Editorial Open Access
Copyright ©2012 Baishideng Publishing Group Co., Limited. All rights reserved.
World J Gastrointest Surg. Aug 27, 2012; 4(8): 190-198
Published online Aug 27, 2012. doi: 10.4240/wjgs.v4.i8.190
Enhanced recovery for colorectal surgery: Practical hints, results and future challenges
Gianpiero Gravante, Department of Colorectal Surgery, Pilgrim Hospital, Boston, Lincolnshire PE21 9QS, United Kingdom
Muhammad Elmussareh, Department of Surgery, Leicester Royal Infirmary, Leicester, Leicestershire LE1 5WW, United Kingdom
Author contributions: Gravante G and Elmussareh M directly participated in the study in terms of contributions to conception and design, acquisition of data, and analysis or interpretation of data and both wrote the manuscript and revised it critically.
Correspondence to: Gianpiero Gravante, MD, Department of Colorectal Surgery, Pilgrim Hospital, Castle Road, Boston, Lincolnshire PE21 9QQ, United Kingdom. ggravante@hotmail.com
Telephone: +44-11-62588244 Fax: +39-6-233216592
Received: October 31, 2011
Revised: July 14, 2012
Accepted: August 2, 2012
Published online: August 27, 2012

Abstract

Enhanced recovery after surgery (ERAS) protocols are now achieving worldwide diffusion in both university and district hospitals with special interest in colorectal surgery. The optimization of the patient’s preoperative clinical conditions, the careful intraoperative administration of fluids and drugs and the postoperative encouragement to resume the normal physiological functions as early as possible has produced results in a large amounts of studies. These approaches successfully challenged long-standing and well-established perioperative managements and finally achieved the status of gold standard treatments for the perioperative management of uncomplicated colorectal surgery. Even more important, it seems that the clinical improvement of the patient’s clinical management through ERAS protocols is now reaching his best outcomes (length of stay of 4-6 d after the operation) and therefore any further measures add little to the results already established (i.e., the adjunct of laparoscopic surgery to ERAS). Still dedicated meetings and courses around the world are exploring new aspects including the improvement the preoperative nutrition status to provide the energy necessary to face the surgical stress, the preoperative individuation of special requirements that could be properly addressed before the date of surgery and therefore would reduce the number of unnecessary days spent in hospital once fully recovered (i.e., rehabilitation, social discharges), and finally the development of an important web of out-of-hours direct access in order to individuate alarm symptoms in those patients at risk of complications that could prompt an early readmission.

Key Words: Enhanced recovery, Fast track, Colorectal surgery, Length of stay



INTRODUCTION

Enhanced recovery after surgery (ERAS) is a series of perioperative protocols that aim to improve the patient’s ability to face major operations and consequently ameliorate his postoperative recovery[1]. ERAS interventions focus on those key factors that usually keep patients in hospital and make them dependent on drugs and specialist assistance following uncomplicated surgery, namely the need for parenteral analgesia, the administration of intravenous fluids and confinement to bed[2]. Pillars of ERAS protocols cover all the perioperative phases by removing or decreasing the influence of such factors and promoting good habits that favour the recover of physiological functions. Therefore, they avoid mechanical bowel preparations (MBPs) and preoperative fasting before surgery and administer high carbohydrate meals until few hours from the operation; they limit the administration of fluids tailoring them to the real patient’s necessities during surgery; they encourage the resumption of an oral diet and early mobilization after surgery as well as they decrease the use of regular opioids using pain killers with less impact on the gut function[2-5].

Since their introduction ERAS protocols faced large resistances because they targeted diffuse and time-validated clinical practices[6]. These were mostly based on tradition, personal experiences, and surgical teaching that helped their historical perpetration. However, the growing amount of data available has showed now how such practices were not necessary or contributed to the adverse effects of the surgical trauma. As a result the most immediate and visible effect of ERAS introduction is a significant shortening of the length of stay (LOS) in hospital and therefore a better redistribution of the available resources. Nowadays ERAS is routine in large university hospitals and is also spreading to district general hospitals with special interests in colorectal operations[7].

PROTOCOLS
Preoperative period

Different ERAS protocols are available for colorectal surgery (Table 1). In most of them patients receive a preoperative functional assessment in order to target the eventual specific postoperative requirements and provide him with an adequate care organised for his necessities. Also, the preoperative visit would counsel the patients about the purposes and goals of the enhanced recovery addressing their expectations from the surgical recovery and reassuring them about the purposes of the early discharge. This should not be perceived as an economic necessity, but, when feasible and appropriate, is an integrated part of the treatment that avoids prolonged stays in wards where the risk of transmitted infections is significant.

