurer SG, Su ET, Aharonoff GB, Zuckerman JD.The effects of nutritional status on outcome after hipfracture. J Orthop Trauma 1999;13(3):164–9.
46. Klein JD, Hey LA, Yu CS, et al. Perioperative nutrition andpostoperative complications in patients undergoing spinalsurgery. Spine 1996;21(22):2676–82.
47. Dannhauser A, Van Zyl JM, Nel CJ. Preoperative nutritionalstatus and prognostic nutritional index in patients withbenign disease undergoing abdominal operations—Part I. JAm Coll Nutr 1995;14(1):80–90.
48. Jagoe RT, Goodship TH, Gibson GJ. The influence ofnutritional status on complications after operations forlung cancer. Ann Thorac Surg 2001;71(3):936–43.
49. Mazolewski P, Turner JF, Baker M, Kurtz T, Little AG. Theimpact of nutritional status on the outcome of lung volumereduction surgery: a prospective study. Chest 1999;116(3):693–6.
50. van Bokhorstde van der Schueren MAE, van Leeuwen PA,Kuik DJ, et al. The impact of nutritional status on theprognoses of patients with advanced head and neck cancer.Cancer 1999;86(3):519–27.
51. Lavernia CJ, Sierra RJ, Baerga L. Nutritional parametersand short term outcome in arthroplasty. J Am Coll Nutr1999;18(3):274–8.
52. Patterson BM, Cornell CN, Carbone B, Levine B, ChapmanD. Protein depletion and metabolic stress in elderlypatients who have a fracture of the hip. J Bone Jt SurgAm 1992;74(2):251–60.
53. Rey-Ferro M, Castano R, Orozco O, Serna A, Moreno A.Nutritional and immunologic evaluation of patients withgastric cancer before and after surgery. Nutrition1997;13(10):878–81.
54. Guo CB, Ma DQ, Zhang KH. Applicability of the generalnutritional status score to patients with oral and max-illofacial malignancies. Int J Oral Maxillofac Surg1994;23(3):167–9.
55. Guo CB, Zhang W, Ma DQ, Zhang KH, Huang JQ. Hand gripstrength: an indicator of nutritional state and the mix ofpostoperative complications in patients with oral and max-illofacial cancers. Br J Oral Maxillofac Surg 1996;34(4):325–7.
56. Pedersen NW, Pedersen D. Nutrition as a prognosticindicator in amputations. A prospective study of 47 cases.Acta Orthop Scand 1992;63(6):675–8.
57. Mohler JL, Flanigan RC. The effect of nutritional status andsupport on morbidity and mortality of bladder cancerpatients treated by radical cystectomy. J Urol 1987;137(3):404–7.
58. Malone DL, Genuit T, Tracy JK, Gannon C, Napolitano LM.Surgical site infections: reanalysis of risk factors. J Surg Res2002;103(1):89–95.
59. Sandstrom R, Drott C, Hyltander A, et al. The effect ofpostoperative intravenous feeding (TPN) on outcomefollowing major surgery evaluated in a randomized study.Ann Surg 1993;217(2):185–95.
60. Correia MI, Caiaffa WT, da Silva AL, Waitzberg DL. Riskfactors for malnutrition in patients undergoing gastroen-terological and hernia surgery: an analysis of 374 patients.Nutr Hosp 2001;16(2):59–64.
61. Bozzetti F, Gianotti L, Braga M, Di CV, Mariani L. Reducingpostoperative complications through nutrients administra-tion in cancer patients. in press.
62. Butters M, Straub M, Kraft K, Bittner R. Studies onnutritional status in general surgery patients by clinical,
anthropometric, and laboratory parameters. Nutrition1996;12(6):405–10.
63. Lumbers M, New SA, Gibson S, Murphy MC. Nutritionalstatus in elderly female hip fracture patients: comparisonwith an age-matched home living group attending daycentres. Br J Nutr 2001;85(6):733–40.
64. Haugen M, Homme KA, Reigstad A, Teigland J. Assessmentof nutritional status in patients with rheumatoid arthritisand osteoarthritis undergoing joint replacement surgery.Arthritis Care Res 1999;12(1):26–32.
65. Saito T, Kuwahara A, Shigemitsu Y, et al. Factors related tomalnutrition in patients with esophageal cancer. Nutrition1991;7(2):117–21.
66. Weimann A, Meyer HJ, Muller MJ, et al. Significance ofpreoperative weight loss for perioperative metabolicadaptation and surgical risk in patients with tumors ofthe upper gastrointestinal tract. Langenbecks Arch Chir1992;377:45–52.
67. Bollschweiler E, Schroder W, Holscher AH, Siewert JR.Preoperative risk analysis in patients with adenocarcinomaor squamous cell carcinoma of the oesophagus. Br J Surg2000;87(8):1106–10.
68. Takagi K, Yamamori H, Morishima Y, Toyoda Y, Nakajima N,Tashiro T. Preoperative immunosuppression: its relationshipwith high morbidity and mortality in patients receivingthoracic esophagectomy. Nutrition 2001;17(1):13–7.
