Clinical Review & Education

JAMA Surgery | Review

Enhanced Recovery After Surgery

A Review
Olle Ljungqvist, MD, PhD; Michael Scott, MD; Kenneth C. Fearon, MD, PhD

CME Quiz at
IMPORTANCE Enhanced Recovery After Surgery (ERAS) is a paradigm shift in perioperative jamanetworkcme.com
care, resulting in substantial improvements in clinical outcomes and cost savings.

OBSERVATIONS Enhanced Recovery After Surgery is a multimodal, multidisciplinary approach

to the care of the surgical patient. Enhanced Recovery After Surgery process implementation
involves a team consisting of surgeons, anesthetists, an ERAS coordinator (often a nurse or a
physician assistant), and staff from units that care for the surgical patient. The care protocol is
based on published evidence. The ERAS Society, an international nonprofit professional
society that promotes, develops, and implements ERAS programs, publishes updated
guidelines for many operations, such as evidence-based modern care changes from overnight
fasting to carbohydrate drinks 2 hours before surgery, minimally invasive approaches instead
of large incisions, management of fluids to seek balance rather than large volumes of
Author Affiliations: Faculty of
intravenous fluids, avoidance of or early removal of drains and tubes, early mobilization, and Medicine and Health, School
serving of drinks and food the day of the operation. Enhanced Recovery After Surgery of Health and Medical Sciences,
protocols have resulted in shorter length of hospital stay by 30% to 50% and similar Department of Surgery, rebro
University, rebro, Sweden
reductions in complications, while readmissions and costs are reduced. The elements of the
(Ljungqvist); Royal Surrey County
protocol reduce the stress of the operation to retain anabolic homeostasis. The ERAS Society National Health Service Foundation
conducts structured implementation programs that are currently in use in more than 20 Trust, University of Surrey, Guildford,
countries. Local ERAS teams from hospitals are trained to implement ERAS processes. Audit England (Scott); Department
of Anesthesiology, Virginia
of process compliance and patient outcomes are important features. Enhanced Recovery Commonwealth University School
After Surgery started mainly with colorectal surgery but has been shown to improve of Medicine, Richmond (Scott);
outcomes in almost all major surgical specialties. Clinical Surgery, School of Clinical and
Surgical Sciences, University of
Edinburgh, Royal Infirmary,
CONCLUSIONS AND RELEVANCE Enhanced Recovery After Surgery is an evidence-based care Edinburgh, Scotland (Fearon).
improvement process for surgical patients. Implementation of ERAS programs results in Corresponding Author: Olle
major improvements in clinical outcomes and cost, making ERAS an important example of Ljungqvist, MD, PhD, Faculty
value-based care applied to surgery. of Medicine and Health, School
of Health and Medical Sciences,
Department of Surgery, rebro
JAMA Surg. 2017;152(3):292-298. doi:10.1001/jamasurg.2016.4952 University Hospital, SE-701 85
Published online January 11, 2017. rebro, Sweden
([email protected]).

T
he Enhanced Recovery After Surgery (ERAS) protocol was Track, was published in 1994.1 This study showed a reduction in length
developed by a group of academic surgeons in Europe in of stay in the intensive care unit by about 20%. A year later, Bardram
2001 when they formed the ERAS Study group (Table 1). et al2 reported a substantial shortening of recovery time in 8 pa-
Although the term fast-track surgery had been described, the group tients undergoing sigmoid resection who were discharged 2 days af-
wanted to emphasize that the key surgical end point is the quality, ter surgery. This publication was followed by a report by Kehlet and
rather than speed, of recovery. The concept rested on several com- Mogensen3 of a larger series confirming a rapid recovery after sig-
ponents: a multidisciplinary team working together around the moid resection using a multimodal approach. Kehlet, a surgeon, pro-
patient; a multimodal approach to resolving issues that delay recov- moted thoracic epidural anesthesia as a way of controlling pain, im-
ery and cause complications; a scientific, evidence-based ap- provingmobility,andreducingpostoperativeileus.Concurrently,other
proach to care protocols; and a change in management using inter- ERAS group members were addressing perioperative care from an
active and continuous audit. This review describes the development endocrine4 and metabolic viewpoint. This approach included the roles
of ERAS, how these ideas are brought into practice, and how they of specific amino acids in perioperative nutrition,5 inflammation and
are now spreading to various disciplines of surgical practice, as well protein metabolism in surgical patients with cancer,6 and metabolic
as some of the main outcome improvements and an implementa- preparation using a preoperative carbohydrate drink to avoid effects
tion strategy to achieve sustained outcome improvements. of fasting.7 The group was focused on enhancing recovery and reduc-
A project to improve outcomes of coronary artery bypass sur- ing complications by modifying the metabolic response to surgical in-
gery by bundling perioperative treatments under a concept name, Fast sult rather than just limiting length of stay.

