0915 PENXXX10.

1177/01486071
ish Oil Lipid Emulsion on Pancreaticoduodenectomy / Zhu et alJournal
ion

Original Communication

Effect of Parenteral Fish Oil Lipid Emulsion in Parenteral Journal of Parenteral and Enteral
Nutrition
Nutrition Supplementation Combined With Enteral Nutrition Volume 37 Number 2
March 2013 236-242
Support in Patients Undergoing Pancreaticoduodenectomy © 2012 American Society
for Parenteral and Enteral Nutrition
DOI: 10.1177/0148607112450915
jpen.sagepub.com
hosted at
online.sagepub.com
Xinhua Zhu, MD; Yafu Wu, BS; Yudong Qiu, MD; Chunping Jiang, BS;
and Yitao Ding, MSc

Abstract
Background: The effect of parenteral fish oil lipid emulsion in parenteral nutrition (PN) supplementation combined with enteral nutrition
(EN) support on pancreaticoduodenectomy (PD) was investigated with a randomized controlled clinical trial at the Affiliated Drum
Tower Hospital. Materials and Methods: Seventy-six patients who underwent PD in the Department of Hepatobiliary Surgery were
randomly divided into 2 groups: the polyunsaturated fatty acid (PUFA) group (n = 38) and control group (n = 38). Patients in the PUFA
group received parenteral fish oil lipid emulsion supplementation combined with early EN support for 5 days after PD. Venous blood
samples were obtained for assay on the day before surgery and on day 6 after surgery. Results: Compared with the results of the control
group, a significant difference was seen in the extent of the decrease in total protein and prealbumin in the PUFA group (P < .05). Alanine
aminotransferase (ALT), aspartate aminotransferase (AST), and lactate dehydrogenase (LDH) were significantly decreased on day 6 in
the PUFA group (P < .01), and a significant difference was seen in the extent of decrease in ALT, AST, and LDH in the PUFA group (P
< .05). The ratio of infectious complications in the PUFA group was significantly decreased, as well as the postoperative hospital stay (P
< .05), and there was no hospital mortality in this study. Conclusion: Parenteral fish oil lipid emulsion in PN supplementation combined
with EN support can greatly improve the nutrition state and liver function of patients, decrease the incidence of infectious morbidities,
and shorten the postoperative hospital stay. (JPEN J Parenter Enteral Nutr. 2013;37:236-242)

Keywords
fish oil lipid; pancreaticoduodenectomy; nutrition support; metabolism

Clinical Relevancy Statement

The immunomodulation of nutrition support supplemented
with ω-3 fatty acids has been more widely used in elective
gastrointestinal surgery, and the clinical trials on ω-3 fatty
acids in patients receiving pancreaticoduodenectomy (PD) are
scarce. The results of this study have shown that parenteral
fish oil lipid emulsion in parenteral nutrition supplementation
combined with enteral nutrition support can greatly improve
the nutrition state and liver function of patients, decrease the
incidence of infectious morbidities, and shorten the postopera-
tive hospital stay. These findings are clinically relevant for
guiding surgeons in perioperative medications in PD.
Introduction
Patients who are candidates for pancreaticoduodenectomy (PD)
often have associated comorbidities such as diabetes, jaundice,
and protein-energy malnutrition. PD is associated with a high
incidence of postoperative complications, even when the proce-
dure is performed at high-volume centers. The high rate of
complications is likely multifactorial but may include overall
nutrition debilitation in that most patients with periampullary
tumors present with significant weight loss. Postoperative nutri-
tion support therapy may be important in these patients.
Recent studies have shown that early postoperative enteral
nutrition (EN) enhanced immunocompetence, reduced clinical
infection rates, and maintained gut structure and function.
Also, EN is believed to be safer and less expensive than paren-
teral nutrition (PN). However, postoperative total enteral feed-
ing is associated with complications such as diarrhea,
abdominal distention, and abdominal cramps. These symptoms
worsen with increasing caloric intake and finally lead
From Medical School of Nanjing University, Nanjing, China.
Financial disclosure: The authors are grateful for financial support from
the Jiangsu Province Government Foundation (No. ZX200605).
Received for publication March 8, 2012; accepted for publication
May 16, 2012.
This article originally appeared online on June 14, 2012.
Corresponding Author:
Yitao Ding, Department of Hepatobiliary Surgery, Affiliated Drum Tower
Hospital, Medical School of Nanjing University, Zhongshang Rd 321,
Nanjing 210008, China.
Email: drzhuxh@hotmail.com.

