Eras

Clinica Cli nicall Re Review& view& Edu Educat cation ion

JAMA Surge Surgery ry | Revie Review w

‘Enhan ‘En hanced ced Reco ecove very ry Aft After er Sur Surge gery ry A Review OlleLjungqvist, OlleLjungqvis t, MD,PhD; Mich Michael ael Scot Scott, t, MD; Ken KennethC. nethC. Fe Fearon,MD, aron,MD, PhD†

Enhanced Enhanc ed Rec Recov overy ery Afte Afterr Sur Surger geryy (ER (ERAS)is AS)is a par paradi adigm gm shi shift ft in per periop iopera erativ tivee care,, res care result ultingin ingin sub substa stanti ntial al imp improv roveme ementsin ntsin cli clinic nical al outc outcome omess and cos costt sav saving ings. s. IMPORTANCE

Enhanced Enhan ced Recov Recovery ery After Surge Surgery ry is a multi multimodal, modal, multi multidisci disciplina plinary ry approac approach h to the car caree of thesurgi thesurgical cal pati patient.Enhan ent.Enhanced ced Rec Recov overy ery Aft After er Sur Surger geryy pro proces cesss imp implem lement entati ation on involv inv olves es a teamconsi teamconsisti sting ng of sur surgeo geons,anest ns,anesthet hetist ists, s, an ERA ERASS coo coordi rdinat nator or (of (often ten a nur nurse se or a physic phy sician ian ass assist istant ant), ), andstaff fro from m uni units ts tha thatt car caree for the sur surgic gical al pati patient ent.. Th Thee car caree prot protoco ocoll is based on publi published shed evide evidence. nce. The ERAS Societ Societyy, an inter internation national al nonpr nonprofit ofit profes professiona sionall societyy that promote societ promotes, s, devel develops, ops, and imple implements ments ERAS progr programs, ams, publi publishes shes update updated d guidel gui deline iness for man manyy ope operat ration ions, s, suc such h as evi eviden dencece-bas based ed mod modern ern car caree cha change ngess fro from m ov overn ernigh ightt fasting fasti ng to carboh carbohydrate ydrate drink drinkss 2 hours befor beforee surge surgery ry,, mini minimally mally inv invasive asive approac approaches hes inst instead ead of lar large ge inc incisi isions ons,, man manage agemen mentt of flui fluids ds to see seekk bal balanc ancee rath rather er tha than n lar large ge vol volume umess of intrav int raveno enous us flu fluids ids,, avo avoida idanceof nceof or earl earlyy rem remov oval al of dra drainsand insand tube tubes, s, earl earlyy mob mobili ilizati zation,and on,and servingof serv ingof dri drinksand nksand foo food d the day of the ope operat ration ion.. Enh Enhanc anced ed Rec Recove overy ry Aft After er Sur Surgery gery protoco prot ocols ls hav havee res result ulted ed in sho shorterlengthof rterlengthof hos hospit pital al sta stayy by 30%to 50% andsimil andsimilar ar reducti redu ctionsin onsin com compli plicat cation ions, s, whi while le rea readmi dmissi ssions ons andcosts are redu reduced ced.. Th Thee ele elemen ments ts of the protoco prot ocoll red reduce uce thestressof the ope operat ration ion to reta retain in ana anabol bolic ic hom homeos eostas tasis.The is.The ERA ERASS Soc Societ ietyy conduc con ducts ts str structu uctured red imp implem lement entatio ation n prog program ramss tha thatt are cur curren rently tly in use in mor moree tha than n 20 countr cou ntries ies.. Loc Local al ERA ERASS tea teams ms fro from m hos hospit pitals als are trai trained ned to imp implem lement ent ERA ERASS pro proces cesses ses.. Aud Audit it of proc process ess com compli plianc ancee and pat patien ientt out outcom comes es are imp importa ortant nt fea feature tures. s. Enh Enhanc anced ed Rec Recov overy ery Afterr Sur Afte Surger geryy sta startedmainl rtedmainlyy wit with h col colore orectalsurge ctalsurgery ry but hasbeen sho shown wn to imp improv rovee outcome outc omess in alm almostall ostall maj major or sur surgic gical al spe specia cialti lties. es.

