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Clinical Nutrition 39 (2020) 612e631
Contents lists available at ScienceDirect
Clinical Nutrition
journal homepage: http://www.elsevier.com/locate/clnu
ESPEN Guideline
ESPENguideline on clinical nutrition in acute and chronic pancreatitis
a, * b c d
Marianna Arvanitakis , Johann Ockenga , Mihailo Bezmarevic , Luca Gianotti ,
e f, g € h i j
Zeljko Krznaric , Dileep N. Lobo , Christian Loser , Christian Madl , Remy Meier ,
k l m n
MaryPhillips , Henrik Højgaard Rasmussen , Jeanin E. Van Hooft , Stephan C. Bischoff
a Department of Gastroenterology, Erasme University Hospital ULB, Brussels, Belgium
b Department of Gastroenterology, Endocrinology and Clinical Nutrition, Klinikum Bremen Mitte, Bremen, Germany
c Department of Hepatobiliary and Pancreatic Surgery, Clinic for General Surgery, Military Medical Academy, University of Defense, Belgrade, Serbia
d School of Medicine and Surgery, University of Milano-Bicocca and Department of Surgery, San Gerardo Hospital, Monza, Italy
e Department of Gastroenterology, Hepatology and Nutrition, Clinical Hospital Centre & School of Medicine, Zagreb, Croatia
f Gastrointestinal Surgery, Nottingham Digestive Diseases Centre, National Institute for Health Research. (NIHR) Nottingham Biomedical Research Centre,
Nottingham University Hospitals NHS Trust, University of Nottingham, Queen's Medical Centre, Nottingham, NG7 2UH, UK
g MRC Versus Arthritis Centre for Musculoskeletal Ageing Research, School of Life Sciences, University of Nottingham, Queen's Medical Centre, Nottingham
NG7 2UH, UK
h Medical Clinic, DRK-Kliniken Nordhessen, Kassel, Germany
i Division of Gastroenterology and Hepatology, Krankenanstalt Rudolfstiftung, Krankenanstaltenverbund Wien (KAV), Vienna, Austria
j AMB-Praxis-MagenDarm Basel, Basel, Switzerland
k Department of Nutrition and Dietetics, Royal Surrey County Hospital NHS Foundation Trust, Guildford, UK
l Centre for Nutrition and Bowel Disease, Department of Gastroenterology, Aalborg University Hospital, Faculty of Health, Aalborg University, Aalborg,
Denmark
mDepartment of Gastroenterology & Hepatology, Amsterdam Gastroenterology and Metabolism, Amsterdam UMC, University of Amsterdam, Amsterdam,
the Netherlands
n Institute of Nutritional Medicine, University of Hohenheim, Stuttgart, Germany
articleinfo summary
Article history: Bothacuteandchronicpancreatitis are frequent diseases of the pancreas, which, despite being of benign
Received 29 December 2019 nature, are related to a significant risk of malnutrition and may require nutritional support. Acute
Accepted 8 January 2020 necrotizing pancreatitis is encountered in 20% of patients with acute pancreatitis, is associated with
increased morbidity and mortality, and may require artificial nutrition by enteral or parenteral route, as
Keywords: well as additional endoscopic, radiological or surgical interventions. Chronic pancreatitis represents a
Acute pancreatitis chronic inflammation of the pancreatic gland with development of fibrosis. Abdominal pain leading to
Chronic pancreatitis decreasedoralintake, as well as exocrine and endocrine failure are frequent complications of the disease.
Pancreatic diseases All of the above represent risk factors related to malnutrition. Therefore, patients with chronic pancre-
Nutrition atitis should be considered at risk, screened and supplemented accordingly. Moreover, osteoporosis and
Nutritional support
Medical nutrition increased facture risk should be acknowledged in patients with chronic pancreatitis, and preventive
measures should be considered.
©2020 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.
