Nutrition in Clinical Practice

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Hypocaloric, High-Protein Nutrition Therapy for Critically Ill Patients With Obesity
Roland N. Dickerson
Nutr Clin Pract 2014 29: 786 originally published online 21 July 2014
DOI: 10.1177/0884533614542439
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research-article2014

NCPXXX10.1177/0884533614542439Nutrition in Clinical PracticeDickerson

Pivotal Paper

Hypocaloric, High-Protein Nutrition Therapy

for Critically Ill Patients With Obesity

Nutrition in Clinical Practice

Volume 29 Number 6
December 2014 786791
2014 American Society
for Parenteral and Enteral Nutrition
DOI: 10.1177/0884533614542439
ncp.sagepub.com
hosted at
online.sagepub.com

Roland N. Dickerson, PharmD, BCNSP1

Abstract
We published the first article that addressed hypocaloric, high-protein enteral nutrition therapy for critically ill patients with obesity more
than 10 years ago. This study demonstrated that it was possible to successfully achieve this mode of therapy with a commercially available
high-protein enteral formula and concurrent use of protein supplements. This study was also the first to demonstrate improved clinical
outcomes with the use of hypocaloric, high-protein nutrition therapy. The results of this study, its unique findings, and shortcomings are
discussed. Subsequent studies have added clarity to the effective use of this therapy, including its use in home parenteral nutrition patients,
patients with class III obesity, and older patients with obesity. (Nutr Clin Pract. 2014;29:786-791)

Keywords
enteral nutrition; obesity; trauma; wound healing; critical illness; nutritional support; parenteral nutrition

In 2002, we published results of a study evaluating the effect

of hypocaloric, high-protein enteral tube feeding on nutrition
and clinical outcomes of critically ill obese trauma patients
(Figure 1).1 This was the first study to demonstrate improved
clinical outcomes with hypocaloric, high-protein nutrition
therapy compared with eucaloric, high-protein nutrition therapy in critically ill obese patients. In addition, it was the first
study to report the technique of implementing this therapy by
the enteral route for obese patients as opposed to previous
studies whereby patients were given parenteral nutrition
(PN). The purpose of this Pivotal Paper review is to discuss
the past, present, and future of hypocaloric, high-protein
nutrition therapy for hospitalized patients with obesity and
how the findings in this study published more than a decade
ago still apply today.

Prevailing Belief System

The practice of most nutrition support practitioners in the
1980s and 1990s was to provide the hospitalized patient with
obesity full hypercaloric nutrition therapy to maximize the
ability for patients to heal their wounds and recover from their
acute illness. At that time, the practice of providing excessive
amounts of calories by todays standards was commonly
accepted but was being challenged by numerous emerging
indirect calorimetry studies for assessing energy expenditure
and requirements of various hospitalized patient populations.
Clinicians did not routinely address the metabolic ramifications of feeding obese hospitalized patients. Obesity was considered a health issue that was to be addressed only after the
patient was discharged from the hospital. Unfortunately, this
doctrine was ingrained in practice for decades without any scientific evidence to support its validity.

Conceptual Framework for Hypocaloric,

High-Protein Nutrition Therapy
Hypocaloric feeding is defined as providing an energy intake
less than measured or estimated energy expenditure, whereas
hypercaloric feeding is providing a caloric intake in excess of
caloric requirements. Eucaloric feeding is intended to provide
an energy intake sufficient to meet caloric demands. A highprotein intake reflects a nitrogen content sufficient to achieve
nitrogen equilibrium or positive nitrogen balance for most
patients. Hypocaloric, high-protein feeding is often mistaken
for hypocaloric feeding or permissive underfeeding. Permissive
underfeeding or hypocaloric feeding allows for both calorie
and protein deficits, whereas the intent of hypocaloric, highprotein nutrition therapy is to provide a caloric deficit while
ensuring adequate or sufficient protein intake.
Shaw et al2 and Kinney3 pioneered the concept that energy
and nitrogen should be considered separately in designing
feeding regimens. This concept was derived from studies that
indicated that the attainment of positive nitrogen balance and
potential restoration of lean body mass could be attained in
protein-malnourished patients without excessive energy intake.
They proposed that excessive energy intake may lead to

From 1University of Tennessee College of Pharmacy, Memphis, Tennessee.