69. Padillo FJ, Andicoberry B, Muntane J, et al. Factorspredicting nutritional derangements in patients withobstructive jaundice: multivariate analysis. World J Surg2001;25(4):413–8.
70. Meyer L, Meyer FR, Dralle H, Lippert H, Gastinger I.East German study group for quality control in opera-tive medicine and regional development in surgery.Langenbecks Arch Surg 2005; August 6 (Epub ahead ofprint).
71. Moukarzel AA, Najm I, Vargas J, McDiarmid SV, Busuttil RW,Ament ME. Effect of nutritional status on outcome oforthotopic liver transplantation in pediatric patients.Transplant Proc 1990;22(4):1560–3.
72. Muller MJ, Lautz HU, Plogmann B, Burger M, Korber J,Schmidt FW. Energy expenditure and substrate oxidation inpatients with cirrhosis: the impact of cause, clinicalstaging and nutritional state. Hepatology 1992;15(5):782–94.
73. Shaw Jr BW, Wood RP, Gordon RD, Iwatsuki S, Gillquist WP,Starzl TE. Influence of selected patient variables andoperative blood loss on six- month survival following livertransplantation. Semin Liver Dis 1985;5(4):385–93.
74. Selberg O, Bottcher J, Tusch G, Pichlmayr R, Henkel E,Muller MJ. Identification of high- and low-risk patientsbefore liver transplantation: a prospective cohort study ofnutritional and metabolic parameters in 150 patients.Hepatology 1997;25(3):652–7.
75. Roggero P, Cataliotti E, Ulla L, et al. Factors influencingmalnutrition in children waiting for liver transplants. Am JClin Nutr 1997;65(6):1852–7.
76. Plochl W, Pezawas L, Artemiou O, Grimm M, Klepetko W,Hiesmayr M. Nutritional status, ICU duration and ICUmortality in lung transplant recipients. Intens Care Med1996;22(11):1179–85.
77. Schwebel C, Pin I, Barnoud D, et al. Prevalence andconsequences of nutritional depletion in lung transplantcandidates. Eur Respir J 2000;16(6):1050–5.
78. Linn BS, Robinson DS, Klimas NG. Effects of age andnutritional status on surgical outcomes in head and neckcancer. Ann Surg 1988;207(3):267–73.
ARTICLE IN PRESS
A. Weimann et al.240
79. Weimann A, Muller MJ, Adolph M, et al. Kriterien derUberwachung und des Erfolgs einer kunstlichen Ernahrung.Intensivmed 1997;34:744–8.
80. Weimann A. Appropriate indications for nutritional therapyin the cancer patient. Akt Ernahr-Med 2001;26:167–9.
81. Kornowski A, Cosnes J, Gendre JP, Quintrec Y. Enteralnutrition in malnutrition following gastric resection andcephalic pancreaticoduodenectomy. Hepatogastroenterol-ogy 1992;39(1):9–13.
82. Velez JP, Lince LF, Restrepo JI. Early enteral nutrition ingastrointestinal surgery: a pilot study. Nutrition 1997;13(5):442–5.
83. Hedberg AM, Lairson DR, Aday LA, et al. Economicimplications of an early postoperative enteral feedingprotocol. J Am Diet Assoc 1999;99(7):802–7.
84. Hamaoui E, Lefkowitz R, Olender L, et al. Enteral nutritionin the early postoperative period: a new semi- elementalformula versus total parenteral nutrition. J ParenterEnteral Nutr 1990;14(5):501–7.
85. Moore FA, Feliciano DV, Andrassy RJ, et al. Early enteralfeeding, compared with parenteral, reduces postoperativeseptic complications. The results of a meta-analysis. AnnSurg 1992;216(2):172–83.
86. Mochizuki H, Togo S, Tanaka K, Endo I, Shimada H. Earlyenteral nutrition after hepatectomy to prevent postopera-tive infection. Hepatogastroenterology 2000;47(35):1407–10.
87. Shaw-Stiffel TA, Zarny LA, Pleban WE, Rosman DD, RudolphRA, Bernstein LH. Effect of nutrition status and otherfactors on length of hospital stay after major gastrointest-inal surgery. Nutrition 1993;9:140–5.
88. Neumayer LA, Smout RJ, Horn HG, Horn SD. Early andsufficient feeding reduces length of stay and charges insurgical patients. J Surg Res 2001;95(1):73–7.
89. Weimann A, Muller MJ, Arend J, et al. Lebensqualitat alsKriterium des Erfolgs einer kunstlichen Ernahrung. Inten-sivmed 1998;35:724–6.
90. Bruning PF, Halling A, Hilgers FJ, et al. Postoperativenasogastric tube feeding in patients with head andneck cancer: a prospective assessment of nutritionalstatus and well-being. Eur J Cancer Clin Oncol 1988;24(2):181–8.
91. Hammerlid E, Wirblad B, Sandin C, et al. Malnutrition andfood intake in relation to quality of life in head and neckcancer patients. Head Neck 1998;20(6):540–8.
92. Guidelines for the use of parenteral and enteral nutrition inadult and pediatric patients. J Parenter Enteral Nutr2002;26(1 Suppl.):1SA–138SA.