Table 1 Types of enhanced recovery after surgery protocols adopted.
Ref.PreoperativeIntraoperativePostop (first 24 h)Day 1Day 2Day 3Day 4Additional comments
Kahokehr et al[8,9]Nutritional supplementationThoracic epiduralAll IV fluid stoppedRemoval of urinary catheterRemoval of epiduralEarly mobilization and physiotherapy
NBM two hours preinductionShort acting anaestheticsProphylactic antiemetics
Carbohydrate loadingIntraoperative fluids: 1000 mL of crystalloid and 500 mL of colloidEarly oral feeding
No bowel preparationProphylactic antiemetics at induction (Dexamethasone)Nutritional supplementation
Functional assessment and goal settingNo drains or NG tubesNo opioids
King et al[12-14]Nutrition supplementationThoracic epiduralFree fluidAll IV fluid stoppedRemoval of epidural Regular NSAIDSRemoval of urinary catheter for rectal resectionsAim for discharge on day 3 for colonic or day 5 for rectal resection
Blazeby et al[15]Optimised pre-morbid health statusIntraoperative fluids: 2000 mL of crystalloidNutritional supplementationRegular paracetamolMorphine for breakthroughProvision of hospital contact numbers, review on ward if problems within 2 wk
Faiz et al[16]Functional assessment and goal settingMinimal-access surgeryPatient sat out in chair3 high-protein/high-calorie drinkReview in outpatient clinic on day 12
Stoma nurseLocal anaesthetic infiltration to the largest woundNormal diet offered
Bowel preparation in left-sided resectionsNo drains or NG tubesPatient sat out in chair
Start walking
Removal of urinary catheter for colonic resections
Laxatives
Jottard et al[7]Nutrition supplementationThoracic epiduralFree fluidAll IV fluid stoppedUse of anti-emetics
Functional assessment and goal settingStandard anesthetic protocolNormal diet offeredEarly mobilization
No bowel preparationPrevention of intraoperative hypothermiaPostoperative nutritional care
No drains or NG tubes
Maessen et al[20,21]Nutrition supplementation1Thoracic epiduralOral analgesiaAll IV fluid stoppedRemoval of epidural Removal of urinary catheter
Nygren et al[22]Functional assessment and goal settingPrevention of intraoperative hypothermiaPatient sat out in chairNutritional supplements > 400 mL
Hendry et al[23]No bowel preparationTransverse/curved incisionNutritional supplementsNormal diet offered
Free fluid > 800 mLPatient sat out in chair
Soop et al[26]Nutrition supplementationThoracic epiduralProphylactic antiemeticsRegular paracetamol and NSAIDSPatient sat out in chairPatient sat out in chairEpidural removed (at least)
Patient sat out in chair
Raymond et al[28]Nutrition supplementation Functional assessment and goal settingThoracic epiduralEarly mobilization/resumption of diet
Intra-operative targeted fluid management
No NG tube
Turunen et al[10]Functional assessment and goal settingThoracic epiduralRemoval of urinary catheterEarly mobilization/resumption of diet
Preoperative feedingHigh-oxygen PNo routine opioids, regular paracetamol and NSAIDS
Bowel preparationPrevention of hypothermiaFluid restriction
No drains or NG tubes
Senagore et al[35]No NG tubePCARemoval of urinary catheter
Free fluidsNormal diet offered
regular NSAIDs, gabapentin, hydroxycodone if needed
No drains
Wennstrom et al[11]Functional assessment and goal settingThoracic epiduralFree fluidEpidural removed
No bowel preparationShort acting anaestheticsPatient sat out in chairUrinary catheter removal
Preoperative oral hydrationNo opioids
Mohn et al[18]Nutrition supplementationThoracic epiduralPatient sat out in chairRemoval of urinary catheter Patient sat out in chairEpidural removedRegular laxatives twice daily
Functional assessment and goal settingTotal intravenous anaesthesiaNormal diet offered
Bowel preparationIntra-operative targeted fluid managementRegular paracetamol and NSAIDs, opioids for breakthroughRestricted postoperative intravenous fluids
Prophylactic antiemetics
Short midline incisions
No drains or NG tubes
Teeuwen et al[17]Nutrition supplementationThoracic epiduralFree fluidsNormal diet offeredEpidural removed
Bowel preparation in left-sided resectionsTransverse incisions except in Crohn's disease and rectal surgeryNutritional supplementsIntravenous fluid administrationUrinary catheter removal
Intra-operative targeted fluid management (hypotension treated with vasopressors)Patient sat out in chairStart walkingRegular Paracetamol NSAIDs, opioids for breakthrough
Prophylactic antiemetics
No drains or NG tubes
Ahmed et al[24,25]Nutrition supplementationHigh inspired oxygenFree fluidsStart walkingRegular paracetamol NSAIDs, opioids for breakthrough
Functional assessment and goal settingConcentrationSoft diet offered
No bowel preparationTransverse incisionsPatient sat out in chair
No drains or NG tubes
Kirdak et al[19]Nutrition supplementationThoracic epiduralStart walkingNG tubes and urinary catheters removed (except pelvic dissection)Removal urinary catheter (low pelvic operations) and drainsEpidural removed
Bowel preparationPelvic drains with rectal dissectionsSoft diet offeredRegular paracetamol
Urinary, central venous, and nasogastric catheters were routinely usedPatient sat out in chairCentral venous catheters removed
Start walkingNormal diet

