Okabayashi T, Kobayashi M, Nishimori I, Sugimoto T, Akimori T, Namikawa T, Okamoto K, Onishi S, Araki K. Benefits of early postoperative jejunal feeding in patients undergoing duodenohemipancreatectomy. World J Gastroenterol 2006; 12(1): 89-93
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Dr Michiya Kobayashi, Department of Tumor Surgery, Kochi Medical School, Nankoku, Kochi 783-8505, Japan
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Takehiro Okabayashi, Michiya Kobayashi, Tekeki Sugimoto, Toyokazu Akimori, Tsutomu Namikawa, Ken Okamoto, Keijiro Araki, Department of Tumor Surgery, Kochi Medical School, Nankoku, Kochi 783-8505, Japan
Isao Nishimori, Saburo Onishi, Department of Gastroenterology and Hepatology, Kochi Medical School, Nankoku, Kochi 783-8505, Japan
ORCID number: $[AuthorORCIDs]
Co-correspondence to: Michiya Kobatashi
Correspondence to: Dr Michiya Kobayashi, Department of Tumor Surgery, Kochi Medical School, Nankoku, Kochi 783-8505, Japan
Telephone: +81-88-880-2370 Fax: +81-88-880-2371
Received: June 16, 2005 Revised: June 28, 2005 Accepted: July 8, 2005 Published online: January 7, 2006
AIM: To study whether early postoperative enteral nutrition reduces the incidence of complications and/or improves nutritional status following duodenohemipancreatectomy (DHP).
METHODS: We studied 39 patients who underwent DHP for a peri-ampullary mass. Twenty-three patients received total parental nutrition and then started to have an oral intake of nutrition between postoperative day (POD) 7 and 14 [late postoperative enteral nutrition (LPEN) group]. Sixteen patients started to have enteral feeding through a jejunostomy catheter the day after the operation [early postoperative enteral nutrition (EPEN) group]. The incidence of complications and laboratory data at the early postoperative stage were studied in comparison between LPEN and EPEN groups.
RESULTS: Serum levels of albumin and total protein in the EPEN group were significantly higher than those in the LPEN group. The loss of body mass index was significantly suppressed in the EPEN group as compared to the LPEN group. The lymphocyte count decreased immediately after the operation was restored significantly faster in the EPEN group than in the LPEN group. The EPEN group showed significantly fewer incidences of postoperative pancreatic fistulas, as well as a significantly shorter length of hospitalization than the LPEN group. There were no significant differences in the incidences of other postoperative complications between the two groups, such as delayed gastric emptying, surgical site infection, cholangitis, and small bowel obstruction.
CONCLUSION: EPEN is a safe and beneficial opportunity for patients who have undergone DHP for a peri-ampullary mass.
Citation: Okabayashi T, Kobayashi M, Nishimori I, Sugimoto T, Akimori T, Namikawa T, Okamoto K, Onishi S, Araki K. Benefits of early postoperative jejunal feeding in patients undergoing duodenohemipancreatectomy. World J Gastroenterol 2006; 12(1): 89-93
Postoperative nutritional support was shown to reduce the incidence of complications and/or to shorten the hospitalization period[1,2]. Recently, early postoperative enteral nutrition (EPEN) has been proposed as the novel method for nutritional support after surgery, especially after gastric and colorectal resection[3-9]. Several studies suggested that EPEN possibly improves also the postoperative outcome of patients after duodenohemipancreatectomy (DHP)[10-13], which is one of the most invasive operations in the upper abdominal surgery with a high incidence of postoperative complications[14-19]. Whereas, EPEN has been introduced with complications such as troubles of jejunal feeding tube and delayed gastric emptying[10-13,20,21]. Taken together, the overall benefit of EPEN after DHP remains controversial.
The purpose of the present study was to evaluate the influence of EPEN on the incidence of postoperative complications. Moreover, by analyzing a variety of clinical parameters including laboratory data, body mass index (BMI), and the duration of hospitalization, we attempted to determine which method of postoperative nutritional support, enteral or non-enteral, was more advantageous in the total management of patients who had undergone DHP.
