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The Effect of Malnutrition on Morbidity After Surgery for Chronic Pancreatitis

Posted on: Friday, 8 July 2005, 03:01 CDT

Protein-energy malnutrition is a notable problem in the management of patients with chronic pancreatitis. The effect of malnutrition on pancreatic surgery is not well known. The records of 313 consecutive patients who underwent lateral pancreaticojejunostomy (LPJ, n = 152), pancreaticoduodenectomy (PD, n = 78), or distal pancreatectomy (DP, n = 83) for chronic pancreatitis were retrospectively reviewed and analyzed. Subjective Global Assessment, Nutritional Risk Index, and Instant Nutritional Assessment were used to assess the nutritional state. An average of all three nutritional indexes was established, and patients were categorized into well nourished (n = 101) as well as mild (n = 91), moderate (n = 94), and severe malnourished (n = 27). Poor nutritional state was associated with an increase in postoperative complication rate (LPJ: well nourished 14%, mild 25%, moderate 31%*, severe 50%*; PD: well nourished 44%, mild 44%, moderate 60%, severe 88%*; DP: well nourished 17%, mild 13%, moderate 30%, severe 55%*; *P < 0.045 vs well nourished). Low serum albumin levels also increased operative morbidity. The increase in morbidity was reflected by a higher rate of infectious complications as well as increased ICU stay. Body mass index and weight loss did not contribute to change in outcome. Malnutrition was associated with a higher incidence of postoperative complications after surgery for chronic pancreatitis. An increase in operative morbidity might be related to decreased protein synthesis and impaired immunocompetence.

PROTEIN-ENERGY MALNUTRITION is a common end-stage manifestation in patients with chronic pancreatitis.1 The reason for malnutrition in chronic pancreatitis is diverse. A major factor is decreased caloric intake due to postprandial pain causing food fear. Nausea, a common clinical finding, can also lead to anorexia.1 There is debate whether gastroparesis with delay in gastric emptying and subsequent sensation of nausea is part of the disease process of chronic pancreatitis.2 Decrease in gastrointestinal motility during acute onsets of pancreatic inflammation or chronic use of narcotic analgesics is conceivable and could cause similar symptoms. The pancreas is the major source of digestive enzymes for lipid, protein, and carbohydrates. Patients with chronic pancreatitis are prone to develop exocrine insufficiency. Progressive failure of pancreatic exocrine function leads to excessive loss of fat in form of steatorrhea. Steatorrhea usually occurs after pancreatic lipase output has fallen to less than 10 per cent of normal due to severe acinar cell destruction or complete ductal obstruction within the head.3 This can be observed in 30 per cent of patients with chronic pancreatitis.1 Steatorrhea can lead to a rapid intestinal transit with decreased contact time of chyme with intestinal mucosa. It makes a major contribution to weight loss and muscle wasting.1 Similarly, carbohydrate maldigestion occurs when amylase secretion has fallen to less than 10 per cent of normal.4 Loss of protein in form of creatorrhea and malabsorption of fat-soluble vitamins is rare.1 The efficacy of the already diminished amount of pancreatic digestive enzymes is decreased by the presence of abnormally low pH levels in the duodenum. This is due to continuous gastric acid secretion with decreased amount of pancreatic bicarbonate secretion.5,6 A decrease in duodenal pH can cause bile acid precipitation, which contributes to lipid malabsorption.7 Intestinal obstruction of the duodenum with food intolerance is observed in 1 per cent of patients with chronic pancreatitis.8 Ongoing alcohol consumption and socioeconomic factors may also affect caloric intake.1 Due to the chronicity of the disease, resting energy expenditure is increased in many patients.9 Despite all these influences on malnutrition, body weight in patients with chronic pancreatitis is usually maintained until flares of acute pain with diminished oral intake occur.1

Malnutrition can compromise protein synthesis, resulting in impaired wound healing, decreased immunocompetence, endocrine imbalance, and breakdown of gastrointestinal mucosal barrier.10 It is therefore not surprising that malnutrition is well known to have an adverse effect on outcome after most surgical procedures.10 Reports about the effect on pancreatic surgery are scarce. The aim of this study was to evaluate the influence of malnutrition on operative morbidity for chronic pancreatitis. We compared operative results in well nourished patients with malnourished patients.