Various protocols evaluate the nutritional status of patients, and, when necessary, oral supplementation is administered. Patients are usually fed until two hours before induction to avoid unnecessary consumption of body nutrients[8-11]. Few studies specified the necessity of a carbohydrate loading to prepare the body to the surgical stress and this seems a promising field of research[8,9]. Most studies do not administer MBP but some of them still use it in case of high-risk anastomosis (i.e., left-sided colonic resections)[12-17]. Only few authors use MBP routinely nowadays[10,18,19].

Intraoperative period

The leading concept of ERAS for the intraoperative phase is to administer drugs and fluids to the minimum dose effectively required by the patient and the operation. The avoidance of excessive amounts of drugs during surgery prevents their postoperative side-effects and accelerates the recovery. In this view, some authors administer short-acting anaesthetics to tailor them to the ongoing surgical necessity and to stop them quickly when not required anymore[8,9,11]. Similarly, intraoperative fluids are carefully given ranging from 1000 mL crystalloids and 500 mL colloids[8,9] to a total of 2000 mL crystalloids[12-16]. Intraoperative hypothermia is always avoided (Table 1).

Another important concept is that the control of postoperative pain already starts with some simple but effective intraoperative measures. Thoracic epidural can easily control postoperative pain after the operation. The simple infiltration of local anesthetics in the largest wound at the end of surgery also contribute to a better pain control[12-16]. Finally, transverse or curved incisions should be preferred when feasible[20-23].

Postoperative period

In the postoperative period the general purpose of ERAS is to resume the normal physiological activities and to stop the artificial introduction of fluids and drugs as soon as tolerated by patients. In this view, the administration of intravenous fluids, already restricted during the operation, is definitely discontinued during the first postoperative hours in most studies[18]. Early oral feeding is started in the form of free fluids up to 800 mL[8,9,20-23], a soft diet[24,25], or oral nutritional supplementation (one high-protein/high-calorie drink)[12-16] along with regular antiemetics to prevent nausea[8,9,17,18]. To facilitate the resumption of bowel motility patients avoid regular opioids (still used for breakthrough pain), receive oral analgesia in the form of regular Paracetamol and non-steroidal antinflammatory drugs (with proton-pump inhibitors coverage)[26] and are encouraged to sit out in chair. Rarely patients are encouraged to start walking after the operation[19] although this target is usually achieved on the first postoperative day[24,25]. Nasogastric tubes or drains are avoided to facilitate mobilisation and feeding but few authors maintain them after pelvic surgery[19].

During the 1st postoperative day the diet is built up to a normal meal or three high-protein/high-calorie drinks[12-16], and some laxatives may be used to stimulate the bowel function[12-16]. The urinary catheter is removed in most colonic resections exception made for pelvic surgery where it can last until the 2nd or 3rd postoperative day[12-16,19]. On the second postoperative day the epidural is removed and by the 4th or 5th day patients are evaluated for discharge.

RESULTS
LOS and readmission rates

Nine studies compared LOS between ERAS and conventional care (CC) in colorectal surgery[7,9,14,17,18,20,22,27,28] (Table 2). In all of them the LOS was reduced of about 54%-61% following ERAS protocols[14] and the ERAS median hospital stay was 4-6 d compared to 8-9 d following CC[7,9,17,20,27,28]. There was no evidence that the relative effect of ERAS on LOS varied according to the type of surgery (laparoscopic, laparoscopic converted, open)[14]. In one study ERAS reduced the LOS equally in both laparoscopic (from a median of 7 d to a median of 5 d) and open surgery (from a median of 9 d to a median of 7 d)[28]. However, there was no change or improvement in the time taken to return to full activity for either group[28].