CME Quiz at jamanetworkcme.com jamanetworkcme.com

OBSERVATIONS

Enhanced Enhanc ed Rec Recov overy ery Afte Afterr Sur Surgeryis geryis an evi eviden dencece-bas based ed car caree improv imp roveme ement nt pro proces cesss for sur surgic gical al pati patient ents. s. Imp Implem lement entatio ation n of ERA ERASS prog program ramss res result ultss in major maj or imp improv roveme ementsin ntsin cli clinic nical al outc outcome omess and cos cost, t, mak makingERAS ingERAS an imp importa ortant nt exa exampl mplee of value-based value -based care applie applied d to surge surgery ry.. CONCLUSIONS AND RELEVAN RELEVANCE CE

JAMA Surg. 2017; 2017;152(3):292 152(3):292-298. -298. doi doi::10.1001/jamasurg.2016.4952

Published Publish ed onlin onlinee Janua January ry 11, 2017 2017..

T

he Enhan Enhanced ced Recov Recovery ery After Surge Surgery ry (ERAS)protocolwas developed by a group of academic surgeons in Europe in 2001 when they formed the ERAS Study group ( Table 1). fast-track ack surgery hadbeendescribed,thegroup Althoughtheterm fast-tr hadbeendescribed,thegroup wanted wan ted to emp emphas hasizethat izethat the ke keyy sur surgic gical al endpoint is the qua qualit lityy, ratherthan speed,of recov recovery ery.. Theconcept restedon sever several al components: a multidisciplinary team working together around the patient; patie nt; a multi multimodalapproachto modalapproachto resol resolvingissue vingissuess thatdelay reco recovvery and cause complications; a scientific, evidence-based approachto proa chto car caree prot protoco ocols;and ls;and a cha chang ngee inmanag inmanageme ementusinginte ntusinginterractivee andcontin activ andcontinuousaudit.Thisreviewdescr uousaudit.Thisreviewdescribesthe ibesthe dev develop elopment ment of ERAS, how these ideas are br ought into practice, and how they are now spread spreadingto ingto vari various ous disci disciplinesof plinesof surgi surgical cal practi practice, ce, as well as some of the main outcome improvements and an implementation strat strategy egy to achie achieve ve susta sustained ined outcom outcomee impro improvemen vements. ts. A project to improve outcomes of coronary artery bypass surgeryby bund bundlingperio lingperiopera perativetreatm tivetreatmentsundera entsundera conc conceptname, eptname,Fast 2 92 92

JA MA MA S u r

March March 20 2017 17 Vo Volume152,Numb lume152,Number3 er3 (Reprinted)

Author Affiliations: Fac Facultyof ultyof

Medicine and Healt Medicine Health, h, Scho School ol of Healt Health h and Medic Medical al Scien Sciences, ces, Departmentof Depar tmentof Surge Surgery ry,, Örebr Örebro o University,, Örebro,Sweden University (Ljungqvis (Ljun gqvist); t); Roy Royal al Surre Surreyy Count Countyy National Natio nal Healt Health h Servi Service ce Fou Foundatio ndation n Trust, Tr ust, Univ Universit ersityy of Surre Surrey,Guildford y,Guildford,, England Engla nd (Scot (Scott); t); Depar Departmen tmentt of Anesthesiology Anesthesiology,, Virginia Commonwealth University School of Medic Medicine,Richmond(Scott); ine,Richmond(Scott); Clinicall Surge Clinica Surgery ry,, Scho School ol of Clinic Clinical al and Surgical Surgic al Scien Sciences, ces, Univ Universit ersityy of Edinburgh, Royal Infirmary, Edinburgh, Scotland (Fearon). Corresponding Author: Olle

Ljungqvist,MD, PhD Ljungqvist,MD, PhD,, Fac Faculty ulty of Medic Medicine ine and Health Health,, Scho School ol of Healt Health h and Medic Medical al Scien Sciences, ces, Departmentof Depar tmentof Surge Surgery ry,, Örebr Örebro o UniversityHospital,SE-7 Unive rsityHospital,SE-701 01 85 Örebro, Sweden ([email protected] [email protected])).

Track ,waspublishedin1994. ,waspublishedin1994. 1 Thisstudyshowedareductioninlength

