Preoperative Issues in Clinical Nutrition* Stephen A. McClave, MD; Harvy L. Snider, MD, FCCP; and David A. Spain, MD
Allowing a patient’s nutritional state to deteriorate through the perioperative period adversely affects measureable outcome related to nosocomial infection, multiple organ dysfunction, wound healing, and functional recovery. Careful preoperative nutritional assessment should include a determination of the level of stress, an evaluation of the status of the GI tract, and the development of specific plans for securing enteral access. Patients already demonstrating compromise of nutritional status (defined by > 10% weight loss and serum albumin level < 2.5 g/dL) should be considered for a minimum of 7 to 10 days of nutritional repletion prior to surgery. Widespread use of total parenteral nutrition in unselected patients is unwarranted, may actually worsen outcome, and should be reserved for preoperative nutritional support only in severely malnourished patients in whom the GI tract is unavailable. Compared with the parenteral route, use of perioperative enteral feeding has been shown to provide more consistent and beneficial results, and can be expected to promote specific advantages in long-term morbidity and mortality. (CHEST 1999; 115:64S–70S)
of nutritional status in the critically D eterioration ill patient undergoing major surgery is associated with reduced systemic immunity, exaggerated stress response, organ system dysfunction, poor wound healing, and delayed functional recovery. Weight loss, hypoalbuminemia, and other purported signs of protein calorie malnutrition have long been predictors of poor surgical outcome.1–3 In the past, perioperative nutritional support has been synonymous with total parenteral nutrition (TPN). A high rate of septic complications and negligible impact on patient outcome with this route of therapy have raised question about the overall utility of nutritional support and the risk of interfering with the normal adaptive metabolic response to injury.4 Increasing evidence suggests that the “motor” of the multiple organ failure sepsis syndrome is the GI tract, the integrity of which affects immune defenses, organ function, and whether the stress response is provoked or attenuated.5 Much more consistent and beneficial responses are being seen with the provision of perioperative nutritional support by the enteral route.
*From the Departments of Medicine (Drs. McClave and Snider) and Surgery (Dr. Spain), University of Louisville School of Medicine and Veterans Affairs Medical Center, Louisville, KY. Correspondence to: Stephen A. McClave, MD, Professor of Medicine, Division of Gastroenterology/Hepatology, University of Louisville School of Medicine, 550 S Jackson St, Louisville, KY 40292 64S
Comparison of Enteral and Parenteral Nutrition A favorable impact on patient outcome with enteral tube feeding (ETF) compared with TPN has been shown in several prospective randomized controlled trials (PRCTs) in a variety of disease processes ranging from trauma,6 – 8 to head injury,9,10 to pancreatitis.11–13 The proposed mechanism for this difference, which has been extrapolated from animal studies, is that loss of gut integrity with increased translocation of bacterial products (predominantly Gram-negative coloforms), in combination with a heightened immune response induced by ischemia or hypotension, results in activation of the arachidonic acid cascade.14 The sequence of events is complex and incompletely understood.15 Evidence suggests that multiple organ failure sepsis syndrome and the systemic inflammatory response syndrome result from the immunosuppressive effects of prostaglandin E2, the proinflammatory action of leukotriene B4, and the thrombogenic/vasoconstrictive response induced by thromboxane A2, all of which are released by this cascade. A second mechanism contributing to septic complications may involve loss of gut-associated lymphoid tissue with decreased antigen processing and stimulation of mucosal-associated lymphoid tissue at distant sites (ie, lung, kidneys).14 Many aspects of this process have been demonstrated in humans in PRCTs comparing ETF and TPN.14 Compromise of gut integrity with reduced small-bowel absorption was demonstrated in one Perioperative Cardiopulmonary Evaluation and Management
study with decreased D-xylose and vitamin A absorption and increased lactose intolerance in a control group receiving TPN.9 Attenuation of the stress response by ETF was shown in one study by a more rapid return of interleukin-6 levels to normal,6 and in a second study by reduced acute phase proteins, less systemic endotoxin exposure, and reduced overall oxidant stress.11 Hyperglycemia and insulin requirements were decreased in two studies.9,13 Multiple studies have shown reduced cost of nutrition support.12,13,16 An effect on patient outcome with ETF has been suggested by reduced rates of nosocomial infection,6 – 8,12,17 better return of cognitive function in head injury patients,9,18 and reduced mortality.6