Table 2 Clinical characteristics of studies examined.
Ref.Type of studyPatients (n)Sex (males%)Age (yr)Type of surgeryApproachLength of stay (d)MorbidityMortalityReadmissionComments
King et al[14]Prospective case series6031 (52)72 ± 11ERAS5.811 (18%)2 (3%)7 (12%)ERAS ↓ hospital stay
8645 (52)70 ± 11Conventional10.7 (P < 0.001)24 (28%)6 (7%)8 (9%)
Maessen et al[20]Observational study425--Resections above peritoneal reflectionERAS5 d---Delay in discharge was due to the development of major complications
Maessen et al[21]Case series12167 (55)66 ± 12Resections above peritoneal reflection without stomaERASDischarge delay = 1 d---↓ in hospital stay may relate to changes in organization of care and not to a shorter recovery period
5222 (42)64 ± 12Resections above peritoneal reflection without stomaConventionalDischarge delay = 2 d
Jottard et al[7]Prospective ERAS group matched with historical data36--ERAS6 (3-27)---ERAS was implemented in a district general hospital
92--Conventional9 (3-64)---
Hendry et al[23]Prospective case series1035498 (48.10)59 (69-78)ERAS6 (4-8)294 (28.40%)17 (1.60%)86 (8.60%)Higher ASA, advanced age, sex (male) and rectal surgery associated with delayed mobilization, morbidity and prolonged stay
Mohn et al[18]Prospective ERAS group matched with historical data9440 (43)66ERAS29 (31%)1 (1%)14 (15%)ERAS ↓ hospital stay
15368 (44.40)71 (15-90)Conventional11 (5-108)27 (18%)1 (1%)-
Nygren et al[22]Prospective ERAS group matched with historical data99--ERAS-18%1-15%1ERAS ↓ time to resumption of oral diet, mobilization and passage of stool, improved lung function, ↓ morbidity and hospital stay but ↑ readmissions
692765 ± 2Conventional8.6 ± 0.6/7 for colonic resection17 (37%) for colonic02 (4%) for colonic
12.7 ± 1.2/11 for rectal resection12 (52%) for rectal resection1 (4%) for rectal
Ahmed et al[24]Retrospective case series231101 (44)68 (56-76)Elective open bowel resectionERAS6 (5-9)--Lower ASA grade, use of epidurals and avoidance of regular oral opiates are associated with an earlier discharge
Kahokehr[9]Prospective case series100-68 (31-92)ERAS4 (3-46)---Lower ASA score, transverse incision laparotomy and laparoscopy associated with earlier discharge
Teeuwen et al[17]Prospective ERAS group matched with historical data6122 (36.1)57 ± 17.6elective open colonic or rectal resectionERAS6 (3- 50)9 (14.8%)0%2 (3.3%)ERAS ↓ morbidity and hospital stay
122--Conventional9 (3-138)33.60%1.60%1.60%
Bryans et al[34]Retrospective case series20--Colorectal surgery with stoma (excluding abdominoperineal resection)ERASmean = 7---ERAS ↓ hospital stay and ability to manage stoma
20Conventionalmean = 20
Kahokehr et al[8]Prospective case series74--Open right hemicolectomyERASMedian (43-28)---No difference in morbidity or surgical recovery
39Laparoscopic right hemicolectomyConventional5 (2-18)

Significant predictors for longer discharges using ERAS protocols are the patient’s fitness for surgery [American society of anesthesiologists (ASA) score greater than 1][9,20,23,24], higher physiological and operative severity score for the enumeration of mortality and morbidity scores[20], the use of oral opiates in the post-operative period[24], age[20,23,24], rectal surgery[23], complex resections[20], the development of major complications[20] and the inability to discharge patients when they had reached functional recovery[20]. In fact, the increase in LOS with age might be attributed to delayed discharge related to difficulties in arranging social care (see below). Contrasting results were reported for the postoperative duration of epidurals [24,29] and the use of a transverse vs midline incision[9,24], sex[9,23].

The readmission rate after ERAS is 3%-15% and is similar to CC[14,17,23,24]. Only Nygren showed a significant higher readmission rates after ERAS (4% vs 15 %)[22].