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Zhu et al 237

to discontinuance of enteral feeding.1,2 On the basis of our Table 1. Comparison of Fatty Acid Compositions in Parenteral
experience and the findings of previous studies, we believe Lipid Emulsions per 10 g.
that PN combined with early EN support is the optimal nutri- Standard
tion method for patients who received PD. Lipid
ω-3 fatty acids, mainly consisting of eicosapentaenoic acid Emulsion
(EPA) and docosahexaenoic acid (DHA), are essential, poly- Fatty Acid (Control PUFA
unsaturated fatty acids (PUFAs) derived from fish oil. Compositions Group) Omegaven Group
Supplementation with ω-3 fatty acids may downregulate pro- Oil source, %  
inflammatory cytokine production and modulate eicosanoid  Soybean 50 0 40.9
synthesis.3-5 The immunomodulation of nutrition support sup-  Safflower 0 0 0
plemented with ω-3 fatty acids has been proven to be benefi-   Coconut (MCT) 50 0 40.9
cial in reducing postoperative infectious complications and  Olive 0 0 0
length of hospital stay among patients undergoing elective gas-  Fish 0 100 18.2
trointestinal surgery, especially in those who were malnour- Phytosterols, mg/L NP 0 0
ished preoperatively.6,7 Because the clinical trials on ω-3 fatty α-Tocopherol, mg/L 100 150–296 109.1–135.6
acids in patients receiving PD are scarce, we investigated the Fat composition, g  
effect of parenteral fish oil lipid emulsion in PN supplementa-   Palmitic (16:0) 0.55 0.25–1 0.50–0.63
tion combined with EN support on PD with a randomized con-   Stearic (18:0) 0.2 0.05–0.2 0.17–0.18
trolled clinical trial.   Olic (18:1) 1.16 0.6–1.3 1.14–1.27
  Linoleic (18:2) 2.66 0.1–0.7 2.20–2.31
  α-Linolenic (18:3) 0.1 <0.2 <0.12
Patients and Methods   EPA (20:5) 0 1.28–2.82 0.23–0.51
Patients and Randomization   Arachidonic (20:4) 0 0.1–0.4 0.02–0.07
  DHA (22:5) 0 1.44–3.09 0.26–0.56
From January 2006 to December 2010, we prospectively Data as provided by manufacturers. DHA, docosahexaenoic acid; EPA,
investigated 76 patients (51 men and 25 women; mean age, eicosapentaenoic acid; MCT, medium-chain triglyceride; NP, not pro-
52.0 years [range, 38–67 years]) who had undergone PD for vided; PUFA, polyunsaturated fatty acid.
periampullary tumors in the Department of Hepatobiliary
Surgery at the Affiliated Drum Tower Hospital of the
Medical School of Nanjing University, China, where the The primary end point of this study was the occurrence of a
authors work. Patients with manifest metabolic diseases (eg, major complication, and a secondary end point was any com-
diabetes mellitus and hyperthyroidism), severe hemorrhagic plication 30 days after hospital discharge. The Nutrition Risk
disease, ongoing infection, inflammatory bowel diseases, or Screening 2002 (NRS 2002) scoring system was used in this
severe renal abnormality were excluded. The selection crite- study, and the postoperative NRS 2002 scores of all patients
ria for patients in this study included (1) a clinical history, were ≥3, which meant all patients needed nutrition support.
symptoms, signs, and imaging material to define PD indica-
tion; (2) no obvious contraindication for PD; and (3) under-
standing the objective and adverse reactions of the study and
Treatment
completing the fully informed consent. After PD, these PN was given around the clock for 5 days from the first day
patients were randomized into 2 groups based on a random- after PD. Nitrogen intake was 0.25 g/kg body weight/d, caloric
ization chart generated by the Statistical Analysis System intake was 125.4 kJ/kg/d, and lipid intake was 1.1 g/kg/d.
(SAS, Cary, NC). The 2 groups were (1) PN without supple- Nonprotein calories were given as dextrose (5.0 g/kg/d) and
mentation of ω-3 fatty acids combined with early EN support fat emulsion in a ratio of 2:1. The only source of lipids in the
(control group, 38 patients) and (2) PN supplemented with control group was the standard lipid emulsion (20% emulsion,
ω-3 fatty acids combined with early EN support (PUFA 5.5 mL/kg/d, long-chain triglycerides to medium-chain tri-
group, 38 patients). glycerides 1:1; Huarui Pharmaceuticals, Jiangsu, China). In
This was a randomized controlled clinical study carried out the PUFA group, ω-3 fish oil lipid emulsion (Omegaven, 10%,
in the Department of Hepatobiliary Surgery according to the 2 mL/kg/d; Fresenius Kabi AG, Bad Homburg VDH, Germany)
principles and guidelines of the Helsinki Declaration of 1975, replaced part of the standard lipid emulsion. The fatty acid
as revised in 2000. The protocol was approved by the ethics compositions of parenteral regimens given to both groups of
committee of the Affiliated Drum Tower Hospital. Voluntary patients are listed in Table 1. Patients in the control and PUFA
informed consent of the patients was obtained prior to study groups received 1.5 g amino acids/kg/d, administered as a
enrollment. commercially available branched-chain amino acid solution