Does Deterioration of Nutritional Status Affect Surgical Outcome? Opinions on the length of time a previously normal individual can be starved without adverse effects ranges from as long as 12 to 14 days to as little as 72 h.4,19 –21 No PRCTs exist to support any of these positions. A well-nourished person should have a 7to 10-day energy and protein reserve, such that starvation alone over this time period in the absence of severe injury or illness should be well tolerated.19 While some reports claim that development of protein calorie malnutrition affecting patient outcome does not occur until after 12 to 14 days of starvation,4 others contend that the stress and hypermetabolism of critical illness and major surgery shorten this time period to 5 to 7 days.4,19 Still, others refer to a 72-h window of opportunity, coinciding with transition from the ebb to flow phase of injury, after which any benefit from the enteral route of feeding is lost.21 In a very early report, weight loss was shown to be an indicator of operative risk in 50 patients undergoing gastric resection for peptic ulcer disease, where a correlation was seen between preoperative weight loss and postoperative complications.1 A more recent prospective study used percent ideal body weight, percent weight loss, serum albumin level, and arm muscle circumference to evaluate noncancer patients preoperatively.2 Patients with at least one abnormality of these markers had a significant increase in the incidence of overall complications (48% vs 23%, p , 0.05), in major complications (31% vs 9%, p , 0.05), and in length of stay (29 vs 14 days, p , 0.05), when compared respectively with patients in whom all markers were normal.2 In another prospective study of patients undergoing elective surgery involving resection of a portion of the upper GI tract, patients with weight loss alone . 10% faired no worse than control subjects without weight loss.3 However, those patients with . 10%
weight loss with some evidence of physiologic impairment (defined by abnormal serum protein levels, maximal inspiratory pressure, hand grip dynanometry, or body composition) sustained a significantly higher incidence of major complications (primarily septic).3 In a prospective study of female patients undergoing surgery for femoral neck fracture, the thinnest of three groups preoperatively (defined by percent ideal body weight . 2 SDs below the mean) had significantly lower oral intake, a more prolonged period of rehabilitation, and a higher overall mortality.22 Interestingly, nutritional intervention in the perioperative period does not necessarily reverse the abnormalities in the traditional markers. Significant improvement in weight, prealbumin levels, and certain anthropometric measures was seen in response to tube feeding in severely malnourished, underweight female subjects with femoral neck fractures when compared with control subjects.22 This effect was not seen in women who were only moderately malnourished and underweight.22 Albumin levels that improved after surgery in a group given dietary supplements compared with control subjects were probably more related to the reduction in major complications than the adequacy of caloric provision.23 In a third study, anthropometric measures and grip dynamometry did not change significantly in a group receiving preoperative TPN, despite a clear-cut benefit with reduced postoperative morbidity compared with control subjects.24 A lack of response in these markers suggests that they may not always reflect nutritional status and that they may be insensitive, in the short term, to changes in nutritional status.24
Does Nutritional Intervention Affect Surgical Outcome? Much of the support for TPN, for the existence of nutrition support teams, and for the goal of achieving positive nitrogen balance has been based largely on uncontrolled studies and the basic belief that life cannot be sustained without nutrient sustenance.4 The true impact of nutritional intervention can be ascertained only in PRCTs in which study patients are compared with control subjects who receive no nutritional therapy. To our knowledge, only two such studies have shown a clear benefit of preoperative TPN on hospital course following major surgery.24,25 In the most quoted study (reported in two parts),25,26 patients undergoing surgery for GI or pancreatic cancer who received preoperative TPN with a glucose solution had a significant twofold decrease in major postoperative complications and a fourfold CHEST / 115 / 5 / MAY, 1999 SUPPLEMENT
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decrease in mortality when compared with control subjects who were treated with IV fluid resuscitation and regular hospital diet. Interestingly, a third arm of the study included patients receiving a similar amount of calories via TPN, but one half of the nonprotein calories given were comprised of lipids.25 This group had postoperative complications and mortality that were similar to those of control subjects, suggesting that any benefit from the preoperative TPN may have been lost by the immunosuppressive effects of the lipid emulsion.25,26 A second trial involving a smaller number of patients undergoing resection of hepatocellular carcinoma demonstrated that preoperative TPN significantly lowered postoperative morbidity compared with control subjects receiving no nutritional therapy (34% vs 55%; p 5 0.02).24 Weight loss was less, liver function (as measured by indocyanine green) was better, and there was a lower incidence of ascites requiring diuretic therapy in the group receiving 7 days of preoperative TPN.24 The largest study, the Veterans Affairs Cooperative Study,27 was designed to substantiate the perioperative use of TPN. It was performed in 395 malnourished (mostly male) patients undergoing abdominal or thoracic surgical procedures.27 Surprisingly, the TPN group had a higher percent of infectious complications compared with unfed control subjects (14.1% vs 6.4%; p 5 0.01). Patients who were borderline or mildly malnourished had no demonstratable benefit from TPN. Only a subset of severely malnourished patients