Mortality and morbidity

Most studies found no significant differences in mortality rates between ERAS and CC which ranged between 1.6% and 2% [17,18,22,23,27]. The overall morbidity rate after ERAS is 18%-28% (anastomotic leak 2%-5%, reoperation rate 7.4%)[23,24] (Table 2). Morbidity rates were lower than those published for the same units before the introduction of an ERAS protocol (35%)[27]. However, contrasting results were reported by other articles. Some studies showed similar overall complication rates[14,17,22] for both colonic and rectal resections[22], others claimed lower morbidity rates after ERAS (14.8% vs 33.6%)[17], others higher rates with ERAS but only for minor complications (nausea, wound infection)[18]. Morbidity was predicted by ASA grade III–IV, male sex and rectal surgery[30], while low BMI or advanced age were not associated with it[23].

FUTURE CHALLENGES
Laparoscopic vs open resection on ERAS

Randomized trials involving the application of ERAS protocols to laparoscopic surgery showed conflicting results[12,31] (Table 3). A recent review of the published literature suggests that little additional benefit is added by laparoscopy to an already well-established ERAS program[32] especially in terms of postoperative quality of life[13], but a large multicentre study is still ongoing[33]. Patients who underwent laparoscopic surgery had a shorter LOS than those having open surgery (4-6 d for the laparoscopic group vs 6-10 d for the open group) for both colonic and rectal surgery[12,16]. Readmission rates also were lower after laparoscopic surgery (5.8% vs 22.0%)[16]. No significant differences were found in the overall morbidity (52% after laparoscopic vs 42% after open surgery) and major morbidity (15% after laparoscopic vs 26% after open surgery)[8,12,16] while contrasting results were reported for mortality rates: one study showed no significant differences[12] while another claimed higher mortality after open surgery[16]. Differently, Basse et al[31] did not reveal significant differences in LOS or morbidity between groups, but these authors excluded patients with rectal anastomoses (requiring a stoma) and those not living independently at home that required social setting for discharge. In fact, the social discharge is a problem that was also faced by Kahokehr and colleagues in their study (see below)[8].

Table 3 Other colorectal studies involving enhanced recovery after surgery patients.
Ref.Type of studyPatients (n)ApproachComments
Soop et al[26]RCT9 vs 9Complete or hypocaloric postoperative enteral nutrition on ERASComplete enteral nutritions was associated with minimal postop insulin resistance, hyperglycemia and nitrogen losses
King et al[12]RCT43 vs 19Lap vs open resections on ERAS patientsReduced hospital stay and with laparoscopic resections
King et al[13]RCT41 vs 19Lap vs open resections on ERAS patientsLaparoscopic surgery achieves quicker return to daily activities
Kirdak et al[19]RCT14 vs 13Preop. dexamethasone vs placebo on ERAS patientsPreoperative dexamethasone has no significant effects on the inflammatory response or outcomes
Turunen et al[10]RCT29 vs 29Epidural anesthesia vs control for laparoscopic resection on ERASThe epidural G. needed less oxycodone than the control G. Until 12 h postop. Epidural alleviated pain, reduced opioids requirements
Raymond et al[28]Retrospective case series179 vs 144Lap vs open resections on ERAS patientsLaparoscopic surgery achieves quicker return to daily activities
Blazeby et al[15]Prospective20Laparoscopic assisted and openQOL evaluation. Patients liked quicker discharges, few were dissatisfied due to complications requiring readmissions
Senagore et al[35]RCT22 vs 21 vs 21Standard vs lactated Ringer’s vs hetastarch-lactated Ringer’s periop fluidIndividualized intraoperative fluid management with crystalloid reduced overall fluid administration compared to colloid
Faiz et al[16]Prospective non-randomized191 vs 50Lap vs open resections on ERAS patientsLaparoscopic has advantages over open approach also in ERAS patients
Wennstrom et al[11]Prospective32ERASPostoperative survey on QOL following discharge: fatigue, nausea and bowel disturbances
Ahmed et al[25]Case series100 vs 95ERAS audit protocols application vs ERAS clinical practiceObservance to ERAS protocol was lower outside clinical trials
Functional recovery and delay in discharge