Patients and Methods

The records of 313 consecutive patients who underwent operation for chronic pancreatitis at the Department of Surgery, Medical University of South Carolina, from 1995 through 2002 were retrospectively reviewed and analyzed. The study group consisted of 152 patients who underwent lateral pancreaticojejunostomy (69 females, 83 males, mean age 47 years, range 14 to 72 years), 78 patients who underwent pancreaticoduodenectomy (42 females, 36 males, mean age 45 years, range 21 to 74 years), and 83 patients who underwent distal pancreatectomy (40 females, 43 males, mean age 46 years, range 18 to 73 years). The principal indications for operation were chronic pain intractable to medical and endoscopie treatment, terminal biliary stenosis, duodenal stenosis, pancreatic duct disruption with pseudocyst or fistula, and suspicion for a malignant pancreatic lesion. All patients received preoperative broad-spectrum antibiotic prophylaxis with second-generation cephalosporins or equivalent drugs. Morbidity and mortality included complications during operation, hospitalization, or within 30 days of discharge after operation. Pancreatic leak was defined as drainage more than 50 mL/day of amylase-rich fluid after postoperative day 6. Fluid was considered amylase-rich if the amylase level was greater than 150 units/L and at least threefold serum level. Delayed gastric emptying was defined as need for gastric decompression beyond postoperative day 10 or inability to tolerate regular diet after postoperative day 14. A diagnosis of an intra-abdominal abscess required a fluid collection on computed tomography as well as positive cultures from the source. Operative specimens were reevaluated and microscopically classified according to the degree of fibrosis. The extent and distribution of fibrosis was graded from 1 to 12 using a previously established scoring system.11

Patients' nutritional status was assessed using the following indexes: Subjective Global Assessment (SGA),12 Nutritional Risk Index (NRI),13 and Instant Nutritional Assessment (INA).14 SGA was retrospectively evaluated using data from admission and prior clinic visits, including weight change, dietary intake change, gastrointestinal symptoms, functional capacity, degree of physical stress due to underlying disease, and physical findings of malnutrition. According to these findings, patients were categorized into well nourished, moderately malnourished, and severely malnourished. NRI was calculated using serum albumin level, patient's weight at admission, and patient's usual weight, which was defined as the patient's stable weight more than 6 months prior to admission. The formula applied was NRI = (1.519 serum albumin [g/ L]) + 41.7 (present weight/usual weight). Nutritional status was considered well nourished for NRl greater than 100, mildly malnourished for NRI 97.5 to 100, moderately malnourished for NRI 83.5 to less than 97.5, and severely malnourished for NRI less than 83.5. INA classified patients in four categories of nutritional status: well nourished (serum albumin ≥3.5 g/dL, blood lymphocyte count ≥1500 cells/mm^sup 3^), mildly malnourished (serum albumin ≥3.5 g/dL, blood lymphocyte count <1500 cells/ mm^sup 3^), moderately malnourished (serum albumin <3.5 g/dL, blood lymphocyte count ≥1500 cells/mm^sup 3^), and severely malnourished (serum albumin <3.54 g/dL, blood lymphocyte count <1500 cells/mm^sup 3^). To evaluate overall nutritional status, SGA, NRI, and INA were averaged and patients were categorized into well nourished, mildly malnourished, moderately malnourished, and severe malnourished.

Data is reported as percentage or median standard error unless otherwise specified. The χ^sup 2^ contingency test, Fisher's exact test, and the Student's t test were used to analyze the data. P values <0.05 were considered significant. For multivariate backward regression analysis, the SAS version 9.0 computer software (SAS Institute, Inc., Cary, NC) was used.