Financial disclosure: None declared.
This article originally appeared online on July 21, 2014.
Corresponding Author:
Roland N. Dickerson, PharmD, BCNSP, University of Tennessee College
of Pharmacy, 881 Madison Avenue, Suite 345, Memphis, TN 38163, USA.
Email: rdickerson@uthsc.edu

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Figure 1. First page of Pivotal Paper as published in Nutrition in 2002. Reprinted from Nutrition, 18(3), Dickerson RN, Boschert KJ,
Kudsk, KA, Brown RO, Hypocaloric enteral tube feeding in critically ill obese patients, 241-246, 2002, with permission from Elsevier.

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Nutrition in Clinical Practice 29(6)

increased deposition of body fat, which may be undesirable for

certain patient populations. The early body composition studies from Hill and Church4 confirmed their assumptions. From
these data, it was envisioned that by providing a low-calorie,
high-protein nutrition regimen, positive nitrogen balance with
lean body mass gain could be achieved while losing body fat
due to a negative caloric deficit. Conversely, a high-calorie,
low-protein regimen sufficient to achieve nitrogen equilibrium
or positive nitrogen balance would likely lead to abundant
body fat gain with minimal or no lean body mass gain. A modest protein and calorie intake sufficient to achieve positive
nitrogen balance or nitrogen equilibrium would likely lead to
minimal changes in lean body mass or body fat.

Previous Studies With Hypocaloric, High

Protein Nutrition Therapy for Acutely Ill
Patients With Obesity
Dickerson et al5 conducted the first study of hypocaloric, highprotein PN therapy in a case series of 13 acutely ill, obese patients.
Most patients required PN due to an anastomotic leak from gastric bypass surgery. Patients were given 881 331 nonprotein
kilocalories as glucose (~50% of measured energy expenditure)
and 2.1 0.6 g/kg ideal body weight (IBW)/d of protein (total
caloric intake ~70% of measured energy expenditure) for 48 31
days (range, 12119 days). Despite an average weight loss of 2.3
2.7 kg/wk, patients achieved net protein anabolism, as evidenced by positive nitrogen balance (NB) or nitrogen equilibrium (mean NB, +2.4 1.9 g/d), and increases in serum protein
concentrations. Respiratory quotient values obtained during the
indirect calorimetry measurement indicated that endogenous net
fat oxidation contributed to 68% 19% of nonprotein energy
expenditure. All patients exhibited complete tissue healing of
wounds, abscess cavities, and closure of fistulae.
This case series was followed by 2 small prospective, randomized controlled trials for the use of hypocaloric, high-protein nutrition therapy for acutely ill surgical patients with
obesity from Burge et al6 and Choban et al.7 Caloric intake for
the first study6 was designed to provide about half of resting
energy expenditure as nonprotein kilocalories for the hypocaloric group (n = 9) compared with 100% of resting energy
expenditure for the eucaloric group (n = 7). Both groups
received 2 g/kg IBW/d of protein. PN was provided for a total
of 8.6 3.0 days. No difference was noted in nitrogen balance
or serum protein concentration changes between groups. In the
second study,7 caloric intake was dosed according to weight
rather than measured resting energy expenditure. About half of
the patients in each group were intensive care unit (ICU)
patients. Thirty obese surgical patients were randomly assigned
to receive either a eucaloric (22 5 kcal/kg actual weight/d or
36 4 kcal/kg IBW/d) or hypocaloric (14 kcal/kg actual
weight/d or 22 3 kcal/kg IBW/d) PN regimen. Protein intakes
were the same for both groups (1.2 0.2 g/kg actual weight/d
or 2.0 0.1 g/kg IBW/d). No difference was noted in NB

between groups (3.6 4.1 g/d vs 4.0 4.2 g/d, respectively),

length of hospital stay, or mortality. However, patients who
received the eucaloric PN regimen tended to require more
insulin (61 61 units/d vs 36 47 units/d) for a greater number
of days (8.0 2.5 days vs 3.2 2.7 days, P < .05). It should be
noted that the reported insulin requirements data would likely
be different today since this study was conducted prior to our
current knowledge regarding the importance of glycemic control for critically ill patients.8,9