ofstayintheintensivecareunitbyabout20%.Ayearlater,Bardram et al2 reported a substantial shortening of recovery time in 8 patients tien ts unde undergoi rgoingsigmoi ngsigmoid d rese resectio ction n whowere disc discharg harged ed 2 daysaftersurgery tersurg ery.. Th This is pu publi blicat catio ion n wasfoll wasfollowe owed d by a re repor portt by Ke Kehl hlet et an and d 3 Mogensen of a larger series confirming a rapid recovery after sigmoidresectionusin moidresec tionusingg a mul multimo timodalapproac dalapproach.Kehle h.Kehlet, t, a surg surgeon eon,, promoted mote d thor thoraci acicc epid epidural ural anes anesthes thesia ia as a way of con control trollin lingg pain pain,, improvingmobility,andreducingpostoperativeileus.Concurrently,other ERAS group members were addressing perioperative perioperative care from an endocrine4 andmetabolicviewpoint.Thisapproachincludedtheroles of spe specifi cificc amin amino o acid acidss in peri perioper operativ ativee nutr nutritio ition, n,5 inflamm inflammation ation and protein prot ein meta metaboli bolism sm in surg surgicalpatient icalpatientss withcancer withcancer,,6 and metabolic preparationusingapreoperativecarbohydratedrinktoavoideffects offasting.7 Thegroupwasfocusedonenhancingrecoveryandreducingcomplicationsbymodifyingthemetabolicresponsetosurgicalinsultt rath sul rather er thanjust limi limitin tingg len length gth of sta stayy.

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Enhanced RecoveryAfter Surgery

Table 1. Member Sites andLeads of the OriginalEnhanced Recovery AfterSurgeryStudy Group Formed in 2001

Review ClinicalReview & Education

Table 2. ERASSocietyGuideline Elementsfor Colonic Resections Element

Target Effect and/or Comment

Unive rsity and Hospital

Countr y

Lead(s)

Preadmission

U ni ve rs it y o f Ed inb ur gh

U ni te d Kingdom

Ken Fearon

Cessation of smoking and excessive intake of alcohol

Reduce complications

Karolinska Institutet and Ersta Hospital Stockholm

Sweden

Olle Ljungqvist


University of Copenhagen and Hvidovre Hospital

Denmark

Henrik Kehlet

Preoperative nutritional screening and, as needed, assessment and nutritional support

Norway

Arthur Revhaug

Medical optimization of chronic disease


University of Northern Norway and Tromsö Hospital U ni ve rs it y o f M aa st ri cht

T he Netherlands

Martin von Meyenfeldt, Cornelius DeJong

Preoperative

The ERAS group gathered inLondon in2001 to produce a protocolthatwouldoptimizeoutcomesbasedonpublishedevidence.8 Thegroupalsopublishedreportsofvariableoutcomesinsimilarsurgical procedures and populations demonstrating that perioperativecare,ratherthantheactualoperation,dictatedtheoutcomes. 9 Severalsurveysconfirmedthatperioperativecarewasvariableacross NorthernEuropeandthattherewasminimaladoptionofevidencebasedpractices.10 Thegroup worked together developing ERASby testing protocols, running symposia, and involving national health ministries (such as the Enhanced Recovery Partnership Programme in the UnitedKingdom). AlthoughERAS concepts became widelyrecognized,therewasstillminimalchangeacrossmosthealth care systems. The ERAS Society (http://www.erassociety.org) was foundedtofocusandconsolidateprogressnotonlythroughresearch and education but also by developing models for implementation of best perioperative practices.

A fundamentalchallenge inthe care ofthe surgical patientlieswith the journey the patient makes through various parts of the hospital:outpatientclinics, preoperative units, theoperatingroom,postoperative recovery facility, and the ward. Each unit has its own focus, personnel, andspecialists. Each unit affects theones to follow by thetreatmentchoices made. For example, ifthe surgeon orders oral bowel preparation, the anesthetist may face a dehydratedpatienttomanageoninductionofanesthesia.Fewstakeholdersinthe surgicalpathwayhavethe opportunityto seea patientthroughthe entirejourney.Hospitalstaffareoftenfocusedonmanagingtheimmediate clinical situation with little opportunity for strategic thinking.Thereare24coreelementsofERAScarethathavescientificsupport for their use (Table 2). These components are distributed alongthe patient pathway and delivered by different departments and professionals withinthe hospital (Figure), which explains why the surgeon, as the clinician with overall responsibility for the patient, has the best opportunity for a comprehensive view to guide the process. Consistentagreementontheendpointsofmanagementiscriticalforcoordinatedaction.Forexample,thepatientismedicallysuitable to leave the hospital when the following conditions are true: heorshecaneatanddrinktofulfilldailyneeds,thebowelsaremoving, pain is controlledby oral analgesics, he or sheis capable of sufficient mobility for self-care,and thereare no complications requiring hospital care.