In the pre-ERAS era 90% of patients were not discharged on the day that criteria were fulfilled. Wound care and symptoms pointing towards an anastomotic leakage were the most important reasons for a medical appropriate delay of discharge[21]. With regards for the stoma independence, 60% of patients audited in the pre-ERAS era were taking more than 8 d to be deemed stoma-independent and only 15% were able in less than 5 d. Following the introduction of ERAS protocols the percentage of patients not discharged on the day that criteria were fulfilled decreased to 34%-87%[20,21], 75% of patients achieved stoma independence in 5 d or less and only 5% took 8 or more days - the figures completely reversed compared to the pre-ERAS era[34]. Results achieved represent a huge step forward especially considering that they simply reflect an optimization of the patients’ management and of the impact of surgery without the necessity to introduce any additional procedures into clinical practice. At the same time they also show us that 13%-66% of patients are still not discharged when deemed medically fit by one or two days[24]. Various authors feel that ERAS protocols ultimately optimized the patient’s medical fitness for discharge and that nowadays a further reduction of the LOS must relate to changes in the organization of care and not to shorter recovery periods. This could be obtained in example by evidencing those social factors that can delay the discharge and therefore organizing the available resources outside the hospitals well in advance the operation. In example, older patients leaving alone and likely requiring specialist assistance or short admissions to nursing homes or rehabilitative structures can be individuated during the preoperative counseling and necessary arrangements well planned before surgery.

When asked about their experience with the ERAS programs, most patients appreciated a planned short hospital stay because it was perceived that better recovery could be achieved in the home environment[15] (Table 3). However, some of them reported feeling vulnerable at home so shortly after major surgery and those who experienced complications were less satisfied with the process[15]. The first period at home is the most troublesome and the main problems perceived are fatigue, nausea and bowel disturbances (not pain)[11] (Table 3). In this view, it is necessary that ERAS programs are paralleled by the development of services aimed to provide direct contacts and accesses to healthcare resources that could reassure patients about their recovery when normal or quickly individuate suspicious symptoms that require readmissions[8,15]. A direct telephone contact is a simple measure that might alleviate the patient anxiety and maintain the continuity of care from health professionals[11].

Footnotes

Peer reviewer: Dr. Imtiaz Wani, Department of Surgery, SMHS Hospital, Srinagar, Kashmir 190009, India

