ORIGINAL ARTICLE

Gastroenterology & Hepatology

http://dx.doi.org/10.3346/jkms.2012.27.3.261 • J Korean Med Sci 2012; 27: 261-267

Postoperative Nutritional Effects of Early Enteral Feeding

Compared with Total Parental Nutrition in Pancreaticoduodectomy
Patients: A Prosepective, Randomized Study
Joon Seong Park1, Hye-Kyung Chung2, The benefits of early enteral feeding (EEN) have been demonstrated in gastrointestinal
Ho Kyoung Hwang1, Jae Keun Kim1, surgery. But, the impact of EEN has not been elucidated yet. We assessed the postoperative
and Dong Sup Yoon1 nutritional status of patients who had undergone pancreaticoduodenectomy (PD)
1
according to the postoperative nutritional method and compared the clinical outcomes of
Departments of Surgery and 2Nutritional Services,
Gangnam Severance Hospital, Yonsei University two methods. A prospective randomized trial was undertaken following PD. Patients were
Health System, Seoul, Korea randomly divided into two groups; the EEN group received the postoperative enteral feed
and the control group received the postoperative total parenteral nutrition (TPN)
Received: 7 June 2011 management. Thirty-eight patients were included in our analyses. The first day of bowel
Accepted: 1 November 2011
movement and time to take a normal soft diet was significantly shorter in EEN group than
Address for Correspondence: in TPN group. Prealbumin and transferrin were significantly reduced on post-operative day
Dong-Sup Yoon, MD (POD) 7 and were slowly recovered until POD 90 in the TPN group than in the EEN group.
Department of Surgery, Gangnam Severance Hospital, Yonsei
University College of Medicine, 612 Eunju-ro, Gangnam-gu, EEN group rapidly recovered weight after POD 21 whereas it was gradually decreased in
Seoul 135-720, Korea TPN group until POD 90. EEN after PD is associated with preservation of weight compared
Tel: +82.2-2019-2444, Fax: +82.2-3462-5994
E-mail: [email protected] with TPN and impact on recovery of digestive function after PD.
This study was supported by a faculty research grant of Yonsei
University College of Medicine in 2007 (6-2007-0120). Key Words:  Early Enetral Feeding; TPN; Nutrition; Pancreaticoduodenectomy
This article was presented at The European Society for Clinical
Nutrition and Metabolism 2008 (ESPEN 2008), Florence, Italia,
September 13-16, 2008.

INTRODUCTION the postoperative nutritional method between EEN and TPN,

and compared the clinical outcomes of the two modes.
Pancreaticoduodenectomy (PD) is currently considered as the
treatment choice for carcinoma in periampullary regions. In re- MATERIALS AND METHODS
cent years, this procedure has been rapidly developed and has
become safer and more efficient in high volume centers (1). PD Patients
results in a loss of gastric pacemaker and a partial pancreatic In this open, randomized, single center, parallel group trial, we
resection, and such physiologic consequence leads to a high investigated a long term effect of EEN on postoperative weight
incidence of postoperative malnutrition. Though many surgeons change comparing with TPN management in pancreaticoduo-
consider that this postoperative malnutrition is an unavoidable denectomy patients. We included patients over 18 yr of age who
sequence of PD, the importance of nutritional status which in- received PD with malignant periampullary pathology at Gang-
fluences patients’ quality of life, cannot be ignored. nam Severance Hospital of Yonsei University Health System be-
  Postoperative nutritional support was shown to reduce the tween May 2007 and December 2008. Exclusion criteria includ-
incidence of complications and to shorten the hospital stay. ed: 1) a history of major abdominal or pelvic surgery; 2) patients
Recently, early enteral feeding (EEN), in comparison with total with metastatic disease and palliative surgery; 3) a history of
parenteral nutrition (TPN), has become a standard manage- abdominal or pelvic radiation; 4) patients currently taking ste-
ment pathway for nutritional support after gastrointestinal sur- roid or other immunosuppressive medications. Patients receiv-
gery (2-7). However, clinical data on postoperative EEN after ing preoperative nutritional support were also excluded.
PD are very limited, and reports available are focused only on
early postoperative results such as the safety and efficacy of EEN Operative procedures
after PD (8-11). All patients underwent exploratory laparotomy followed by py-
  In this prospective study, we assessed the postoperative nu- lorus preserving pancreatoduonectomy (PPPD) or conventional
tritional status of patients who had undergone PD according to PD as previously described (12). Pancreaticojejunostomy was