Structured preoperative information and engagement of the patient and relatives or caretakers

Reduce anxiety, involve the patient to improve compliance with protocol

Preoperative carbohydrate treatment

Reduce insulin resistance, improve well-being, possibly faster recovery

Preoperative prophylaxis against thrombosis

Reduce thromboembolic complications

Preoperative prophylaxis against infection

Reduce infection rates

Prophylaxis against nausea and vomiting

Minimize postoperative nausea and vomiting

Intraoperative

The Rationale of ERAS

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a

Minimal invasive surgical techniques

Reduce complications, faster recovery, reduce pain

Standardized anesthesia, avoiding long-acting opioids

Avoid or reduce postoperative ileus

Maintaining fluid balance to avoid over- or underhydration, administer vasopressors to support blood pressure control

Reduce complications, reduce postoperative ileus

Epidural anesthesia for open surgery

Reduce stress response and insulin resistance, basic postoperative pain management

Restrictive use of surgical site drains

Support mobilization, reduce pain and discomfort, no proven benefit of use

Removal of nasogastric tubes before reversal of anesthesia

Reduce the risk of pneumonia, support oral intake of solids

Control of body temperature using warm air flow blankets and warmed intravenous infusions


Postoperative Early mobilization (day of surgery)

Support return to normal movement

Early intake of oral fluids and solids (offered the day of surgery)

Support energy and protein supply, reduce starvation-induced insulin resistance

Early removal of urinary catheters and intravenous fluids (morning after surgery)

Support ambulation and mobilization

Use of chewing gums and laxatives and peripheral opioid-blocking agents (when using opioids)

Support return of gut function

Intake of protein and energy-rich nutritional supplements

Increase energy and protein intake in addition to normal food

Multimodal approach to opioid-sparing pain control

Pain control reduces insulin resistance, supports mobilization

Multimodal approach to control of nausea and vomiting

Minimize postoperative nausea and vomiting and support energy and protein intake

Prepare for early discharge

Avoid unnecessary delays in discharge

Audit of outcomes and process in a multiprofessional, multidisciplinary team on a regular basis

Control of practice (a key to improve outcomes)

Abbreviation: ERAS, EnhancedRecovery AfterSurgery. a

Fordetails and references, see theguidelinesat http://www.erassociety.org.

The ERAS elements of the program for colonic resection are listed in Table 2. Most of the solutionsto problems delaying recoveryare evident once theperioperative care pathwayis exhibitedin (Reprinted) JAMA Surger March 2017 Volum 152 Number3

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EnhancedRecovery AfterSurgery

Clinical Review & Education Review

Figure. EnhancedRecovery AfterSurgery(ERAS) Flowchart Preadmission

Surgery

Anesthesia

Nursing

Preoperative

Postoperative

Preadmission nutritional support Cessation of smoking Control alcohol intake

Selective bowel preparation

Minimal invasive surgery Minimize drains and tubes

Early removal of drains and tubes Stop intravenous fluids

Medical optimization

Preoperative carbohydrates No NPO PONV prophylaxis

Regional analgesia Opioid-sparing anesthesia Balanced fluids Temperature control

Multimodal opioid-sparing pain control

Early mobilization Early oral intake of fluids and solids Postdischarge follow-up

Preoperative information

A typical ERASflowchart overviewindicating differentERAS protocolitems to be performedby different professions and disciplinesin differentparts of the hospital during the patient journey. Thewedge-shaped arrows depicting each time periodmoveintotheperiod tofollow toindicatethat alltreatments given

affectlater treatments. No NPO indicates fasting guidelines recommending intakeof clearfluidsand specific carbohydratedrinks until 2 hoursbefore anesthesia; PONV, postoperativenausea and vomiting.Reprinted with permissionfrom Olle Ljungqvist, MD,PhD.

total,whichisoftenbestachievedinamultidisciplinarymeeting.This method is how the ERAS Society runs its various implementation programs.

The Patient’s Journey

Multimodal Care No single element by itself will improve outcomes of surgery. The approach to perioperative care must be multimodal, usingall available elementsof care that improve recovery. Thekeyis toseek synergy betweenoneprocess element andthe next.Since elementsof ERAS are implemented by different medical and health care specialties working in different departments, a multidisciplinary approach is necessary. The elements of care are carried out by many professionals: nurses, dieticians,and physiotherapistsalongsidephysicians and surgeons.