93. Sagar S, Harland P, Shields R. Early postoperative feedingwith elemental diet. Br Med J 1979;1(6159):293–5.
94. Ryan Jr JA, Page CP, Babcock L. Early postoperative jejunalfeeding of elemental diet in gastrointestinal surgery. AmSurg 1981;47(9):393–403.
95. Bastow MD, Rawlings J, Allison SP. Benefits of supplemen-tary tube feeding after fractured neck of femur: arandomised controlled trial. Br Med J (Clin Res Ed)1983;287(6405):1589–92.
96. Shukla HS, Rao RR, Banu N, Gupta RM, Yadav RC. Enteralhyperalimentation in malnourished surgical patients.Indian J Med Res 1984;80:339–46.
97. Smith RC, Hartemink RJ, Hollinshead JW, Gillett DJ. Finebore jejunostomy feeding following major abdominalsurgery: a controlled randomized clinical trial. Br J Surg1985;72(6):458–61.
98. Muggia-Sullam M, Bower RH, Murphy RF, Joffe SN, FischerJE. Postoperative enteral versus parenteral nutritional
support in gastrointestinal surgery. A matched prospectivestudy. Am J Surg 1985;149(1):106–12.
99. Adams S, Dellinger EP, Wertz MJ, Oreskovich MR, Simono-witz D, Johansen K. Enteral versus parenteral nutritionalsupport following laparotomy for trauma: a randomizedprospective trial. J Trauma 1986;26(10):882–91.
100. Bower RH, Talamini MA, Sax HC, Hamilton F, Fischer JE.Postoperative enteral vs. parenteral nutrition. A rando-mized controlled trial. Arch Surg 1986;121(9):1040–5.
101. Moore FA, Moore EE, Jones TN, McCroskey BL, Peterson VM.TEN versus TPN following major abdominal trauma—re-duced septic morbidity. J Trauma 1989;29(7):916–22.
102. Delmi M, Rapin CH, Bengoa JM, Delmas PD, Vasey H,Bonjour JP. Dietary supplementation in elderly patientswith fractured neck of the femur. Lancet 1990;335(8696):1013–6.
103. Schroeder D, Gillanders L, Mahr K, Hill GL. Effects ofimmediate postoperative enteral nutrition on body com-position, muscle function, and wound healing. J ParenterEnteral Nutr 1991;15(4):376–83.
104. Kudsk KA, Croce MA, Fabian TC, et al. Enteral versusparenteral feeding. Effects on septic morbidity after bluntand penetrating abdominal trauma. Ann Surg 1992;215(5):503–11.
105. Meyenfeldt von M, Meijerink W, Roufflart M, BuilmaassenM, Soeters P. Perioperative nutritional support: a rando-mized clinical trial. Clin Nutr 1992;11:180–6.
106. Iovinelli G, Marsili I, Varrassi G. Nutrition support aftertotal laryngectomy. J Parenter Enteral Nutr 1993;17(5):445–8.
107. Dunham CM, Frankenfield D, Belzberg H, Wiles C, CushingB, Grant Z. Gut failure—predictor of or contributorto mortality in mechanically ventilated blunt traumapatients? J Trauma 1994;37(1):30–4.
108. Beier-Holgersen R, Boesby S. Influence of postoperativeenteral nutrition on postsurgical infections. Gut 1996;39(96):833–5.
109. Baigrie RJ, Devitt PG, Watkin DS. Enteral versus parenteralnutrition after oesophagogastric surgery: a prospectiverandomized comparison. Aust NZ J Surg 1996;66(10):668–70.
110. Carr CS, Ling KD, Boulos P, Singer M. Randomised trial ofsafety and efficacy of immediate postoperative enteralfeeding in patients undergoing gastrointestinal resection.BMJ 1996;312(7035):869–71.
111. Keele AM, Bray MJ, Emery PW, Duncan HD, Silk DB. Twophase randomised controlled clinical trial of postoperativeoral dietary supplements in surgical patients. Gut 1997;40(3):393–9.
112. Watters JM, Kirkpatrick SM, Norris SB, Shamji FM, Wells GA.Immediate postoperative enteral feeding results in im-paired respiratory mechanics and decreased mobility. AnnSurg 1997;226(3):369–77.
113. Reynolds JV, Kanwar S, Welsh FK, et al. 1997 Harry M. VarsResearch Award. Does the route of feeding modify gutbarrier function and clinical outcome in patients aftermajor upper gastrointestinal surgery? J Parenter EnteralNutr 1997;21(4):196–201.
114. Sand J, Luostarinen M, Matikainen M. Enteral or parenteralfeeding after total gastrectomy: prospective randomisedpilot study. Eur J Surg 1997;163(10):761–6.
115. Shirabe K, Matsumata T, Shimada M, et al. A comparison ofparenteral hyperalimentation and early enteral feedingregarding systemic immunity after major hepatic resec-tion—the results of a randomized prospective study.Hepatogastroenterology 1997;44(13):205–9.
ARTICLE IN PRESS
ESPEN Guidelines on Enteral Nutrition 241
116. Singh G, Ram RP, Khanna SK. Early postoperative enteralfeeding in patients with nontraumatic intestinal perfora-tion and peritonitis. J Am Coll Surg 1998;187(2):142–6.