© 2012 The Korean Academy of Medical Sciences. pISSN 1011-8934

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0)
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 Park JS, et al.  •  Early Enetral Nutrition in Pancreaticoduoencetomy

performed with duct to mucosa anastomosis in all patients. No ceive postoperative TPN management (Fig. 1). Enteral feeding
pancreaticogastrostomies were performed. End-to-side hepati- (Jevity RTH, Abbott Laboratories, IL, USA) was started within
cojejunostomy was performed 15 cm proximal to the pancreat- 24 hr postoperatively at a rate of 20 mL/h. The velocity was pro-
icojejunostomy with single-layer interrupted sutures. An antecol- gressively increased by 20 mL/d until reaching full nutritional
ic duodenojejunostomy (or gastrojejunostomy) was constructed goal (25 kcal/kg). Enteral feeding was delivered by an infusion
using a two-layered anastomosis. At the end of surgery, patients pump for 18 h/day with 6 hr of a rest period.
were randomized in the operating room using a sealed envelop   In the control group, TPN was initiated on the first postoper-
to either EEN or TPN group. Feeding nasojejunal tube was placed ative day. All patients received TPN solution that has 25 kcal/kg
into patients randomized to enteral feeding group. Just before every day. The ratio of glucose to lipid in this solution was 2:1,
closing the wound, 8 Fr feeding tube (Kangaroo, Sherwood Medi- and nonprotein calorie to nitrogen (kcal/kg) was 100:1. Multivi-
cal, Tullemore, Ireland) with the guide wire in the lumen was tamins, electrolytes, trace elements and insulin were also in-
inserted by the anesthetist through the naris and pushed down cluded in the TPN solution. All nutrient solutions were prepared
until distal tip of the tube was 20 cm aborally from the duode- daily under aseptic conditions. Infusion was performed through
nojejunostomy or gastrojejunostomy anastomosis. After recon- a central venous catheter using an injection micro pump. Enter-
struction, a closed suction, silicon drain (Jackson-Pratt, Baxter al or parenteral infusion was continued until the patient’s oral
Health Care Corp., Deerfield, IL, USA), was placed from the right intake reached approximately 800 kcal/d.
upper quadrant posterior to the pancreaticojejunal and biliary   According to the policy of our department, antacid drugs for
anastomoses. stress ulcer prophylaxis and octreotide (Sandostatin® 150 μg,
Novartis, East Hanover, NJ, USA) was administered to all patients
Assessment of nutrition for 7 days postoperatively. Patients were given sips of water be-
We examined nutritional status of all patients, and the parame- tween postoperative days 4 and 5 and then proceed to a regular
ters included weight, laboratory parameters, and the Patient diet within 7 days.
Generated Subjective Global Assessment (PG-SGA) at baseline
and postoperative 7th, 14th, 21th, and 90th day by a dietitian. A Clinical data and complications
full diet history was performed, and energy intake and protein Members of the surgical staff did not participate in the recorded
intake were calculated. For each component of scored PG-SGA, postoperative complications. PD related complications, such as
points (0-4) were awarded depending on the impact of the symp- delayed gastric emptying and pancreatic fistula, were defined
tom on nutritional status. A score ≥ 9 indicates a critical need by the International Pancreas Study Group (13, 14). Enteral feed-
for nutritional intervention. ing related complications, abdominal cramps and distention,
diarrhea (defined as more than three bowel movements per
Postoperative Nutrition Support day), vomiting, and aspiration were considered adverse effects.
Patients were randomized into two groups, the EEN group to Adverse effects were treated according to the following proto-
receive postoperative enteral feed and the control group to re- col: 1) abdominal clamping pain was treated first with analgesic