Unique Scientific Contribution

Prior to our study, all studies examining the influence of hypocaloric, high-protein nutrition therapy for patients with obesity
were done via PN rather than enteral nutrition (EN). It is more
difficult to provide this mode of therapy by the enteral route
since it requires the inclusion of modular protein supplementation in addition to the fixed macronutrient enteral formula.
This is in contrast to previous studies with PN therapy, whereby
macronutrient components could be easily adjusted in the final
PN admixture. Another difference in our study from the other
works was that our population was comprised solely of critically ill ICU patients with obesity. Previous studies with hypocaloric, high-protein nutrition therapy included patients who
were hospitalized, but most were not critically ill ICU patients.
The acuity of our patient population was evident by a mean
negative NB as opposed to previous works that demonstrated
mean positive NB. Finally, our study was the first to demonstrate improved clinical outcomes with use of hypocaloric,
high-protein nutrition therapy as opposed to a higher calorie
isonitrogenous regimen in critically ill patients with obesity.
We retrospectively compared the nutrition and clinical efficacies of eucaloric and hypocaloric high-protein enteral feeding
in 40 critically ill adult patients with traumatic injuries and obesity. All patients were in the trauma or surgical ICUs at the time
of study, had normal renal and hepatic function, and had
received at least 7 days of enteral tube feeding. Patients were
stratified according to caloric intake as eucaloric (> 20 kcal/kg
adjusted weight/d or > 25 kcal/kg IBW/d) or hypocaloric (20
kcal/kg adjusted body weight/d or 25 kcal/kg IBW/d).
Adjusted body weight was estimated by the following: Adjusted
body weight (kg): [(Actual body weight IBW) 0.25] + IBW.
Target protein intake was 2 g/kg IBW/d for both groups.
Most of the eucaloric feeding group was given a standard highprotein enteral formula (1 kcal/mL, 62 g protein/L), whereas
the majority of the hypocaloric, high-protein feeding group
was given the same standard high-protein enteral formula with
an additional 25 g of protein added per liter of formula to make
a 1.1-kcal/mL, 87-g protein/L formulation. The protein powder
was added to the enteral formula and blenderized in the pharmacy under clean conditions before administration to the
patient. The enteral tube feedings were managed by the
Nutrition Support Service. Clinical events and nutrition data
were examined over a 4-week period. There were no

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differences between groups with respect to age, weight, body

mass index (BMI), Acute Physiology and Chronic Health
Evaluation II (APACHE II) score, or injury severity score
(ISS). Patients who were stratified to the eucaloric group (n =
12) received an average of 19 kcal/kg actual weight/d (30
kcal/kg IBW) and 1.8 g/kg IBW of protein, whereas the hypocaloric group received 11 kcal/kg actual weight/d (22 kcal/kg
IBW) and 1.5 g/kg IBW/d of protein. Protein intakes averaged
2.0 0.4 g/kg IBW/d and 2.0 0.5 g/kg IBW/d during the
second weeks NB study for the eucaloric and hypocaloric
groups, respectively. Mean NB balance was 1.4 6.0 g/d and
2.7 5.6 g/d for each group, respectively. No significant difference in serum prealbumin concentration recovery was noted
between groups. The most striking findings of this study relate
to clinical outcomes. Unlike the previous comparative studies,6,7 an improvement in clinical outcomes was observed with
use of a hypocaloric, high-protein regimen, as evidenced by a
significant decrease in ICU length of stay (29 16 days vs 19
10 days, P < .03), decreased antibiotic days (27 17 days vs
17 12 days, P < .03), and a trending decrease in ventilator
days (24 17 days vs. 16 12 days, P < .09). It should be
emphasized that the intent of hypocaloric, high-protein nutrition therapy in our study was to avoid complications associated
with overfeeding since the critically ill obese patient is particularly susceptible to these complications.10,11 Weight loss was
considered a welcome secondary benefit and not a primary
clinical outcome marker.
Limitations of this study include its small sample size and
retrospective study design. With any retrospective or prospective observational study comparing different methods of therapy, potential bias in patient assignment to a particular
therapeutic regimen should be questioned. Close inspection of
our data reveals that the hypocaloric group tended to be more
obese than the eucaloric group (mean BMI of 41 vs 36 kg/m2).
This modest difference in patient selection between groups
occurred due to initial reluctance by some clinicians at our institution at that time to employ this novel mode of therapy except
in cases of class III (BMI 40 kg/m2) obesity. As clinicians at
our institution gained experience with hypocaloric, high-protein enteral feeding, the selection of patients relaxed to include
those with class I and II obesity. As a result of this minor selection bias, patients in the hypocaloric group tended to have more
comorbidities (eg, diabetes, hypertension, sleep apnea/
hypoventilation syndrome) from their obesity, although these
data were statistically insignificant. Given these modest differences in patient groups and current knowledge regarding clinical outcomes for those with severe obesity,12,13 the hypocaloric
group (with a greater proportion of patients with class III obesity) would have been anticipated to potentially exhibit worse
clinical outcomes compared with the eucaloric group and not
improved outcomes, as demonstrated in this study. Another
limitation of this study is that patients in both groups did not
consistently achieve their intended caloric and protein goals.
This is a common occurrence for hospitalized patients who