117. Sullivan DH, Nelson CL, Bopp MM, Puskarich-May CL, WallsRC. Nightly enteral nutrition support of elderly hip fracturepatients: a phase I trial. J Am Coll Nutr 1998;17(2):155–61.
118. Beattie AH, Prach AT, Baxter JP, Pennington CR. Arandomised controlled trial evaluating the use of enteralnutritional supplements postoperatively in malnourishedsurgical patients. Gut 2000;46(6):813–8.
119. MacFie J, Woodcock NP, Palmer MD, Walker A, Townsend S,Mitchell CJ. Oral dietary supplements in pre- and post-operative surgical patients: a prospective and randomizedclinical trial. Nutrition 2000;16(9):723–8.
120. Espaulella J, Guyer H, Diaz-Escriu F, Mellado-Navas JA,Castells M, Pladevall M. Nutritional supplementation ofelderly hip fracture patients. A randomized, double-blind,placebo-controlled trial. Age Ageing 2000;29(5):425–31.
121. Braga M, Gianotti L, Gentilini O, Parisi V, Salis C, Di CV.Early postoperative enteral nutrition improves gut oxyge-nation and reduces costs compared with total parenteralnutrition. Crit Care Med 2001;29(2):242–8.
122. Malhotra A, Mathur AK, Gupta S. Early enteral nutritionafter surgical treatment of gut perforations: a prospectiverandomised study. J Postgrad Med 2004;50(2):102–6.
123. Smedley F, Bowling T, James M, et al. Randomized clinicaltrial of the effects of preoperative and postoperative oralnutritional supplements on clinical course and cost of care.Br J Surg 2004;91(8):983–90.
124. Mack LA, Kaklamanos IG, Livingstone AS, et al. Gastricdecompression and enteral feeding through a double-lumen gastrojejunostomy tube improves outcomes afterpancreaticoduodenectomy. Ann Surg 2004;240(5):845–51.
125. Sullivan DH, Nelson CL, Klimberg VS, Bopp MM. Nightlyenteral nutrition support of elderly hip fracture patients: apilot study. J Am Coll Nutr 2004;23(6):683–91.
126. Pacelli F, Bossola M, Papa V, et al. Enteral vs. parenteralnutrition after major abdominal surgery: an even match.Arch Surg 2001;136(8):933–6.
127. Bozzetti F, Braga M, Gianotti L, Gavazzi C, Mariani L.Postoperative enteral versus parenteral nutrition in mal-nourished patients with gastrointestinal cancer: a rando-mised multicentre trial. Lancet 2001;358(9292):1487–92.
128. Martignoni ME, Friess H, Sell F, et al. Enteral nutritionprolongs delayed gastric emptying in patients afterWhipple resection. Am J Surg 2000;180(1):18–23.
129. Lim ST, Choa RG, Lam KH, Wong J, Ong GB. Total parenteralnutrition versus gastrostomy in the preoperative prepara-tion of patients with carcinoma of the oesophagus. Br JSurg 1981;68(2):69–72.
130. McArdle AH, Reid EC, Laplante MP, Freeman CR. Prophylaxisagainst radiation injury. The use of elemental diet prior toand during radiotherapy for invasive bladder cancer and inearly postoperative feeding following radical cystectomyand ileal conduit. Arch Surg 1986;121(8):879–85.
131. Fletcher JP, Little JM. A comparison of parenteral nutritionand early postoperative enteral feeding on the nitrogenbalance after major surgery. Surgery 1986;100(1):21–4.
132. Nissila MS, Perttila JT, Salo MS, Havia TV. Natural killer cellactivity after immediate postoperative enteral and par-enteral nutrition. Acta Chir Scand 1989;155(4–5):229–32.
133. Magnusson J, Tranberg KG, Jeppsson B, Lunderquist A.Enteral versus parenteral glucose as the sole nutritionalsupport after colorectal resection. A prospective, rando-mized comparison. Scand J Gastroenterol 1989;24(5):539–49.
134. Hwang TL, Huang SL, Chen MF. Early nasoduodenal feedingfor the post-biliary surgical patient. J Formos Med Assoc1991;90(10):993–7.
135. Suchner U, Senftleben U, Eckart T, et al. Enteral versusparenteral nutrition: effects on gastrointestinal functionand metabolism. Nutrition 1996;12(1):13–22.
136. Hochwald SN, Harrison LE, Heslin MJ, Burt ME, Brennan MF.Early postoperative enteral feeding improves whole bodyprotein kinetics in upper gastrointestinal cancer patients.Am J Surg 1997;174(3):325–30.
137. Beier-Holgersen R, Brandstrup B. Influence of early post-operative enteral nutrition versus placebo on cell-mediated immunity, as measured with the Multitest CMI.Scand J Gastroenterol 1999;34(1):98–102.
138. Brooks AD, Hochwald SN, Heslin MJ, Harrison LE, Burt M,Brennan MF. Intestinal permeability after early postopera-tive enteral nutrition in patients with upper gastrointest-inal malignancy. J Parenter Enteral Nutr 1999;23(2):75–9.