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238 Journal of Parenteral and Enteral Nutrition 37(2)

Table 2. Ranges and Averages of the Calories, Protein, Fat, and Carbohydrates in the Enteral and Parenteral Regimens.

POD Nutrition Support Calories, kJ Protein, g Fat, g Carbohydrates, g

POD1 PN, average (range) 7649.4 (6081.9–10,282.8) 91.5 (72.8–123.0) 67.1 (53.3–90.2) 305.0 (242.5–410.0)
  EN 83.6 0 0 5
POD2 PN, average (range) 7649.4 (6081.9–10,282.8) 91.5 (72.8–123.0) 67.1 (53.3–90.2) 305.0 (242.5–410.0)
  EN 418 0 0 25
POD3 PN, average (range) 6447.6 (4880.1–9081.0) 84 (65.3–115.5) 59.6 (45.8–82.7) 257.5 (195.0–362.5)
  EN 1201.8 7.5 7.5 47.5
POD4 PN, average (range) 5559.4 (3991.9–8192.8) 76.5 (57.8–108.0) 52.1 (38.3–75.2) 235.0 (172.5–340.0)
  EN 2090 15 15 70
POD5 PN, average (range) 3469.0 (1901.9–6102.8) 61.5 (42.8–93.0) 37.1 (23.3–60.2) 165.0 (102.5–270.0)
  EN 4180 30 30 140
POD6 PN 0 0 0 0
  EN, average (range) 7649.4 (6081.9–10,282.8) 54.9 (43.65–73.8) 54.9 (43.65–73.8) 256.2 (203.7–344.4)

EN, enteral nutrition; PN, parenteral nutrition; POD, postoperative day.