The ERAS Team The core of changingpracticeand realizingthe benefits of ERAS is a team of the key individuals from the involved units. The medical leadership is most commonly a surgeon, supported by an anesthetist. TheERAS clinicalleadershold the medical responsibility for the ERAS program, and their role as local champions is important.11 The ERAS project manager is commonly a nurse, who facilitates the resources and management approval to enact change. The ERAS coordinator(in Europe often a nurse or, in theUnited States, a physician assistant) fills a key role as the “engine” of the ERAS team, with time devoted to managing practical matters, which might include such tasks as composing and distributing memos and instructions, managing reporting and feedback to the units, and arranging for continuous training of new personnel. This individual is well positioned to manage the audit process. Participation from the other disciplines, including special services such as dietetics, occupational therapy, and physiotherapy, is critical to sustained performance. 294

Intraoperative

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Consistent and well-attended team meetings are critical to implementation andimprovementof theERAS program (Figure). At the outset, a unit should meet weekly to audit compliance and implement necessary changes to improve practice.Aftersome time, the meeting frequencycan be reduced to everyotherweek,but attendance at meetings must remainan establishedcommitment foreach team member.

Evidence-Based Guidelines The ERAS Group publishedan initialconsensus document on perioperative care for colonic resections 8 and later one for colorectal surgery.12 After the ERAS Society was formed in 2010, the Society publishedaseriesofguidelines(Table3)andspecialpaperswithprocedure-specificrecommendations,which formthebasis forthe protocolsbuiltintotheauditsystem.Societymembershavealsotested the efficacy of the guidelines. For example, in a single-center report of more than 900 consecutive patients, improved compliance with the colorectal surgery guidelines resulted in a shorter length of stay, fewer complications,and fewer readmissions.13 Afollow-upstudyfromtheERAS InteractiveAudit systemwithmorethan 2300consecutivepatientsin13unitsin7countriesconfirmedthese results.14

Audit Because of the complexity of the care process, the team is helped byperformingcontinuousauditofthecareprocessandpatientoutcomesto maintain a comprehensive view. Basedon the guidelines, theERASSocietyhasdeveloped a specificauditsystemfor this purpose,the ERAS InteractiveAuditSystem,whichis used inthe ERAS Implementation Programs (http://www.erassociety.org) and is

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Table 3. ERASSocietyGuidelines

a

Procedure and Topic

Year of Publication

Colonic resection

2012

Rectal resection

2012

Pancreaticoduodenectomy

2012

Cystectomy

2013

Gastric resection

2014

Anesthesia protocols

2015

Anesthesia pathophysiology

2015

M aj or g yn ec ol og y ( pa rt s 1 a nd 2 )

2 01 5

Bariatric surgery

2016

Liver resection

2016

Head and neck cancer surgery

2016

Breast reconstruction

2017

Hip and knee replacement

Under production

T ho ra ci c n onc ar di ac s ur ge ry

U nde r p ro du ct io n

Esophageal resection

Under production

Abbreviation: ERAS, EnhancedRecovery AfterSurgery. a

For updates andfreedownload, goto http://www.erassociety.org.

currentlyavailable in France, Germany, Norway, Portugal,Spain,the Netherlands, the United Kingdom, Sweden, Canada, the United States, Mexico, Brazil, Colombia, Argentina, Singapore, the Philippines, New Zealand, Israel, Uruguay, Chile, and South Africa. Health care professionals, and perhaps surgeons in particular, tend to believe that their care and outcomes are better than they actually are. Duringyearsof work with theERASprograms,we have rarelyencountered surgeons who believed that theirpatients who underwentcolorectal surgery arehospitalized formore than 3 to 4 days. However, even in the countriesthat adhere most strongly to the ERAS protocol, national and individual hospital data for these patientsstillreflectanaveragelengthofstayof7to8days.Inmany countries, thehospitalstaysare longeror dataon lengthof stay are notavailable (Swedish ColorectalCancerRegistry15; NationalHealth Service Scotland; National Bowel Cancer Audit report 2015 16; and Officefédéral dela statistique médicaledeshôpitaux,Suisse201617). Finally, some surgical teams believe that they adhereto ERAS principles while, in fact, they are using them only in part. Compliance with 70% to 80% or more of the elements of the ERAS protocol appears to be important to improve outcomes.11

Implementation of ERAS Recently, interest in ERAS has grownsubstantially, revealinga deficit in education and training,as few courses are targetedto hospitalteams.Implementationofnewpracticesisdifficult,andnewtreatmentsare slowto disseminate to active practice.Evidencesuggests that change in clinical practice occurs 15 years after clear evidence is available.10 There is a need to support the medical and surgical communityto implementnew and bettercare more quickly. About 310 million major operations are performed annually.18 Data suggest that ERAS processescanreduce complications by10% to20% ormorebysupportingunitstoadoptevidence-basedcare. 13,14,19,20 The primary vision of the ERAS Society is to help units use current best practice. Since its foundation, the ERAS Society has been ac jamasurgery.