Pancreas cancer/Periampulllary carcinoma

PreOP PG-SGA, Anthropometric, Biochemical measurement

OP Pancreaticoduodenectomy/Pylorus Preserving Pancreaticoduodenectomy

EEN group (N = 20) TPN group (N = 20)

POD 7 Anthropometric, Biochemical measurement

POD 14 Anthropometric, Biochemical measurement

POD 21 PG-SGA, Anthropometric, Biochemical measurement

POD 90 PG-SGA, Anthropometric, Biochemical measurement Fig. 1. Study outline.

262   http://jkms.org http://dx.doi.org/10.3346/jkms.2012.27.3.261

Park JS, et al.  •  Early Enetral Nutrition in Pancreaticoduoencetomy

drug; in patients with persistent symptoms despite the drug ad- board of Yonsei University (3-2007-0022) and was registered on
ministration, infusion rate was reduced by 20 mL/h or tempo- the Clinical Trial.gov (ID no: NCT00809081). Signed informed
rarily stopped for 6-12 hr and resumed at a slower rate; 2) abdom- consent was collected from all recruited patients.
inal bloating was treated first by prokinetics drug; in patients
with persistent symptoms despite the drug administration, in- RESULTS
fusion rate was reduced by 20 mL/h or temporarily stopped for
6-12 hr and resumed at a slower rate; 3) vomiting was treated by Clinical and preoperative nutritional characteristics of
a temporary stop of infusion followed by diagnostic procedures; patients
if there was no intestinal obstruction, infusion was resumed at A total of 40 patients were recruited and randomized to either
the slower rate; 4) diarrhea was treated by reducing the infusion the TPN or EEN treatment group (Fig. 2). Two patients withdrew
rate by 20 mL/h or temporarily stopping it for 6-12 hr, which was from the study because their nasojejunal tubes were acciden-
resumed at a slower rate; in patients with persistent diarrhea, tally dislodged. Thirty-eight patients (18 EEN and 20 TPN) were
Clostridium difficile infection was always ruled out. analyzed. The mean age of patients was 61.0 yr ( ± 11.9 yr) and
consisted of 19 men and 19 women. Five patients underwent
Sample size PD, and 33 underwent PPPD. Pathologic diagnoses were pan-
The primary end point of the study was a change in weight. Sec- creatic carcinoma in 14 patients, bile duct cancer in 11, adeno-
ondary end-points were rates of delayed gastric empting and carcinoma of the ampulla of Vater in 11, and duodenal carcino-
pancreatic fistula, duration of hospital stay and change of nutri- ma in 3. The patient demographics and nutritional parameters
tional index on postoperative days 7, 14, 21, and 90. Postopera- of both groups are shown in Table 1. The preoperative weight
tive weight loss after PD for periampullary carcinoma was 13.5%, loss significantly changed in the EEN group compared to the
and based on the results achieved in a previous study, the aim TPN group. The two groups showed no significant differences
of this study was to reduce this weight loss rate by 50% in the
group receiving the EEN (13). Based on this, a sample size of 40 Table 1. Clinical and preoperative nutritional parameters
(20 in each group) was necessary to show this difference at a 5%
EEN group TPN group
significance with a power of 80%, allowing for a drop out rate of Parameters P value
(n = 18) (n = 20)
10%. Sex 0.194
Male 7 12
Statistical analysis Female 11 8
Age (yr) 62.7 ± 10.3 61.3 ± 13.2 0.272
Continuous variables are expressed as mean ± standard devia-
Co-morbid disease 0.335
tion (SD). Differences in variables between groups were tested Yes 5 3
using Student’s t-test, chi-square test, or Fisher’s exact test. How- No 13 17
ever, nonparametric tests (Kruskal-Wallis or Mann-Whitney Weight (kg) 63.6 ± 9.2 62.7 ± 8.5 0.732
Weight loss (kg) 3.1 ± 3.6 1.9 ± 1.4 0.009
test) were used for variables with skewed distributions. P values
BMI (kg/m2 ) 23.8 ± 3.9 23.5 ± 2.1 0.390
less than 0.05 were considered statistically significant. Total protein (g/dL) 6.9 ± 0.6 7.1 ± 0.5 0.298
Albumin (g/dL) 3.8 ± 0.5 4.0 ± 0.4 0.110
Ethics statement Prealbumin (mg/L) 240.0 ± 81.1 266.7 ± 69.5 0.800
The protocol of this was approved by the institutional review Transferrin (g/L) 2.3 ± 0.4 2.3 ± 3.7 0.729
PG-SGA (score) 5.3 ± 3.5 4.3 ± 2.5 0.274
PG-SGA 0.566
A 14 17
Assessed for total 40 patients B 4 3
Pathologic origin 0.111
Pancreas cancer 9 5
Periamupllary cancer 9 15
Randomization
Operation procedure 0.544
PD 3 2
Pylorus preserving PD 15 18
EEN group (N = 20) TPN group (N = 20) Major vessel resection 0.911
Yes 2 2
No 16 18
2 patients dropout : tube self removal
Operation time (min) 333.1 ± 95.0 268.0 ± 40.4 0.110
Blood loss (mL) 858.3 ± 270.2 627.5 ± 319.1 0.935
EEN group (N = 18) TPN group (N = 20) EEN, Early Enteral Nutrition; TPN, Total Pareneteral Nutrition; PD, Pancreaticoduode-
nectomy; BMI, Body mass Index; PG-SGA, Patient Generated Subjective Global Assess-
Fig. 2. Trial profile. ment.