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 Enhanced Recovery After Surgery Review Clinical Review & Education

Table 1. Member Sites and Leads of the Original Enhanced Recovery Table 2. ERAS Society Guideline Elements for Colonic Resectionsa
After Surgery Study Group Formed in 2001
Element Target Effect and/or Comment
University and Hospital Country Lead(s) Preadmission
University of Edinburgh United Ken Fearon Cessation of smoking and excessive Reduce complications
Kingdom intake of alcohol
Karolinska Institutet and Sweden Olle Ljungqvist Preoperative nutritional screening Reduce complications
Ersta Hospital Stockholm and, as needed, assessment and
University of Copenhagen Denmark Henrik Kehlet nutritional support
and Hvidovre Hospital Medical optimization of chronic Reduce complications
University of Northern Norway Norway Arthur Revhaug disease
and Troms Hospital Preoperative
University of Maastricht The Martin von Meyenfeldt, Structured preoperative information Reduce anxiety, involve the patient
Netherlands Cornelius DeJong and engagement of the patient and to improve compliance with protocol
relatives or caretakers
Preoperative carbohydrate Reduce insulin resistance, improve
The ERAS group gathered in London in 2001 to produce a pro- treatment well-being, possibly faster recovery
tocol that would optimize outcomes based on published evidence.8 Preoperative prophylaxis against Reduce thromboembolic
thrombosis complications
The group also published reports of variable outcomes in similar sur-
Preoperative prophylaxis against Reduce infection rates
gical procedures and populations demonstrating that periopera- infection
tive care, rather than the actual operation, dictated the outcomes.9 Prophylaxis against nausea and Minimize postoperative nausea and
Several surveys confirmed that perioperative care was variable across vomiting vomiting
Intraoperative
Northern Europe and that there was minimal adoption of evidence-
Minimal invasive surgical Reduce complications, faster
based practices.10 The group worked together developing ERAS by techniques recovery, reduce pain
testing protocols, running symposia, and involving national health Standardized anesthesia, avoiding Avoid or reduce postoperative ileus
ministries (such as the Enhanced Recovery Partnership Pro- long-acting opioids
gramme in the United Kingdom). Although ERAS concepts became Maintaining fluid balance to avoid Reduce complications, reduce
over- or underhydration, administer postoperative ileus
widely recognized, there was still minimal change across most health vasopressors to support blood
care systems. The ERAS Society (http://www.erassociety.org) was pressure control
Epidural anesthesia for open surgery Reduce stress response and insulin
founded to focus and consolidate progress not only through research resistance, basic postoperative pain
and education but also by developing models for implementation management
of best perioperative practices. Restrictive use of surgical site drains Support mobilization, reduce pain
and discomfort, no proven benefit
of use
Removal of nasogastric tubes before Reduce the risk of pneumonia,
reversal of anesthesia support oral intake of solids
The Rationale of ERAS Control of body temperature using Reduce complications
warm air flow blankets and warmed
A fundamental challenge in the care of the surgical patient lies with intravenous infusions
the journey the patient makes through various parts of the hospi- Postoperative
tal: outpatient clinics, preoperative units, the operating room, post- Early mobilization (day of surgery) Support return to normal movement
operative recovery facility, and the ward. Each unit has its own fo- Early intake of oral fluids and solids Support energy and protein supply,
(offered the day of surgery) reduce starvation-induced insulin
cus, personnel, and specialists. Each unit affects the ones to follow resistance
by the treatment choices made. For example, if the surgeon orders Early removal of urinary catheters Support ambulation and mobilization
oral bowel preparation, the anesthetist may face a dehydrated pa- and intravenous fluids (morning
after surgery)
tient to manage on induction of anesthesia. Few stakeholders in the
Use of chewing gums and laxatives Support return of gut function
surgical pathway have the opportunity to see a patient through the and peripheral opioid-blocking
entire journey. Hospital staff are often focused on managing the im- agents (when using opioids)
Intake of protein and energy-rich Increase energy and protein intake in
mediate clinical situation with little opportunity for strategic think- nutritional supplements addition to normal food
ing. There are 24 core elements of ERAS care that have scientific sup- Multimodal approach to Pain control reduces insulin
port for their use (Table 2). These components are distributed opioid-sparing pain control resistance, supports mobilization
along the patient pathway and delivered by different departments Multimodal approach to control Minimize postoperative nausea and
of nausea and vomiting vomiting and support energy and
and professionals within the hospital (Figure), which explains why protein intake
the surgeon, as the clinician with overall responsibility for the pa- Prepare for early discharge Avoid unnecessary delays in
discharge
tient, has the best opportunity for a comprehensive view to guide
Audit of outcomes and process in a Control of practice (a key to improve
the process. multiprofessional, multidisciplinary outcomes)
Consistent agreement on the end points of management is criti- team on a regular basis
cal for coordinated action. For example, the patient is medically suit- Abbreviation: ERAS, Enhanced Recovery After Surgery.
able to leave the hospital when the following conditions are true: a
For details and references, see the guidelines at http://www.erassociety.org.
he or she can eat and drink to fulfill daily needs, the bowels are mov-
ing, pain is controlled by oral analgesics, he or she is capable of suf- The ERAS elements of the program for colonic resection are
ficient mobility for self-care, and there are no complications requir- listed in Table 2. Most of the solutions to problems delaying recov-
ing hospital care. ery are evident once the perioperative care pathway is exhibited in

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 Clinical Review & Education Review Enhanced Recovery After Surgery

Figure. Enhanced Recovery After Surgery (ERAS) Flowchart

Preadmission Preoperative Intraoperative Postoperative

Preadmission nutritional Early removal of drains

support Minimal invasive surgery
Surgery Selective bowel preparation and tubes
Cessation of smoking Minimize drains and tubes
Stop intravenous fluids
Control alcohol intake