139. Hu QG, Zheng QC. The influence of enteral nutrition inpostoperative patients with poor liver function. World JGastroenterol 2003;9(4):843–6.
140. Braunschweig CL, Levy P, Sheean PM, Wang X. Enteralcompared with parenteral nutrition: a meta-analysis. Am JClin Nutr 2001;74(4):534–42.
141. Peter JV, Moran JL, Phillips-Hughes J. A metaanalysis oftreatment outcomes of early enteral versus early parent-eral nutrition in hospitalized patients. Crit Care Med2005;33(1):213–20.
142. Dhaliwal R, Jurewitsch B, Harrietha D, Heyland DK.Combination enteral and parenteral nutrition in criticallyill patients: harmful or beneficial? A systematic review ofthe evidence. Intens Care Med 2004;30(8):1666–71.
143. The Veterans Affairs Total Parenteral Nutrition CooperativeStudy Group. Perioperative total parenteral nutrition insurgical patients. N Engl J Med 1991;325(8):525–32.
144. Heyland DK, Montalvo M, MacDonald S, Keefe L, Su XY,Drover JW. Total parenteral nutrition in the surgicalpatient: a meta-analysis. Can J Surg 2001;44(2):102–11.
145. MacFie J. European round table: the use of immunonu-trients in the critically ill. Clin Nutr 2004;23(6):1426–9.
146. Braga M, Gianotti L, Radaelli G, et al. Perioperativeimmunonutrition in patients undergoing cancer surgery:results of a randomized double-blind phase 3 trial. ArchSurg 1999;134(4):428–33.
147. Senkal M, Zumtobel V, Bauer KH, et al. Outcome and cost-effectiveness of perioperative enteral immunonutrition inpatients undergoing elective upper gastrointestinal tractsurgery: a prospective randomized study. Arch Surg1999;134(12):1309–16.
148. Tepaske R, Velthuis H, Oudemans-van Straaten HM, et al.Effect of preoperative oral immune-enhancing nutritionalsupplement on patients at high risk of infection aftercardiac surgery: a randomised placebo-controlled trial.Lancet 2001;358(9283):696–701.
149. Braga M, Gianotti L, Vignali A, Carlo VD. Preoperative oralarginine and n-3 fatty acid supplementation improvesthe immunometabolic host response and outcome aftercolorectal resection for cancer. Surgery 2002;132(5):805–14.
150. Braga M, Gianotti L, Nespoli L, Radaelli G, Di Carlo V.Nutritional approach in malnourished surgical patients: aprospective randomized study. Arch Surg 2002;137(2):174–80.
151. Gianotti L, Braga M, Nespoli L, Radaelli G, Beneduce A,Di Carlo V. A randomized controlled trial of preoperativeoral supplementation with a specialized diet in patients
ARTICLE IN PRESS
A. Weimann et al.242
with gastrointestinal cancer. Gastroenterology 2002;122(7):1763–70.
152. Braga M, Gianotti L. Preoperative immunonutrition: cost-benefit analysis. J Parenter Enteral Nutr 2005;29(1Suppl.):S57–61.
153. Marik PE, Zaloga GP. Early enteral nutrition in acutely illpatients: a systematic review. Crit Care Med 2001;29(12):2264–70.
154. Schilder JM, Hurteau JA, Look KY, et al. A prospectivecontrolled trial of early postoperative oral intake followingmajor abdominal gynecologic surgery. Gynecol Oncol1997;67(3):235–40.
155. Stewart BT, Woods RJ, Collopy BT, Fink RJ, Mackay JR, KeckJO. Early feeding after elective open colorectal resections:a prospective randomized trial. Aust NZ J Surg1998;68(2):125–8.
156. Moiniche S, Bulow S, Hesselfeldt P, Hestbaek A, Kehlet H.Convalescence and hospital stay after colonic surgery withbalanced analgesia, early oral feeding, and enforcedmobilisation. Eur J Surg 1995;161(4):283–8.
157. Kompan L, Vidmar G, Spindler-Vesel A, Pecar J. Is earlyenteral nutrition a risk factor for gastric intolerance andpneumonia? Clin Nutr 2004;23(4):527–32.
158. Daly JM, Bonau R, Stofberg P, Bloch A, Jeevanandam M,Morse M. Immediate postoperative jejunostomy feeding.Clinical and metabolic results in a prospective trial. Am JSurg 1987;153(2):198–206.
159. Kemen M, Senkal M, Homann HH, et al. Early postoperativeenteral nutrition with arginine-omega-3 fatty acids andribonucleic acid-supplemented diet versus placebo incancer patients: an immunologic evaluation of Impact.Crit Care Med 1995;23(4):652–9.
160. Braga M, Gianotti L, Gentilini O, Liotta S, Di CV. Feedingthe gut early after digestive surgery: results of a nine-yearexperience. Clin Nutr 2002;21(1):59–65.
161. Seven H, Calis AB, Turgut S. A randomized controlled trialof early oral feeding in laryngectomized patients. Laryngo-scope 2003;113(6):1076–9.