receive intragastric nutrition therapy,14 especially for those who

are critically ill.15 In a separate study from a similar period, we
reported that critically ill trauma patients received an average of
about two-thirds of what was prescribed during the first week of
EN therapy.15 Surgical/diagnostic procedures and gastric feeding intolerance were the most prevalent etiologies for the temporary interruptions in continuous enteral feeding.15 Since
publication of this Pivotal Paper, we have improved our gastric
feeding delivery by defining population-specific prokinetic
pharmacotherapy for gastric feeding intolerance,16 raising our
gastric residual volume threshold for feeding intolerance evaluation,16 and, for select patients, temporarily increasing the
enteral feeding rate to account for anticipated time off feedings
due to scheduled surgical procedures.17

Validation
Since our article was published in 2002, there have been a few
published studies evaluating the use of hypocaloric, high-protein nutrition therapy for patients with obesity.18-21 In addition,
2 national organization guidelines13,22 and 1 consensus workshop report23 published after this article have advocated the use
of hypocaloric, high-protein nutrition therapy for hospitalized
patients with obesity.
Details regarding those studies published after this Pivotal
Paper are given below.

Hypocaloric, High-Protein Home PN

Therapy for Patients With Postoperative
Bariatric Surgery Complications
Hamilton and coworkers21 reported the results of 23 patients
who were given home PN for postoperative complications following a gastric bypass procedure. Patients received an average of 14 kcal/kg actual body weight/d and 1.2 g/kg actual
body weight/d of protein for a median duration of 1.5 months.
The patients weights decreased from a median of 113 kg
to 107 kg (P < .001). Mean serum albumin concentration
improved from 2.8 0.5 g/dL to 3.2 0.6 g/dL (P = .004).
Most of the patients (83%) were weaned off home PN to
resume an oral diet, 2 were transferred to tube feeding, and 1
was transferred to another physicians care. Frequency of home
PN complications was comparable with that reported by others. The authors concluded that hypocaloric, high-protein
home PN was efficacious in maintaining adequate nutrition
while allowing weight loss in morbidly obese patients to
recover from complications of bariatric surgery.