(20%; Huarui Pharmaceuticals). The proportion of nonprotein
calories with nitrogen in both groups was 501.6 kJ/1 g. The
ω-3 fish oil lipid emulsion–containing solutions were prepared
by a clinical pharmacist under aseptic conditions and adjusted
to the weight of each individual patient. The amino acids, fat
emulsion, and dextrose mixture with electrolytes, vitamins,
and trace elements were administered through a central venous
catheter.
All patients had a conventionally placed common gastric
tube preoperatively. When gastrojejunostomy was finished,
anesthesiologists placed the nasojejunal nutrition tubes (10F;
NUTRICIA Pharmaceutical Co, Shanghai, China) from the
nasal cavity to the output loops of the jejunum, about 20–25
cm, with the help of a surgeon. Then the jejunum nutrition tube
filar guide was taken out after adjustment to the proper
position.
The surgical treatment was standardized, and lymph node
dissection was performed according to the definition provided
by Pedrazzoli et al.8 PD was performed by 3 groups of sur-
geons using the same technique. Postoperatively, all the
patients received the same antibiotics.
EN was given around the clock in this study. The infusion
of 100 mL of 5% glucose and sodium chloride injection (GNS)
through a nasojejunal feeding tube commenced within 24
hours after surgery and 500 mL of 5% GNS on postoperative
day (POD) 2. On POD 3, 250 mL of Peptisorb liquid (2092
kJ/500 mL; NUTRICIA Pharmaceutical Co) and 250 mL of
5% GNS were given. Patients received 500 mL of Peptisorb
liquid on POD 4 and 1000 mL of Peptisorb liquid on POD 5.
From POD 3, the recipe of PN was adjusted according to the
amount of EN, and the total caloric intake of PN and EN was
125.4 kJ/kg/d. PN was stopped on POD 6, and all patients in
both groups reached the maximum volume of total caloric
intake by Peptisorb liquid (30 mL/kg/d). Oral intake started on
POD 7, and EN was stopped when the patients tolerated an oral
diet with an oral intake over 1000 kcal/d.
The body weight of the patients in this study varied from
48.5–82.0 kg, with the average of 61.0 kg. On the basis of the
range and average of weight, we listed the ranges and averages
of the calories, protein, fat, and carbohydrates both in the
enteral and parenteral regimens in Table 2.
Assessment
Venous heparin blood samples were obtained on day –1 (the
day before surgery) and day 6 after surgery. Three types of
measurement were carried out. First, we carried out a nutri-
tion-associated assessment, which included serum albumin,
prealbumin (PAB), total protein (TP), transferrin (TF), and
total lymphocyte counts (TLCs). Serum albumin, PAB, TP,
and TF were determined by an automatic biochemistry ana-
lyzer (Hitachi 7600; Hitachi, Tokyo, Japan). TLC was per-
formed by an automatic blood cell analyzer (Coulter STKS;
Coulter, Hialeah, FL). The prognostic nutrition index (PNI)
was calculated as PNI = 0.005 × TLC (106/L) + serum albumin
(g/L). The normal value of PNI was more than 50, and PNI
values <40 indicated malnutrition. Nitrogen balance was cal-
culated as N balance (g N/d) = [protein intake (g/d)/6.25] –
[urinary urea (g/24 h)/2.14 + 3 g (nitrogen lost in skin and
stool per day)]. Second, a liver function assessment was car-
ried out, which included measurements of serum total bilirubin
(TB), direct bilirubin (DB), alanine aminotransferase (ALT),
aspartate aminotransferase (AST), and lactate dehydrogenase
(LDH). Liver function was determined by an automatic bio-
chemistry analyzer (Hitachi 7600). Finally, the assessment of
clinical outcome was based on postoperative investigations on
complications. Postoperative complications were graded
according to the Clavien-Dindo classification,9 which was
validated in pancreatic surgery.10 Complications graded as
III–V were considered major. Pancreatic fistula was defined
according to the International Study Group on Pancreatic
Fistula criteria.11 Operative mortality was defined as in-hospital