tively involved in implementation of these evidence-based processes. To develop an implementation program, the ERAS group workedwithchange-managementspecialistsintheNetherlandsand SwedentohelpimplementERASguidelinesandprotocols.Byusing this method, theDutchteam helpedmore than 30 colorectalunits improve their outcomes by using ERAS recommendations. With a structuredimplementationprogramthatlasted10months,theunits’ meanlengthofstaydecreasedfrom9to10daysto6days. 21 Asubsequentfollow-upinthe10mostsuccessfulunitsshowedthatlength of stay in most of the units had increased again. This increase correlatedwith a reduction in compliance with ERAS pathway elements in the absence of ongoing education and audit. 22 Based on thisexperience,theERASSocietydevelopedanimplementationprogram rooted in sustainability.23 A growing amount of literature on barrierstoimplementationreportsthatfactorsthatenablethesuccessful implementation of ERAS include not only a willingness to changeto ERAS, formation of multidisciplinary teams and thereby improved communication and collaboration, and support by hospital management but also standardization of order sets and care processesand theuse of audit.24,25 Goodlocal leadershipand local champions are important success factors.11 Conversely, barriers to implementationareageneralresistancetochange,lackoftimeand staff, and poor communication, collaboration, and coordination between departments.24,25 It is also important to implementadditional changes in light of new evidence. In colorectal surgery, the ERAS Society has revised theguidance3 times in 10 years anda fourth revision is under way. Building a system that is ready to make the next change is the key to quicken the pace of implementation of better care. An important goal forthe ERAS Society isto build a network of hospitalsaround theworld that uses a consistent audittool.The resulting data set will facilitate research, including the development of new ERAS protocols. The ERAS Society includes active centers in several countries that are trained to implement ERAS processes intheircountryor region. Thesecenterscan usethecentralized, internet-based audit system that establishes the platform forthe introduction of the next change. Enhanced Recovery After Surgery pathways continue to be developed, and current evidence is reexamined by the ERAS guidelines group to keep up to date with changesinpractice.Anexampleisthemoveawayfromroutinethoracicepiduralanesthesiafor laparoscopic colorectalsurgery26 infavor of combining spinal analgesia or transverse abdominis plane blockswith general anesthesia.By having manycenters contribute to the audit process, changes in care pathways can be introduced andthedownstreameffectmeasured.Itisequallyimportanttomaintainconsistent compliance with the ERAS protocol once it is introduced.A follow-upstudy 3 to 6 years after a successful implementationoftheERASprotocolrevealedthatlossofcontinuousfeedback with audit during a postimplementation program was a reason for diminishingeffectiveness. 25 Remindersand boosters in education, updatesin small groups, and retaining the ERAS coordinator were other factorsbelievedto be important for sustainability.

Elements of ERAS TheERAS Societyguidelinesfor colonicresectionsin Table2 andthe Figure are examples of elements commonly used in this (Reprinted) JAMA Surger March 2017 Volum 152 Number3

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procedure.27,28 Enhanced Recovery After Surgery programs typicallycontainseveralelementswith1emphasisincommon:theyminimize stress and improve the response to stress. By maintaining homeostasis, the patient avoids catabolism with consequent loss of protein, muscle strength, and cellular dysfunction.29 The reduction of insulin resistance promotes adequate cellular function during injury to the tissue. The following series of elements contributes to this goal: preoperative nutritional support for the patient who is malnourished, carbohydrate loading before surgery to minimize postoperative insulin resistance, epidural or spinal analgesia to reduce the endocrine stress response, anti-inflammatory drugs to reduce the inflammatory response, early feeding after surgery to secure energy intake, and optimal pain control to avoid stress and insulinresistance. Enhanced Recovery After Surgery processes also aim to minimize fluid shifts. Too little fluid can cause a reduction in perfusion and organ dysfunction, whereas intravenous salt and fluid overload is recognized as a major cause of postoperative ileus and its complications.30,31 Maintaining euvolemia,cardiac output,and delivery of oxygen and nutrients to the tissues are important to preserve cellular function, particularly when there is tissue injury and need forrepair. Once patients areeuvolemic, vasopressorsmay be usedasrequiredtomaintainmeanarterialpressure.Targetingminimalweightchange(30mL/kgnetintakeofintravenousfluid,keepingweight gain within2 kg) is typically recommended. Postoperativeintravenousfluidsaregenerallydiscontinuedatabout24hours after surgery. A patient progressing normally on an ERAS pathway should be drinking, eating, mobilizing, and sleeping on the day afteroperation.TheERASprogramalsoavoidsseveraltraditionalcare elements that have been shown to be harmful, such as theroutine useofnasogastrictubes,prolongedurinarycatheterization,andprolonged or inappropriate use of abdominal drains.