Obesity and Nutrition Support: Is Bigger

Different?
Obesity is associated with a variety of metabolic perturbations
that can be adversely affected by nutrition support therapy, particularly if the patient is overfed or acutely ill. The extent of

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Nutrition in Clinical Practice 29(6)

these metabolic derangements may be further exacerbated as

the severity of obesity increases. Choban et al13 combined their
databases from their previous studies to understand how severity of obesity influences metabolic response to nutrition therapy. Seventy patients, 48 with class I and II obesity and 22 with
class III obesity, were retrospectively evaluated. Our most
important findings were differences in protein requirements
between groups to achieve nitrogen equilibrium in the presence
of critical illness. Regression analysis between NB and protein
intake indicated that critically ill ICU patients with class I or II
obesity required ~1.92 g/kg IBW/d to achieve nitrogen equilibrium, whereas those with class III obesity required ~2.5 g/kg
IBW/d or more to achieve nitrogen equilibrium. There was no
difference in protein requirements between hospitalized, non
critically ill patients as related to extent of obesity. Nitrogen
equilibrium for this subset of patients, irrespective of class of
obesity, was achieved at ~1.71.8 g/kg IBW/d.
As a result of this study, our current target goal protein intakes
are at least 2 g/kg IBW/d for our critically ill patients with a BMI
of 3039.9 kg/m2 and at least 2.5 g/kg IBW/d for those with a
BMI 40 kg/m2 as long as severe renal or hepatic dysfunction is
not evident. The adequacy of this target is evaluated by a subsequent NB study and the protein goal adjusted if necessary.

Hypocaloric, High-Protein Nutrition for

Older Patients
Clinicians may be concerned that the senescent kidney may not
effectively excrete the increased amount of urea produced during a hypocaloric, high-protein nutrition regimen. Another
confounding issue is that older patients may experience resistance to anabolic stimuli, including amino acids, to stimulate
muscle protein synthesis.24-26 Previous data indicate that this
anabolic resistance can be overcome by provision of additional
amino acids for both stressed and unstressed older adults.26,27
Taken together, these data suggest that older patients may
require more protein to achieve an equivalent NB than do
young patients and may be at higher risk for azotemia.
Liu et al28 studied 12 patients 60 years or older and 18
patients <60 years of age with obesity who received a hypocaloric, high-protein PN regimen for an average of 13 days. Both
age groups received 18 kcal/kg actual weight/d. Protein intakes
were also similar between groups at ~1.9 g/kg IBW/d and ~1.8
g/kg IBW/d, respectively. NB tended to be lower for the older
group at 0.2 5.0 g/d vs 3.4 3.9 g/d for the younger group
(P = .06). Serum urea nitrogen concentration and clinical outcomes were not evaluated.
We presumed the trending difference in NB between age
groups in the Liu et al28 study was due to anabolic resistance of
aging and hypothesized that an insufficient amount of protein
was given to overcome this resistance. To test this hypothesis,
we retrospectively compared 33 older (aged 60 years) and 41
younger (aged 1859 years) patients with obesity and traumatic
injuries who received a hypocaloric, high-protein EN or PN

regimen.20 On average, the older patients received 21 5 kcal/kg

IBW/d, whereas the younger patients received 18 4 kcal/kg
IBW/d (P = .002). When given isonitrogenous regimens (protein
intake, 2.3 0.3 g/kg IBW/d vs 2.3 0.2 g/kg IBW/d), no significant difference was noted in NB between older and younger
patients (3.2 5.7 g/d vs 4.9 9.0 g/d, respectively). About
half of the patients from each group achieved a positive NB or
nitrogen equilibrium. Parallel improvements in serum prealbumin concentrations were also noted between groups. Clinical
outcomes (survival, duration of ICU stay, duration of hospital
stay, days of mechanical ventilation, days of antibiotic therapy,
and incidence of infections) were not different between age
groups. Older patients experienced a greater serum urea nitrogen
concentration during nutrition therapy than did younger patients
(30 14 mg/dL vs 20 9 mg/dL, P = .001), but none of the
patients had evidence of renal failure or required hemodialysis
or a restriction in protein intake. We concluded that older patients
with traumatic injuries had an NB equivalent to younger trauma
patients when given adequate protein intake. In addition, older
patients may be at greater risk for developing azotemia, and
close monitoring during hypocaloric, high-protein nutrition therapy is warranted.20