Results

Demographics

Seventy-eight patients underwent pancreaticoduodenectomy (PD), including Whipple procedure (54) and pylorus-preserving pancreaticoduodenectomy (24). Lateral pancreaticojejunostomy (LPJ) was performed in 152 patients, including Partington-Rochelle procedure (116) and Frey procedure (36). Thirty-six patients within this group required biliary bypass. Distal pancreatectomy (DP) was performed in 83 patients and included splenectomy in 72. Thirty-two per cent of the 313 patients were well nourished, 29 per cent were mildly malnourished, 30 per cent were moderately malnourished, and 9 per cent were severely malnourished. The incidence of preoperatively evaluated clinical features typical fo\r chronic pancreatitis is listed in Table 1. Serum albumin level and blood lymphocyte count both used to determine the degree of malnutrition were as expected decreased in malnourished patients. Chronic diseases potentially affecting albumin levels like diabetes mellitus, liver dysfunction, renal insufficiency, thyroid disease, and adrenal disease were equally distributed throughout the groups. Preoperative total parenteral nutrition was used more frequently in malnourished patients (Table 1). Fibrosis scores available for pancreaticoduodenectomy and distal pancreatectomy specimen showed no significant correlation to degree of malnutrition or serum albumin level (PD: well nourished 6 0.9, mildly malnourished 6 0.6, moderately malnourished 9 0.7, severely malnourished 7 1.2; DP: well nourished 10 0.6, mildly malnourished 9 0.6, moderately malnourished 9 0.5, severely malnourished 9 0.6). Complete obstruction of the pancreatic duct within the head or neck potentially causing exocrine insufficiency was not associated with degree of malnutrition or serum albumin level (well nourished 15%, mildly malnourished 11 %, moderately malnourished 12%, severely malnourished 33%).

TABLE 1. Disease-Related Characteristics

Nutritional State, Preoperative Albumin Level, and Operative Complications

The overall postoperative complication rate after lateral pancreaticojejunostomy, pancreaticoduodenectomy, and distal pancreatectomy was 23 per cent, 54 per cent, and 27 per cent, respectively. Mild degree of malnutrition did not affect operative morbidity when compared to well-nourished patients. Patients with moderate malnutrition had a higher rate of complications, which was only significant within the lateral pancreaticojejunostomy group. Severely malnourished patients had according to odds ratio a 6.0 to 8.8 times increased risk for perioperative complications compared to well-nourished patients in all three operative groups (Table 2). Mortality was not influenced by nutritional status. The types of complications are listed in Table 3. Extraabdominal complications in decreasing frequency included wound infection, pneumonia, urinary tract infection, respiratory failure, sepsis from nonabdominal source, wound dehiscence, cerebral stroke, and acute renal failure. There was no difference comparing each individual complication with degree of malnutrition. After combining infectious complications like intraabdominal abscess, pancreatic or biliary leak associated with intra-abdominal infection, cholangitis, wound infection, pneumonia, urinary tract infection, infectious colitis, and line sepsis, analysis of the data showed that infectious complications were seen more frequently in severely malnourished patients who underwent pancreatic resection. Malnutrition in patients undergoing pancreatic drainage did not influence the incidence of infectious morbidity (Table 2). Multivariate regression analysis demonstrated that infectious complications were the source for the malnutrition- associated increase in overall morbidity after pancreatic resection but not after drainage procedure. Overall, 18 per cent of patients experienced infectious complications (LPJ 11%, PD 26%, DP 23%).

TABLE 2. Perioperative Complication Rate Dependent on Degree of Malnutrition*

TABLE 3. Perioperative Complications Observed After Surgery for Chronic Pancreatitis*

Low preoperative serum albumin levels defined as equal or less than 3.0 g/dL were found in 29 per cent of patients. This was associated with an increase in perioperative complication rate (Table 4). Infectious complications were more frequent in patients with low preoperative albumin level undergoing pancreatic resection (Table 4). Multivariate regression analysis demonstrated that low albumin levels were the predominant source of the increase in infectious and overall complications seen in severely malnourished patients.

TABLE 4. Perioperative Complication Rate Dependent on Preoperative Serum Albumin Level*

The increase in overall complication rate was independent of preoperative total parenteral nutrition use. Multivariate regression analysis showed that preoperative total parenteral nutrition itself did not alter operative morbidity, and it was not responsible for the increase in malnutrition-associated morbidity. Preoperative total blood lymphocyte count did not correlate with overall operative complications and infectious complications. Body mass index was 22.6 0.4 for patients undergoing lateral pancreaticojejunostomy, 25.4 1.2 for pancreaticoduodenectomy, and 26.1 0.6 for distal pancreatectomy. Body mass index was not associated with operative morbidity. Unintentional weight loss greater than 10 per cent of usual body weight during the last 6 month prior to operation had no impact on operative morbidity.