1. Introduction cornerstones of management [3]. A significant amount of research
has shown the superiority of enteral over parenteral nutrition in
Acute pancreatitis (AP) is the most common acute gastrointes- ANP, creating a paradigm shift a decade ago and modifying the
tinal disease requiring hospital admission [1], with the outcome management strategy [3]. Nevertheless, additional questions
beingfavorableinmostcases(80%)[2].However,acutenecrotizing regarding the timing, route and type of enteral nutrition (EN), as
pancreatitis (ANP) may develop in up to 20% of patients and is well as the place of oral refeeding, are still the objects of clinical
associated with significant rates of early organ failure (38%), need investigations.
for intervention (38%), and death (15%) [2]. Catabolism is very high Chronic pancreatitis (CP) is a disease in which recurrent in-
in this setting; therefore, nutritional support is one of the flammatory episodes lead to replacement of the pancreatic pa-
* Corresponding author. renchymabyfibrousconnectivetissue [4]. The major consequence
E-mail address: Marianna.arvanitaki@erasme.ulb.ac.be (M. Arvanitakis). of CP is the loss of functional exocrine and endocrine pancreatic
https://doi.org/10.1016/j.clnu.2020.01.004
0261-5614/© 2020 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.
M. Arvanitakis et al. / Clinical Nutrition 39 (2020) 612e631 613
Abbreviations MUST Malnutrition Universal Screening Tool
NAFLD NonAlcoholic Fatty Liver Disease
ACS Abdominal Compartment Syndrome ONS Oral Nutritional Supplements
ANP Acute Necrotizing Pancreatitis PEG-J Percutaneous Endoscopic Gastrostomy with Jejunal
AP Acute Pancreatitis Extension
BMI Body Mass Index PEI Pancreatic Exocrine Insufficiency
CP Chronic Pancreatitis PERT Pancreatic Enzyme Replacement Therapy
DPEJ Direct Percutaneous Endoscopic Jejunostomy PN Parenteral Nutrition
DXA Dual-energy X-ray Absorptiometry PPI Proton Pump Inhibitor
EN Enteral Nutrition RCT Randomized Controlled Trial
IAH Intra-abdominal Hypertension SIBO Small Intestinal Bacterial Overgrowth
IAP Intra-abdominal Pressure VARD Video-assisted Retroperitoneal Debridement
MCT MediumChainTriglycerides
tissue, thus resulting in both exocrine and endocrine insufficiency practice point (GPP) is based on experts' opinions due to the lack
[4]. Pain is also frequently encountered in patients with CP, and of studies, here, the wording can be chosen deliberately.
seems to be related to a multitude of factors such as pancreatic Online voting on the recommendations was performed on the
neural remodeling and neuropathy, increased intraductal and guideline-services.com platform. All ESPEN members were invited
parenchymal pressure, pancreatic ischemia and acute inflamma- toagreeordisagreewiththerecommendationsandtocommenton
tion during an acute relapse [5]. Both pain and loss of pancreatic them. A first draft of the guideline was also made available to the
functioncanleadtomalnutritioninpatientswithCP[4].Moreover, participants; on that occasion 36 recommendations and all seven
other long-term consequences such as osteoporosis are frequently statements reached an agreement of >90%, six recommendations
overlooked, despite their potential impact on quality of life in pa- reached an agreement of 75e90% and no recommendation an
tientswithCP.Therefore,screeningformalnutritionandnutritional agreementof<75%.Thoserecommendationswithanagreementof
supportplayacrucialpartinthemultimodalmanagementrequired >90%, which means a strong consensus (Table 3) were passed
in this setting. directly; all others were revised according to the comments and
Although recent guidelines for AP [2] and CP [4] have been votedonagainduringaconsensusconference,whichtookplaceon
published, a dedicated consensus on nutritional support in 29th April 2019. All recommendations received an agreement of
pancreatic diseases is lacking. >90%. During the consensus conference, one of the original rec-
ommendations was considered redundant and one statement was
2. Methods transformed into a recommendation. Therefore, the guideline
comprises42recommendationsandsixstatements.Tosupportthe
Thepresentguideline was developed according to the standard recommendationsandtheassignedgradesofrecommendation,the
operating procedure for ESPEN guidelines [6]. The guideline was ESPEN guideline office created evidence tables of relevant meta-
developed byan expert group of 13 authors from eleven European analyses, systematic reviews and randomized controlled trials
countries. (RCTs). These evidence tables are available online as supplemental
material to this guideline.