MATERIALS AND METHODS
We investigated a total of 39 patients who had undergone DHP for a peri-ampullary mass from 2000 to 2005 at Kochi Medical School, including 24 men and 15 women (mean age of 67.5 years; 43-82 years). Among these 39 patients, there were 14 cases of pancreatic invasive ductal carcinoma, 11 of cholangiocarcinoma, 7 of intraductal papillary mucinous neoplasms, 4 of carcinoma of the papilla of Vater, 1 of gastrointestinal stromal tumor, 1 of primary sclerosing cholangitis, and 1 of metastatic renal cell carcinoma (Table 1). All patients underwent a complete perioperative physical examination and laboratory investigations. Moreover, a variety of relevant parameters regarding the operative procedure and anesthesia were recorded in all cases.
IPMN: Intraductal papillary mucinous neoplasm; CPV: Carcinoma of the papilla of Vater; Other diseases: Gastrointestinal stromal tumor, primary sclerosing cholangitis, and pancreatic metastasis of renal cell carcinpma
In all patients, the reconstructive technique was used to anastomose the pancreas first, followed by the hepatic duct and the duodenum with a Braun anastomosis. The pancreatic-enteric anastomosis was performed as a pancreaticojejunostomy in an end-to-side fashion. In patients of the EPEN group, a feeding jejunostomy catheter was placed at the end of surgery and before closing the wound through the anterior wall of the stomach using a modified Witzel technique. Furthermore, in all cases of pylorus-preserving pancreaticoduodenectomy (PpPD), the gastrostomy tube was inserted from the afferent loop of the jejunum into the stomach for the purpose to prevent delayed gastric emptying.
We determined the amount of calories required for postoperative nutrition according to the Harris-Benedict equation. Some patients received total parenteral nutrition and then started to have oral intake of nutrition usually between POD 7 and 14, as determined late postoperative enteral nutrition (LPEN) group. The second group of patients started to have EPEN through a catheter-feeding jejunostomy on POD 1 (within 24 h after surgery), as determined EPEN group. Enteral feeding was started at a rate of 20 mL/h and gradually increased by 10 mL/h a day up to the final rate (70 mL/h).
Laboratory and clinical investigations
The operation time, blood loss volume, and amount of blood transfusion during and after the surgery were carefully recorded. Samples for laboratory investigations were taken on POD 1, 4, 6, and 14. The laboratory parameters included serum levels of total protein, albumin, total bilirubin, cholinesterase, alanine transaminase, aspartate transaminase, lactate dehydrogenase, alkaline phosphatase, gamma-glutamyl transpeptidase, amylase, urea nitrogen, and creatinine. The BMI was measured before surgery and on POD 6 and 14. Postoperative complications, including surgical site infection, leakage from anastomosis, pancreatic fistula, cholangitis, small bowel obstruction and delayed gastric emptying, were carefully monitored every day. The duration of hospitalization was defined as the time from the day of the surgery to the day of discharge. The progress of all patients, following their discharge from hospital, was monitored by our hospital.
We determined the occurrence of pancreatic fistula based on the following criteria: the concentrations of amylase and lipase in the drainage fluid being three times higher than that in the serum on consecutive PODs, and the drainage volume being more than 10 mL/d. Amylase and/or lipase concentrations in the serum and drainage fluid were checked on POD 1, 3, 4, 5, and 7, and twice a week thereafter[23-25].
We tested for statistical significance using the χ2 test, the Fisher’s exact test and the t test. P < 0.05 was considered statistically significant. Where appropriate, values were expressed as mean ± SD.
We retrospectively reviewed 39 patients who had undergone DHP between 2000 and 2004 at Kochi Medical School, and subdivided them into two groups, 23 patients in the LPEN group and 16 patients in the EPEN group (Table 1). Hospital mortality was 2.6%. There were no significant differences between the two groups in age, gender, and the incidence of underlying diseases.