http://dx.doi.org/10.3346/jkms.2012.27.3.261 http://jkms.org   263

 Park JS, et al.  •  Early Enetral Nutrition in Pancreaticoduoencetomy

in age, sex, comorbidity, operative blood loss and preoperative (33.3%) grade C. Chyle abdomen developed in one patient in
nutritional index. each group, which was resolved after temporary reduction of
enteral nutrition and oral feeding.
Postoperative course
The first day of bowel movement and the time to take a soft diet Side Effects of Early Enteral Nutrition
was significantly shorter in EEN group than in TPN group. Hospi- There were no aspiration episodes or enteral feeding associated
tal stay was shorter in the EEN group without significance (Table intestinal ischemia. Enteral nutrition was relatively well tolera-
2). There were no cases of hospital mortality. Details of compli- ble to the patients. In EEN group, 4 of 18 patients developed side
cations are shown in Table 2. Overall, 13 of 38 patients (34.2%) effects for enteral nutrition. For instance, one patient had diar-
had postoperative complications, and the complication rates of rhea, one had an abdominal distention, one had a sore throat,
two groups were similar to each other. Pancreatic fistula and de- and one had nausea and vomiting. All side effects were relieved
layed gastric emptying were the most common complications with a conservative management and a temporary reduction of
in this study. the amount of enteral nutrition.
  Overall, 3 of 38 patients developed pancreatic fistula as de-
fined by the ISGPF criteria (13) and the overall incidence was Postoperative Nutritional Index
7.9%. Two (66.7%) patients had grade A, and the other (33.3%) All nutritional parameters decreased until POD 7 and increased
grade C. Pancreatic fistula grade C occurred in the EEN group gradually thereafter.
and was resolved after reinsertion of percutaneous drainage.   The level of serum albumin, and total protein decreased, and
  Overall, 3 of 38 patients developed delayed gastric emptying PG-SGA in the early postoperative days and gradually increased
(DGE) as defined by the ISGPS criteria (14) and the overall inci- in the late postoperative days, but there was no significant dif-
dence was 7.9%. Two (66.7%) patients had grade A, and one ference between two groups (Table 3). In the EEN group, body
weight gradually decreased until POD 14, but rapidly recovered
Table 2. Postoperative course
on POD 21. In contrast, body weight gradually decreased until
EEN group TPN group POD 90 in TPN group (P = 0.005). The rapid turnover proteins
Clinical findings P value
(n = 18) (n = 20)
such as prealbumin and transferrin were more significantly re-
Postoperative Energy requirement 1393.6 ± 192.7 1425.6 ± 218.7 0.646
(kcal/kg) duced on POD 7 and slowly recovered until POD 90 in the TPN
First day of bowel movement (day) 2.7 ± 0.4 5.2 ± 1.2 0.041 group than in the EEN group (Fig. 3).
First day of soft diet (day) 7.2 ± 2.4 7.9 ± 3.9 0.020
Duration of artificial nutrition 5.7 ± 2.7 6.7 ± 4.4 0.365 DISCUSSION
Hospital stays (days) 23.2 ± 12.5 25.3 ± 10.0 0.991
Postoperative complications
Pancreaticojejunostomy leak 2 1 0.485 Traditionally, feeding for patients after gastrointestinal surgery
Delayed Gastric Emptying 2 1 0.485 started when flatus or defecation indicated the return of bowel
Chyle abdomen 1 1 0.939
function. However, in recent years, early enteral nutrition in gas-
Wound infection 2 1 0.485
Postoperative bleeding 0 1 0.336 trointestinal surgery should be recommended whenever possi-
Intraabdominal fluid collection 0 1 0.336 ble. The benefits of EEN have been demonstrated to be more
EEN, Early Enteral Nutrition; TPN, Total Pareneteral Nutrition. physiological, better preventive in morphologic and functional