Regional analgesia
Preoperative carbohydrates Multimodal opioid-sparing
Opioid-sparing anesthesia
Anesthesia Medical optimization No NPO pain control
Balanced fluids
PONV prophylaxis
Temperature control

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

A typical ERAS flowchart overview indicating different ERAS protocol items to affect later treatments. No NPO indicates fasting guidelines recommending
be performed by different professions and disciplines in different parts of the intake of clear fluids and specific carbohydrate drinks until 2 hours before
hospital during the patient journey. The wedge-shaped arrows depicting each anesthesia; PONV, postoperative nausea and vomiting. Reprinted with
time period move into the period to follow to indicate that all treatments given permission from Olle Ljungqvist, MD, PhD.

total, which is often best achieved in a multidisciplinary meeting. This

method is how the ERAS Society runs its various implementation The Patients Journey
programs.
Consistent and well-attended team meetings are critical to imple-
mentation and improvement of the ERAS program (Figure). At the
outset, a unit should meet weekly to audit compliance and imple-
Multimodal Care
ment necessary changes to improve practice. After some time, the
No single element by itself will improve outcomes of surgery. The meeting frequency can be reduced to every other week, but atten-
approach to perioperative care must be multimodal, using all avail- dance at meetings must remain an established commitment for each
able elements of care that improve recovery. The key is to seek syn- team member.
ergy between one process element and the next. Since elements of
ERAS are implemented by different medical and health care spe-
cialties working in different departments, a multidisciplinary ap-
Evidence-Based Guidelines
proach is necessary. The elements of care are carried out by many
professionals: nurses, dieticians, and physiotherapists alongside phy- The ERAS Group published an initial consensus document on peri-
sicians and surgeons. operative care for colonic resections8 and later one for colorectal
surgery.12 After the ERAS Society was formed in 2010, the Society
published a series of guidelines (Table 3) and special papers with pro-
cedure-specific recommendations, which form the basis for the pro-
The ERAS Team
tocols built into the audit system. Society members have also tested
The core of changing practice and realizing the benefits of ERAS is a the efficacy of the guidelines. For example, in a single-center re-
team of the key individuals from the involved units. The medical port of more than 900 consecutive patients, improved compli-
leadership is most commonly a surgeon, supported by an anesthe- ance with the colorectal surgery guidelines resulted in a shorter
tist. The ERAS clinical leaders hold the medical responsibility for the length of stay, fewer complications, and fewer readmissions.13 A fol-
ERAS program, and their role as local champions is important.11 The low-up study from the ERAS Interactive Audit system with more than
ERAS project manager is commonly a nurse, who facilitates the 2300 consecutive patients in 13 units in 7 countries confirmed these
resources and management approval to enact change. The ERAS results.14
coordinator (in Europe often a nurse or, in the United States, a phy-
sician assistant) fills a key role as the engine of the ERAS team,
with time devoted to managing practical matters, which might
Audit
include such tasks as composing and distributing memos and
instructions, managing reporting and feedback to the units, and Because of the complexity of the care process, the team is helped
arranging for continuous training of new personnel. This individual by performing continuous audit of the care process and patient out-
is well positioned to manage the audit process. Participation from comes to maintain a comprehensive view. Based on the guidelines,
the other disciplines, including special services such as dietetics, the ERAS Society has developed a specific audit system for this pur-
occupational therapy, and physiotherapy, is critical to sustained pose, the ERAS Interactive Audit System, which is used in the ERAS
performance. Implementation Programs (http://www.erassociety.org) and is

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 Enhanced Recovery After Surgery Review Clinical Review & Education