S- Editor Song XX L- Editor A E- Editor Xiong L

References
1.  Fearon KC, Ljungqvist O, Von Meyenfeldt M, Revhaug A, Dejong CH, Lassen K, Nygren J, Hausel J, Soop M, Andersen J. Enhanced recovery after surgery: a consensus review of clinical care for patients undergoing colonic resection. Clin Nutr. 2005;24:466-477.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1001]  [Cited by in F6Publishing: 924]  [Article Influence: 48.6]  [Reference Citation Analysis (0)]
2.  Varadhan KK, Lobo DN, Ljungqvist O. Enhanced recovery after surgery: the future of improving surgical care. Crit Care Clin. 2010;26:527-47, x.  [PubMed]  [DOI]  [Cited in This Article: ]
3.  Lassen K, Soop M, Nygren J, Cox PB, Hendry PO, Spies C, von Meyenfeldt MF, Fearon KC, Revhaug A, Norderval S. Consensus review of optimal perioperative care in colorectal surgery: Enhanced Recovery After Surgery (ERAS) Group recommendations. Arch Surg. 2009;144:961-969.  [PubMed]  [DOI]  [Cited in This Article: ]
4.  Burch J, Wright S, Kennedy R. Enhanced recovery pathway in colorectal surgery. 1: Background and principles. Nurs Times. 2009;105:23-25.  [PubMed]  [DOI]  [Cited in This Article: ]
5.  Fearon KC, Luff R. The nutritional management of surgical patients: enhanced recovery after surgery. Proc Nutr Soc. 2003;62:807-811.  [PubMed]  [DOI]  [Cited in This Article: ]
6.  Soop M, Nygren J, Ljungqvist O. Optimizing perioperative management of patients undergoing colorectal surgery: what is new? Curr Opin Crit Care. 2006;12:166-170.  [PubMed]  [DOI]  [Cited in This Article: ]
7.  Jottard KJ, van Berlo C, Jeuken L, Dejong C. Changes in outcome during implementation of a fast-track colonic surgery project in a university-affiliated general teaching hospital: advantages reached with ERAS (Enhanced Recovery After Surgery project) over a 1-year period. Dig Surg. 2008;25:335-338.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 23]  [Cited by in F6Publishing: 25]  [Article Influence: 1.6]  [Reference Citation Analysis (0)]
8.  Kahokehr A, Sammour T, Zargar-Shoshtari K, Srinivasa S, Hill AG. Recovery after open and laparoscopic right hemicolectomy: a comparison. J Surg Res. 2010;162:11-16.  [PubMed]  [DOI]  [Cited in This Article: ]
9.  Kahokehr AA, Sammour T, Sahakian V, Zargar-Shoshtari K, Hill AG. Influences on length of stay in an enhanced recovery programme after colonic surgery. Colorectal Dis. 2011;13:594-599.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 26]  [Cited by in F6Publishing: 29]  [Article Influence: 2.2]  [Reference Citation Analysis (0)]
10.  Turunen P, Carpelan-Holmström M, Kairaluoma P, Wikström H, Kruuna O, Pere P, Bachmann M, Sarna S, Scheinin T. Epidural analgesia diminished pain but did not otherwise improve enhanced recovery after laparoscopic sigmoidectomy: a prospective randomized study. Surg Endosc. 2009;23:31-37.  [PubMed]  [DOI]  [Cited in This Article: ]
11.  Wennström B, Stomberg MW, Modin M, Skullman S. Patient symptoms after colonic surgery in the era of enhanced recovery--a long-term follow-up. J Clin Nurs. 2010;19:666-672.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 32]  [Cited by in F6Publishing: 29]  [Article Influence: 2.1]  [Reference Citation Analysis (0)]
12.  King PM, Blazeby JM, Ewings P, Franks PJ, Longman RJ, Kendrick AH, Kipling RM, Kennedy RH. Randomized clinical trial comparing laparoscopic and open surgery for colorectal cancer within an enhanced recovery programme. Br J Surg. 2006;93:300-308.  [PubMed]  [DOI]  [Cited in This Article: ]
13.  King PM, Blazeby JM, Ewings P, Kennedy RH. Detailed evaluation of functional recovery following laparoscopic or open surgery for colorectal cancer within an enhanced recovery programme. Int J Colorectal Dis. 2008;23:795-800.  [PubMed]  [DOI]  [Cited in This Article: ]
14.  King PM, Blazeby JM, Ewings P, Longman RJ, Kipling RM, Franks PJ, Sheffield JP, Evans LB, Soulsby M, Bulley SH. The influence of an enhanced recovery programme on clinical outcomes, costs and quality of life after surgery for colorectal cancer. Colorectal Dis. 2006;8:506-513.  [PubMed]  [DOI]  [Cited in This Article: ]
15.  Blazeby JM, Soulsby M, Winstone K, King PM, Bulley S, Kennedy RH. A qualitative evaluation of patients' experiences of an enhanced recovery programme for colorectal cancer. Colorectal Dis. 2010;12:e236-e242.  [PubMed]  [DOI]  [Cited in This Article: ]
16.  Faiz O, Brown T, Colucci G, Kennedy RH. A cohort study of results following elective colonic and rectal resection within an enhanced recovery programme. Colorectal Dis. 2009;11:366-372.  [PubMed]  [DOI]  [Cited in This Article: ]
17.  Teeuwen PH, Bleichrodt RP, Strik C, Groenewoud JJ, Brinkert W, van Laarhoven CJ, van Goor H, Bremers AJ. Enhanced recovery after surgery (ERAS) versus conventional postoperative care in colorectal surgery. J Gastrointest Surg. 2010;14:88-95.  [PubMed]  [DOI]  [Cited in This Article: ]
18.  Mohn AC, Bernardshaw SV, Ristesund SM, Hovde Hansen PE, Røkke O. Enhanced recovery after colorectal surgery. Results from a prospective observational two-centre study. Scand J Surg. 2009;98:155-159.  [PubMed]  [DOI]  [Cited in This Article: ]