Hypocaloric Nutrition Containing

Inadequate Protein Intake Is Harmful
In an observational cohort study of nutrition practices from
numerous ICUs from different countries, 60-day mortality was
evaluated in 2772 mechanically ventilated patients with respect
to BMI and nutrition intake.18 Of the 2772 patients, 162 and
171 had class II or III obesity. When a hypocaloric diet was
combined with an inadequate protein intake (average daily
caloric and protein intakes of 1009 kcal/d and 46 g/d, respectively) and given to hospitalized patients with class II obesity
(BMI of 3539.9 kg/m2), mortality was worsened. It is unclear
why all obese patients in this study received, on average, only
54%55% of what was prescribed and did not receive protein
supplements. It is also unclear why increased mortality was not
evident for those patients with class III obesity in addition to
those with class II obesity. This author would interpret and
summarize these data as during hypocaloric nutrition therapy,
an inadequate protein intake is harmful.

Future Considerations
A large, prospective, randomized controlled trial is warranted
to ascertain whether hypocaloric, high-protein nutrition therapy offers a significant therapeutic advantage over eucaloric or
hypercaloric feeding with respect to clinical outcomes and
avoidance of complications from overfeeding for hospitalized
and critically ill patients with obesity. Preliminary research
indicates that pharmaconutrition supplementation designed to
target the inflammatory response associated with obesity may
also be beneficial.29 The role of arginine, citrulline, and fish oil

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may have a greater role in dampening the exaggerated inflammatory response to acute illness in the hospitalized obese
patient than previously anticipated.29 Although randomized
controlled trials of these pharmaconutrients during critical illness for obese patients are lacking, future research may define
the role of these agents as adjuvant therapy for the metabolic
management of the critically ill patient with obesity.

Conclusion
The obesity epidemic is worsening in the United States and
spreading worldwide. It is unavoidable for the clinician caring
for hospitalized patients to not be involved in the metabolic
management of acutely ill patients with obesity. This Pivotal
Paper suggests clinical outcomes of critically ill obese patients
are at least equivalent and potentially improved by use of
hypocaloric, high-protein nutrition therapy compared with
eucaloric high-protein feeding. Future research will facilitate
further understanding regarding the appropriate metabolic
management of these complex patients.

References
1. Dickerson RN, Boschert KJ, Kudsk KA, Brown RO. Hypocaloric enteral
tube feeding in critically ill obese patients. Nutrition. 2002;18:241-246.
2. Shaw SN, Elwyn DH, Askanazi J, Iles M, Schwarz Y, Kinney JM. Effects
of increasing nitrogen intake on nitrogen balance and energy expenditure
in nutritionally depleted adult patients receiving parenteral nutrition. Am J
Clin Nutr. 1983;37:930-940.
3. Elwyn DH. Nutritional requirements of adult surgical patients. Crit Care
Med. 1980;8:9-20.
4. Hill GL, Church J. Energy and protein requirements of general surgical
patients requiring intravenous nutrition. Br J Surg. 1984;71:1-9.
5. Dickerson RN, Rosato EF, Mullen JL. Net protein anabolism with hypocaloric parenteral nutrition in obese stressed patients. Am J Clin Nutr.
1986;44:747-755.
6. Burge JC, Goon A, Choban PS, Flancbaum L. Efficacy of hypocaloric total
parenteral nutrition in hospitalized obese patients: a prospective, doubleblind randomized trial. JPEN J Parenter Enteral Nutr. 1994;18:203-207.
7. Choban PS, Burge JC, Scales D, Flancbaum L. Hypoenergetic nutrition
support in hospitalized obese patients: a simplified method for clinical
application. Am J Clin Nutr. 1997;66:546-550.
8. Finfer S, Chittock DR, Su SY, et al. Intensive versus conventional glucose
control in critically ill patients. N Engl J Med. 2009;360:1283-1297.
9. van den Berghe G, Wouters P, Weekers F, et al. Intensive insulin therapy
in critically ill patients. N Engl J Med. 2001;345:1359-1367.
10. Dickerson RN. Hypocaloric feeding of obese patients in the intensive care
unit. Curr Opin Clin Nutr Metab Care. 2005;8:189-196.
11. Dickerson RN, Drover JW. Monitoring nutrition therapy in the critically
ill patient with obesity. JPEN J Parenter Enteral Nutr. 2011;35:44S-51S.
12. Dickerson RN. The obesity paradox in the ICU: real or not? Crit Care.
2013;17:154.