receiving TPN had fewer noninfectious complications than control subjects (5% vs 43%; p 5 0.03), complications that were related to healing wounds (anastomotic leaks, bronchopleural fistulas) and maintaining normal organ function.27 The experience with postoperative TPN has been dismal. In a PRCT of patients undergoing major pancreatic resection for malignancy, use of postoperative TPN was associated with a higher incidence of major complications compared with no therapy (45% vs 23%; p , 0.001).28 In a second, larger study of patients undergoing acute or elective major surgical procedures, no clinical benefit was seen in those patients receiving postoperative TPN compared with control subjects receiving no therapy.29 In fact, 20% of study patients developed a protracted, complicated course. Those patients placed on a regimen of TPN had a higher mortality rate than control subjects who had a similar complicated course but did not receive TPN.29 In summarizing the data on perioperative TPN, widespread use in unselected patients undergoing major surgery is not warranted. Worse outcome has been shown with use of postoperative TPN alone. Preoperative TPN for a minimum of 7 to 10 days, 66S
particularly in patients with severe malnourishment, may reduce postoperative morbidity. Experience with perioperative enteral nutrition has been much more consistent with more favorable outcomes, although the PRCTs tend to be smaller in size and fewer in number. Patients with obstructive jaundice undergoing percutaneous transhepatic biliary drainage,30 who were randomized to receive a mean of 20 days of preoperative nutritional hyperalimentation (86% by the enteral route), showed a decrease in postoperative morbidity from 46.8 to 17.8% (p , 0.05) and a decrease in mortality from 12.5 to 3.5% (p , 0.05) when compared with control subjects receiving no additive nutritional support.30 In a second study,31 malnourished patients undergoing surgery were randomized to receive preoperative enteral hyperalimentation or a routine hospital diet. Those patients receiving nasogastric feeding for 10 days prior to surgery showed a significant improvement in body weight, serum protein levels, and multiple anthropometric measures compared with control subjects. Wound infections were three times more common (37.2% vs 10.4%) and mortality was doubled (11.7% vs 6.0%) in control subjects compared with the study patients.31 In a third study, patients with squamous cell carcinoma of the head and neck were randomized as outpatients to receive a regular diet with nocturnal supplements for 10 to 21 days prior to surgery, and they were compared with a control group receiving a regular diet alone.32 Postoperative complications in the patients who received supplements were one half those of the control subjects (32% vs 59%).32 Data supporting use of postoperative enteral feeding are more substantial. One of the more quoted studies in trauma patients compared a study group placed on a regimen of immediate jejunostomy feeding after major abdominal trauma with a control group given IV fluid resuscitation for 5 to 7 days and allowed to return to normal diet on their own.8 Although a small percentage of patients in both groups had to be “rescued” with TPN after 7 days, the study group receiving enteral feeding had a significantly lower incidence of sepsis than control subjects (26% vs 4%; p , 0.05).8 In a small study of patients undergoing liver transplant, a control group receiving early postoperative nasoenteric feeding had a significantly lower incidence of viral infections than control subjects receiving no additive enteral support (0% vs 17%, p , 0.05).33 The most impressive data involved two large studies in women undergoing surgery for femoral neck fractures.22,23 In the larger study,22 744 women were classified at the time of surgery by anthropometric measures into one of three groups designated as well-nourished, thin (between 1 and 2 SDs below the mean), and very Perioperative Cardiopulmonary Evaluation and Management
thin (. 2 SDs below the mean). Only thin and very thin patients were randomized postoperatively to receive standard diet with nocturnal tube feeding vs regular diet during hospitalization to discharge. Results were most dramatic for those patients in the very thin group, in which study patients receiving nocturnal feeds had significant reductions in the duration of their long-term rehabilitation following surgery.22 Mortality was 8% in study patients vs 21.7% in control subjects, but this difference did not reach significance.22 Enterally supplemented patients in the thin group also showed significant reductions in rehabilitation time compared with control subjects.22 In a similar, but smaller study, elderly women with femoral neck fractures were randomized to daily oral supplements in addition to regular diet vs regular diet alone following surgery.23 The supplements given as nocturnal feeds were continued throughout their hospital stay for a mean of 32 days. A favorable clinical outcome (defined by occurrence of # 1 minor and no major complications) was seen in 56% of study patients vs 13% of control subjects (p , 0.05), a difference that was sustained throughout 6 months of rehabilitation.23 In summary, use of perioperative ETF appears to be well tolerated and more consistently benefits postoperative morbidity and mortality. Preoperative ETF in the nutritionally compromised patient may be underutilized in current practice. Accurate nutritional assessment and preoperative planning of nutritional support are needed for optimal results.
