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Journal of the Chinese Medical Association 75 (2012) 459e463


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Original Article

Combined enteral feeding and total parenteral nutritional support improves


outcome in surgical intensive care unit patients
Min-Hui Hsu a, Ying-E. Yu b, Yueh-Miao Tsai b, Hui-Chen Lee c, Ying-Che Huang d,
Han-Shui Hsu a,b,e,*
a
Institute of Emergency and Critical Care Medicine, National Yang-Ming University School of Medicine, Taipei, Taiwan, ROC
b
Total Parenteral Nutrition Team, Taipei Veterans General Hospital, Taipei, Taiwan, ROC
c
Division of Experimental Surgery, Department of Surgery, Taipei Veterans General Hospital, Taipei, Taiwan, ROC
d
Department of Anesthesiology and Critical Care, Taipei Veterans General Hospital, Taipei, Taiwan, ROC
e
Division of Thoracic Surgery, Department of Surgery, Taipei Veterans General Hospital, Taipei, Taiwan, ROC
Received November 30, 2011; accepted March 7, 2012

Abstract

Background: For intensive care unit (ICU) patients with gastrointestinal dysfunction and in need of total parenteral nutrition (TPN) support, the
benefit of additional enteral feeding is not clear. This study aimed to investigate whether combined TPN with enteral feeding is associated with
better outcomes in surgical intensive care unit (SICU) patients.
Methods: Clinical data of 88 patients in SICU were retrospectively collected. Variables used for analysis included route and percentage of
nutritional support, total caloric intake, age, gender, body weight, body mass index, admission diagnosis, surgical procedure, Acute Physiology
and Chronic Health Evaluation (APACHE) II score, comorbidities, length of hospital stay, postoperative complications, blood glucose values and
hospital mortality.
Results: Wound dehiscence and central catheter infection were observed more frequently in the group of patients receiving TPN calories less
than 90% of total calorie intake ( p ¼ 0.004 and 0.043, respectively). APACHE II scores were higher in nonsurvivors than in survivors
( p ¼ 0.001). More nonsurvivors received TPN calories exceeding 90% of total calorie intake and were in need of dialysis during ICU admission
( p ¼ 0.005 and 0.013, respectively). Multivariate analysis revealed that the percentage of TPN calories over total calories and APACHE II scores
were independent predictors of ICU mortality in patients receiving supplementary TPN after surgery.
Conclusion: In SICU patients receiving TPN, patients who could be fed enterally more than 10% of total calories had better clinical outcomes
than patients receiving less than 10% of total calorie intake from enteral feeding. Enteral feeding should be given whenever possible in severely
ill patients.
Copyright Ó 2012 Elsevier Taiwan LLC and the Chinese Medical Association. All rights reserved.

Keywords: enteral feeding; outcome; total parenteral nutrition

1. Introduction a standard supplement for hospitalized patients who need


aggressive treatment, especially patients in the intensive care
Parenteral nutritional support, since its introduction by unit (ICU). In these patients, the postoperative hypermetabolic
Dudrick et al1 in the late 1960s, has been considered state may lead to an increased energy expenditure and
impaired wound healing, and may result in organ dys-
function.1e4 Although the preferred route of providing nutri-
* Corresponding author. Dr. Han-Shui Hsu, Division of Thoracic Surgery,
Department of Surgery, Taipei Veterans General Hospital, 201, Section 2,
tional support to these patients is enteral, most of the time,
Shih-Pai Road, Taipei 112, Taiwan, ROC. enteral nutrition (EN) alone is not able to meet the energy
E-mail address: hsuhs@vghtpe.gov.tw (H.-S. Hsu). needs of these patients because of gastrointestinal intolerance,

1726-4901/$ - see front matter Copyright Ó 2012 Elsevier Taiwan LLC and the Chinese Medical Association. All rights reserved.
http://dx.doi.org/10.1016/j.jcma.2012.06.017
460 M.-H. Hsu et al. / Journal of the Chinese Medical Association 75 (2012) 459e463