Table 3. Prealblumin, total protein, BMI and PG-SGA (score) data preoperative and on postoperative days at 7, 14, 21, and 90 for patients given Early Enteral Nutrition (EEN)
versus Total Parenteral Nutrition (TPN). Values are Mean (± standard deviation)
Variables Pre Op POD 7 POD 14 POD 21 POD 90
Total protein (g/dL)*
EEN 6.9 ± 0.6 5.8 ± 0.3 6.6 ± 0.8 7.0 ± 0.7 7.5 ± 0.4
TPN 7.1 ± 0.5 5.5 ± 0.6 6.4 ± 0.4 6.9 ± 0.6 7.5 ± 0.2
Albumin (g/dL)*
EEN 3.8 ± 0.5 3.2 ± 0.4 3.5 ± 0.4 3.7 ± 0.4 4.1 ± 0.3
TPN 4.0 ± 0.4 3.3 ± 0.3 3.5 ± 0.3 3.7 ± 0.4 4.1 ± 0.4
BMI (kg/m2 )†
EEN 23.8 ± 3.9 23.6 ± 3.9 22.9 ± 4.0 23.7 ± 5.1 24.3 ± 4.9
TPN 23.5 ± 2.1 23.3 ± 2.2 22.4 ± 2.1 21.8 ± 2.1 21.4 ± 1.8
PG-SGA (score)*
EEN 5.3 ± 3.9 7.7 ± 3.0 4.3 ± 2.1 3.2 ± 2.9
TPN 4.3 ± 2.5 8.1 ± 3.1 5.1 ± 3.4 3.4 ± 2.7
*There was no significant difference between the EEN and TPN Group at any time point; †BMI was significantly recovered on postoperative day 21 in EEN group compared to
TPN group (P = 0.005). POD, Postoperative day.