Nutritional Assessment The term “protein calorie malnutrition” refers to an older concept based on parameters that have been shown recently to be impractical, poorly reproducible, insensitive, inappropriate, and unreliable in distinguishing patients who need aggressive nutritional support from those who do not.2,19,34 The term might be better replaced by the concept of risk for nutritional deterioration. A thin patient undergoing elective cholecystectomy should tolerate several days of starvation without incident. A trauma patient may be well nourished immediately before his or her injury, but then may suddenly be at great risk for deterioration of nutritional status and in need of aggressive support. Anthropometric measures (ie, arm muscle circumference, triceps skin-fold thickness, creatinine height index) are limited by intraobserver and interobserver variation, right/left arm dominance, and poor sensitivity to sudden changes in nutritional status.34 Skin tests for cell-mediated immunity in preoperative patients are of little value due to low frequency of anergy.2 Visceral protein
levels (ie, albumin, prealbumin, transferrin) are valuable prognostic indicators for use on initial evaluation and are still used in most surgical studies to define “malnourished” patients.27 Fluid shifts, increased vascular permeability, extravascular extravasation, and change in hepatic prioritization of protein synthesis induced by the stress response limit serial use of these proteins as a marker for nutritional status or as a monitor for adequacy of nutritional support.34,35 Tests to evaluate body composition such as total body nitrogen or potassium levels, dual radiographic absorptiometry, or bioelectrical impedance are difficult to perform in the critically ill patient, are expensive and impractical outside of the research setting, and may be inaccurate with massive fluid shifts and hemodynamic instability.19 In contrast, muscle function testing is probably underutilized. Tests such as hand grip dynamometry and maximal inspiratory pressure are simple to perform, inexpensive, sensitive, and may be a valid indicator of skeletal muscle dysfunction and increased risk for postoperative complications.19 Weight as a percentage of ideal body weight (IBW) or as a percentage of weight lost from the patient’s usual weight is still one of the best markers to identify patients who may already have compromised nutritional status.1,2,28 A recent proposed revision of the International Classification of Diseases, ninth revision, codes for protein calorie malnutrition has simplified nutritional assessment, basing definitions on four parameters: percent weight loss from usual weight, percent IBW, serum albumin level, and inability to eat for $ 7 days (actual or predicted).19 Weight lost as a percentage of the patient’s usual weight is considered mild if # 10%, moderate between 10% and 20%, and severe if $ 20%.19 Significant marasmus is suggested by actual weight , 85% of IBW. Serum albumin levels are considered moderately depressed if , 3.2 g/dL, or severely depressed if , 2.5 g/dL.19 Thus, significantly malnourished patients defined by the parameters of . 10% weight loss and serum albumin level , 2.5 g/dL, with major surgery pending, should be considered for at least 7 days of preoperative nutritional repletion and early postoperative support.19 A key aspect of nutritional assessment is to define the patient’s level of stress and degree of critical illness. The APACHE (acute physiology and chronic health evaluation) III scoring system, Ranson criteria for pancreatitis, and Adjusted Trauma Index (ATI) scores are useful for this purpose. An important concept is that subtle changes in management decisions are more likely to affect patient outcome with greater degrees of critical illness. In severely ill trauma patients with ATI . 24, use of the enteral route of feeding was associated with fewer infections CHEST / 115 / 5 / MAY, 1999 SUPPLEMENT