2.1. Methodology of guideline development
2.2. Search strategy
Based on the standard operating procedures for ESPEN guide-
lines and consensus papers, the first step of the guideline devel- A comprehensive literature research including systematic re-
opment was the formulation of so-called PICO questions which views, controlled clinical trials and cohort studies, with the key-
address specific patient groups or problems, interventions, wordsandfilters presented in Table 4 was performed. We initially
compare different therapies and are outcome-related [6]. In total, searched Pubmed, Cochrane Library and EMBASE for recent,
31 PICO questions were created and split into two main chapters, rigorous systematic reviews and meta-analyses that answered our
“Acute pancreatitis” and “Chronic Pancreatitis”. To answer these clinical questions. In the absence of these, we looked for compar-
PICO questions, a literature search was performed to identify suit- ative studies, whether randomized or not. The search phrases
able meta-analyses, systematic reviews and primary studies, pub- included the following terms: (acute pancreatitis OR acute necro-
lished from 1977 up to December 2018. The PICO questions were tizing pancreatitis OR chronic pancreatitis OR pancreatitis OR
allocated to subgroups/experts for the different subjects who hypertriglyceridemic pancreatitis OR hyperlipidemic pancreatitis)
created 42 recommendations and seven statements. For grading AND (nutritional status OR nutritional assessment OR nutritional
the literature, the grading system of the Scottish Intercollegiate screening OR malnutrition OR oral feeding OR enteral nutrition OR
Guidelines Network (SIGN) was used [7]. Allocation of studies to tube feeding OR parenteral nutrition OR intravenous nutrition OR
the different levels of evidence is shown in Table 1. Supportive of timing OR formula OR formulation OR nasogastric tube OR naso-
the recommendations, the working group added commentaries to jejunal tube OR digestive intolerance OR necrosectomy OR mini-
therecommendationswherethebasesoftherecommendationsare mally invasive OR increased intra-abdominal pressure OR
explained. abdominal compartment syndrome OR open abdomen OR immu-
The recommendations were graded according to the levels of nonutrition OR glutamine OR antioxidants OR probiotics OR
evidence assigned (Table 2). The wording of the recommenda- enzyme supplementation OR enzyme replacement therapy OR
tions reflect the grades of recommendations, level A is indicated micronutrients OR macronutrients OR nutrient deficiency OR diet
by “shall”, level B by “should” and level 0 by “can/may”. The good OR fat OR nitrogen OR dietary protein OR carbohydrates oral
614 M. Arvanitakis et al. / Clinical Nutrition 39 (2020) 612e631
Table 1
Levels of evidence.
1þþ High quality meta-analyses, systematic reviews of RCTs, or RCTs with a very low risk of bias
1þ Well-conducted meta-analyses, systematic reviews, or RCTs with a low risk of bias
1- Meta-analyses, systematic reviews, or RCTs with a high risk of bias
2þþ High quality systematic reviews of case control or cohort studies. High quality case control or cohort studies with a very
low risk of confounding or bias and a high probability that the relationship is causal
2þ Well-conducted case control or cohort studies with a low risk of confounding or bias and a moderate probability that the relationship is causal
2- Case control or cohort studies with a high risk of confounding or bias and a significant risk that the relationship is not causal
3 Non-analytic studies, e.g. case reports, case series
4 Expert opinion
AccordingtotheScottishIntercollegiateGuidelines Network(SIGN)gradingsystem.Source:SIGN50:Aguidelinedeveloper'shandbook.QuickreferenceguideOctober2014
[SIGN 50]. RCT ¼ randomized controlled trial.
Table 2
Grades of recommendation [6].
A At least one meta-analysis, systematic review, or RCT rated as 1þþ, and directly applicable to the target
population; or A body of evidence consisting principally of studies rated as 1þ, directly applicable to the target population,
and demonstrating overall consistency of results
B Abodyofevidence including studies rated as 2þþ, directly applicable to the target population; or A body of evidence
including studies rated as 2þ, directly applicable to the target population and demonstrating overall consistency
of results; or Extrapolated evidence from studies rated as 1þþ or 1þ
0 Evidence level 3 or 4; or Extrapolated evidence from studies rated as 2þþ or 2þ
GPP Good practice points/expert consensus: Recommended best practice based on the clinical experience of the guideline development group
RCT ¼ randomized controlled trial.