Outcomes With the ERAS Protocol There aremany stakeholdersin surgical care, with ERAS processes putting the patient at the center. Professionals from various disciplinesaswellasmanagers,politicians,payers,andthegeneralpublic are involved, as are the medical device and pharmaceutical industries. Length of Stay The broader ERAS principles have been published for many types ofproceduresinallmajorsurgicalspecialties.Theearlystudiesshowinga 2-day hospital stay after sigmoid resection2,3 were often met with disbelief, and some thought (incorrectly) that it was careful selectionofpatientsthatresultedinashortenedlengthofstay.Now, diversegroupspublishingonconsecutiveseriesandusingERASprinciples show consistent results, 32 and, with the addition of laparoscopic techniques, the same results have been demonstrated in patients with complex medical conditions.33 Complications A meta-analysis of randomized trials of the ERAS protocol in patientsundergoingcolorectal surgeryshowed that complicationrates werereducedbyupto50%whenERASprincipleswereused. 19 This finding was confirmed in a larger series.20 Further data from more 296

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than 900consecutivepatients with colorectalcancer showed the effectiveness of ERAS protocols and highlighted the importance of compliance: the better the compliance to the protocol, the better theoutcomesintermsofcomplications,lengthofprimaryandtotal stay, andreadmissions.13,14 Thesestudiesrevealedthatnotonlywere overallcomplicationsreducedwithbettercompliance,butthemost severe complications, which resulted in reoperationsor admission to the intensivecare unit,decreasedas mortality improved.14,34 Fit patients undergoing colorectal cancer surgery using ERAS principles and laparoscopicsurgery can be dischargedwithin 24 hours, witha mean lengthof stay of2.7 days.35 Colorectal surgery wasthe basis forthe development of ERAS and still dominates the literature; however, in many other surgical domains, the implementation of ERAS patient care and principles of process improvement have improved outcomes. Studied areas include liver resections 36 ; pancreatic, gastric, and esophageal surgery37,38; thoracic surgery39; major urologicsurgery40; gynecologicsurgery41;orthopedicsurgery42,43;andemergencysurgery.44

Financial Effects of the Implementation of ERAS Althoughmost reportsof ERAS come from singleunits,with developersandearlyadoptersachievingsomeofthebestresults,thechallenge lies with having most surgical procedures performed using ERAS principles. In the United Kingdom, the National Health Service ran the Enhanced Recovery Partnership Programme,45 based on lectures by expertsand early adopters along with the provision of treatment protocols and advice. Theprogram encompassednot onlycolorectalsurgerybutalsocystectomy,gynecologicsurgery,and hip and knee replacement. Adoption of some of the ERAS elements wasincentivized by bonus payments,but most of themaintenance of ERAS pathways relied on local peer groups to continue thepathwaysin whatevermanner theyconsidered appropriate.Although some units continue to produce excellent results, the Enhanced Recovery Partnership Programmelacked resources to support sustainability, and the overall results have been difficult to discern in national statistics. In Alberta, Canada, the state health care service worked with the ERAS Society to implement ERAS, starting with colorectalsurgery.TheERASSocietyprovidedtraininginthefirst2hospitals,which arenow supporting trainingin other hospitalsusingthe same principles. Thefirst results are promising,with shorter stay (reduction from 6 to 4½days)and an 11%reduction incomplications.46 There were 8% fewer readmissions anda shorterstay for those readmitted, saving$2800 to $5900 per patient.

Long-term Benefits of ERAS The longer-term benefits of rapid, uncomplicated recovery using ERAS principlesare lesswell known. Medium-termoutcomeshave been sparsely studied,47 andlong-term dataon outcomes are now beginningto appear. One observationalstudy in 4500patientsundergoing hip and knee replacement showed that 2-year mortality wassignificantlyloweredaftertheintroductionofERASprinciples. 48 A reporton more than 900patientswithcolorectalcancer showed that, with compliance above 70%with theERAS preoperativeand

