Unplanned intubation: When and why does this deadly complication occur?

Unplanned intubation: When and why does this deadly complication occur? Daniel P. Milgrom, BS,a Victor C. Njoku, MD,a Alison M. Fecher, MD,a E. Molly Kilbane, RN,a and Henry A. Pitt, MD,b Indianapolis, IN, and Philadelphia, PA

Background. Risk factors for unplanned intubation have been delineated, but details regarding when and why reintubations occur as well as strategies for prevention have not been defined. Methods. Over a 2-year period, 104 of 3,141 patients (3.3%) monitored via the American College of Surgeons-National Surgical Quality Improvement Program required unplanned intubation. These patients were compared to those who remained extubated and were characterized by (1) the operation performed; (2) the postoperative day when reintubation occurred; and (3) the underlying causes. Results. Patients who required reintubation were significantly older (65.8 years) and were more likely to be male (55%) and to have several comorbidities, weight loss (16%), dependency (14%), or sepsis (9%). The operations complicated most commonly by unplanned intubation were gastrectomy (13%), nephrectomy (10%), colectomy (9%), pancreatectomy (8%), hepatectomy (7%), and enterectomy (6%). The most common causes and median postoperative days were sepsis (33%, day 8) and aspiration/pneumonia (31%, day 4). Sepsis was due most commonly to an abdominal or pelvic abscess (74%), which was frequently not recognized despite an inflammatory response. Aspiration occurred most commonly after upper abdominal operations (78%) despite signs of diminished bowel function. Conclusion. Postoperative sepsis and aspiration/pneumonia account for two thirds of unplanned intubations. Opportunities for management of patients exist for the prevention of this deadly complication. (Surgery 2013;154:376-83.) From the Department of Surgery,a Indiana University, Indianapolis, IN; and Temple University Health System,b Philadelphia, PA

UNPLANNED INTUBATION is an uncommon but potentially deadly postoperative complication.1-5 Adverse pulmonary outcomes may be subdivided into 3 categories: unplanned intubation, prolonged ventilation, and pneumonia. Together, these pulmonary problems have been termed postoperative respiratory failure. Subtle but real differences exist among these 3 adverse pulmonary outcomes. At the same time, considerable overlap occurs with these pulmonary complications. For example, approximately one half of reintubated patients also have prolonged intubation (longer than 48 h), and nearly one third also develop pneumonia. Thus, by focusing on patients who experience unplanned intubation, the potential of improving patient outcomes may be leveraged. Presented at the Academic Surgical Congress New Orleans, LA, February 5–7, 2013. Accepted for publication May 10, 2013. Reprint requests: Henry A. Pitt, MD, Temple University Health System, 3509 N. Broad St., Boyer Pavilion E938, Philadelphia, PA 19140. E-mail: [email protected]. 0039-6060/$ - see front matter Ó 2013 Mosby, Inc. All rights reserved. http://dx.doi.org/10.1016/j.surg.2013.05.006

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Risk factors for postoperative respiratory failure and unplanned intubation have been reported.1-5 Potential causes, including anesthesia mismanagement, narcotic overdose, fluid overload, excess secretions, cardiopulmonary complications, aspiration/pneumonia, and severe sepsis, have been described. In addition, strategies for prevention of these pulmonary complications have been published.6-7 A detailed analysis of a number of patients experiencing unplanned intubation to determine the causes, the timing, and the details of patient management has not been performed. Thus, the aims of this study were to determine when and why unplanned intubation occurs as well as whether and how this pulmonary complication can be prevented. METHODS ACS-NSQIP at Indiana University Hospital. The American College of Surgeons-National Surgical Quality Improvement Program (ACS-NSQIP) is a prospective, multicenter clinical registry created to provide feedback on risk-adjusted outcomes for quality-improvement purposes. The sampling strategy, data abstraction procedures, variables collected, and structure have been published.8-10 During the first 12 months of the study period