tively involved in implementation of these evidence-based pro-

Table 3. ERAS Society Guidelinesa
cesses. To develop an implementation program, the ERAS group
Procedure and Topic Year of Publication worked with change-management specialists in the Netherlands and
Colonic resection 2012 Sweden to help implement ERAS guidelines and protocols. By using
Rectal resection 2012 this method, the Dutch team helped more than 30 colorectal units
Pancreaticoduodenectomy 2012 improve their outcomes by using ERAS recommendations. With a
Cystectomy 2013 structured implementation program that lasted 10 months, the units
Gastric resection 2014 mean length of stay decreased from 9 to 10 days to 6 days.21 A sub-
Anesthesia protocols 2015 sequent follow-up in the 10 most successful units showed that length
Anesthesia pathophysiology 2015 of stay in most of the units had increased again. This increase
Major gynecology (parts 1 and 2) 2015 correlated with a reduction in compliance with ERAS pathway ele-
Bariatric surgery 2016 ments in the absence of ongoing education and audit.22 Based on
Liver resection 2016 this experience, the ERAS Society developed an implementation pro-
Head and neck cancer surgery 2016 gram rooted in sustainability.23 A growing amount of literature on
Breast reconstruction 2017 barriers to implementation reports that factors that enable the suc-
Hip and knee replacement Under production cessful implementation of ERAS include not only a willingness to
Thoracic noncardiac surgery Under production change to ERAS, formation of multidisciplinary teams and thereby
Esophageal resection Under production
improved communication and collaboration, and support by hos-
pital management but also standardization of order sets and care
Abbreviation: ERAS, Enhanced Recovery After Surgery.
processes and the use of audit.24,25 Good local leadership and local
a
For updates and free download, go to http://www.erassociety.org.
champions are important success factors.11 Conversely, barriers to
implementation are a general resistance to change, lack of time and
currently available in France, Germany, Norway, Portugal, Spain, the staff, and poor communication, collaboration, and coordination
Netherlands, the United Kingdom, Sweden, Canada, the United between departments.24,25
States, Mexico, Brazil, Colombia, Argentina, Singapore, the It is also important to implement additional changes in light of
Philippines, New Zealand, Israel, Uruguay, Chile, and South Africa. new evidence. In colorectal surgery, the ERAS Society has revised
Health care professionals, and perhaps surgeons in particular, the guidance 3 times in 10 years and a fourth revision is under way.
tend to believe that their care and outcomes are better than they Building a system that is ready to make the next change is the key
actually are. During years of work with the ERAS programs, we have to quicken the pace of implementation of better care.
rarely encountered surgeons who believed that their patients who An important goal for the ERAS Society is to build a network of
underwent colorectal surgery are hospitalized for more than 3 to 4 hospitals around the world that uses a consistent audit tool. The re-
days. However, even in the countries that adhere most strongly to sulting data set will facilitate research, including the development
the ERAS protocol, national and individual hospital data for these of new ERAS protocols. The ERAS Society includes active centers
patients still reflect an average length of stay of 7 to 8 days. In many in several countries that are trained to implement ERAS processes
countries, the hospital stays are longer or data on length of stay are in their country or region. These centers can use the centralized, in-
not available (Swedish Colorectal Cancer Registry15; National Health ternet-based audit system that establishes the platform for the in-
Service Scotland; National Bowel Cancer Audit report 201516; and troduction of the next change. Enhanced Recovery After Surgery
Office fdral de la statistique mdicale des hpitaux, Suisse 201617). pathways continue to be developed, and current evidence is reex-
Finally, some surgical teams believe that they adhere to ERAS prin- amined by the ERAS guidelines group to keep up to date with
ciples while, in fact, they are using them only in part. Compliance changes in practice. An example is the move away from routine tho-
with 70% to 80% or more of the elements of the ERAS protocol racic epidural anesthesia for laparoscopic colorectal surgery26 in fa-
appears to be important to improve outcomes.11 vor of combining spinal analgesia or transverse abdominis plane
blocks with general anesthesia. By having many centers contribute
to the audit process, changes in care pathways can be introduced
and the downstream effect measured. It is equally important to main-
Implementation of ERAS
tain consistent compliance with the ERAS protocol once it is intro-
Recently, interest in ERAS has grown substantially, revealing a defi- duced. A follow-up study 3 to 6 years after a successful implemen-
cit in education and training, as few courses are targeted to hospi- tation of the ERAS protocol revealed that loss of continuous feedback
tal teams. Implementation of new practices is difficult, and new treat- with audit during a postimplementation program was a reason for
ments are slow to disseminate to active practice. Evidence suggests diminishing effectiveness.25 Reminders and boosters in education,
that change in clinical practice occurs 15 years after clear evidence updates in small groups, and retaining the ERAS coordinator were
is available.10 There is a need to support the medical and surgical other factors believed to be important for sustainability.
community to implement new and better care more quickly. About
310 million major operations are performed annually.18 Data sug-
gest that ERAS processes can reduce complications by 10% to 20%
or more by supporting units to adopt evidence-based care.13,14,19,20
Elements of ERAS
The primary vision of the ERAS Society is to help units use current The ERAS Society guidelines for colonic resections in Table 2 and the
best practice. Since its foundation, the ERAS Society has been ac- Figure are examples of elements commonly used in this

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 Clinical Review & Education Review Enhanced Recovery After Surgery

