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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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...Clinical nutrition e contents lists available at sciencedirect journal homepage http www elsevier com locate clnu espen guideline espenguideline on in acute and chronic pancreatitis a b c d marianna arvanitakis johann ockenga mihailo bezmarevic luca gianotti f g h i j zeljko krznaric dileep n lobo christian loser madl remy meier k l m maryphillips henrik hojgaard rasmussen jeanin van hooft stephan bischoff department of gastroenterology erasme university hospital ulb brussels belgium endocrinology klinikum bremen mitte germany hepatobiliary pancreatic surgery clinic for general military medical academy defense belgrade serbia school medicine milano bicocca san gerardo monza italy hepatology centre zagreb croatia gastrointestinal nottingham digestive diseases national institute health research nihr biomedical hospitals nhs trust queen s ng uh uk mrc versus arthritis musculoskeletal ageing life sciences drk kliniken nordhessen kassel division krankenanstalt rudolfstiftung krankenanstalte...

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