which induces protein-energy malnutrition and poorer clinical intake (appropriate TPN and EN received), age, gender, body
outcomes.5e8 Combined supplemental parenteral nutrition and weight, body mass index (BMI), basal energy expenditure,
enteral feeding was able to meet the energy and protein targets admission diagnosis, surgical procedure, Acute Physiology
when enteral feeding alone failed to achieve the caloric goal and Chronic Health Evaluation (APACHE) II score, comor-
recommended in some studies.9e13 Many patients in the ICU bidities (hypertension, diabetes mellitus, cardiovascular
experience malnutrition due to gastrointestinal dysfunction, disease, chronic obstructive pulmonary disease, chronic
which results from severe infection or postoperative compli- kidney disease), TPN indication, central venous catheter
cations. At admission, these patients are usually in need of insertion days, length of hospital stay, length of stay in ICU,
total parenteral nutrition (TPN).4,14 However, TPN has been length of ventilation, length of TPN supplied, postoperative
reported to be associated with hyperglycemia, development of complications, blood glucose values, and hospital mortality.
mucosal atrophy and a loss of epithelial carrier function,
impaired immune system, and increased risk of infection in
2.1. Statistical analysis
critical illness.15e19 Some authors have suggested that,
regardless of the route and formula of nutrition given,
Statistical analysis was performed with SPSS 16.0 (SPSS
supplying adequate nutrition is important in severely ill
Inc., Chicago, IL, USA). Data are presented as means and
patients.20e23 De Jonghe et al21 pointed out that physicians
standard deviation, and categorical variables as percentages.
need to pay more attention to providing appropriate nutritional
Student’s t test and chi-square test were used to compare
support for critical illness, and that inadequate delivery of EN
continuous variables and proportions. Clinical factors related
and a low rate of nutrition prescription resulted in low caloric
to hospital mortality were analyzed in a multivariate regres-
intake in ICU patients. Recently, Klek et al,23 in their study
sion model. A p value <0.05 was considered statistically
investigating a group of 167 malnourished surgical patients,
significant.
concluded that postoperative nutritional intervention generated
comparable results regardless of the route of the formula used.
For ICU patients with gastrointestinal dysfunction and in need 3. Results
of TPN for nutritional support, the benefit of additional enteral
feeding is not clear. The aim of this study was to investigate Table 1 shows the demographic data of 88 patients in the
whether combined TPN with enteral feeding is associated with SICU. More patients had comorbidities including cardiovas-
better outcomes in surgical intensive care unit (SICU) patients. cular disease and chronic renal disease in the group of patients
receiving TPN calories exceeding 90% of total calories given
2. Methods ( p ¼ 0.035). No significant differences were found in nutri-
tional parameters, including body weight, BMI, and serum
The clinical data of 88 patients who were admitted to the albumin, between groups. Moreover, the mean blood glucose
SICU in Taipei Veterans General Hospital from January 2007 levels were not different between groups during the period in
to December 2009 requiring TPN supply in the postoperative which TPN was given. Patients receiving TPN calories
period were retrospectively reviewed. The ethics committee of exceeding 90% of total calories had lower total calorie intake
the Taipei Veteran General Hospital approved this study. The than did patients receiving TPN calories less than 90% of total
type of nutrition (enteral or parenteral) and the amount of calories given ( p < 0.005). The postoperative complications
nutrient calories prescribed for each patient were recorded. are shown in Table 2. The most common complications
TPN supplement was given if the patient could not tolerate EN encountered in these patients were septic shock and pneu-
due to gastrointestinal dysfunction or complications for more monia. Wound dehiscence and central catheter infection were
than 7 days or if 60% of the caloric requirements could not be observed more frequently in the group of patients receiving
achieved via the enteral route. EN was allowed to be given to TPN calories less than 90% of total calorie intake ( p ¼ 0.004
the patients when possible if the patients were able to tolerate and 0.043, respectively). More patients (56.5%) receiving TPN
it. The total calories of TPN were determined by using the calories more than 90% of total calorie intake developed renal
HarriseBenedict equation,21 consisting of 50% dextrose failure during their stay in the ICU compared with patients
associated with 10% amino acid (moriamine-SN) and 20% fat receiving TPN calories less than 90% of total calorie intake.
emulsion (lipovenous or SMOF lipid). Additional fluids, The results of comparison between survivors and nonsurvivors
electrolytes, vitamins, and trace elements were provided as are shown in Table 3. The hospital stay was longer among
clinically indicated. Parenteral nutrition was infused via survivors. The APACHE II scores were higher in nonsurvivors
a central venous catheter. The 88 patients were divided into than in survivors ( p ¼ 0.001). More nonsurvivors received
two groups according to the percentage of TPN calories to be TPN calories more than 90% of total calorie intake and were
received over the patients’ total daily calories. Forty-two in need of dialysis during admission to ICU than survivors
patients received TPN as 60% to 90% of total calories, and ( p ¼ 0.005 and 0.013, respectively). Multivariate analysis
46 patients had TPN supplement of more than 90% of total revealed that the percentage of TPN calories over total daily
calories. Demographic data and clinical outcomes of these calories and APACHE II scores were independent predictors
patients were collected by chart review, including the route of of ICU mortality in patients receiving TPN supplement after
nutritional support (enteral, parenteral, or both), daily caloric surgery (Table 4).
M.-H. Hsu et al. / Journal of the Chinese Medical Association 75 (2012) 459e463 461