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(calendar year 2010) at Indiana University Hospital, a systematic, random sampling process that employed an 8-day cycle, whereby the first 40 general surgery cases that fulfilled the inclusion and exclusion criteria was employed. During the second 12 months of the study period (calendar year 2011) at Indiana University Hospital, the ACS-NSQIP Procedure Targeted sampling methodology was utilized. Four services were sampled: general surgery, gynecology, plastic surgery, and urology. Ten procedures were targeted: colectomy, hepatectomy, pancreatectomy, proctectomy, ventral hernia, hysterectomy, breast reconstruction, breast reduction, cystectomy, and nephrectomy. These services and procedures were targeted at Indiana University Hospital because general surgery, orthopedic surgery, neurosurgery, and vascular surgery were being monitored via the ACS-NSQIP Procedure Targeted program during 2011 at the Methodist Hospital, a sister academic medical center within Indiana University Health. Unplanned intubation. Over a 24-month period, 104 (3.3%) of the 3,141 patients undergoing operations and monitored by the ACS-NSQIP underwent unplanned intubation at Indiana University Hospital. The ACS-NSQIP definition of unplanned intubation was employed. The patients undergoing unplanned intubation were compared to the patients who remained extubated during the study’s time period. The patients undergoing unplanned intubation were characterized by demographics, the operation performed, the underlying risk factors, and the postoperative day (POD) when reintubation occurred. The majority of the unplanned intubation events were secondary to sepsis or aspiration/pneumonia. These patients were analyzed further to determine the underlying cause as well as whether patient management could have been altered. Therefore, this study is a retrospective analysis of prospectively collected data. Sepsis and aspiration/pneumonia. Patients who underwent unplanned intubation secondary to sepsis or aspiration/pneumonia were then further characterized. General data included diagnosis, reason for reintubation, age, and sex. Preoperative variables included diagnosis of obstructive sleep apnea, gastroparesis, gastroesophageal reflux disease, duodenal obstruction, bowel obstruction, cholangitis, diabetes mellitus, obesity (defined as body mass index >30), cancer, inflammatory bowel disease, chronic immunosuppressive therapy, preoperative hypoalbuminemia (<3.5 g/dL), as well as use of a gastric acid secretion inhibitor and tobacco use. Postoperative variables included

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systemic inflammatory response syndrome (SIRS) 72, 48, or 24 h prior to unplanned intubation; presence of a positive blood culture before unplanned intubation; use of antibiotics within the 24-h period prior to reintubation; and implementation of the Surviving Sepsis Campaign11 within the 72 h prior to unplanned intubation. Postoperative variables also included level of care; presence of nasogastric tube, gastric tube, or jejunal-tube; diet; use of narcotics, antiemetics, or naloxone prior to reintubation; bowel anastomotic leak, pancreatic fistula, biliary leak, fluid collection, location and drainage of fluid collection, or line infection; and reoperation. To gather this information, the medical records, pathology reports, and discharge summaries were reviewed. Permission to conduct this study was obtained from the Institutional Review Board at the Indiana University School of Medicine. Statistical analysis. Data including mean, median, range, percentages, and standard deviation were analyzed in Excel 2012 (Microsoft, Redmond, WA) and by SPSS (Armonk, NY). The v2, Student t test, and multivariable analysis were employed as appropriate. A P value of less than .05 was accepted as statistically significant. RESULTS Patient demographics. The demographics of the 104 patients who experienced unplanned intubation and the 3,041 who were not reintubated are presented in Table I. The patients undergoing unplanned intubation were significantly older and more likely to be male, to have been transferred from an acute-care hospital, and to be American Society of Anesthesiologists class 4 or 5. In addition, they were more likely to have multiple comorbidities, to be partially or totally dependent, to have lost weight, to have an open wound, to be on steroids, and to have sepsis or septic shock. Operations. During the 24-month period, the operations captured most frequently with ACS-NSQIP at Indiana University Hospital, in order of frequency, were: (1) pancreatectomy, (2) ventral herniorrhaphy, (3) colectomy, (4) hepatectomy, (5) biliary operations, (6) enterectomy or enterolysis, (7) thyroidectomy, (8) pancreatic debridement, (9) nephrectomy, (10) cystectomy, (11) exploratory laparotomy, and (12) gastrectomy. The incidence of unplanned intubation by procedure is presented in Fig 1. The reintubation rates did not differ between open (8.5%) and laparoscopic (10.3%) colectomies; however, unplanned intubation occurred much more commonly after proximal (12.6%) than

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Table I. Demographics of patients with and without unplanned intubation

Number Age (mean y) Male (%) Race (%) White African American Hispanic Other Transferred* (%) ASA class > 3(%) Body mass index Diabetesy (%) Hypertension (%) Smoking Dyspneaz (%) COPD (%) Cardiac procedure (%)x Dependent (%)k Weight loss (%){ Open wound (%) Steroid use (%) Sepsis/shock (%)