PpPD was carried out in 26 cases and PD in 13 cases. The frequencies of PpPD and intra-operative radiotherapy (IOR) were significantly higher in the EPEN group than in the LPEN group, because we started IOR for all patients with pancreatic carcinoma in 2002 (P < 0.05). There were no significant differences between the two groups in other parameters (Table 2) including operation time, blood loss volume, and the proportion of patients who received blood transfusion including red blood cells in mannitol-adenine-phosphate solution (RC-MAP) and fresh frozen plasma (FFP).
PD: Pancreaticoduodenectomy; PpPD: Pylorus-preserving pancreaticoduodenectomy; RC-MAP: Red cells in mannitol-adenine-phosphate solution; FFP: Fresh frozen plasma; IOR: intra-operative radiotherapy.
The baseline preoperative values of all laboratory parameters were comparable between the two groups. In the postoperative course, however, several parameters showed a significant difference. The lymphocyte count decreased immediately after the operation (at POD 1) in both groups (Figure 1), which was more obviously seen in the EPEN group compared to the LPEN group (P < 0.05), probably due to the higher incidence of IOR (Table 2). However, during POD 1 and 4, lymphocyte count in the LPEN group continuously decreased, but increased in the EPEN group. There was no significant difference between the two groups in lymphocyte count at POD 4 and thereafter. The serum levels of albumin (Figure 2) and the total protein (data not shown) decreased immediately after the operation in both groups. However, albumin levels at POD 4, 6, and 14 (Figure 2) and total protein levels at POD 6 and 14 (data not shown) in the EPEN group were significantly higher than those in the LPEN group. These findings in the restoration of nutritional parameters were consistent with the alteration in BMI. Loss of BMI was significantly suppressed in the EPEN group as compared to the LPEN group (Table 3).
Figure 1 Peripheral lymphocyte coun.aP<0.05 vs LPEN.
Figure 2 Serum albumin level.aP<0.05 vs LPEN.
Table 3 Postoperative outcome of patients with pancreatic surgery.
LPEN group(n = 23)
EPEN group(n = 16)
21.75 ± 3.16
22.58 ± 2.60
20.43 ± 2.67
2.40 ± 2.59
20.14 ± 2.50
22.38 ± 2.55
Postoperative complications (%)
Surgical site infection
Small bowel obstruction
Delayed gastric emptying
Length of hospitalization (days)
44.3 ± 19.0
31.7 ± 8.8
NS: not significant
None of the cases had a complication of anastomotic leakage. The EPEN group had a significantly lower incidence of pancreatic fistula than the LPEN group (P < 0.05). There was no significant difference between the two groups in the incidence of other postoperative complications, including surgical site infection, ventral hernia, cholangitis, small bowel obstruction, and delayed gastric emptying (Table 3). Finally, the EPEN group also required a significantly shorter length of hospital stay than the LPEN group (P < 0.01).
In the present study, we employed 39 patients who underwent DHP and subdivided them into two groups according to the procedures of the postoperative nutritional support: the EPEN and LEPN groups. There was no significant difference in baseline profiles between the two groups except for the following two parameters, which should be considered in the analysis of the results. First, the number of patients with PD was greater in the LPEN group than in the EPEN group. EPEN after DHP was introduced in our department in 2002, in order to assess its utility. Until then, almost all patients who underwent PD for a peri-ampullary mass were postoperatively administered with total parenteral nutrition. However, we believed that there were no significant differences in the surgical procedure because two surgeons performed the pancreatic surgery in this study period. Second, the number of patients with IOR was much greater in the EPEN group than the LPEN group. The difference was caused by the fact that we started IOR for all patients with pancreatic carcinoma in 2002[26-28].