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Zhu et al 239

death or death occurring within 30 days after discharge. Table 3. Preoperative Clinical Data, Intraoperative Factors, and
Follow-up for infectious and noninfectious complications Histopathology for Patients Enrolled in the Study.
was carried out for 30 days after hospital discharge. Group Control Group PUFA Group
Readmission within 30 days after discharge was also
recorded.12 Sex, M/F, No. 26/12 25/13
Age, y, mean ± SD 51.9 ± 9.3 53.1 ± 8.6
Patients with jaundice, % 78.9 84.2
Statistical Analysis Patients with preoperative 52.6 47.3
ENBD, %
Results are expressed as mean ± SD. The statistical signifi-
Preoperative hemoglobin, 11.6 ± 0.8 12.2 ± 0.6
cance of the data was determined by Student t tests or χ2 tests. g/L, mean ± SD
Statistical calculation was performed with SAS. A P value of Preoperative serum 38.2 ± 3.1 37.1 ± 4.6
<.05 was considered significant. albumin, g/L, mean ± SD
Duration of surgery, min, 324.2 ± 62.7 336.9 ± 52.2
mean ± SD
Results Operative blood loss, mL, 637.5 ± 238.6 686.1 ± 189.3
A total of 76 patients were enrolled in the study, including 38 mean ± SD
patients in the control group and 38 patients in the PUFA Blood transfusion, % 26.3 31.6
group. The mean age of the patients was 52.0 years (range, Histopathologic finding,  
38–67 years). Demographic and preoperative clinical data, No.
  Pancreatic head 10 12
including age, sex, preoperative hemoglobin, preoperative
carcinoma
serum albumin, and the ratio of patients with jaundice or pre-
 Distal 14 11
operative endoscopic nasal biliary drainage (ENBD), are sum- cholangiocarcinoma
marized in Table 3. With respect to intraoperative factors,  Periampullary 12 14
including operation time, blood loss, number of patients who adenocarcinoma
received a blood transfusion, and histopathological diagnosis,  Duodenal 2 1
there were no significant differences between the 2 groups in adenocarcinoma
any of these parameters (P > .05).
ENBD, endoscopic nasal biliary drainage; F, female; M, male; PUFA,
polyunsaturated fatty acid.
Nutrition-Associated Assessment
No significant difference in preoperative nutrition-associated AST, and LDH in the PUFA group (P < .05). Also, no signifi-
assessment was seen between the 2 groups. Compared with the cant difference in TB and DB was seen between the 2 groups
results on the day before PD, a decrease in TP, PAB, TF, and (P > .05; Table 5).
PNI was observed on day 6 in all patients in this study, as well
as a significant decrease in TP and PAB in the control group
(P < .05), with no significant difference (P > .05) in the PUFA
Clinical Outcome
group (Table 4). A prognostic score for major morbidity after PD recently has
Compared with the results of the control group, a signifi- been proposed by Braga et al.12 We have listed the predictive
cant difference was seen in the extent of decrease in TP and risk score of major complications after PD in 2 groups (Table 6).
PAB (P < .05) in the PUFA group. However, no significant There were no significant differences between the 2 groups in
difference of TF and PNI was seen between the 2 groups (P > the score categorized in 4 risk classes (P > .05).
.05). Nitrogen balance was negative in both groups on day 6, Table 7 reports postoperative outcome in the 2 groups.
and there was no significant difference between the 2 groups Reoperation was necessary in 3 patients, and the causes of
(Table 4). reoperation were early bleeding (1 case in the PUFA group),
late bleeding (1 case in the control group), and abdominal
abscess (1 case in the control group). Two patients with intes-
Liver Function Assessment tinal obstruction were readmitted in this study. The rate of
No significant difference in preoperative liver function assess- grade I complications and postoperative hospital stay in the
ment was seen between the 2 groups. Compared with the PUFA group was significantly decreased (P < .05), and there
results on the day before surgery, a significant decrease in was no hospital mortality in our study (Table 7).
ALT, AST, TB, DB, and LDH was observed on day 6 in both Postoperative complications in detail are reported in Table 8.
groups (P < .05), as well as a very significant decrease in ALT, Twenty-two patients in the control group (4 cases of pneumo-
AST, and LDH in the PUFA group (P < .01). nia, 4 cases of abdominal abscess, 3 cases of bile leak, 1 case
Compared with the results of the control group, a signifi- of pancreatic fistula, 2 cases of cholangitis, 5 cases of wound
cant difference was seen in the extent of the decrease in ALT, infection, and 3 cases of urinary tract infection) and 14