Unplanned intubation

No reintubation

104 65.8 ± 12.3 54.8

3,041 55.7 ± 15.0 41.1

P value <.01 <.01 <.01

92.3 4.8 1.0 1.9 17.3 23.1 28.9 29.8 62.5 28.8 12.5 17.3 17.4

88.4 8.4 0.6 2.6 8.7 6.2 29.4 17.3 44.2 22.7 7.5 4.8 4.5

<.01 <.001 NS <.001 <.001 NS NS <.001 <.001

14.4 16.3 8.7 8.7 8.6

4.0 6.0 3.9 4.9 3.3

<.001 <.001 <.02 NS <.01

*From an acute care hospital. yNon-insulin dependent and insulin dependent. zWith moderate exertion and at rest. xAngioplasty and surgical. kPartially and totally. {10% or more in 6 months prior to surgery. ASA, American Society of Anesthesiologists; COPD, chronic obstructive pulmonary disease.

Fig 1. Incidence of unplanned intubation by procedure.

distal (2.4%) pancreatectomy. Of note, reintubation occurred in only 3% of patients undergoing pancreatic debridement, most likely because extubation was delayed in many of these patients.

Fig 2. (A) Causes of unplanned intubation. (B) Median postoperative day (POD) for reintubation.

Thyroidectomy was the least likely (1.4%) to be complicated by unplanned intubation. Causes and timing of unplanned intubation. The most common underlying causes of unplanned intubation are presented in Fig 2, A. Sepsis was the most common cause (33%), followed by aspiration/pneumonia (31%). Excess secretions (8%) and fluid overload (5%) were much less common. Other potential causes, such as anesthesia mismanagement, narcotic overdose, and cardiac complications, were uncommon. The median POD for reintubation by cause is presented in Fig 2, B. The median POD for sepsis was day 8 (range, 2 to 28 days). For aspiration/pneumonia, the median POD was day 4 (range, 2 to 27 days). The median POD for excess secretions also was day 4, with a smaller range of 3 to 11 days. For fluid overload, the median POD was day 3 (range, 2 to 27 days). The demographics of patients with sepsis and aspiration/pneumonia as the underlying cause for unplanned intubation are presented in Table II. Compared to all 104 reintubated patients (Table I),

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Table II. Demographics of patients with sepsis and aspiration/pneumonia

Table III. Outcomes of patients with and without unplanned intubation

Sepsis Aspiration/pneumonia Number Age (mean y) Male (%) Obesity (%)* Diabetes (%)y Smoking (%) OSA (%) GERD (%) Acid inhibitor (%)z Gastroparesis (%) Duodenal obstruction (%) Bowel obstruction (%) IBD (%) Cancer (%) Immunosuppression (%)x Hypoalbuminemia (%)k

34 64.3 52.9 41.2 44.1 44.1 8.8 17.7 55.9 2.9 5.9 23.5 2.9 61.8 17.7 76.5

32 65.1 68.8 31.3 31.3 53.1 3.1 21.9 37.5 6.3 6.5 3.1 9.4 53.1 18.8 56.3

*BMI > 30. yNon-insulin and insulin dependent. zAny medication that suppresses gastric acid. xSteroids and other immunosuppressive medications. kLess than 3.5 mg/dL. IBD, Inflammatory bowel disease; GERD, gastroesophageal reflux disease; OSA, obstructive sleep apnea.

the 34 patients with sepsis as the cause were more likely to be obese (44%), to have diabetes (44%), and to be smokers (44%). Gastroparesis (3%) and duodenal obstruction (6%) were uncommon, but 8 of these 34 patients (24%) presented with bowel obstruction. In addition, the majority had an underlying cancer (62%) and hypoalbuminemia (77%). In these patients, the most common operations were pancreatectomy (32%), colectomy (24%), and hepatectomy (15%); 88% were open, and 6% were converted to open. The 32 patients with aspiration/pneumonia as the cause for unplanned intubation were more likely to be male (69%) and to be smokers (53%). In addition, 9% had inflammatory bowel disease, 53% had cancer, and 56% had low preoperative serum albumin levels. Of note, 25 of these aspiration/pneumonia patients (78%) underwent an upper abdominal operation (stomach, pancreas, liver, or small bowel). Pancreatectomy was the most common (38%), followed by colectomy (16%) and enterectomy (13%); 78% were open, 3% were converted to open, 13% were laparoscopic, and 6% were robotic. Outcomes. The outcomes of the 104 patients who experienced unplanned intubation and the 3,041 who were not reintubated are presented in Table III. Mortality after 30 days was markedly greater in the patients who underwent unplanned