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than use of the parenteral route (11.1% vs 47.6%; p , 0.005).17 In patients with lesser disease severity and ATI scores , 24, no significant differences in rates of infection were seen between the two routes of nutritional support.17 Control of hyperglycemia on the first day following major surgery was shown to significantly impact the incidence of severe infections later in the hospital course (20% with poor control and glucose levels . 220 U vs 0% with good control, p , 0.05).36 By the second postoperative day, when patients were less critically ill, control of glucose level no longer affected the incidence of later infections.36 Another key aspect of nutritional assessment is evaluation of the status of the GI tract. The term “ileus” and slogans such as “if the gut works, use it” are misleading and their use should be avoided. These references incorrectly imply that the gut turns off and on as a single unit. The gut never stops “working” in the sense that absorption of luminal nutrients probably never stops. It is not always safe to permit bowel absorption in a patient with hemodynamic instability or vasopressor therapy who is at risk for intestinal ischemia. It may be appropriate to delay enteral feeding until patients are not receiving vasopressive therapy and fully resuscitated. Gastric tonometry, by indirectly measuring intramucosal pH, may emerge as a useful tool in reducing the risk of gut wall ischemia.37 An important factor in tolerance of enteral feeding is the degree and level at which intestinal contractility has been maintained. Abdominal bloating or distention, nausea, vomiting, or high residual volumes in response to feeding may be used to assess gastric contractility, while passage of stool and flatus may reflect colonic contractility. Bowel sounds are only an approximate measure of smallbowel contractility and are not required for low rates of enteral infusion. Gut disuse, status of intestinal villi, and whether standard formulas can be assimilated normally are clinical judgments that need to be made at the bedside. Energy expenditure and caloric requirements can vary tremendously in the critically ill patient and may be difficult to determine using only predictive equations. Critically ill patients monitored over 24 h can vary up to 35% about a mean level. Daily variability in resting energy expenditure can range as high as 46% early in hospitalization when a patient is more critically ill, decreasing to , 12% during recovery when the patient is in more stable condition.38 Caloric requirements are best measured by indirect calorimetry. Despite reports of . 200 similar equations described in the literature, none is more commonly used nor any more accurate (or inaccurate) than the Harris-Benedict equation.38 The simplified empiric formula of 22 to 25 kcal/kg of actual body 68S
weight per day correlates to the measured resting energy expenditure in a similar fashion to these more sophisticated equations.39 Predictive equations, though, are inherently inaccurate in the individual patient.38 The importance of accuracy of the nutritional support regimen is underscored by reports that increased mortality was seen in pancreatitis patients with a persistently negative nitrogen balance and in trauma patients with a cumulative 10,000calorie deficit.40,41 The most important aspect of nutritional assessment for the patient anticipating major surgery is to plan the method by which enteral access is to be secured for postoperative nutritional support. More options for tube placement are available preoperatively. The procedure can be done electively without interfering with surgery or it can be performed intraoperatively. This avoids the situation of performing endoscopic or radiographic procedures on a patient with poor postoperative intestinal motility and recent gut anastomoses.