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240 Journal of Parenteral and Enteral Nutrition 37(2)

Table 4. Comparison of Nutrition-Associated Assessment in the 2 Groups.

Decrease (Day –1
Normal Value Group Day –1 Day 6 to Day 6)
TP, g/L 62–85 Control group 64.86 ± 6.52 60.52 ± 7.24a 4.34 ± 1.87
  PUFA group 63.36 ± 7.02 62.31 ± 7.41 1.05 ± 0.46b
PAB, mg/L 0–800 Control group 194.15 ± 54.24 125.64 ± 61.49a 68.51 ± 27.41
  PUFA group 191.24 ± 61.68 162.15 ± 51.16 29.09 ± 12.28b
TF, g/L 2.2–12 Control group 2.62 ± 0.89 2.27 ± 0.59 0.35 ± 0.73
  PUFA group 2.49 ± 0.72 2.20 ± 0.68 0.29 ± 0.81
PNI >50 Control group 49.81 ± 8.37 43.28 ± 7.82 5.53 ± 8.31
  PUFA group 51.47 ± 6.22 44.82 ± 8.15 6.65 ± 5.73
Nitrogen balance, g/d Control group –(23.91 ± 14.17)  
  PUFA group –(25.62 ± 12.83)  

PAB, prealbumin; PNI, prognostic nutrition index; PUFA, polyunsaturated fatty acid; TP, total protein; TF, transferrin.
a
Signifies the results on day 6 are significantly different from the results on day –1 (P < .05).
b
Signifies the PUFA group is significantly different from the control group (P < .05).

Table 5. Comparison of Liver Function in the 2 Groups.

Decrease (Day 6
Normal Value Group Day –1 Day 6 to Day –1)
ALT, µ/L 5–40 Control group 142.4 ± 43.2 96.6 ± 39.5a 45.8 ± 21.6
  PUFA group 135.2 ± 36.4 67.4 ± 24.9b 67.8 ± 26.2c
AST, µ/L 8–40 Control group 102.5 ± 31.2 64.2 ± 38.6a 38.3 ± 16.4
  PUFA group 95.4 ± 36.3 40.3 ± 26.6b 55.1 ± 29.1c
TB, µmol/L 5–20.5 Control group 108.4 ± 28.6 47.3 ± 27.5a 61.1 ± 25.2
  PUFA group 116.7 ± 30.1 51.6 ± 24.2a 65.1 ± 28.5
DB, µmol/L 1.7–6.8 Control group 75.4 ± 26.5 30.4 ± 24.9a 45.0 ± 23.8
  PUFA group 81.7 ± 35.6 32.5 ± 26.8a 49.2 ± 28.1
LDH, µ/L 109–245 Control group 357.8 ± 78.6 274.5 ± 92.4a 83.3 ± 53.1
  PUFA group 316.4 ± 85.2 183.6 ± 70.1b 132.8 ± 74.8c

ALT, alanine aminotransferase; AST, aspartate aminotransferase; DB, direct bilirubin; LDH, lactate dehydrogenase; PUFA, polyunsaturated fatty acid;
TB, total bilirubin.
a
Signifies the results on day 6 are significantly different from the results on day –1 (P < .05).
b
Signifies the results on day 6 are very significantly different from the results on day -1 (P < .01).
c
Signifies the PUFA group is significantly different from the control group (P < .05).