Unplanned No intubation reintubation Number Mortality (%)* Superficial/deep SSI (%) Organ/space SSI (%) Wound disruption (%) Pneumonia (%) Ventilator > 48 h (%) Renal insufficiency (%) Acute renal failure (%) Urinary tract infection (%) CVA (%) Cardiac arrest (%) Myocardial infarction (%) Transfusion (%)y Venous thrombosis (%)z Sepsis (%) Septic shock (%) Return to OR (%)x LOS (days [IQR]) Readmission (%)k

P value

104 26.9 10.6

3,041 1.1 6.1

— <.001 NS

26.9 5.8 44.2 71.2 8.7 12.5 12.5

3.3 1.0 1.0 2.1 0.7 0.5 2.3

<.001 <.001 <.001 <.001 <.001 <.001 <.001

2.9 16.3 6.7

0.1 0.2 0.5

<.001 <.001 <.001

40.4 7.7

13.6 1.4

<.001 <.001

5.1 1.4 4.3 5 (7) 8.4

<.01 <.001 <.001 <.05 <.02

11.5 57.7 27.9 19 (19) 15.4

*At 30 days postoperatively. yIntra- or postoperatively within 72 h. zRequiring therapy. xUnplanned for a surgical procedure. kAll cause within 30 days. CVA, Cerebrovascular accident; LOS, length of stay, median after operation; OR, operating room; SSI, surgical site infection.

intubation (27%) compared to the patients who were not reintubated (1.1%). All other adverse outcomes presented in Table III also were significantly more common in the patients after unplanned intubation. Other pulmonary and septic complications were very common. In a multivariable analysis of the 15 outcomes, which were significantly different, the 8 variables predictive for unplanned intubation in this model were return to the OR (P < .001), septic shock (P < .001), cardiac arrest (P < .001), acute renal failure (P < .01), transfusion (P < .05), myocardial infarction (P < .05), urinary tract infection (P < .05), and renal insufficiency (P < .05). Outcomes for the 34 patients with sepsis and the 32 patients with aspiration/pneumonia are presented in Table IV. Two thirds of the patients with sepsis as the underlying cause had an organ/space infection and nearly one third had a gastrointestinal (GI) anastomotic leak. One third required percutaneous drainage, and 17 of these

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Table IV. Outcomes of patients with sepsis and aspiration/pneumonia Sepsis Aspiration/pneumonia Number Mortality (%)* Superficial/deep SSI (%) Organ/space SSI (%) Pneumonia (%) Ventilator > 48 h (%) Line infection (%) Urinary tract infection (%) GI leak (%) Pancreatic fistula (%) Bile leak (%) Percutaneous drainage (%) Return to OR (%)y

34 32.4 5.9 67.7 26.5 23.5 8.8 32.4 32.4 11.8 23.5 32.4 50.0

32 50.0 34.4 6.3 62.5 12.5 3.2 9.4 6.3 0.0 6.5 9.4 3.2

Fig 3. Percentage of sepsis patients meeting SIRS criteria by hours prior to reintubation.

*At 30 days postoperatively. yUnplanned for a surgical procedure. GI, Gastrointestinal; OR, operating room; SSI, surgical site infection.

patients (50%) underwent a second operation. Of the 32 patients with aspiration/pneumonia, 16 (50%) died within 30 days of their index operations. Aspiration was documented in 18 of these patients (56%) on a median POD of 6. Delays in diagnosis or treatment. In the 34 patients with sepsis as the underlying cause, the percentage of patients meeting the criteria of SIRS is presented in Fig 3. At 72 h and 48 h prior to reintubation, 50% and 47% of patients, respectively, met SIRS criteria. Prior to reintubation, 13 of the 34 patients (38%) had positive blood cultures, and 16 (47%) were on systemic antibiotics. The complete Surviving Sepsis Campaign bundle was employed in only 1 patient (3%). At the time of reintubation, 11 of these patients with sepsis (32%) were in intensive care units, whereas 8 (24%) were in progressive care units. For the 32 patients with aspiration/pneumonia as the underlying cause, the percentage of patients with GI problems or receiving medications to influence GI function is presented in Fig 4. The median day of removal of the nasogastric tube was POD 2 in 17 of the 22 patients who had nasogastric tubes; 9 patients had a gastrostomy or jejunostomy tube. Of the patients who aspirated (28%), 9 were on a liquid diet, and an additional 6 patients (19%) were receiving solid diets. At the time of reintubation, 6 of these patients with aspiration/ pneumonia (19%) were in intensive care units, and 9 (28%) were in progressive care units. DISCUSSION Unplanned intubation is a serious postoperative complication that is associated with a high