Table 1 Table 2
Demographic data of surgical patients receiving TPN in ICU (n ¼ 88). Comparison of postoperative complications between groups.
TPN calories TPN calories p TPN calories TPN calories p
&90% >90% &90% >90%
(n ¼ 42) (n ¼ 46) (n ¼ 42) (n ¼ 46)
Age (y) 69.9  15.2 74.5  14.9 0.155 Pneumonia 18 (42.9) 18 (39.1) 0.445
Male (%) 31 (73.8) 35 (76.1) 0.499 Abdominal abscess 15 (35.7) 13 (28.3) 0.301
APACHE II score 23.7  6.3 26.2  5.4 0.062 Bacteremia 8 (19.0) 13 (28.3) 0.223
Fungemia 5 (11.9) 4 (8.7) 0.441
Admission diagnosis (%)
Septic shock 17 (44.7) 25 (59.5) 0.136
Cancer (all sites)
ARDS 7 (16.7) 2 (4.3) 0.059
Rectum cancer 5 (11.9) 0 (0.0) 0.022
Wound dehiscence 7 (16.7) 0 (0.0)* 0.004
Pancreas cancer 4 (9.5) 1 (2.2) 0.153
Pancreatitis 3 (7.1) 7 (15.2) 0.197
Stomach cancer 1 (2.4) 4 (8.7) 0.210
Renal failure 14 (33.3) 26 (56.5)* 0.024
Colon cancer 1 (2.4) 4 (8.7) 0.210
Hepatic failure 2 (4.8) 4 (8.7) 0.383
Nonmalignant Wound infections 10 (23.8) 14 (30.4) 0.324
Peptic ulcer 5 (11.9) 3 (6.5) 0.307 UTI 9 (21.4) 13 (28.3) 0.312
Intestinal obstruction 2 (4.8) 2 (4.3) 0.657 CVC tip infections 15 (35.7) 8 (17.4)* 0.043
Acute pancreatitis 6 (14.3) 3 (6.5) 0.199 Intra-abdominal infections 5 (11.9) 4 (8.7) 0.441
UGI bleeding 1 (2.4) 4 (8.7) 0.210 ARDS ¼ acute respiratory distress syndrome; CVC ¼ central venous catheter;
Comorbid conditions (%) UTI ¼ urinary tract infections.
Hypertension 22 (52.4) 25 (54.3) 0.512 * p < 0.05.
DM 10 (23.8) 15 (32.6) 0.250
Cardiovascular disease 2 (4.8) 9 (19.6)* 0.035 enteral feeding had a remarkably high mortality. Elke et al,25
COPD 5 (11.9) 1 (2.2) 0.082
in their observational study enrolling 415 patients concluded
Chronic kidney disease 2 (4.8) 9 (19.6)* 0.035
that the use of parenteral nutrition was associated with an
Nutritional parameters increased risk of death and that EN should be provided even
Body weight (kg) 62.7  12.8 63.8  12.0 0.697
for the most severely ill patients. In an animal study, Omata
2
BMI (kg/m ), (%) and colleagues26 found that EN could reverse TPN-induced
0e18.5 6 (18.2) 7 (18.4) 0.752
impairment of hepatic immunity. They suggested that enteral
18.5e24 14 (42.4) 13 (34.2)
>24 13 (39,4) 18 (47.4) feeding should be given to induce recovery of hepatic
Serum albumin (g/dL) 2.3  0.3 2.3  0.4 0.449 immunity and reduce infectious complications.
Serum blood glucose (mg/dL) 166.7  34.6 168.4  51.7 0.859 One of the most common complications during parenteral
TPN calories (kcal/d) 1486.0  228.9 1564.0  206.9 0.097 nutritional support is catheter and bloodstream infection.17,18,
Total calories intake (kcal/d) 1825.7  250.5 1682.2  219.2 0.005 27,28
Increased parenteral caloric intake is also an indepen-
Data are presented as n or means  SD. APACHE ¼ Acute Physiology and dent risk factor for bloodstream infection in patients receiving
Chronic Health Evaluation, BMI ¼ body mass index; COPD ¼ chronic
TPN.18 Recently, in a randomized and multicenter trial
obstructive pulmonary disease; DM ¼ diabetes mellitus, PPU ¼ perforated
peptic ulcer; TPN ¼ total parenteral nutrition; UGI bleeding ¼ upper enrolling more than 4000 critically ill patients, Casaer et al29
gastrointestinal bleeding. reported that patients receiving early initiation of parenteral
* p < 0.05. nutrition to supplement insufficient EN had increased ICU
infections and higher incidence of cholestasis. Sena et al30
4. Discussion reported that in critically ill trauma patients who were able
to tolerate some EN, early parenteral nutrition administration
ICU patients inevitably experience malnutrition due to poor was associated with increased infectious morbidity and poorer
gastrointestinal function. EN alone usually is not able to fulfill clinical outcomes. The authors pointed out that patients in the
the energy requirements of these patients. However, whether combination EN and PN group might have received more
parenteral nutritional support can improve patients’ outcomes calories, which resulted in the increased infection rate. In our
or just result in more complications in these critically ill study, the patients receiving more calories from enteral
patients is unclear. The predisposing factors related to the feeding also had an increased rate of catheter tip infection in
clinical outcome may include the administration route, the comparison with the patients receiving fewer calories from
number of calories, and the type of nutrients given. In this enteral feeding, although the mean blood glucose values were
study, we investigated the role of EN in surgical patients who not different between groups.
received TPN during admission to the ICU, and subsequently In this study, we observed that patients receiving more
observed better outcomes in patients who could be partially calories from enteral feeding had better outcomes but stayed
fed, even at only 10e40% of total calories, than in patients longer than patients receiving nutrition only from TPN. These
who had nutritional support from parenteral nutrition alone. findings are consistent with those of Elke et al.25 In their study,
Our study again confirmed the importance of EN in critical length of hospital stay was significantly different among the
illness. Dunham et al24 reported that in mechanically venti- nutrition groups, which included groups of exclusively
lated blunt trauma patients, the patients who could not tolerate parenteral nutrition, exclusively EN, and mixed parenteral and
462 M.-H. Hsu et al. / Journal of the Chinese Medical Association 75 (2012) 459e463