ICU Stay

Postoperative stay in the intensive care unit (ICU) was more frequently used in patients with poor nutritional status after pancreatic resection (LPJ: well nourished 2%, mild 4%, moderate 8%, severe 13%; PD: well nourished 6%, mild 11%, moderate 32%*, severe 50%*; DP: well nourished 0%, mild 13%, moderate 9%, severe 45%*, *P < 0.04). Need for stay in the intensive care unit was associated with low albumin level after distal pancreatectomy (LPJ: normal albumin 3% vs low albumin 8%, P > 0.05; PD: normal albumin 15% vs low albumin 32%, P > 0.05; DP: normal albumin 2% vs low albumin 33%, P < 0.001). The increased need for ICU care in malnourished patients was primarily due to infectious complications (infectious complications after LPJ: ward 10% vs ICU 29%, PD: ward 16% vs ICU 63%*, DP: ward 16% vs ICU 70%*, *P< 0.001).

Hospital Length of Stay and Readmissions

Postoperative hospital length of stay was 8 1.0 days after lateral pancreaticojejunostomy, 15 1.9 days after pancreaticoduodenectomy, and 8 1.6 days after distal pancreatectomy. Hospital length of stay was not significantly affected by degree of malnutrition (LPJ: well nourished 7 0.8 days, mild 8 0.6 days, moderate 8 3.8 days, severe 8 2.3 days; PD: well nourished 15 2.0 days, mild 14 3.8 days, moderate 16 2.6 days, severe 27 7.7 days; DP: well-nourished 8 0.6 days, mild 8 2.0 days, moderate 8 1.3 days, severe 12 10.3 days). There is a trend toward increased hospital length of stay for patients who had a pancreatic resection and low albumin level, which was significant within the distal pancreatectomy group (LPJ: normal albumin 8 1.5 vs low albumin 8 3.5 days, P > 0.05; PD: normal albumin 14 2.1 vs low albumin 22 3.5, P > 0.05; DP: normal albumin 8 0.7 vs low albumin 13 4.3, P < 0.05). Hospital readmissions within the first postoperative year due to pancreatitis-related problems were similar in relation to malnutrition and albumin level (LPJ: 21% of patients; PD: 44% of patients; DP: 30% of patients).

Discussion

Malnutrition is an eminent problem in management of pancreatic disease. Yet, little data is available on the effect of preoperative nutritional state on outcome after pancreatic operations. Low preoperative serum albumin levels are known to have an unfavorable impact on morbidity and mortality after most general surgery procedures.15 For pancreatic surgery, recent studies have shown that preoperative hypoalbuminemia is associated with increased operative mortality after pancreaticoduodenectomy for periampullary malignancy.16,17 After pancreatic resection or drainage for benign and malignant disease, increased morbidity has been linked to low preoperative albumin levels.18

Our retrospective study suggests that moderate and severe malnutrition causes an increase in operative complication rate after surgery for chronic pancreatitis. Mild malnutrition did not seem to make a difference in morbidity. It seems that the reason for this malnutrition-associated morbidity is different for patients with pancreatic resection and drainage. In patients undergoing pancreatic resection in form of pancreaticoduodenectomy or distal pancreatectomy, the increased incidence of overall operative morbidity was based on an increase in infectious complications. Preoperative albumin level, which had a strong impact on defining nutritional state through the nutritional indexes applied, was the main reason for the observed increase in infectious complications. Infectious complications subsequently led to increased overall morbidity and increased use of treatment in the intensive care unit. There was a trend toward increased hospital length of stay in patients with poor nutritional state, which statistically was not significant. For pancreatic drainage in form of lateral pancreaticojejunostomy, the increased overall morbidity in malnourished patients was also due to low albumin levels. A difference in infectious complications, need for intensive care unit management, and hospital length of stay was not noticeable. Mortality was not influenced by nutritional state. Preoperative total parenteral nutrition did not improve operative outcome. Body mass index and weight loss was not associated with changes in operative morbidity.