Table 3 Recommendation 1
Classification of the strength of consensus.
Strong consensus Agreement of >90% of the participants
Consensus Agreement of >75e90% of the participants
Majority agreement Agreement of 50e75% of the participants
Noconsensus Agreement of <50% of the participants All patients with predicted mild to moderate AP should be
According to the AWMF (Arbeitsgemeinschaft der Wissenschaftlichen Medi- screened using validated screening methods such as the
zinischen Fachgesellschaften, Association of the Scientific Medical Societies in Nutritional Risk Screeninge2002(NRS-2002);however,the
Germany) methodology [8]. patients with predicted severe AP should always be
considered at nutritional risk.
Table 4 Grade of Recommendation B e Strong consensus (100%
Criteria for systematic search for literature e databases, filters and keywords. agreement).
Publication date From 1977 to December 2018
Language English
Databases Pubmed, EMBASE, Cochrane library
Filters human Commentary
Publication type Cohort study, controlled trial, systematic review
Keywords Acute pancreatitis, chronic pancreatitis, nutrition Fortunately, the majority of patients with AP have predicted
mildormoderatelysevereformsofthediseasethatareself-limited
supplementation OR medium chained triglycerides OR osteopo- withfullyrecoveryinlessthanaweek,inwhomoralfeedingcanbe
rosis OR osteopenia). started within few days after the onset of AP [9]. Gut-barrier
Finally, 88 articles were selected for the AP chapter, and 111 dysfunction may occur in up to 60% of patients with AP; mostly
articles for the CP chapter. in severe AP and it is thought to lead to bacterial translocation and
infection of necrosis [10]. Along with the increased catabolic state
related to the disease, patients with predicted severe AP are
3. Results considered at nutritional risk [11]. Nevertheless, malnourished
patients should also be considered at nutritional risk, even if they
3.1. Acute pancreatitis have predicted mild AP, because of their pre-existing condition.
Similarly, patients with increased alcohol consumption are
1. Which patients with AP are considered at nutritional risk? frequently malnourished [12]. Scoring systems such as the NRS
Statement 1 2002 [13], can be helpful in identifying these patients [14e17].
These scores have been validated in hospitalized, as well as criti-
cally ill patients. Nevertheless, no studies have validated these
Patients with AP should be considered at moderate to high scoring systems in a specific population of patients with AP [18].
nutritional risk, because of the catabolic nature of the dis- Alowbodymassindex(BMI)mayalsoidentifypatientswhoare
ease and because of the impact of the nutritional status for at nutritional risk. Nevertheless, obesity is a known risk factor for
disease development. severe AP and is, therefore, a disease severity-related nutritional
risk [19].
Strong consensus (97% agreement).
2. Is early oral feeding feasible in patients with predicted mild AP?
M. Arvanitakis et al. / Clinical Nutrition 39 (2020) 612e631 615
Recommendation 2 Recommendation 4
Oral feeding shall be offered as soon as clinically tolerated In patients with AP and inability to feed orally, EN shall be
andindependentofserumlipaseconcentrationsinpatients preferred to parenteral nutrition (PN).
with predicted mild AP. Grade of Recommendation A e Strong consensus (97%
Grade of Recommendation A e Strong consensus (100% agreement).
agreement).
Commentary
Recommendation 3
EN is supposed to preserve the integrity of the gut mucosa,
stimulate intestinal motility, prevent bacterial overgrowth, and
increase the splanchnic blood flow [10]. Currently there are twelve
Low-fat, soft oral diet shall be used when reinitiating oral RCTs and eleven systematic reviews/meta-analyses including a
feeding in patients with mild AP. Cochrane-standard meta-analysis which clearly prove that in pa-
tients with severe AP, EN is safe and well-tolerated, with significant
Grade of Recommendation A e Strong consensus (100% decreases in complication rates, multi-organ failure, and mortality,
agreement). compared with PN [31e41]. The meta-analysis by Al-Omran et al.