Fig 4. Percentage of aspiration/pneumonia patients with GI problems or medications prior to reintubation. GI, Gastrointestinal.

incidence of pneumonia, prolonged ventilation, and mortality.1-6 This detailed analysis of 104 patients experiencing reintubation confirmed these prior observations as well as previous reports detailing risk factors, including advanced age, male sex, multiple comorbidities, and frailty.1-6,12,13 Sepsis due to abdominal and pelvic abscesses and aspiration/pneumonia accounted for two thirds of the reintubations. The median timing for sepsis was 8 days, whereas aspiration/pneumonia presented at a median of 4 days, although the range was wide for both complications. Delays in the diagnosis and treatment of these underlying causes contributed to the need for reintubation and, in some cases, may have been preventable. The 30-day mortality of 27% experienced by the patients requiring unplanned intubation in this study is similar to that reported by others.1-6 With

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nearly 60% experiencing septic shock, 44% having pneumonia, 21% developing renal insufficiency or failure, and 16% experiencing cardiac arrest, the fact that nearly three quarters of these patients were alive at 30 days is a testament to the ability of their physicians to manage these remarkable ill patients. The incidence of pneumonia (44%) and prolonged ventilation (71%) in this series is greater than in some reports.1,2,5,6 The high rate of pneumonia may be due to a low threshold for performing a bronchoaveolar lavage by our intensivists. In addition, the relatively high percentage of patients requiring prolonged intubation also may be a reflection of the patient population, which required a high rate of percutaneous and operative drainage. In this analysis, the operations that were complicated most commonly by unplanned intubation were gastrectomy, pancreatoduodenectomy, and nephrectomy. Most patients undergoing gastrectomy and pancreatoduodenectomy have cancer, weight loss, and hypoalbuminemia; undergo open operations; and are prone to delayed gastric emptying and/or infected intra-abdominal fluid collections. Much of the literature concerning postoperative complications in these patients has focused on organ/space infections, prolonged durations of stay, and increased costs.14,15 The current analysis, however, documents that unplanned intubation is also a substantial risk in patients undergoing major upper-abdominal operations. This analysis documented that the 4 most common underlying causes of unplanned intubation were sepsis, aspiration/pneumonia, excess secretions, and fluid overload. The timing of most of these complications had a broad range, but the median times were moderately predictable. Intra-abdominal and pelvic sepsis resulted in reintubation at a median of 8 days postoperatively. In comparison, aspiration, excess secretions, and fluid overload occurred at a median of 6, 4, and 3 days, respectively. In recent years, efforts to remove nasogastric tubes and progress diets rapidly have decreased the durations of stay but may have increased the risk for aspiration in a subset of patients.16 Patients who are smokers with underlying pulmonary disease and excess secretions required reintubation on day 4. Prevention in these patients requires more robust efforts to achieve smoking cessation and preoperative antibiotic treatment for chronic bronchitis as well as incentive spirometry and continuous positive airway pressure.6,17-19 Fluid overload occurred at a median of 3 days postoperatively as

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intra-abdominal fluid was being mobilized. Judicious management of fluids is required to prevent this relatively early postoperative cause of reintubation.20,21 In one third of patients who required reintubation, sepsis was the underlying cause. Because nearly one quarter of these patients also had bowel obstruction preoperatively is a new observation. These patients with bowel obstruction, like those requiring gastrectomy and pancreatoduodenectomy, are prone to altered bowel function as well as intra-abdominal abscesses after operation. In two thirds of the patients in whom sepsis was the underlying cause, the source was an organ/space infection. GI (32%), bile (24%), and pancreatic (12%) leaks were common, as were urinary tract infections (32%). In comparison, line infections (9%) were less common. During this period at Indiana University Hospital, catheter-associated blood-stream infections occurred in only 1% of patients after operation. Efforts to improve preoperative nutrition and to prevent intra-abdominal infections by means of various strategies also may prevent unplanned intubation.14,22,23 Early drain removal may be another preventive strategy.24 Half of the patients who required reintubation due to sepsis and aspiration (data not shown) met criteria for SIRS 72 h before reintubation. Further evaluation of these patients, especially if 6 to 8 days have passed since operation and they are not progressing, is warranted. Having an appropriate threshold to draw blood cultures and to institute appropriate antibiotics is important for timely diagnosis and treatment. Having a low threshold to perform abdominal and pelvic computed tomography scans in these patients also is appropriate. When sepsis is confirmed, draining collections and instituting a treatment bundle in a timely manner are crucial.11,22,23 The decision to reoperate is difficult but often appropriate. In this analysis, one third of the 32 sepsis patients were drained percutaneously, and one half were returned to the operating room for drainage. Earlier diagnoses and treatments for sepsis may have prevented reintubation in some of these patients. Unplanned intubation was due to aspiration/ pneumonia in more than 30% of the patients in this analysis. Aspiration/pneumonia as the cause for reintubation was a negative prognostic indicator; only 50% were alive 30 days postoperatively. Nearly 80% of these patients had operations proximal to the ileocecal valve. Whether epidural analgesia is advisable in these patients remains controversial.25 Upper GI bleeding, vomiting, the