The nutritional indexes applied in this study were designed to evaluate protein as well as energy malnutrition. Using these tests, we showed that protein-energy malnutrition is associated with increased operative morbidity. Isolated protein malnutrition usually presents in form of hypoalbuminemia without weight loss due to unique diets.19 This can be seen in chronic pancreatitis patients with symptoms of post-prandial pain maintaining on plain carbohydrate-based foods as sole source of caloric intake. Isolated energy malnutrition on the other hand usually presents with weight loss and hypoalbuminemia due to decreased overall caloric intake.19 This study showed an increase in operative morbidity for hypoalbuminemia but not for weight loss. It is therefore conceivable that the increase in operative morbidity was due to protein malnutritio\n and not a decrease in overall energy resources. Exocrine insufficiency as a contributor to protein malnutrition cannot be evaluated in this retrospective study. However, clinical symptoms of chronic diarrhea, degree of pancreatic fibrosis, and presence of complete duct obstruction as potential indicators of exocrine insufficiency did not correlate with degree of measured malnutrition and serum albumin level. It is not evident from the data whether low albumin levels, which seem to be the common ground of increase morbidity, resemble the degree of malnutrition, inflammation, or both. On the one hand, hypoalbuminemia could be a result of malnutrition from smoldering disease causing decreased tissue healing and impaired immunocompetence, leading to an increased complication rate. On the other hand, hypoalbuminemia as an acute-phase protein could be just a marker of more advanced disease with peripancreatic inflammation from recurrent acute exacerbations, complications from duct disruption, or sinistral portal hypertension, making the operation more challenging and causing a potential increase in morbidity.

Infectious complications were seen more frequently in patients who were malnourished and underwent pancreatic resection. This increase in infectious complications was not associated with a decrease of blood lymphocyte count, which is a strong marker for immunocompetence. Similar experiences have been reported by others with preoperative total lymphocyte count not affecting outcome after pancreatic surgery.18 Because it appears that impairment of immunologie function through malnutrition might not be the single source of the rise in infectious morbidity, other mechanisms are conceivable. Studies have shown that compromised intestinal mucosal barrier either through severe acute pancreatitis,20 obstructive jaundice,21 chronic alcohol use,22 or malnutrition23 can result in translocation of enteric bacteria and potentially raise the incidence of intra-abdominal infections.

In conclusion, malnutrition evaluated by clinical and laboratory testing was associated with a higher incidence in postoperative morbidity after surgery for chronic pancreatitis. An increase in operative complications might be related to decreased protein synthesis and impaired immunocompetence.

DISCUSSION

AARON S. FINK, M.D. (Decatur, GA): Numerous studies have established the strong association between malnutrition and poor outcome following general surgical procedures. Such an association would seem particularly germane to pancreatic disease, given the frequency with which malnutrition may be observed in patients with such disorders. A recent study by Billingsley et al.1 provides an excellent example of this relationship. These authors took avail of the robust database assembled within the VA's National Surgical Quality Improvement Program (NSQIP) to seek clinical factors predictive of mortality-but importantly NOT morbidity-following pancreaticoduodenectomy. In their study, Billingsley et al.1 were able to review data from 462 patients and found that preoperative hypoalbuminemia was the strongest predictor of mortality following pancreaticoduodenectomy for pancreatic malignancy.

Theoretically, this finding might be of even greater import for patients with chronic pancreatitis, given their propensity for malnutrition. Surprisingly, however, there is very little information in this regard, a situation which Drs. Schnelldorfer and Adams address in their study, which they so nicely presented here today. After reviewing their manuscript, which they so kindly provided, I seek one clarification and raise several questions:

1) In the current study, infectious complications seemed to account for the increased morbidity rate observed in malnourished patients undergoing resections. Yet the authors claim that while patients undergoing drainage procedures had an increased rate of intra-abdominal complications, these were not infectious in nature. Were these complications primarily pancreatic leaks? If so, why weren't infectious complications observed?

2) In this study, nutritional status was assessed using three different schemas: the Subjective Global Assessment (SGA), the Nutritional Risk Index (NR1), and the Instant Nutritional Assessment (INA). While the latter two indices are based on objective data, the former-the SGA-is based on fairly subjective data (e.g., dietary intake change, GI symptoms, functional capacity, etc). As a result, the SGA may offer a less accurate assessment of nutritional status, especially given the retrospective nature of the data acquisition. I wonder if the authors have evaluated the sensitivity or specificity of the various nutritional scores. In addition, it would be of interest to examine how the individual nutritional indices correlate with each other as well as with the specific clinical outcome parameters.