patients in the PUFA group (2 cases of pneumonia, 2 cases of
abdominal abscess, 2 cases of bile leak, 1 case of pancreatic
fistula, 1 cases of cholangitis, 4 cases of wound infection, and
2 cases of urinary tract infection) had infectious complica-
tions. Compared with the result of the control group (57.9%),
the ratio of infectious complications in the PUFA group
(36.8%) was significantly decreased (P < .05). Fifteen
patients in the control group and 14 patients in the PUFA
group had enteral feeding–related complications. No signifi-
cant difference in the ratio of delayed gastric emptying and
hyperglycemia was seen between the 2 groups.
Discussion
PD is associated with a high incidence of postoperative compli-
cations, and an overall morbidity rate of 48% can be anticipated
at major centers.13 The high rate of complications is likely mul-
tifactorial but may include overall nutrition debilitation in that
most patients with periampullary tumors present with a signifi-
cant weight loss due to anorexia and malabsorption and are
expected to have a period of inadequate oral intake for up to 10
days after surgery.14 Perioperative nutrition support can be ben-
eficial in these patients in that it may reduce mortality and
morbidity, as well as the length of hospital stay. A decrease in
nutrition-associated assessment and a negative nitrogen balance
were observed after surgery in all patients in this study, as well
as a significant decrease in TP and PAB in the control group
with no significant difference in the PUFA group.
Early enteral feeding has been shown to decrease postop-
erative septic complications in a meta-analysis of 8 prospec-
tive randomized trials and improve glucose tolerance, protein
kinetics, and wound healing. Furthermore, EN is safer and less