Although the serum levels of albumin and total protein dropped remarkably in all the patients after the operation, they recovered quickly in the EPEN group, and were significantly higher than those in the LPEN group at the early postoperative stage. Consistent with these findings, loss of BMI was significantly suppressed in the EPEN group as compared to the LPEN group. These findings indicate that EPEN modulates a metabolic response, favoring the synthesis of proteins. We believe that nutritional improvement observed in the EPEN group was not influenced by a large proportion of patients with PpPD (87.5%), since PpPD has been reported to provide a long-term nutritional support for operated patients but has not any benefit for nutritional status in early postoperative stage.
Furthermore, the lymphocyte count fell immediately after surgery in the EPEN group probably due to the IOR, resulting in the significantly lower level as compared to the LPEN group (P < 0.05). However, the lymphocyte count in the EPEN group increased thereafter, and reached at the similar level observed in the LPEN group at POD 14. These findings suggest that the administration of EPEN not only improves the nutritional status but also improves whole-body protein kinetics.
There was no significant difference between two groups in the incidence of infectious complications, such as surgical site infection and cholangitis, and also noninfectious complications, such as ventral hernia and small bowel obstruction. Although the EPEN group contained a significantly greater number of patients with PpPD than the LPEN group, there were no significant differences in the occurrence of delayed gastric emptying between the two groups. The incidence of delayed gastric emptying has been reported in 7-36% of patients with DHP[18,30-34]. Usually, the delayed gastric emptying is more frequently seen in patients with PpPD than in patients with PD, and is typically associated with prolonged hospitalization. In our study, tube gastrostomy was created in all patients who underwent PpPD, and thus patients with delayed gastric emptying had no vomiting.
Pancreatic fistula is considered as a major postoperative complication of DHP and has been reported in 5-24% of patients with DHP[23,35-38]. In our study, surprisingly, the incidence of pancreatic fistula was significantly lower in the EPEN group (6.3%) than in the LPEN group (39.1%). There have been some concerns that EPEN could increase the possibility of pancreatic fistulae because of its stimulatory effect on exocrine pancreatic secretion. Our data show that EPEN has no bad influence upon the occurrence of pancreatic fistula but rather works to prevent it.
In conclusion, EPEN is a safe and beneficial procedure for patients who have undergone DHP. EPEN improves early postoperative outcomes, including nutritional status and whole-body protein kinetics. Furthermore, EPEN contributes to a significantly lower incidence of pancreatic fistula, resulting in a shorter duration of hospitalization compared to the LPEN group. Based on these findings, EPEN can provide regular postoperative nutritional support following DHP.
S- Editor Wang XL and Guo SY L- Editor Elsevier HK E- Editor Wang J
Kudsk KA, Croce MA, Fabian TC, Minard G, Tolley EA, Poret HA, Kuhl MR, Brown RO. Enteral versus parenteral feeding. Effects on septic morbidity after blunt and penetrating abdominal trauma.Ann Surg. 1992;215:503-11; discussion 511-3.
Moore FA, Feliciano DV, Andrassy RJ, McArdle AH, Booth FV, Morgenstein-Wagner TB, Kellum JM, Welling RE, Moore EE. Early enteral feeding, compared with parenteral, reduces postoperative septic complications. The results of a meta-analysis.Ann Surg. 1992;216:172-183.
ASPEN Board of Directors: Guidelines for the use of parenteral and enteral nutrition in adult and pediatrric patients. JPEN J Parenter Enteral Nutr. 1993;17:1SA-26SA.
Round table conference on metabolic support of the critically ill patients--March 20-22, 1993. Intensive Care Med. 1994;20:298-299.
Jolliet P, Pichard C, Biolo G, Chioléro R, Grimble G, Leverve X, Nitenberg G, Novak I, Planas M, Preiser JC. Enteral nutrition in intensive care patients: a practical approach. Working Group on Nutrition and Metabolism, ESICM. European Society of Intensive Care Medicine.Intensive Care Med. 1998;24:848-859.
Farreras N, Artigas V, Cardona D, Rius X, Trias M, González JA. Effect of early postoperative enteral immunonutrition on wound healing in patients undergoing surgery for gastric cancer.Clin Nutr. 2005;24:55-65.