3) It is critical to note that the Nutritional Risk Index and the Instant Nutritional Assessment rely heavily upon the serum albumin level. As we have heard, substantial data demonstrates that the albumin level alone correlates with adverse clinical outcome. Indeed, above and beyond the Billingsley article cited previously, the strongest demonstration of this relationship was presented in Gibbs et al. 1999 analysis of NSQIP data accumulated from over 54,000 noncardiac surgery patients.2 In the latter study, both mortality and morbidity continuously increased as serum albumin progressively decreased over the entire range of serum albumin levels. The issue is further complicated by the fact that additional studies-albeit more controversial-suggest that administration of exogenous albumin to achieve a serum albumin of >3 g/dL might lessen morbidity.

4) Obviously, causality is at the heart of the matter, that is, does hypoalbuminemia in and of itself contribute to poor outcomes or is it merely a marker for other "upstream" pathologic processes such as malnutrition or inflammation? In their study, the authors failed to demonstrate any relationship between increased complications and preoperative use of TPN. With this fact in mind, I would appreciate the authors' view of the implication of a low preoperative serum albumin level, as well as their comments on their actual therapeutic approach to the patient requiring elective pancreatic surgery who is found to be hypoalbuminemic.

REFERENCES

1. Billingsley KG, Hur K, Henderson WG, et al. Outcome after pancreaticoduodenectomy for periampullary cancer: an analysis from the Veterans Affairs National Surgical Quality Improvement Program. J Gastrointest Surg 2003;7:484-91.

2. Gibbs J, Cull W, Henderson W, et al. Preoperative serum albumin level as a predictor of operative mortality and morbidity. Arch Surg 1999;134:36-42.

STEPHEN W. BEHRMAN, M.D. (Memphis, TN): Is there anything we can do differently to improve on these results such as longer periods of per-operative TPN?

Secondly, did you happen to analyze your results with respect to either antecedent diabetes or the development of postoperative diabetes and perioperative control of glucose levels in this population? As you know, recent data has suggested a correlation between perioperative hyperglycemia and the development of postoperative infectious complications. Could your greater incidence of septic morbidity in those patients with pancreatic resection have been related to perioperative hyperglycemia?

THOMAS SCHNELLDORFER, M.D. (Charleston, SC): Dr. Fink to answer your first question. Why didn't we see any increased infection rate in the pancreaticojejunostomy group? After this operation, the infectious complications are generally relatively low and that probably has to do with the nature of the operation and therefore significant differences could not be found. If we operated on an additional 150 patients, maybe there would be differences.

Concerning the impact of each individual nutritional index on the outcome, we did not use an individual index to verify this simply because the study is very much limited due to it's retrospective nature like Dr. Fink has mentioned. In order to accommodate for this problem, we tried to broaden our base and put as many factors of malnutrition as possible into the mix. Most factors were very similar in each patient.

Concerning the source of low albumin levels, it is hard to tell whether the low albumin levels were due to malnutrition or are just a marker of severe disease. That's why we also included other markers of malnutrition.

In terms of clinical approaches for patients who come to our clinic with malnutrition, in the past we have used a more subjective approach. We looked at the overall clinical status as well as the nutritional status. If the patient is clinically malnourished and has very severe pancreatic disease with several complications, clinical judgement comes into place to decide whether to proceed and accept a higher complication rate. In essence, there are not any strict guidelines we can provide in terms of whether malnutrition is a contraindication for this elective procedure. However, that factor must be brought into consideration.

Concerning the frequency of diabetes, I didn't present any data today but it is in the manuscript. We have a similar incidence of diabetes in all of these patient groups. We do not think that diabetes influenced the increase of infectious complications in the malnourished patients.

REFERENCES

1. Twersky Y. Bank S: Nutritional deficiencies in chronic pancreatitis. Gastroentcrol Clin North Am 1989;18:543-65.

2. Malfertheiner P, Pieramico O, Buchler M, et al. Gastrointestinal motility in chronic pancreatitis. In: Beger HG, Buchler M, Ditschuneit H, Malfertheiner P, eds. Chronic Pancreatitis: Research and Clinical Management. Berlin: Springer, 1990, pp 229-34.

3. DiMagno EP, Go VL, Summerskill WH. Relations between pancreatic enzyme outputs and malabsorption in severe pancreatic insufficiency. N Engl J M\ed 1973;288:813-5.