13. Choban P, Dickerson R, Malone A, et al. A.S.P.E.N. clinical guidelines:

nutrition support of hospitalized adult patients with obesity. JPEN J
Parenter Enteral Nutr. 2013;37:714-744.
14. Abernathy GB, Heizer WD, Holcombe BJ, Raasch RH, Schlegel KE, Hak
LJ. Efficacy of tube feeding in supplying energy requirements of hospitalized patients. JPEN J Parenter Enteral Nutr. 1989;13:387-391.
15. Morgan LM, Dickerson RN, Alexander KH, Brown RO, Minard G.
Factors causing interrupted delivery of enteral nutrition in trauma intensive care unit patients. Nutr Clin Pract. 2004;19:511-517.
16. Dickerson RN, Mitchell JN, Morgan LM, et al. Disparate response to
metoclopramide therapy for gastric feeding intolerance in trauma patients
with and without traumatic brain injury. JPEN J Parenter Enteral Nutr.
2009;33:646-655.
17. Heyland DK, Murch L, Cahill N, et al. Enhanced protein-energy provision
via the enteral route feeding protocol in critically ill patients: results of a
cluster randomized trial. Crit Care Med. 2013;41:2743-2753.
18. Alberda C, Gramlich L, Jones N, et al. The relationship between nutritional intake and clinical outcomes in critically ill patients: results of
an international multicenter observational study. Intensive Care Med.
2009;35:1728-1737.
19. Choban PS, Dickerson RN. Morbid obesity and nutrition support: is bigger different? Nutr Clin Pract. 2005;20:480-487.
20. Dickerson RN, Medling TL, Smith AC, et al. Hypocaloric, high-protein
nutrition therapy in older vs younger critically ill patients with obesity.
JPEN J Parenter Enteral Nutr. 2013;37:342-351.
21. Hamilton C, Dasari V, Shatnawei A, Lopez R, Steiger E, Seidner D.
Hypocaloric home parenteral nutrition and nutrition parameters in patients
following bariatric surgery. Nutr Clin Pract. 2011;26:577-582.
22. McClave SA, Martindale RG, Vanek VW, et al. Guidelines for the provision and assessment of nutrition support therapy in the adult critically ill
patient: Society of Critical Care Medicine (SCCM) and American Society
for Parenteral and Enteral Nutrition (A.S.P.E.N.). JPEN J Parenter
Enteral Nutr. 2009;33:277-316.
23. McClave SA, Kushner R, Van Way CW III, et al. Nutrition therapy of the
severely obese, critically ill patient: summation of conclusions and recommendations. JPEN J Parenter Enteral Nutr. 2011;35:88S-96S.
24. Guillet C, Prodhomme M, Balage M, et al. Impaired anabolic response of
muscle protein synthesis is associated with S6K1 dysregulation in elderly
humans. FASEB J. 2004;18:1586-1587.
25. Volpi E, Mittendorfer B, Rasmussen BB, Wolfe RR. The response of
muscle protein anabolism to combined hyperaminoacidemia and glucoseinduced hyperinsulinemia is impaired in the elderly. J Clin Endocrinol
Metab. 2000;85:4481-4490.
26. Dickerson RN, Maish GO III, Croce MA, Minard G, Brown RO. Influence
of aging on nitrogen accretion during critical illness [published online
October 11, 2013]. JPEN J Parenter Enteral Nutr.
27. Campbell WW, Crim MC, Dallal GE, Young VR, Evans WJ. Increased
protein requirements in elderly people: new data and retrospective reassessments. Am J Clin Nutr. 1994;60:501-509.
28. Liu KJ, Cho MJ, Atten MJ, et al. Hypocaloric parenteral nutrition support
in elderly obese patients. Am Surg. 2000;66:394-400.
29. McClave SA, Frazier TH, Hurt RT, Kiraly L, Martindale RG. Obesity,
inflammation, and pharmaconutrition in critical illness. Nutrition.
2014;30:492-494.

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