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Park JS, et al.  •  Early Enetral Nutrition in Pancreaticoduoencetomy

EEN Group TPN Group EEN Group TPN Group

400 3.5
350 3
Mean prealbumin (mg/L)

Mean transferrin (g/L)

300
2.5
250
2
200
1.5
150
1
100
50 0.5

0 0
Pre OP POD 7 POD 14 POD 21 POD 90 Pre OP POD 7 POD 14 POD 21 POD 90

Fig. 3. Mean prealbumin and transferring levels on preoperative day and on days 7, 14, 21, and 90 postoperatively *. Error bars: 95% confidence interval. *There was signifi-
cant difference between the EEN and TPN Group at any time point of postoperative days.

alteration of the gut system, and less expensive than TPN (15-17). In the present study, nasojejunal feeding tube was used for all
  Pancreatic leakage is one of the leading postoperative com- EEN patients, and jejunostomy tube was not used according to
plications after PD, and it can lead to prolonged hospital stay, our department policy. That is because any unnecessary enter-
increased costs and mortality. Consequently, pancreatic sur- otomy was a potential source of complications. There were no
geons often prefer postoperative TPN because of the greater risk catheter related major complications in the EEN group except
of pancreatic leakage. However, several reports have suggested for accidentally dislodged nasojejunal tube. In our experience,
that there is no marked difference in pancreatic leakage between tube occlusion can be prevented by irrigating it with 20 mL water
EEN and TPN groups (11, 18). Our study is consistent with pre- every 8 hr and after giving medications. The accidentally dis-
vious reports that EEN is not a significant factor for pancreatic lodgement of nasojejunal tube was the most common phenom-
leakage. enon, and special education and attention must be paid to firm
  In contrast to the report of Martignoni et al. (11), there were nasal fixation. We think that a nasojejunal tube is an effective
no significant differences in the occurrence of delayed gastric tool for providing enteral feeding after PD.
emptying between the EEN and TPN groups. The main differ-   In our study, EEN related adverse effect occurred in 22.2%
ence between the report of Martignoni et al and the present study and were resolved by reduction or temporary interruption of
was the cyclic infusion of enteral nutrition. Certainly, the cyclic infusion. All patients in EEN group reached the nutritional goal
enteral nutrition has advantages for patients over continuous without having difficulty by following the infusion protocol. This
enteral nutrition because it is closer to the natural form of en- may be attributed to the fact that our protocol started at a slow
teral nutrition (19). Our results demonstrate that EEN does not flow rate with careful and progressive increase in the feeding
increase the incidence of delayed gastric emptying after PD. volume. Also, this can prevent abdominal distension caused by
Moreover, EEN promotes faster recovery of bowel peristalsis by reaching the nutritional goal too aggressively and early (24).
reducing time to recanalize for passing gas and feces.   In usual practice, the parenteral nutrition begins at goal rates,
  Our results are not consistent with the findings of Brennan et whereas the enteral feedings advance to goal rate over several
al. (9), who suggested that TPN was associated with increased days. Although the level of rapid turnover proteins such as pre-
infectious complications. The main difference between the re- albumin and transferrin dropped in all the patients after the op-
port of Brennan et al. and this study was caloric load. They pro- eration, it was recovered significantly fast in the EEN group in
vided high calories at a rate of 30-35 kcal/day, which is consid- the early postoperative period. These results indicate that EEN
ered relative overfeeding today, and this overfeeding may in- modulates a metabolic response, favoring the synthesis of pro-
crease postoperative complications when compared with per- teins.
missive underfeeding (20). However, a routine use of TPN does   It has been shown that patients can maintain a normal body
not seem to provide any benefit because the high rate of glucose weight after surgery, but it is frequently less than their preoper-
intolerance observed in TPN patients. ative body weight (25-27). Kozuscheck et al. (28) reported that
  There are several methods to deliver enteral nutrition after PD. 85% of patients who had undergone PPPD reached the preop-
Nasojejunal tube provides a cost effective and desirable method erative body weight one year after surgery. However, in the pres-
of enteral nutrition without the morbidity from an additional ent study, preoperative body weight restored in 3 weeks in the
enterotomy (21). However, the frequency of nasojejunal tube EEN group, and recovery of weight 3 weeks after the operation
dislodgement and occlusion was as high as 35% to 100% (22, 23). was significantly better in the EEN patients than in the TPN pa-

http://dx.doi.org/10.3346/jkms.2012.27.3.261 http://jkms.org   265

 Park JS, et al.  •  Early Enetral Nutrition in Pancreaticoduoencetomy

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