procedure.27,28 Enhanced Recovery After Surgery programs typi- than 900 consecutive patients with colorectal cancer showed the
cally contain several elements with 1 emphasis in common: they mini- effectiveness of ERAS protocols and highlighted the importance of
mize stress and improve the response to stress. By maintaining ho- compliance: the better the compliance to the protocol, the better
meostasis, the patient avoids catabolism with consequent loss of the outcomes in terms of complications, length of primary and total
protein, muscle strength, and cellular dysfunction.29 The reduction stay, and readmissions.13,14 These studies revealed that not only were
of insulin resistance promotes adequate cellular function during overall complications reduced with better compliance, but the most
injury to the tissue. The following series of elements contributes to severe complications, which resulted in reoperations or admission
this goal: preoperative nutritional support for the patient who is to the intensive care unit, decreased as mortality improved.14,34 Fit
malnourished, carbohydrate loading before surgery to minimize patients undergoing colorectal cancer surgery using ERAS prin-
postoperative insulin resistance, epidural or spinal analgesia to ciples and laparoscopic surgery can be discharged within 24 hours,
reduce the endocrine stress response, anti-inflammatory drugs to with a mean length of stay of 2.7 days.35
reduce the inflammatory response, early feeding after surgery to Colorectal surgery was the basis for the development of ERAS
secure energy intake, and optimal pain control to avoid stress and and still dominates the literature; however, in many other surgical
insulin resistance. domains, the implementation of ERAS patient care and principles
Enhanced Recovery After Surgery processes also aim to mini- of process improvement have improved outcomes. Studied areas
mize fluid shifts. Too little fluid can cause a reduction in perfusion include liver resections36; pancreatic, gastric, and esophageal
and organ dysfunction, whereas intravenous salt and fluid over- surgery37,38; thoracic surgery39; major urologic surgery40; gyneco-
load is recognized as a major cause of postoperative ileus and its logic surgery41; orthopedic surgery42,43; and emergency surgery.44
complications.30,31 Maintaining euvolemia, cardiac output, and de-
livery of oxygen and nutrients to the tissues are important to pre-
serve cellular function, particularly when there is tissue injury and
Financial Effects of the Implementation of ERAS
need for repair. Once patients are euvolemic, vasopressors may be
used as required to maintain mean arterial pressure. Targeting mini- Although most reports of ERAS come from single units, with devel-
mal weight change (30 mL/kg net intake of intravenous fluid, keep- opers and early adopters achieving some of the best results, the chal-
ing weight gain within 2 kg) is typically recommended. Postopera- lenge lies with having most surgical procedures performed using
tive intravenous fluids are generally discontinued at about 24 hours ERAS principles. In the United Kingdom, the National Health Ser-
after surgery. A patient progressing normally on an ERAS pathway vice ran the Enhanced Recovery Partnership Programme,45 based
should be drinking, eating, mobilizing, and sleeping on the day af- on lectures by experts and early adopters along with the provision
ter operation. The ERAS program also avoids several traditional care of treatment protocols and advice. The program encompassed not
elements that have been shown to be harmful, such as the routine only colorectal surgery but also cystectomy, gynecologic surgery, and
use of nasogastric tubes, prolonged urinary catheterization, and pro- hip and knee replacement. Adoption of some of the ERAS ele-
longed or inappropriate use of abdominal drains. ments was incentivized by bonus payments, but most of the main-
tenance of ERAS pathways relied on local peer groups to continue
the pathways in whatever manner they considered appropriate. Al-
though some units continue to produce excellent results, the En-
Outcomes With the ERAS Protocol
hanced Recovery Partnership Programme lacked resources to sup-
There are many stakeholders in surgical care, with ERAS processes port sustainability, and the overall results have been difficult to
putting the patient at the center. Professionals from various disci- discern in national statistics.
plines as well as managers, politicians, payers, and the general pub- In Alberta, Canada, the state health care service worked with
lic are involved, as are the medical device and pharmaceutical the ERAS Society to implement ERAS, starting with colorectal sur-
industries. gery. The ERAS Society provided training in the first 2 hospitals, which
are now supporting training in other hospitals using the same prin-
Length of Stay ciples. The first results are promising, with shorter stay (reduction
The broader ERAS principles have been published for many types from 6 to 4 days) and an 11% reduction in complications.46 There
of procedures in all major surgical specialties. The early studies show- were 8% fewer readmissions and a shorter stay for those readmit-
ing a 2-day hospital stay after sigmoid resection2,3 were often met ted, saving $2800 to $5900 per patient.
with disbelief, and some thought (incorrectly) that it was careful
selection of patients that resulted in a shortened length of stay. Now,
diverse groups publishing on consecutive series and using ERAS prin-
Long-term Benefits of ERAS
ciples show consistent results,32 and, with the addition of laparo-
scopic techniques, the same results have been demonstrated in The longer-term benefits of rapid, uncomplicated recovery using
patients with complex medical conditions.33 ERAS principles are less well known. Medium-term outcomes have
been sparsely studied,47 and long-term data on outcomes are now
Complications beginning to appear. One observational study in 4500 patients un-
A meta-analysis of randomized trials of the ERAS protocol in pa- dergoing hip and knee replacement showed that 2-year mortality
tients undergoing colorectal surgery showed that complication rates was significantly lowered after the introduction of ERAS principles.48
were reduced by up to 50% when ERAS principles were used.19 This A report on more than 900 patients with colorectal cancer showed
finding was confirmed in a larger series.20 Further data from more that, with compliance above 70% with the ERAS preoperative and

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 Enhanced Recovery After Surgery Review Clinical Review & Education