Enteral Access The type of enteral access is determined by the anticipated needs of a particular patient. The level at which to infuse feeding, duration of feeding preoperatively and postoperatively, and the need to simultaneously decompress the stomach are factors that need to be taken into account when selecting the proper access device. Ultimately, the decision for the specific tube or placement method is related to local expertise and physician preferences. Nasoenteric tubes placed into the stomach or small bowel are ideal for perioperative feeding in the short term for periods , 30 days.20 In most cases, these tubes can be placed at bedside with the tip located in the stomach. Jejunal placement should be considered if there is evidence of significant reflux or tracheal aspiration, gastroduodenoparesis following major surgery, or pancreatitis.13,20 Passage into the small bowel may be facilitated by use of metoclopramide, cisapride, patient positioning, small-bore tubes, or a tube with an unweighted tip,20 although the success of these maneuvers is questionable.42 In a patient with significant gastroparesis at significant risk for aspiration, simple placement of the feeding tube past the pylorus may not be adequate, as duodenal atony may often be present as well. Although radiographic placement can be expected routinely to deliver the tube to the distal duodenum, endoscopic placement may be required to place the tube at or beyond the ligament of Treitz.43,44 Jejunal placement below the ligament of Treitz may be Perioperative Cardiopulmonary Evaluation and Management
facilitated endoscopically by placing the tube over a guidewire, as opposed to dragging the tube into place.45 Securing the nasoenteric feeding tube, particularly after endoscopic or radiographic placement, is important, as displacement can occur in 40 to 60% of cases.44,46,47 The mean life span for a feeding tube remaining in place appears to be about 10 days.20,44,47 Displacement is not always limited to patients with altered mental status.46 Mittens, arm boards, abdominal posies, and binders all help in protecting the tube. Bridling the tube with a small five-gauge neonatal feeding tube can be done at the bedside, is well tolerated, and may be more preferable to the patient and physician than suturing the tube to the face. A hemoclip device may be utilized to clip a string at the end of the tube to the small-bowel mucosa, to hold the tube temporarily in place until nausea, vomiting, retching, or intestinal dysmotility subsides. Placement of a percutaneous endoscopic gastrostomy (PEG) or jejunostomy (PEJ) tube should be considered for long-term feeding for periods . 30 days. Placement of a surgical jejunostomy tube with or without a decompressive gastrostomy should be considered in patients undergoing certain procedures, such as extensive gastrectomy or pancreatic debridement. No significant differences in success of placement have been described for the push, pull, or introducer type of PEG kits.48,49 A recent prospective comparison of the effectiveness of PEG vs nasogastric tubes showed that a greater percentage of prescribed calories were provided with use of the PEG (93% vs 55%, p , 0.05), due primarily to dislodgement of the nasogastric tubes.50 Surgical placement of gastrostomy or jejunostomy tubes in comparison to the percutaneous or nasoenteric methods has no difference in morbidity, mortality, or overall tube function, but may incur more expense and require longer recovery time.20 The Stamm gastrostomy may be the preferred surgical procedure of choice. The Witzel gastrostomy, in which the tube is tunneled through the gastric wall toward the fundus, is difficult to convert later to a PEG/PEJ if intolerance develops. Care should be taken in selecting the percutaneous or surgical gastrostomy tube, in the event that gastric feeds are not tolerated and a compatible jejunostomy tube has to be placed through the existing PEG site. Not all PEG kits are designed to be easily converted to the PEG/PEJ method. PEGs may be secured by placing T-fasteners, switching to a button PEG (such that traction dislodges the connecting tube), or converting to surgical placement.
Conclusion Nutritional assessment of the critically ill patient anticipating a major operation is crucial, as deterioration of nutritional status is a key factor in surgical outcome. The route, manner, and adequacy of the nutritional support regimen affects the degree of stress response, the incidence of nosocomial infection/multiple organ failure, wound healing, length of hospitalization, and mortality. Patients with evidence of compromised nutritional status (as suggested by weight loss and hypoalbuminemia) should be considered for preoperative nutritional support over a 7- to 10-day period, preferably by the enteral route. Nutritional assessment in the preoperative period should include a thorough evaluation of the status of the gut with explicit plans for placement of enteral access. References 