162. Kompan L, Kremzar B, Gadzijev E, Prosek M. Effects ofearly enteral nutrition on intestinal permeability and thedevelopment of multiple organ failure after multipleinjury. Intens Care Med 1999;25(2):157–61.
163. Brown RO, Hunt H, Mowatt-Larssen CA, Wojtysiak SL,Henningfield MF, Kudsk KA. Comparison of specialized andstandard enteral formulas in trauma patients. Pharma-cotherapy 1994;14(3):314–20.
164. Moore FA, Moore EE, Kudsk KA, et al. Clinical benefits of animmune-enhancing diet for early postinjury enteral feed-ing. J Trauma 1994;37(4):607–15.
165. Daly JM, Lieberman MD, Goldfine J, et al. Enteral nutritionwith supplemental arginine, RNA, and omega-3 fatty acidsin patients after operation: immunologic, metabolic, andclinical outcome. Surgery 1992;112(1):56–67.
166. Bower RH, Cerra FB, Bershadsky B, et al. Early enteraladministration of a formula (Impact) supplemented witharginine, nucleotides, and fish oil in intensive care unitpatients: results of a multicenter, prospective, rando-mized, clinical trial. Crit Care Med 1995;23(3):436–49.
167. Daly JM, Weintraub FN, Shou J, Rosato EF, Lucia M. Enteralnutrition during multimodality therapy in upper gastro-intestinal cancer patients. Ann Surg 1995;221(4):327–38.
168. Kudsk KA, Minard G, Croce MA, et al. A randomized trial ofisonitrogenous enteral diets after severe trauma. Animmune-enhancing diet reduces septic complications. AnnSurg 1996;224(4):531–40.
169. Gianotti L, Braga M, Vignali A, et al. Effect of route ofdelivery and formulation of postoperative nutritionalsupport in patients undergoing major operations formalignant neoplasms. Arch Surg 1997;132(11):1222–9.
170. Heslin MJ, Latkany L, Leung D, et al. A prospective,randomized trial of early enteral feeding after resection ofupper gastrointestinal malignancy. Ann Surg 1997;226(4):567–77.
171. Mendez C, Jurkovich GJ, Garcia I, Davis D, Parker A, MaierRV. Effects of an immune-enhancing diet in criticallyinjured patients. J Trauma 1997;42(5):933–40.
172. Senkal M, Mumme A, Eickhoff U, et al. Early postoperativeenteral immunonutrition: clinical outcome and cost-com-parison analysis in surgical patients. Crit Care Med1997;25(9):1489–96.
173. Weimann A, Bastian L, Bischoff WE, et al. Influence ofarginine, omega-3 fatty acids and nucleotide-supplemen-ted enteral support on systemic inflammatory responsesyndrome and multiple organ failure in patients aftersevere trauma. Nutrition 1998;14(2):165–72.
174. Snyderman CH, Kachman K, Molseed L, et al. Reducedpostoperation infections with an immune-enhancing nutri-tional supplement. Laryngoscope 1999;109(6):915–21.
175. Heys SD, Walker LG, Smith I, Eremin O. Enteral nutritionalsupplementation with key nutrients in patients withcritical illness and cancer: a meta-analysis of randomizedcontrolled clinical trials. Ann Surg 1999;229(4):467–77.
176. Beale RJ, Bryg DJ, Bihari DJ. Immunonutrition in thecritically ill: a systematic review of clinical outcome. CritCare Med 1999;27(12):2799–805.
177. Heyland DK, Novak F, Drover JW, Jain M, Su X, Suchner U.Should immunonutrition become routine in critically illpatients? A systematic review of the evidence. JAMA2001;286(8):944–53.
178. Montejo JC, Zarazaga A, Lopez-Martinez J, et al. Immuno-nutrition in the intensive care unit. A systematic reviewand consensus statement. Clin Nutr 2003;22(3):221–33.
179. Farreras N, Artigas V, Cardona D, Rius X, Trias M, GonzalezJA. Effect of early postoperative enteral immunonutritionon wound healing in patients undergoing surgery for gastriccancer. Clin Nutr 2005;24(1):55–65.
180. Strickland A, Brogan A, Krauss J, Martindale R, Cresci G. Isthe use of specialized nutritional formulations a cost-effective strategy? A national database evaluation.J Parenter Enteral Nutr 2005;29(1 Suppl.):S81–91.
181. Consensus recommendations from the US summitt onimmune-enhancing enteral therapy. J Parenter EnteralNutr 2001;25(2 Suppl.):S61–3.
182. Garcia-de-Lorenzo A, Zarazaga A, Garcia-Luna PP, et al.Clinical evidence for enteral nutritional support withglutamine: a systematic review. Nutrition 2003;19(9):805–11.
183. Houdijk AP, Rijnsburger ER, Jansen J, et al. Randomisedtrial of glutamine-enriched enteral nutrition on infectiousmorbidity in patients with multiple trauma. Lancet1998;352(9130):772–6.
184. Conejero R, Bonet A, Grau T, et al. Effect of a glutamine-enriched enteral diet on intestinal permeability andinfectious morbidity at 28 days in critically ill patientswith systemic inflammatory response syndrome: a rando-mized, single-blind, prospective, multicenter study. Nutri-tion 2002;18(9):716–21.