intraoperative protocol, mortality fell by 42% compared with pa- worldwide and by hosting professional meetings and events for many
tients with compliance below 70%.34 In this study, the data were ad- national groups. The ERAS Society has hosted an Annual World Con-
justedforseveralvariables,includingage,sex,bodymassindex,Ameri- gress since 2012 and is active in currently mining the substantial data
can Society of Anesthesiologists score, surgical procedure, and available from the ERAS Interactive Audit System. The system pro-
pathologic findings. The data show an association rather than causa- vides the basis for both prospective trials and audit research. Audit-
tion and other biases may have contributed directly or indirectly. For based research is completed using large numbers of patients on the
example, the group with higher compliance had fewer complica- same pathway. Making a single-step change and analyzing the down-
tions, which may have affected the observed outcomes. Periopera- stream effect using regression analysis may be a complementary way
tive complications have been shown to be strongly associated with to study new interventions rather than relying on expensive ran-
poorlong-termoutcomesinverylargesurgicalseries.49 Incancertreat- domized clinical trials.
ment, surgical complications may also delay the initiation of postop-
erative chemotherapy which in turn may contribute to reduced long-
termsurvival.Complicationsalsoincreasethecostofcare.50 Enhanced
Conclusions
Recovery After Surgery programs are thus supporting a combina-
tion of better outcomes and cost savings. Enhanced Recovery After Surgery programs represent a paradigm
shift in how surgical care is delivered and how changes in practice
are disseminated and implemented. These results rely on a new ap-
proach to teamwork, continuous audit, and support of data-driven
The Future of ERAS
change and improvement. Enhanced Recovery After Surgery prac-
As ERAS principles are applied across all surgical specialties, ongo- tices improve the opportunity for rapid, uncomplicated recovery af-
ing innovation must continue to allow processes to improve. There ter surgery with both short- and long-term benefits for patients while
is increasing focus on procedure-specific specialty items to at- improving quality and saving money.
tempt to improve outcomes. The ERAS Society continues to work There is financial pressure surrounding health care spending,
alongside various national ERAS Societies in the European Union, as limited societal funds to support health care meet rising de-
Asia, and the United States. The ERAS Society and its national soci- mands owing to expensive technology, increased patient expecta-
eties also collaborated with established professional specialty tions, and a growing elderly population. In the United States, the
groups, such as the Society of American Gastrointestinal and Endo- 2010 Patient Protection and Affordable Care Act has also delivered
scopic Surgeons, by co-authoring the Manual of Enhanced Recovery51 specific challenges for health care systems by introducing broad-
and have worked closely with ERAS USA (the ERAS Society chapter ened coverage of the population and has gradually implemented
that is recently formed in the United States) as well as supported changes in payment models to make health care systems more re-
the slightly older American Society of Enhanced Recovery. The goal sponsible for costs. Enhanced Recovery After Surgery pathways can
of the ERAS Society is to complement the programs of these na- be a key strategy in addressing these issues by offering improved
tional groups and to offer additional value by coordinating activity quality care for less cost.

ARTICLE INFORMATION Role of the Funder/Sponsor: The funding source hepatic release of glutamine in sepsis. Ann Surg.
Kenneth C. Fearon, MD, PhD, died during the final had no role in the design and conduct of the study; 1998;228(1):131-139.
revision of this article. collection, management, analysis, and 5. van der Hulst RR, van Kreel BK, von Meyenfeldt
interpretation of the data; preparation, review, or MF, et al. Glutamine and the preservation of gut
Accepted for Publication: June 18, 2016. approval of the manuscript; and decision to submit integrity. Lancet. 1993;341(8857):1363-1365.
Published Online: January 11, 2017. the manuscript for publication.
doi:10.1001/jamasurg.2016.4952 6. Fearon KC, Falconer JS, Slater C, McMillan DC,
Additional Contributions: This review is dedicated Ross JA, Preston T. Albumin synthesis rates are not
Author Contributions: Drs Ljungqvist and Fearon to Kenneth C. Fearon, MD, PhD, our close friend, decreased in hypoalbuminemic cachectic cancer
are founding members of the Enhanced Recovery collaborator, and co-author who died during the patients with an ongoing acute-phase protein
After Surgery (ERAS) Study Group and ERAS finalization of this article. response. Ann Surg. 1998;227(2):249-254.
Society. Drs Ljungqvist, Scott, and Fearon are
Executive Officers of the ERAS Society. ERAS is a REFERENCES 7. Nygren J, Thorell A, Jacobsson H, et al.
registered trademark for goods and services owned Preoperative gastric emptying: effects of anxiety
1. Engelman RM, Rousou JA, Flack JE III, et al. and oral carbohydrate administration. Ann Surg.
and provided by the Enhanced Recovery After Fast-track recovery of the coronary bypass patient.
Surgery Society for Perioperative Care. 1995;222(6):728-734.
Ann Thorac Surg. 1994;58(6):1742-1746.
Study concept and design: All authors. 8. Fearon KC, Ljungqvist O, Von Meyenfeldt M,
Acquisition, analysis, or interpretation of data: All 2. Bardram L, Funch-Jensen P, Jensen P, Crawford et al. Enhanced recovery after surgery: a consensus
authors. ME, Kehlet H. Recovery after laparoscopic colonic review of clinical care for patients undergoing
Drafting of the manuscript: All authors. surgery with epidural analgesia, and early oral colonic resection. Clin Nutr. 2005;24(3):466-477.
Critical revision of the manuscript for important nutrition and mobilisation. Lancet. 1995;345(8952):
763-764. 9. Nygren J, Hausel J, Kehlet H, et al. A comparison
intellectual content: All authors. in five European Centres of case mix, clinical
Conflict of Interest Disclosures: Dr Ljungqvist 3. Kehlet H, Mogensen T. Hospital stay of 2 days management and outcomes following either
reported being the founder and a shareholder in after open sigmoidectomy with a multimodal conventional or fast-track perioperative care in
EnCARE AB, Sweden (http://www.encare.se), the rehabilitation programme. Br J Surg. 1999;86(2): colorectal surgery. Clin Nutr. 2005;24(3):455-461.
provider of the ERAS Interactive Audit System. No 227-230.
10. Lassen K, Hannemann P, Ljungqvist O, et al;
other disclosures were reported. 4. Balteskard L, Unneberg K, Mjaaland M, Jenssen Enhanced Recovery After Surgery Group. Patterns
Funding/Support: Dr Ljungqvist was supported by TG, Revhaug A. Growth hormone and insulinlike in current perioperative practice: survey of
funds from Nyckelfonden, rebro, Sweden. growth factor 1 promote intestinal uptake and colorectal surgeons in five northern European
countries. BMJ. 2005;330(7505):1420-1421.