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Zhu et al 241

Table 6. Predictive Risk Score of Major Complications After Table 8. Postoperative Complications in Detail in the 2 Groups.
Pancreaticoduodenectomy in the 2 Groups.
Complications Control Group PUFA Group
Risk Control PUFA
Predictor Categories Score Group Group Pancreatic fistula 1 (2.6) 1 (2.6)
  Grade A 0 0
Pancreatic texture Hard 0 24 23   Grade B 1 (2.6) 1 (2.6)
  Soft 4 14 15   Grade C 0 0
Pancreatic duct >3 mm 0 28 29 Wound infection 5 (13.2) 4 (10.5)
diameter Abdominal abscess 4 (10.5) 2 (5.3)
  ≤3 mm 1 10 9 Bile leak 3 (7.9) 2 (5.3)
Operative blood loss <700 mL 0 23 21 Cholangitis 2 (5.3) 1 (2.6)
  ≥700 mL 4 15 17 Urinary tract infection 3 (7.9) 2 (5.3)
ASA score I 0 20 18 Pneumonia 4 (10.5) 2 (5.3)
  II 2 16 19 Catheter-related sepsis 0 0
  III 6 2 1 Digestive bleeding 2 (5.3) 1 (2.6)
Score categorized in 0–3 13 (34.2) 14 (36.8) Intraperitoneal bleeding 1 (2.6) 2 (5.3)
4 risk classes
Delayed gastric emptying 3 (7.9) 2 (5.3)
  4–7 13 (34.2) 14 (36.8)
Enteral feeding–related 15 (39.5) 14 (36.8)
  8–11 11 (28.9) 9 (23.7)  complications
  12–15 1 (2.6) 1 (2.6)   Abdominal cramps 3 (7.9) 2 (5.3)
  Abdominal distention 6 (15.8) 5 (13.2)
ASA, American Society of Anesthesiologist; PUFA, polyunsaturated fatty
acid. Data are No. of patients or No. (%).  Diarrhea 4 (10.5) 5 (13.2)
 Vomiting 2 (5.3) 2 (5.3)
Hyperglycemia 4 (10.5) 3 (7.9)
Table 7. Postoperative Outcome in the 2 Groups.
Data are No. (%) of patients. Numbers of single-type complications do
Group Control Group PUFA Group not add up to the number of patients within the 2 groups because of the
possible occurrence of more types of complications in some patients.
Complication grade  
PUFA, polyunsaturated fatty acid.
  No complications 15 (39.5) 17 (44.7)
  Grade I 18 (47.4) 11 (28.9)a
  Grade II 23 (60.5) 21 (55.3) groups had enteral feeding–related complications, including
  Grade IIIa 4 (10.5) 3 (7.9)
diarrhea, abdominal distention, and abdominal cramps. These
  Grade IIIb 2 (5.3) 1 (2.6)
symptoms were alleviated by slowing down the enteral trans-
  Grade IVa 0 0
fusion speed or giving medications, and no patient discontin-
  Grade IVb 0 0
ued enteral feeding or dropped out of the study.
  Grade V (mortality) 0 0
Intravenous infusion of fish oil leads to an incorporation of
Reopeation 2 (5.3) 1 (2.6)
Readmission 1 (2.6) 1 (2.6) ω-3 fatty acids in leukocyte cell membrane phospholipids in
Postoperative hospital 15.3 ± 4.3 13.5 ± 3.8a healthy adults, as well as in different patient groups. A higher
  stay, d, mean ± SD ratio of ω-3 to ω-6 fatty acids in membrane phospholipids is
associated with a reduced production of proinflammatory cyto-
Data are No. (%) of patients unless otherwise indicated. Numbers of kines such as interleukin (IL)–1a, IL-1b, and IL-6, as well as
single-type complications do not add up to the number of patients within
tumor necrosis factor (TNF)–α in response to an inflammatory
the 2 groups because of the possible occurrence of more types of compli-
cations in some patients. PUFA, polyunsaturated fatty acid. stimulus.18-20 Twenty-two patients in the control group and 14
a
Signifies the results for the PUFA group are significantly different from in the PUFA group developed infectious complications, and the
the results for the control group (P < .05). ratio of infectious complications in the PUFA group was sig-
nificantly decreased. The reduced length of postoperative hos-
expensive than PN,15,16 although in the previous studies, pital stay in the PUFA group indicated that the time for complete
EN-associated complications were observed in an unexpect- recovery could be shortened by perioperative fish oil adminis-
edly high proportion of patients who received a standard tration. This may be explained by a lower number of complica-
enteral preparation.17 On the basis of these findings, we con- tions. The possible mechanisms of ω-3 fatty acids include
sidered early EN combined with PN as a better mode of post- downregulation of the inflammatory responses to surgery and
operative nutrition support. In the first 3 days after surgery in immune modulation rather than a sole nutrition effect.20
this study, the amount of EN went up slowly to avoid severe The change of transaminase and bilirubin was the most
gastroenteral complications. Twenty-nine patients in the 2 important index to evaluate the liver function of patients after

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242 Journal of Parenteral and Enteral Nutrition 37(2)
PD. All patients in this study underwent PD to remove biliary
obstruction, so ALT, AST, TB, DB, and LDH were signifi-
cantly reduced. PD as a complicated surgery can cause a severe
stress response in the body, which means PD may cause a rapid
release of reactive oxygen species and activate a variety of
inflammatory cytokines such as TNF-α, IL-6, endothelin, and
prostanoids.21,22 Supplementation with ω-3 fatty acids may
downregulate proinflammatory cytokine production and mod-
ulate eicosanoid synthesis.23 The latter molecules lead to the
production of vasodilators with fewer proinflammatory
responses than their n-6 counterparts. Compared with the
results of the control group, a significant difference was seen in
the extent of the decrease in ALT, AST, and LDH in the PUFA
group. ω-3 fatty acids exhibited liver-protective effects, and
this may be associated with an increase in liver perfusion,
improvement in liver microcirculation, and reduction in the
intestinal inflammatory reaction.21,24
In conclusion, we have shown that parenteral fish oil lipid
emulsion in PN supplementation combined with EN support
can greatly improve nutrition states and liver function of
patients, decrease the incidence of infectious morbidities, and
shorten the postoperative hospital stay after PD.
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