Table 3 authors have concluded that negative energy balances are


Comparison of clinical data between survivors and nonsurvivors. correlated with increasing numbers of complications, or that
Variables Survivors Nonsurvivors p infection and higher calorie goals may be necessary to achieve
(n ¼ 31) (n ¼ 57) better outcomes.31e33 In our study, total calorie intake did not
Age (y) 70.5  17.1 73.3  14.0 0.414 affect the outcomes in these patients.
Weight (kg) 60.5  12.3 64.7  1.6 0.127 Our study has limitations because it was a retrospective
BMI (kg/m2) 22.7  4.9 23.8  4.9 0.355
Serum blood 172.3  43.8 165.0  44.5 0.461
study lacking certain detailed information about parenteral and
glucose (g/dL) enteral nutrition, including components of nutrition formula-
Serum CRP (mg/dL) 9.7  6.4 10.7  4.6 0.393 tion used, the competence of gastrointestinal function in each
TPN calories (kcal/d) 1519.6  220.0 1530.7  221.7 0.823 patient, detailed information on drug or antibiotics used during
Total calorie 1797.2  257.1 1725.4  235.3 0.189 ICU admission. Further investigation is warranted to elucidate
intake (kcal/d)
Hospital length of stay (d) 83.5  49.0 42.4  31.9 <0.001
the role of enteral feeding in critically ill patients who have
ICU length of stay (d) 22.9  14.6 24.0  16.6 0.762 moderately impaired gastrointestinal function and are in need
Ventilator duration (d) 33.3  31.4 26.2  19.2 0.265 of parenteral nutritional supplement.
TPN duration (d) 11.7  5.0 13.7  9.7 0.220 In conclusion, our study showed that in patients who sus-
Mean CVC duration (d) 8.1  2.3 9.1  3.3 0.124 tained postoperative complications and were in need of TPN,
Gender those patients who could be fed enterally more than 10% of total
Male 26 (83.9) 40 (70.2) 0.122 calories had better clinical outcomes than patients who received
Female 5 (16.1) 17 (29.8)
less than 10% of total calorie intake from enteral feeding during
APACHE II score hospitalization in the SICU. Enteral feeding should be given
&21 15 (51.7) 7 (14.3) 0.001 whenever possible for these severely ill patients.
>21 14 (48.3) 42 (85.7)
Serum albumin Acknowledgments
(mg/dL), mean
&2.3 15 (48.4) 32 (57.1) 0.287
>2.3 16 (51.6) 24 (42.9) This work was in part supported by the Division of
Experimental Surgery, Department of Surgery, Taipei Veterans
Percentage of TPN
calories/total daily
General Hospital and the Lung Cancer Foundation, in memory
calories of Dr K.S. Lu, Taipei, Taiwan.
&0.9 21 (67.7) 21 (36.8) 0.005
>0.9 10 (32.3) 36 (63.2) References
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