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need for antiemetic medications and, potentially, inappropriate use of oral narcotics were warning signs. The majority of these patients also were being fed a liquid or solid diet at the time of aspiration. Twice-daily interviews and examinations of these patients inquiring about GI function as well as examining for diffuse or localized distension and tympany are key to the prevention of aspiration. Judicious use of antiemetics and codeine-based pain medications as well as early ambulation also are important. Requiring these patients to be NPO; checking abdominal films for ileus, small-bowel, and/or gastric distension; and appropriately reinserting nasogastric tubes will prevent aspiration and unplanned intubation. The primary limitation of this study is the retrospective analysis of the causes of unplanned intubation and the characterization of the clinical setting when sepsis and aspiration/pneumonia were identified. Although an electronic medical record was available, the quality of the clinical notes varied, and daily documentations of the physical examinations were limited. Nevertheless, the recommendations for prevention with respect to sepsis, aspiration, secretions, and fluids are reasonable, given the level of granularity of the data that were available. Another limitation is that not all services were monitored. For example, noncardiac thoracic surgery and otolaryngology were not monitored via NSQIP, although they were included in the University Health System Consortium analysis of postoperative respiratory failure. In 2012, these services were excluded from the analyses by the University Health System Consortium because national definitions excluded esophagectomy and major head and neck operations from respiratory-failure outcomes. Finally, the analysis was performed at an academic medical center with a focus on high volumes of highrisk patients. Thus, the generalizability of this analysis to small hospitals with low-risk patients may be questioned. In conclusion, unplanned intubation is an uncommon but dangerous postoperative complication that occurs most often in older, frail patients with multiple comorbidities. Previous studies have documented risk factors, and those factors were confirmed in this analysis. The current study further defined the underlying operations and causes. Sepsis and aspiration/pneumonia accounted for two thirds of the patients requiring reintubation. Strategies to diagnose and treat intraabdominal abscesses in a more timely fashion and to identify GI dysmotility and alter medications and diets to prevent aspiration should decrease the incidence of unplanned intubation.

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systematic review for the American College of Physicians. Ann Int Med 2006;144:581-95. 19. Ferreyra GP, Baussano I, Squadrone V, et al. Continuous positive airway pressure for treatment of respiratory complications after abdominal surgery: a systematic review and meta-analysis. Ann Surg 2008;247:617-26. 20. Singh S, Kuschner WG, Lighthall G. Perioperative intravascular fluid assessment and monitoring: a narrative review of established and emerging techniques. Anesthesiol Res Prac 2011;2011:231493. 21. Strunden MS, Heckel K, Goetz AE, Reuter DA. Perioperative fluid and volume management: physiological basis, tools and strategies. Ann Intens Care 2011;1:2.

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22. Elias AC, Matsuo T, Grion CM, Cardoso LT, Verri PH. Incidence and risk factors for sepsis in surgical patients: a cohort study. J Crit Care 2012;27:159-66. 23. Fried E, Weissman C, Sprung C. Postoperative sepsis. Curr Opin Crit Care 2011;17:396-401. 24. Bassi C, Dervenis C, Butturini G, Fingerhut A, Yeo C, Izbicki J, et al. International Study Group on Pancreatic Fistula Definition. Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery 2005;138:8-13. 25. Popping DM, Elia N, Marret E, et al. Protective effects of epidural analgesia on pulmonary complications after abdominal and thoracic surgery: a meta-analysis. Arch Surg 2008;143:990-9.