Feo CV, Romanini B, Sortini D, Ragazzi R, Zamboni P, Pansini GC, Liboni A. Early oral feeding after colorectal resection: a randomized controlled study.ANZ J Surg. 2004;74:298-301.
Soop M, Carlson GL, Hopkinson J, Clarke S, Thorell A, Nygren J, Ljungqvist O. Randomized clinical trial of the effects of immediate enteral nutrition on metabolic responses to major colorectal surgery in an enhanced recovery protocol.Br J Surg. 2004;91:1138-1145.
DiFronzo LA, Yamin N, Patel K, O'Connell TX. Benefits of early feeding and early hospital discharge in elderly patients undergoing open colon resection.J Am Coll Surg. 2003;197:747-752.
Rios G, Conrad A, Cole D, Adams D, Leveen M, O'Brien P, Baron P. Trends in indications and outcomes in the Whipple procedure over a 40-year period.Am Surg. 1999;65:889-893.
Brooks AD, Marcus SG, Gradek C, Newman E, Shamamian P, Gouge TH, Pachter HL, Eng K. Decreasing length of stay after pancreatoduodenectomy.Arch Surg. 2000;135:823-830.
Gouma DJ, van Geenen RC, van Gulik TM, de Haan RJ, de Wit LT, Busch OR, Obertop H. Rates of complications and death after pancreaticoduodenectomy: risk factors and the impact of hospital volume.Ann Surg. 2000;232:786-795.
Gianotti L, Braga M, Gentilini O, Balzano G, Zerbi A, Di Carlo V. Artificial nutrition after pancreaticoduodenectomy.Pancreas. 2000;21:344-351.
Lillemoe KD, Cameron JL, Yeo CJ, Sohn TA, Nakeeb A, Sauter PK, Hruban RH, Abrams RA, Pitt HA. Pancreaticoduodenectomy. Does it have a role in the palliation of pancreatic cancer.Ann Surg. 1996;223:718-25; discussion 725-8.
Yeo CJ, Cameron JL, Sohn TA, Lillemoe KD, Pitt HA, Talamini MA, Hruban RH, Ord SE, Sauter PK, Coleman J. Six hundred fifty consecutive pancreaticoduodenectomies in the 1990s: pathology, complications, and outcomes.Ann Surg. 1997;226:248-57; discussion 257-60.
Pedrazzoli S, DiCarlo V, Dionigi R, Mosca F, Pederzoli P, Pasquali C, Klöppel G, Dhaene K, Michelassi F. Standard versus extended lymphadenectomy associated with pancreatoduodenectomy in the surgical treatment of adenocarcinoma of the head of the pancreas: a multicenter, prospective, randomized study. Lymphadenectomy Study Group.Ann Surg. 1998;228:508-517.
Mack LA, Kaklamanos IG, Livingstone AS, Levi JU, Robinson C, Sleeman D, Franceschi D, Bathe OF. Gastric decompression and enteral feeding through a double-lumen gastrojejunostomy tube improves outcomes after pancreaticoduodenectomy.Ann Surg. 2004;240:845-851.
Rai J, Flint LM, Ferrara JJ. Small bowel necrosis in association with jejunostomy tube feedings.Am Surg. 1996;62:1050-1054.
Sonawane RN, Thombare MM, Kumar A, Sikora SS, Saxena R, Kapoor VK, Kaushik SP. Technical complications of feeding jejunostomy: a critical analysis.Trop Gastroenterol. 1997;18:127-128.
Harris JA, Benedict FG. Biometric studies of basal metabolism in man. Washington: Carnegie Institute 1919; .
Gouillat C, Chipponi J, Baulieux J, Partensky C, Saric J, Gayet B. Randomized controlled multicentre trial of somatostatin infusion after pancreaticoduodenectomy.Br J Surg. 2001;88:1456-1462.