was performed to Cochrane-standards on the basis of eight RCTs
with 348 patients and clearly shows that early EN when compared
with initial total PN, significantly decreases mortality by 50% (OR
Commentary 0.50 [95% CI 0.28 to 0.91]), rate of infection (OR 0.39 [95% CI 0.23 to
0.65]), multi-organ failure (0.55 [95% CI 0.37 to 0.81]) as well as the
Mostpatients with AP suffer from disease of a mild to moderate necessity for operation (OR 0.44 [95% CI 0.29 to 0.67]) [35].
severity,non-necrotizingtypewithanuncomplicatedclinicalcourse. Furthermore if only patients with severe AP were included in this
Four RCTs have shown that patients with mild to moderate AP can meta-analysis, mortality further decreased by more than 80% [0.18
tolerate early oral feeding and this strategy is related with a shorter [95% CI 0.006 to 0.58]) [35]. These results were confirmed by more
length of stay compared with conventional oral feeding (introduced recent meta-analyses, including a latest publication including only
after enzyme decrease, pain resolution and bowel movement) critically ill patients with AP [39]. Compared with PN, EN was
[9,20e23]. Furthermore, one of these trials revealed that oral food associatedwithasignificantreductioninoverallmortality(RR0.36,
intake is safe and well-tolerated independently of the course and 95%CI0.20to0.65,p¼0.001)andtherateofmultipleorganfailure
normalizationofserumlipase[20].Immediateoralfeedingwithasoft (RR 0.39, 95% CI 0.21 to 0.73, p ¼ 0.003).
dietseemstobemorebeneficialregardingcaloricintakeandequally
tolerated compared with clear liquid diets [23e25]. A meta-analysis 4. WhatistheoptimaltimingforinitiatingENinpatientswithAP?
confirmed that early oral feeding was feasible in patients with pre- Recommendation 5
dictedmildAPandreducedlengthofstay[26].Arecentmeta-analysis
including 17 studies identified that 16.3% of patients with AP will
subsequentlyhaveintolerancetooralfeeding[27].Predictivefactors
included the presence of pleural effusions and/or collections and ENshouldbestartedearly,within24e72hofadmission,in
severity (higher Ranson/GlasgowandBalthazarscores). case of intolerance to oral feeding.
Hyperlipidemia is the third most common cause of AP and ac-
countsfor4e10%ofcases [28].Itwasreportedthathyperlipidemiais Grade of Recommendation B e Strong consensus (92%
associatedwithaworseprognosisofAPthanotheretiologicalfactors agreement).
[28e30].TheinitialmanagementofhyperlipidemicAPisthesameas
for all other causes of the disease, but subsequent management in
addition to generalized supportive measures may include etiology-
specific targeted therapies. These include initially putting patients Commentary
onanilbymouthregimenfor24e48h,subsequentdietarymodifi-
cations, medical management with the different classes of anti- Several meta-analyses have investigated the clinical effects and
hyperlipidemic agents, in-hospital pharmacological treatment with toleranceofearlyENinpatientswithAPeitherwithin24h[42e44]
insulin and/or heparin and plasmapheresis. Whilst these measures or48h[45e47]ofadmission.Allthesemeta-analysesclearlyreveal
are effective in lowering triglyceride concentrations, they do not thatearlyENisfeasible,safeandwell-toleratedandassociatedwith
appeartoaffecttheoutcomeofAP[28,29].However,tightregulation substantial clinical benefits regarding mortality, organ failure and
oftriglycerideconcentrationafterpresentationwithAPwasfoundto infectious complications for both time-points compared with
reduce the risk of recurrence. These include a low fat diet, encour- delayedEN.Nevertheless,apotentialbiascouldbethatfiveofthese
agementofweightlossandtreatmentwithafibrate,withtheaddi- meta-analysis included studies which had patients receiving PN in
tion of a statin if hypercholesterolemia is present in addition to their control groups [42e46]. One meta-analysis, compared early
hypertriglyceridemia [28]. (within 24 h) with late enteral nutrition (after 72 h), but no com-
parison was made between 24 and 48 h [44].
3. If required, what type of medical nutrition (enteral or paren- In contrast to these data from the aforementioned meta-
teral) is preferable in patients with AP? analyses that provided strong evidence for early EN within
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