4. Hiele M, Ghoos Y, Rutgeerts P, et al. Starch digestion in normal subjects and patients with pancreatic disease, using a 13CO2 breath test. Gastrocnterology 1989;96:503-9.

5. DiMagno EP, Malagelada JR, Go VL, et al. Fate of orally ingested enzymes in pancreatic insufficiency. N Engl J Med 1977; 296:1318-22.

6. Dutta SK, Russell RM, Iber FL. Impaired acid neutralization in the duodenum in pancreatic insufficiency. Dig Dis Sci 1979;24: 775- 80.

7. Andersen JR, Bendtsen F, Ovesen L, et al. Pancreatic insufficiency: duodenal and jejunal pH, bile acid activity, and micellar lipid solubilization. Int J Pancreatol 1990;6:263-70.

8. Rattner DW, Warshaw AL. Venous, biliary, and duodenal obstruction in chronic pancreatitis. Hepatogastroenterology 1990; 37:301-6.

9. Hebuterne X, Hastier P, Peroux JL, et al. Resting energy expenditure in patients with alcoholic chronic pancreatitis. Dig Dis Sci 1996;41:533-9.

10. Howard L, Ashley C. Nutrition in the perioperative patient. Annu Rev Nutr 2003;23:263-82.

11. Ammann RW, Heitz PU, Kloppel G. Course of alcoholic chronic pancreatitis: a prospective clinicomorphologic long-term study. Gastroenterology 1996;111:224-31.

12. Detsky AS, McLaughlin JR, Baker JP, et al. What is subjective global assessment of nutritional status? JPEN 1987;11: 8-13.

13. Buzby GP, Williford WO, Peterson OL, et al. A randomized clinical trial of total parenteral nutrition in malnourished surgical patients. Am J Clin Nutr 1988;47:357-65.

14. Seltzer MH, Bastidas JA, Cooper DM, et al. Instant nutritional assessment. JPEN 1979;3:157-9.

15. Gibbs J, Cull W, Henderson W, et al. Preoperative serum albumin level as a predictor of operative mortality and morbidity. Arch Surg 1999;134:36-42.

16. Billingsley KG, Hur K, Henderson WG, et al. Outcome after pancreaticoduodenectomy for periampullary cancer: an analysis from the Veterans Affairs National Surgical Quality Improvement Program. J Gastrointest Surg 2003;7:484-91.

17. Chou FF, Sheen-Chen SM, Chen YS, et al. Postoperative morbidity and mortality of pancreaticocluodenectomy for periampullary cancer. Eur J Surg 1996;162:477-81.

18. Kudsk KA, Tolley EA, DeWitt RC, et al. Preoperative albumin and surgical site identify surgical risk for major postoperative complications. JPEN 2003;27:1-9.

19. Mora RJF. Malnutrition: organic and functional consequences. World J Surg 1999;23:530-5.

20. Ammori BJ. Role of the gut in the course of severe acute pancreatitis. Pancreas 2003;26:122-9.

21. Parks RW, Clements WD, Smye MG, et al. Intestinal barrier dysfunction in clinical and experimental obstructive jaundice and its reversal by internal biliary drainage. Br J Surg 1996;83: 1345- 9.

22. Banan A, Choudhary S, Zhang Y, et al. Ethanol-induced barrier dysfunction and its prevention by growth factors in human intestinal monolayers. J Pharmacol Exp Ther 1999;291:1075-85.

23. Welsh FK, Farmery SM, MacLennan K, et al. Gut barrier function in malnourished patients. Gut 1998;42:396-401.

THOMAS SCHNELLDORFER, M.D., DAVID B. ADAMS, M.D.

From the Department of Surgery, Medical University of South Carolina, Charleston, South Carolina

Presented at the Annual Scientific Meeting and Postgraduate Course Program, Southeastern Surgical Congress, New Orleans, LA, February 11-15, 2005.

Address correspondence and reprint requests to Thomas Schnelldorfer, M.D., Medical University of South Carolina, Department of Surgery, 96 Jonathan Lucas Street, P.O. Box 250613, Charleston, SC 29425.

Copyright The Southeastern Surgical Congress Jun 2005

Source: American Surgeon, The

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