1 Studley HO. Percentage of weight loss, a basic indicator of surgical risk in patients with chronic peptic ulcer. JAMA 1936; 106:458 – 460 2 Warnold I, Lundholm K. Clinical significance of preoperative nutritional status in 215 noncancer patients. Ann Surg 1984; 199:299 –305 3 Windsor JA, Hill GL. Weight loss with physiologic impairment—a basic indicator of surgical risk. Ann Surg 1988; 207:290 –296 4 Koretz RL. Nutritional supplementation in the ICU: how critical is nutrition for the critically ill? Am J Respir Crit Care Med 1995; 151:570 –573 5 Carrico CK. The elusive pathophysiology of the multiple organ failure syndrome [editorial]. Ann Surg 1993; 218:109 6 Charash WE, Kearney PA, Annus KA, et al. Early enteral feeding is associated with an attenuation of the acute phase/ cytokine response and improved outcome following multiple trauma. J Trauma 1994; 37:1015 7 Moore FA, Moore EE, Jones TN, et al. TEN versus TPN following major abdominal trauma-reduced septic morbidity. J Trauma 1989; 29:916 –923 8 Moore EE, Jones TN. Benefits of immediate jejunostomy feeding after major abdominal trauma—a prospective, randomized study. J Trauma 1986; 26:874 – 881 9 Suchner U, Senftleben U, Eckart T, et al. Enteral versus parenteral nutrition: effects on gastrointestinal function and metabolism. Nutrition 1996; 12:13–22 10 Young B, Ott L, Twyman D, et al. The effect of nutritional support on outcome from severe head injury. J Neurosurg 1987; 67:668 – 676 11 Windsor ACJ, Kanwar S, Li AGK, et al. Compared with parenteral nutrition, enteral feeding attenuates the acute phase response and improves disease severity in acute pancreatitis. Gut 1998; 42:431– 435 12 Kalfarentzos F, Kehagias J, Mead N, et al. Enteral nutrition is superior to parenteral nutrition in severe acute pancreatitis: results of a randomized prospective trial. Br J Surg 1997; 84:1665–1669 13 McClave SA, Greene LM, Snider HL, et al. Comparison of the safety of early enteral vs parenteral nutrition in mild acute pancreatitis. JPEN J Parenter Enteral Nutr 1997; 21:14 –20 14 Moore FA, Feliciano DV, Andrassy RJ, et al. Early enteral CHEST / 115 / 5 / MAY, 1999 SUPPLEMENT
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32 Flynn MB, Leightty FF. Preoperative outpatient nutritional support of patients with squamous cancer of the upper aerodigestive tract. Am J Surg 1987; 154:359 –362 33 Hasse JM, Blue LS, Liepa GU, et al. Early enteral nutrition support in patients undergoing liver transplantation. JPEN J Parenter Enteral Nutr 1995; 19:437– 443 34 Grant JP. Nutritional assessment in clinical practice. Nutr Clin Pract 1986; 1:3–11 35 Fleck A. Acute phase response: implications for nutrition and recovery. Nutrition 1988; 4:109 –117 36 Pomposelli JJ, Baxter JK, Babineau TJ, et al. Early postoperative glucose control predicts nosocomial infection rate in diabetic patients. JPEN J Parenter Enteral Nutr 1998; 22: 77– 81 37 Maynard N, Bihari D, Beale E, et al. Assessment of splanchnic oxygenation by gastric tonometry in patients with acute circulatory failure. JAMA 1993; 270:1203 38 McClave SA, Snider HL. Use of indirect calorimetry in clinical nutrition. Nutr Clin Pract 1992; 7:207–221 39 Hunter DC, Jaksic T, Lewis D, et al. Resting energy expenditure in the critically ill: estimations versus measurement. Br J Surg 1988; 75:875– 878 40 Bartlett RH, Dechert RE, Mault JR, et al. Measurement of metabolism in multiple organ failure. Surgery 1982; 92:771– 779 41 Ranson JHC, Spencer FC. Prevention, diagnosis, and treatment of pancreatic abscess. Surgery 1977; 82:99 –106 42 Spain DA, Reynolds MA, DeWeese RC, et al. Transpyloric nasoenteric feeding in head injured patients does not decrease pulmonary complications. J Trauma 1995; 39:1100 – 1102 43 Gutierrez ED, Balfe DM. Fluoroscopically guided nasoenteric feeding tube placement: results of a 1-year study. Radiology 1991; 178:759 –762 44 Mathus-Vliegen EMH, Tytgat GNJ, Merkus MP. Feeding tubes in endoscopic and clinical practice: the longer the better? Gastrointest Endosc 1993; 39:537–542 45 Baskin WN. Enteral access techniques. Gastroenterologist 1996; 4:S40 –S67 46 McClave SA, Sexton LK, Spain DA, et al. Enteral tube feeding in the intensive care unit: factors impeding adequate delivery. Crit Care Med (in press) 47 Crocker KS, Krey SH, Steffee WP. Performance evaluation of a new nasogastric feeding tube. JPEN J Parenter Enteral Nutr 1981; 5:80 – 82 48 Hogan RB, DeMarco DC, Hamilton JK, et al. Percutaneous endoscopic gastrostomy—to push or pull: a prospective randomized trial. Gastrointest Endosc 1986; 32:253–258 49 Kozarek RA, Ball T, Ryan J. Percutaneous endoscopic gastrostomy—when push comes to shove: a comparison of two insertion methods. Am J Gastroenterol 1986; 81:642– 646 50 Park RHR, Allison MC, Lang J, et al. Randomized comparison of percutaneous endoscopic gastrostomy and nasogastric tube feeding in patients with persisting neurological dysphagia. BMJ 1992; 304:1406 –1409
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