Nakatsuka A, Yamaguchi K, Chijiiwa K, Tanaka M. Octreotide inhibits pancreatic exocrine secretion and prevents pancreatoenterostomy leakage.Int Surg. 2000;85:124-129.
Berberat PO, Friess H, Uhl W, Büchler MW. The role of octreotide in the prevention of complications following pancreatic resection.Digestion. 1999;60 Suppl 2:15-22.
Crane CH, Beddar AS, Evans DB. The role of intraoperative radiotherapy in pancreatic cancer.Surg Oncol Clin N Am. 2003;12:965-977.
Ma HB, Di ZL, Wang XJ, Kang HF, Deng HC, Bai MH. Effect of intraoperative radiotherapy combined with external beam radiotherapy following internal drainage for advanced pancreatic carcinoma.World J Gastroenterol. 2004;10:1669-1771.
Willett CG, Del Castillo CF, Shih HA, Goldberg S, Biggs P, Clark JW, Lauwers G, Ryan DP, Zhu AX, Warshaw AL. Long-term results of intraoperative electron beam irradiation (IOERT) for patients with unresectable pancreatic cancer.Ann Surg. 2005;241:295-299.
Seiler CA, Wagner M, Bachmann T, Redaelli CA, Schmied B, Uhl W, Friess H, Büchler MW. Randomized clinical trial of pylorus-preserving duodenopancreatectomy versus classical Whipple resection-long term results.Br J Surg. 2005;92:547-556.
Miedema BW, Sarr MG, van Heerden JA, Nagorney DM, McIlrath DC, Ilstrup D. Complications following pancreaticoduodenectomy. Current management.Arch Surg. 1992;127:945-99; discussion 945-99;.
Cameron JL, Pitt HA, Yeo CJ, Lillemoe KD, Kaufman HS, Coleman J. One hundred and forty-five consecutive pancreaticoduodenectomies without mortality.Ann Surg. 1993;217:430-45; discussion 430-45;.
van Berge Henegouwen MI, van Gulik TM, DeWit LT, Allema JH, Rauws EA, Obertop H, Gouma DJ. Delayed gastric emptying after standard pancreaticoduodenectomy versus pylorus-preserving pancreaticoduodenectomy: an analysis of 200 consecutive patients.J Am Coll Surg. 1997;185:373-379.
Horstmann O, Becker H, Post S, Nustede R. Is delayed gastric emptying following pancreaticoduodenectomy related to pylorus preservation.Langenbecks Arch Surg. 1999;384:354-359.
Balcom JH, Rattner DW, Warshaw AL, Chang Y, Fernandez-del Castillo C. Ten-year experience with 733 pancreatic resections: changing indications, older patients, and decreasing length of hospitalization.Arch Surg. 2001;136:391-398.
Okabayashi T, Kobayashi M, Sugimoto T, Namikawa T, Okamoto K, Hokimoto N, Araki K. Postoperative pancreatic fistula following distal pancreatectomy for pancreatic neoplasm; can pancreatic fistula be prevented.Hepatogastroenterology. 2004;51:1838-1841.
van Berge Henegouwen MI, De Wit LT, Van Gulik TM, Obertop H, Gouma DJ. Incidence, risk factors, and treatment of pancreatic leakage after pancreaticoduodenectomy: drainage versus resection of the pancreatic remnant.J Am Coll Surg. 1997;185:18-24.
Hashimoto N, Ohyanagi H. Pancreatic juice output and amylase level in the drainage fluid after pancreatoduodenectomy in relation to leakage.Hepatogastroenterology. 2002;49:553-555.
Grobmyer SR, Rivadeneira DE, Goodman CA, Mackrell P, Lieberman MD, Daly JM. Pancreatic anastomotic failure after pancreaticoduodenectomy.Am J Surg. 2000;180:117-120.
Kubota K, Makuuchi M, Takayama T, Sakamoto Y, Harihara Y, Kimura W. Appraisal of two-staged pancreatoduodenectomy: its technical aspects and outcome.Hepatogastroenterology. 2000;47:269-274.