185. Zhou YP, Jiang ZM, Sun YH, Wang XR, Ma EL, Wilmore D. Theeffect of supplemental enteral glutamine on plasma levels,gut function, and outcome in severe burns: a randomized,
ARTICLE IN PRESS
ESPEN Guidelines on Enteral Nutrition 243
double-blind, controlled clinical trial. J Parenter EnteralNutr 2003;27(4):241–5.
186. Rayes N, Hansen S, Seehofer D, et al. Early enteral supplyof fiber and lactobacillus versus conventional nutrition: arandomized controlled trial in patients with major abdom-inal surgery. Nutrition 2002;18:609–15.
187. Falcao De Arruda IS, de Aguilar-Nascimento JE. Benefits ofearly enteral nutrition with glutamine and probiotics inbrain injury patients. Clin Sci (London) 2004;106(3):287–92.
188. Delany HM, Carnevale N, Garvey JW, Moss GM. Post-operative nutritional support using needle catheter feedingjejunostomy. Ann Surg 1977;186(2):165–70.
189. Bruining HA, Schattenkerk ME, Obertop H, Ong GL. Acuteabdominal pain due to early postoperative elementalfeeding by needle jejunostomy. Surg Gynecol Obstet1983;157(1):40–2.
190. Schattenkerk ME, Obertop H, Bruining HA, Van Rooyen W,Van Houten E. Early postoperative enteral feeding by aneedle catheter jejunostomy after 100 esophageal resec-tions and reconstructions for cancer. Clin Nutr 1984;3:47.
191. Strickland GF, Greene FL. Needle-catheter jejunostomy forpostoperative nutritional support. South Med J 1986;79(11):1389–92.
192. Vestweber KH, Eypasch E, Paul A, Bode C, Troidl H.Feinnadel-Katheter-Jejunostomie. Z Gastroenterol 1989;27(Suppl. 2):69–72.
193. Myers JG, Page CP, Stewart RM, Schwesinger WH, SirinekKR, Aust JB. Complications of needle catheter jejunostomyin 2022 consecutive applications. Am J Surg 1995;170(6):547–50.
194. Eddy VA, Snell JE, Morris Jr JA. Analysis of complicationsand long-term outcome of trauma patients with needlecatheter jejunostomy. Am Surg 1996;62(1):40–4.
195. Sarr MG. Appropriate use, complications and advantagesdemonstrated in 500 consecutive needle catheter jejunos-tomies. Br J Surg 1999;86(4):557–61.
196. Biffi R, Lotti M, Cenciarelli S, et al. Complications and long-term outcome of 80 oncology patients undergoing needlecatheter jejunostomy placement for early postoperativeenteral feeding. Clin Nutr 2000;19(4):277–9.
197. Senkal M, Koch J, Hummel T, Zumtobel V. Laparoscopicneedle catheter jejunostomy: modification of the techni-que and outcome results. Surg Endosc 2004;18(2):307–9.
198. Gaddy MC, Max MH, Schwab CW, Kauder D. Small bowelischemia: a consequence of feeding jejunostomy? SouthMed J 1986;79(2):180–2.
199. Brenner DW, Schellhammer PF. Mortality associated withfeeding catheter jejunostomy after radical cystectomy.Urology 1987;30:337–40.
200. Rai J, Flint LM, Ferrara JJ. Small bowel necrosis inassociation with jejunostomy tube feedings. Am Surg1996;62(12):1050–4.
201. Lawlor DK, Inculet RI, Malthaner RA. Small-bowel necrosisassociated with jejunal tube feeding. Can J Surg1998;41(6):459–62.
202. Scaife CL, Saffle JR, Morris SE. Intestinal obstructionsecondary to enteral feedings in burn trauma patients. JTrauma 1999;47(5):859–63.
203. Jorba R, Fabregat J, Borobia FG, Torras J, Poves I, JaurrietaE. Small bowel necrosis in association with early post-operative enteral feeding after pancreatic resection.Surgery 2000;128(1):111–2.
204. Zern RT, Clarke-Pearson DL. Pneumatosis intestinalisassociated with enteral feeding by catheter jejunostomy.Obstet Gynecol 1985;65(3 Suppl.):81S–3S.
205. Schloerb PR, Wood JG, Casillan AJ, Tawfik O, Udobi K.Bowel necrosis caused by water in jejunal feeding. JParenter Enteral Nutr 2004;28(1):27–9.
206. Loser C, Aschl G, Hebuterne X, et al. ESPEN guidelines onartificial enteral nutrition—percutaneous endoscopic gas-trostomy (PEG). Clin Nutr 2005;24(5):848–61.
207. Dennis MS, Lewis SC, Warlow C. Effect of timing andmethod of enteral tube feeding for dysphagic strokepatients (FOOD): a multicentre randomised controlledtrial. Lancet 2005;365(9461):764–72.
208. Ulander K, Jeppsson B, Grahn G. Postoperative energyintake in patients after colorectal cancer surgery. Scand JCaring Sci 1998;12(3):131–8.