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 Clinical Review & Education Review Enhanced Recovery After Surgery

11. Gotlib Conn L, McKenzie M, Pearsall EA, McLeod 25. Ament SM, Gillissen F, Moser A, et al. pathway for esophageal resection: impact on
RS. Successful implementation of an enhanced Identification of promising strategies to sustain length of stay and major outcomes. Reg Anesth Pain
recovery after surgery programme for elective improvements in hospital practice: a qualitative Med. 2015;40(2):139-149.
colorectal surgery: a process evaluation of case study. BMC Health Serv Res. 2014;14(1):641. 39. Madani A, Fiore JF Jr, Wang Y, et al. An
champions experiences. Implement Sci. 2015;10:99. 26. Levy BF, Scott MJ, Fawcett W, Fry C, Rockall TA. enhanced recovery pathway reduces duration of
12. Lassen K, Soop M, Nygren J, et al; Enhanced Randomized clinical trial of epidural, spinal or stay and complications after open pulmonary
Recovery After Surgery (ERAS) Group. Consensus patient-controlled analgesia for patients lobectomy. Surgery. 2015;158(4):899-910.
review of optimal perioperative care in colorectal undergoing laparoscopic colorectal surgery. Br J Surg. 40. Xu W, Daneshmand S, Bazargani ST, et al.
surgery: Enhanced Recovery After Surgery (ERAS) 2011;98(8):1068-1078. Postoperative pain management after radical
Group recommendations. Arch Surg. 2009;144(10): 27. Gustafsson UO, Scott MJ, Schwenk W, et al; cystectomy: comparing traditional versus enhanced
961-969. Enhanced Recovery After Surgery (ERAS) Society recovery protocol pathway. J Urol. 2015;194(5):
13. Gustafsson UO, Hausel J, Thorell A, Ljungqvist for Perioperative Care; European Society for Clinical 1209-1213.
O, Soop M, Nygren J; Enhanced Recovery After Nutrition and Metabolism (ESPEN); International 41. Nelson G, Kalogera E, Dowdy SC. Enhanced
Surgery Study Group. Adherence to the enhanced Association for Surgical Metabolism and Nutrition recovery pathways in gynecologic oncology.
recovery after surgery protocol and outcomes after (IASMEN). Guidelines for perioperative care in Gynecol Oncol. 2014;135(3):586-594.
colorectal cancer surgery. Arch Surg. 2011;146(5): elective colonic surgery: Enhanced Recovery After
571-577. Surgery (ERAS() Society recommendations. World 42. Stowers MD, Manuopangai L, Hill AG, Gray JR,
J Surg. 2013;37(2):259-284. Coleman B, Munro JT. Enhanced Recovery After
14. ERAS Compliance Group. The impact of Surgery in elective hip and knee arthroplasty
enhanced recovery protocol compliance on elective 28. Gustafsson UO, Scott MJ, Schwenk W, et al; reduces length of hospital stay. ANZ J Surg. 2016;86
colorectal cancer resection: results from an Enhanced Recovery After Surgery Society. (6):475-479.
international registry. Ann Surg. 2015;261(6):1153- Guidelines for perioperative care in elective colonic
1159. surgery: Enhanced Recovery After Surgery (ERAS) 43. Jrgensen CC, Madsbad S, Kehlet H; Lundbeck
Society recommendations. Clin Nutr. 2012;31(6): Foundation Centre for Fast-track Hip and Knee
15. Swedish Colorectal Cancer Registry. Tjock-och Replacement Collaborative Group. Postoperative
ndtarmscancer. http://www.kvalitetsregister.se 783-800.
morbidity and mortality in type-2 diabetics after
/hittaregister/registerarkiv 29. Ljungqvist O. Jonathan E. Rhoads lecture 2011: fast-track primary total hip and knee arthroplasty.
/tjockochandtarmscancer.2315.html. Accessed insulin resistance and enhanced recovery after Anesth Analg. 2015;120(1):230-238.
December 7, 2016. surgery. JPEN J Parenter Enteral Nutr. 2012;36(4):
389-398. 44. Roulin D, Blanc C, Muradbegovic M, Hahnloser
16. The Association of Coloproctology of Great D, Demartines N, Hbner M. Enhanced recovery
Britain and Ireland. National Bowel Cancer Audit 30. Lobo DN, Bostock KA, Neal KR, Perkins AC, pathway for urgent colectomy. World J Surg. 2014;
(NBOCA). http://www.acpgbi.org.uk/members Rowlands BJ, Allison SP. Effect of salt and water 38(8):2153-2159.
/groups/nbocap/. Accessed December 7, 2016. balance on recovery of gastrointestinal function
after elective colonic resection: a randomised 45. Simpson JC, Moonesinghe SR, Grocott MP,
17. Office Fdral de la Statistique. Sant: quoi de et al; National Enhanced Recovery Partnership
neuf? https://www.bfs.admin.ch/bfs/fr/home controlled trial. Lancet. 2002;359(9320):1812-1818.
Advisory Board. Enhanced recovery from surgery in