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intraoperative protocol, mortality fell by 42% compared with patientswithcompliancebelow70%.34 Inthisstudy,thedataweread justedfor severalvariables,includingage,sex,bodymassindex,American Society of Anesthesiologists score, surgical procedure, and pathologic findings.The datashowan associationrather thancausationandotherbiasesmayhavecontributeddirectlyorindirectly.For example, the group with higher compliance had fewer complications, which may have affected the observed outcomes. Perioperative complications have been shown to be strongly associated with poorlong-termoutcomesinverylargesurgicalseries.49 Incancertreatment, surgicalcomplicationsmay also delay theinitiationof postoperativechemotherapy whichin turnmaycontributeto reducedlongtermsurvival.Complicationsalsoincreasethecost ofcare.50 Enhanced Recovery After Surgery programs are thus supporting a combinationof better outcomesand cost savings.

worldwideandbyhostingprofessionalmeetingsandeventsformany nationalgroups.TheERASSocietyhashostedanAnnualWorldCongresssince2012andisactiveincurrentlyminingthesubstantialdata availablefrom theERAS Interactive Audit System. Thesystem providesthebasisforbothprospectivetrialsandauditresearch.Auditbasedresearchiscompletedusinglargenumbersofpatientsonthe samepathway.Makingasingle-stepchangeandanalyzingthedownstreameffectusingregressionanalysismaybeacomplementaryway to study new interventions rather than relying on expensive randomized clinical trials.

The Future of ERAS As ERAS principles are applied acrossall surgical specialties, ongoing innovation mustcontinueto allowprocessesto improve. There is increasing focus on procedure-specific specialty items to attempt to improve outcomes. The ERAS Society continues to work alongside various national ERAS Societies in the European Union, Asia, andthe UnitedStates. TheERASSociety andits national societies also collaborated with established professional specialty groups,suchastheSocietyofAmericanGastrointestinalandEndoscopicSurgeons,byco-authoringthe Manual ofEnhancedRecovery 51 andhaveworkedclosely with ERAS USA(theERASSociety chapter that is recently formed in the United States) as well as supported theslightlyolderAmericanSocietyofEnhancedRecovery.Thegoal of the ERAS Society is to complement the programs of these national groups andto offer additional value by coordinatingactivity

Conclusions Enhanced Recovery After Surgery programs represent a paradigm shift in how surgical care is delivered and how changes in practice aredisseminatedandimplemented.Theseresultsrelyonanewapproachto teamwork, continuous audit,and support of data-driven change and improvement. Enhanced Recovery AfterSurgery practicesimprovetheopportunityforrapid,uncomplicatedrecoveryaftersurgerywith bothshort-and long-termbenefitsfor patientswhile improving quality and saving money. There is financial pressure surrounding health care spending, as limited societal funds to support health care meet rising demandsowing to expensivetechnology, increased patient expectations, and a growing elderly population. In the United States, the 2010Patient Protectionand AffordableCare Act hasalso delivered specific challenges for health care systems by introducing broadened coverage of the population and has gradually implemented changes in payment modelsto make healthcare systems more responsible forcosts.EnhancedRecovery AfterSurgerypathwayscan be a key strategy in addressing these issues by offering improved quality care forless cost.

ARTICLE INFORMATION

Roleof the Funder/Sponsor: Thefunding source

†Kenneth C. Fearon, MD,PhD, died during thefinal revision of thisarticle.

hadno role in thedesign andconductof thestudy; collection, management, analysis, and interpretationof the data;preparation,review, or approval of the manuscript; and decision to submit themanuscriptfor publication.

Accepted for Publication: June18, 2016. Published Online: January 11, 2017.

doi:10.1001/jamasurg.2016.4952 Author Contributions: Drs Ljungqvistand Fearon

are founding members of the EnhancedRecovery AfterSurgery(ERAS) StudyGroup and ERAS Society. Drs Ljungqvist, Scott, and Fearon are Executive Officers of theERAS® Society. ERASis a registered trademarkfor goodsand services owned and provided by the EnhancedRecovery After Surgery Society for Perioperative Care. Study concept and design: All authors. Acquisition, analysis, or interpretation of data: All authors. Drafting of the manuscript: All authors.

Additional Contributions: Thisreview is dedicated

hepatic release of glutamine in sepsis. Ann Surg. 1998;228(1):131-139. 5. vanderHulstRR, vanKreelBK, von Meyenfeldt

MF, etal. Glutamineand thepreservationof gut integrity. Lancet . 1993;341(8857):1363-1365. 6. Fearon KC, FalconerJS,Slater C, McMillan DC,

toKennethC. Fearon,MD, PhD, ourclosefriend, collaborator, and co-authorwho died during the finalizationof this article.

RossJA, PrestonT. Albumin synthesis ratesare not decreasedin hypoalbuminemiccachecticcancer patients withan ongoing acute-phase protein response. Ann Surg. 1998;227(2):249-254.

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