19.  Kirdak T, Yilmazlar A, Cavun S, Ercan I, Yilmazlar T. Does single, low-dose preoperative dexamethasone improve outcomes after colorectal surgery based on an enhanced recovery protocol? Double-blind, randomized clinical trial. Am Surg. 2008;74:160-167.  [PubMed]  [DOI]  [Cited in This Article: ]
20.  Maessen J, Dejong CH, Hausel J, Nygren J, Lassen K, Andersen J, Kessels AG, Revhaug A, Kehlet H, Ljungqvist O. A protocol is not enough to implement an enhanced recovery programme for colorectal resection. Br J Surg. 2007;94:224-231.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 382]  [Cited by in F6Publishing: 354]  [Article Influence: 20.8]  [Reference Citation Analysis (0)]
21.  Maessen JM, Dejong CH, Kessels AG, von Meyenfeldt MF. Length of stay: an inappropriate readout of the success of enhanced recovery programs. World J Surg. 2008;32:971-975.  [PubMed]  [DOI]  [Cited in This Article: ]
22.  Nygren J, Soop M, Thorell A, Hausel J, Ljungqvist O. An enhanced-recovery protocol improves outcome after colorectal resection already during the first year: a single-center experience in 168 consecutive patients. Dis Colon Rectum. 2009;52:978-985.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 77]  [Cited by in F6Publishing: 79]  [Article Influence: 5.3]  [Reference Citation Analysis (0)]
23.  Hendry PO, Hausel J, Nygren J, Lassen K, Dejong CH, Ljungqvist O, Fearon KC. Determinants of outcome after colorectal resection within an enhanced recovery programme. Br J Surg. 2009;96:197-205.  [PubMed]  [DOI]  [Cited in This Article: ]
24.  Ahmed J, Lim M, Khan S, McNaught C, Macfie J. Predictors of length of stay in patients having elective colorectal surgery within an enhanced recovery protocol. Int J Surg. 2010;8:628-632.  [PubMed]  [DOI]  [Cited in This Article: ]
25.  Ahmed J, Khan S, Gatt M, Kallam R, MacFie J. Compliance with enhanced recovery programmes in elective colorectal surgery. Br J Surg. 2010;97:754-758.  [PubMed]  [DOI]  [Cited in This Article: ]
26.  Soop M, Carlson GL, Hopkinson J, Clarke S, Thorell A, Nygren J, Ljungqvist O. Randomized clinical trial of the effects of immediate enteral nutrition on metabolic responses to major colorectal surgery in an enhanced recovery protocol. Br J Surg. 2004;91:1138-1145.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 113]  [Cited by in F6Publishing: 124]  [Article Influence: 6.2]  [Reference Citation Analysis (0)]
27.  Nygren J, Hausel J, Kehlet H, Revhaug A, Lassen K, Dejong C, Andersen J, von Meyenfeldt M, Ljungqvist O, Fearon KC. A comparison in five European Centres of case mix, clinical management and outcomes following either conventional or fast-track perioperative care in colorectal surgery. Clin Nutr. 2005;24:455-461.  [PubMed]  [DOI]  [Cited in This Article: ]
28.  Raymond TM, Kumar S, Dastur JK, Adamek JP, Khot UP, Stewart MS, Parker MC. Case controlled study of the hospital stay and return to full activity following laparoscopic and open colorectal surgery before and after the introduction of an enhanced recovery programme. Colorectal Dis. 2010;12:1001-1006.  [PubMed]  [DOI]  [Cited in This Article: ]
29.  Marret E, Remy C, Bonnet F. Meta-analysis of epidural analgesia versus parenteral opioid analgesia after colorectal surgery. Br J Surg. 2007;94:665-673.  [PubMed]  [DOI]  [Cited in This Article: ]
30.  Hendry PO, van Dam RM, Bukkems SF, McKeown DW, Parks RW, Preston T, Dejong CH, Garden OJ, Fearon KC. Randomized clinical trial of laxatives and oral nutritional supplements within an enhanced recovery after surgery protocol following liver resection. Br J Surg. 2010;97:1198-1206.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 84]  [Cited by in F6Publishing: 91]  [Article Influence: 6.5]  [Reference Citation Analysis (0)]
31.  Basse L, Jakobsen DH, Bardram L, Billesbølle P, Lund C, Mogensen T, Rosenberg J, Kehlet H. Functional recovery after open versus laparoscopic colonic resection: a randomized, blinded study. Ann Surg. 2005;241:416-423.  [PubMed]  [DOI]  [Cited in This Article: ]
32.  Khan S, Gatt M, MacFie J. Enhanced recovery programmes and colorectal surgery: does the laparoscope confer additional advantages? Colorectal Dis. 2009;11:902-908.  [PubMed]  [DOI]  [Cited in This Article: ]
33.  Wind J, Hofland J, Preckel B, Hollmann MW, Bossuyt PM, Gouma DJ, van Berge Henegouwen MI, Fuhring JW, Dejong CH, van Dam RM. Perioperative strategy in colonic surgery; LAparoscopy and/or FAst track multimodal management versus standard care (LAFA trial). BMC Surg. 2006;6:16.  [PubMed]  [DOI]  [Cited in This Article: ]
34.  Bryan S, Dukes S. The Enhanced Recovery Programme for stoma patients: an audit. Br J Nurs. 2010;19:831-834.  [PubMed]  [DOI]  [Cited in This Article: ]
35.  Senagore AJ, Emery T, Luchtefeld M, Kim D, Dujovny N, Hoedema R. Fluid management for laparoscopic colectomy: a prospective, randomized assessment of goal-directed administration of balanced salt solution or hetastarch coupled with an enhanced recovery program. Dis Colon Rectum. 2009;52:1935-1940.  [PubMed]  [DOI]  [Cited in This Article: ]