/statistiques/sante.html. Accessed December 7, 31. Bragg D, El-Sharkawy AM, Psaltis E, the UK: an audit of the Enhanced Recovery
2016. Maxwell-Armstrong CA, Lobo DN. Postoperative Partnership Programme 2009-2012. Br J Anaesth.
18. Weiser TG, Haynes AB, Molina G, et al. Estimate ileus: recent developments in pathophysiology and 2015;115(4):560-568.
of the global volume of surgery in 2012: an management. Clin Nutr. 2015;34(3):367-376.
46. Nelson G, Kiyang LN, Crumley ET, et al.
assessment supporting improved health outcomes. 32. Senagore AJ, Whalley D, Delaney CP, Mekhail N, Implementation of Enhanced Recovery After
Lancet. 2015;385(suppl 2):S11. Duepree HJ, Fazio VW. Epidural anesthesia Surgery (ERAS) across a provincial healthcare
19. Varadhan KK, Neal KR, Dejong CH, Fearon KC, analgesia shortens length of stay after laparoscopic system: the ERAS Alberta colorectal surgery
Ljungqvist O, Lobo DN. The Enhanced Recovery segmental colectomy for benign pathology. Surgery. experience. World J Surg. 2016;40(5):1092-1103.
After Surgery (ERAS) pathway for patients 2001;129(6):672-676.
47. Neville A, Lee L, Antonescu I, et al. Systematic
undergoing major elective open colorectal surgery: 33. Delaney CP, Fazio VW, Senagore AJ, Robinson review of outcomes used to evaluate enhanced
a meta-analysis of randomized controlled trials. Clin B, Halverson AL, Remzi FH. Fast track recovery after surgery. Br J Surg. 2014;101(3):159-170.
Nutr. 2010;29(4):434-440. postoperative management protocol for patients
with high co-morbidity undergoing complex 48. Savaridas T, Serrano-Pedraza I, Khan SK, Martin
20. Greco M, Capretti G, Beretta L, Gemma M, K, Malviya A, Reed MR. Reduced medium-term
Pecorelli N, Braga M. Enhanced recovery program abdominal and pelvic colorectal surgery. Br J Surg.
2001;88(11):1533-1538. mortality following primary total hip and knee
in colorectal surgery: a meta-analysis of arthroplasty with an enhanced recovery program:
randomized controlled trials. World J Surg. 2014;38 34. Gustafsson UO, Oppelstrup H, Thorell A, a study of 4,500 consecutive procedures. Acta
(6):1531-1541. Nygren J, Ljungqvist O. Adherence to the Orthop. 2013;84(1):40-43.
21. Gillissen F, Hoff C, Maessen JM, et al. Structured ERAS-protocol is associated with 5-year survival
after colorectal cancer surgery: a retrospective 49. Khuri SF, Henderson WG, DePalma RG, Mosca
synchronous implementation of an enhanced C, Healey NA, Kumbhani DJ; Participants in the VA
recovery program in elective colonic surgery in 33 cohort study. World J Surg. 2016;40(7):1741-1747.
National Surgical Quality Improvement Program.
hospitals in the Netherlands. World J Surg. 2013;37 35. Levy BF, Scott MJ, Fawcett WJ, Rockall TA. Determinants of long-term survival after major
(5):1082-1093. 23-Hour-stay laparoscopic colectomy. Dis Colon surgery and the adverse effect of postoperative
22. Gillissen F, Ament SM, Maessen JM, et al. Rectum. 2009;52(7):1239-1243. complications. Ann Surg. 2005;242(3):326-341.
Sustainability of an enhanced recovery after 36. Song W, Wang K, Zhang RJ, Dai QX, Zou SB. The 50. Vonlanthen R, Slankamenac K, Breitenstein S,
surgery program (ERAS) in colonic surgery. World J Enhanced Recovery After Surgery (ERAS) program et al. The impact of complications on costs of major
Surg. 2015;39(2):526-533. in liver surgery: a meta-analysis of randomized surgical procedures: a cost analysis of 1200
23. Roulin D, Donadini A, Gander S, et al. controlled trials. Springerplus. 2016;5:207. patients. Ann Surg. 2011;254(6):907-913.
Cost-effectiveness of the implementation of an 37. Jeong O, Ryu SY, Park YK. Postoperative 51. Feldman L, Delaney CP, Ljungqvist O, Carli F.
enhanced recovery protocol for colorectal surgery. functional recovery after gastrectomy in patients The SAGES/ERAS Society Manual of Enhanced
Br J Surg. 2013;100(8):1108-1114. undergoing Enhanced Recovery After Surgery: Recovery Programs for Gastrointestinal Surgery. New
24. Pearsall EA, Meghji Z, Pitzul KB, et al. a prospective assessment using standard discharge York, NY: Springer; 2015.
A qualitative study to understand the barriers and criteria. Medicine (Baltimore). 2016;95(14):e3140.
enablers in implementing an enhanced recovery 38. Porteous GH, Neal JM, Slee A, Schmidt H, Low
after surgery program. Ann Surg. 2015;261(1):92-96. DE. A standardized anesthetic and surgical clinical

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