209. Bae JM, Park JW, Yang HK, Kim JP. Nutritional status ofgastric cancer patients after total gastrectomy. World JSurg 1998;22(3):254–60.
210. Harrison J, McKiemann J, Neuberger JM. A prospectivestudy on the effect of recipient nutritional status onoutcome in liver transplantation. Transplant Int1997;10:369–74.
211. Figueiredo F, Dickson ER, Pasha T, et al. Impact ofnutritional status on outcomes after liver transplantation.Transplantation 2000;70(9):1347–52.
212. Forli L, Pedersen JI, Bjortuft O, Vatn M, Boe J. Dietarysupport to underweight patients with end-stage pulmonarydisease assessed for lung transplantation. Respiration2001;68(1):51–7.
213. Le Cornu KA, McKiernan FJ, Kapadia SA, Neuberger JM. Aprospective randomized study of preoperative nutritionalsupplementation in patients awaiting elective orthotopicliver transplantation. Transplantation 2000;69(7):1364–9.
214. Chin SE, Shepherd RW, Thomas BJ, et al. Nutritionalsupport in children with end-stage liver disease: arandomized crossover trial of a branched-chain amino acidsupplement. Am J Clin Nutr 1992;56(1):158–63.
215. Plank LD, McCall JL, Gane EJ, et al. Pre- and postoperativeimmunonutrition in patients undergoing liver transplanta-tion: a pilot study of safety and efficacy. Clin Nutr2005;24(2):288–96.
216. Lindell SL, Hansen T, Rankin M, Danielewicz R, Belzer FO,Southard JH. Donor nutritional status—a determinant ofliver preservation injury. Transplantation 1996;61(2):239–47.
217. Plauth M, Merli M, Kondrup J, et al. Guidelines for nutritionin liver disease and transplantation. Clin Nutr 1997;16:43–55.
218. Weimann A, Kuse ER, Bechstein WO, Neuberger JM, PlauthM, Pichlmayr R. Perioperative parenteral and enteralnutrition for patients undergoing orthotopic liver trans-plantation. Results of a questionnaire from 16 Europeantransplant units. Transpl Int 1998;11(Suppl. 1):S289–91.
219. Murray M, Grogan TA, Lever J, Warty VS, Fung J,Venkataramanan R. Comparison of tacrolimus absorptionin transplant patients receiving continuous versus inter-rupted enteral nutritional feeding. Ann Pharmacother1998;32(6):633–6.
220. Wicks C, Somasundaram S, Bjarnason I, et al. Comparisonof enteral feeding and total parenteral nutrition after livertransplantation. Lancet 1994;344(8926):837–40.
221. Hasse JM, Blue LS, Liepa GU, et al. Early enteral nutritionsupport in patients undergoing liver transplantation. JParenter Enteral Nutr 1995;19(6):437–43.
222. Rayes N, Seehofer D, Hansen S, et al. Early enteral supplyof lactobacillus and fiber versus selective bowel deconta-mination: a controlled trial in liver transplant recipients.Transplantation 2002;74(1):123–7.
ARTICLE IN PRESS
A. Weimann et al.244
223. Rayes N, Seehofer D, Theruvath T, et al. Supply of pre- andprobiotics reduces bacterial infection rates after livertransplantation—a randomized, double-blind trial. Am JTransplant 2005;5(1):125–30.
224. Pescowitz MD, Mehta PL, Leapman SB, Milgrom ML, JindalRM, Filo RS. Tube jejunostomy in liver transplant patients.Surgery 1995;117:642–7.
225. Rovera GM, Strohm S, Bueno J, et al. Nutritional monitoringof pediatric intestinal transplant recipients. TransplantProc 1998;30(6):2519–20.
226. Schulz RJ, Dignass A, Pascher A, et al. New dietaryconcepts in small bowel transplantation. Transplant Proc2002;34(3):893–5.
227. Rovera GM, Schoen RE, Goldbach B, et al. Intestinal andmultivisceral transplantation: dynamics of nutritionalmanagement and functional autonomy. J Parenter EnteralNutr 2003;27(4):252–9.
228. Thorell A, Nygren J, Ljungqvist O. Insulin resistance: amarker of surgical stress. Curr Opin Clin Nutr Metab Care1999;2:69–78.
229. Jeejeebhoy KN, Detsky AS, Baker JP. Assessment ofnutritional status. J Parent Enteral Nutr 1990;14(Suppl):1935–55.
230. Lassen K, Dejong CHC, Ljungqvist O, et al. Nutritionalsupport and oral intake after gastric resection in fivenorthern European countries. Dig Surg 2005;22:346–52.
231. Schutz T, Herbst B, Koller M. Methodology for thedevelopment of the ESPEN Guidelines on Enteral Nutrition.Clin Nutr 2006;25(2):203–9.
232. Lochs H, Allison SP, Meier R, Pirlich M, Kondrup J,Schneider St., van den Berghe G, Pichard C. Introductoryto the ESPEN Guidelines on Enteral Nutrition: Terminology,Definitions and General Topics. Clin Nutr 2006;25(2):180–6.