Surg Clin N Am 86 (2006) 1483–1493

Advances in Surgical Nutrition

Juan B. Ochoa, MDa,b,*, David Caba, MD, MSa
a
Department of Surgery, University of Pittsburgh Medical Center Presbyterian,
200 Lothrop Street, Pittsburgh, PA 15213, USA
b
Department of Critical Care, University of Pittsburgh Medical Center Presbyterian,
200 Lothrop Street, Pittsburgh, PA 15213, USA

Dr. Stanley Dudrick, a surgery resident working under Dr. Jonathan

Rhoads, invented total parenteral nutrition (TPN) in 1968, providing a des-
perately needed therapy to those patients who could not eat [1]. Before this,
patients who had a nonfunctional gastrointestinal tract were condemned to
die of malnutrition. TPN has since saved thousands of patients worldwide.
It is not surprising, therefore, that medicine embraced TPN with fervor,
despite the absence of adequate evaluation of its benefits and limitations.
Work on TPN had the unforeseen effect of bringing the discipline of nu-
trition into the spotlight of mainstream medicine. Suddenly, it was impor-
tant for clinicians in virtually every discipline to embrace nutrition. It was
expected of interns and residents to be able to calculate calories and protein
in TPN bags, and to demonstrate that nutrition intervention (NI) were being
done. It became fashionable for clinicians to order high amounts of calories
and protein in what was called ‘‘hyperalimentation.’’ This was done in a
naı̈ve attempt to curtail the progression toward malnutrition caused by
the hypermetabolism of injury [2].
Appropriate trials comparing TPN and enteral nutrition (EN) were even-
tually done, with humbling results. These studies, and the meta-analyses
performed on them, demonstrated that under virtually any circumstance
EN produces better outcomes than TPN whenever the patient’s gastrointes-
tinal tract can be used [3]. These results are observed even though TPN con-
sistently delivers 30% to 50% more calories and protein than conventional
enteral nutrition. Thus we have learned that the benefits of nutrition far sur-
pass the mere provision of nutrients.
NI has gained significantly in complexity, with an increasing array of pos-
sible but not always intuitive decisions. NI, like any other form of medical

* Corresponding author.
E-mail address: ochoajb@upmc.edu (J.B. Ochoa).

0039-6109/06/$ - see front matter Ó 2006 Elsevier Inc. All rights reserved.
doi:10.1016/j.suc.2006.09.002 surgical.theclinics.com
1484 OCHOA & CABA

or surgical therapy, has to demonstrate a beneficial effect on clinical out-

comes. In addition, and more than with other therapies, NI is also expected
to demonstrate adequate cost-effectiveness [4]. The purpose of this article,
therefore, is to review what we know of the different forms of NI, and to
evaluate their practical roles at the bedside. This article analyzes five forms
of NI that virtually cover any decision-making process in surgical/trauma
patients. These are: (1) controlled starvation (CS), (2) TPN, (3) EN,
(4) oral nutritional supplements (ONS), and (5) nutrients with pharmacolog-
ical properties.

Forms of nutrition intervention

Controlled starvation and early enteral nutrition
Short periods of CS have traditionally been allowed in most surgical pa-
tient populations, including patients undergoing elective surgery and the
critically ill. Arguments suggesting that oral intake can only be resumed
until bowel function returns still abound on surgical floors [5]. Most surgical
patients, however, will tolerate oral/enteral intake. The benefits of early
oral/enteral intake cannot be minimized, and a concerted effort toward
changing clinical practices at individual institutions is important.
In 2001, Lewis and colleagues [6] published a meta-analysis on 11 differ-
ent studies in patients undergoing elective gastrointestinal surgery (Fig. 1).
Six of these studies used early oral/enteral nutrition (EEN), whereas 5
used a nasoenteral device or a jejunostomy. In general, oral/enteral intake

Fig. 1. Early enteral nutrition outcome. (Adapted from Lewis SJ, Egger M, Sylvester PA, et al.
Early enteral feeding versus ‘‘nil by mouth’’ after gastrointestinal surgery: systematic review and
meta-analysis of controlled trials. BMJ 2001;323:775; with permission.)
 ADVANCES IN SURGICAL NUTRITION 1485

was started within 24 hours after surgery. The results of this study demon-
strate several important issues:
Early use of oral or enteral intake is associated with a statistically signif-
icant decrease in infection rates (relative risk 0.72, 95% confidence in-
terval, 0.54 to 0.98, P ¼ 0.036). The mean length of stay in hospital was
also reduced (P ¼ 0.001). This observation is also confirmed in criti-
cally ill trauma patients [7]. The decrease in infections is probably
caused by a systemic effect, because decreased infections are observed
at different sites, including the lung, wounds, and the urinary tract.
There is no evidence of increased breakdown of gastrointestinal anastomo-
ses. In fact, EEN is associated with a clear trend toward decreased anas-
tomotic breakdown (relative risk 0.53, 95% confidence interval, 0.26 to
1.08, P ¼ 0.080). Studies performed in rodents demonstrate that oral in-
take is associated with a significant increase in collagen deposition at the
anastomosis and wound strength [8]. Thus, there is no validity to the
widespread idea that nutrients in the lumen will disrupt anastomoses.
There is a trend toward decreased mortality when patients are fed early,
although this did not reach statistical significance.
There is a small (approximately 10%) statistically significant increase in
rates of vomiting. Vomiting, however, does not appear to be associated
with negative physiologic consequences. A recent meta-analysis en-
courages the use of selective rather than routine nasogastric tube de-
compression, demonstrating that its use delays the return of bowel
function and may actually increase pulmonary complications [9].
Lewis and coworkers [6] did not report as to whether caloric goals had
been met in the group of patients receiving early oral intake. Thus,
so far we do not know whether the benefits of early oral intake are
independent of the amounts of calories given.
EEN is also clearly indicated in the critically ill surgical/trauma patient.
A systematic review of EEN has been done by Heyland and colleagues, from
the Canadian Critical Care Nutrition Taskforce (CCCNT) [10]. Eight Level
II studies demonstrate a significant decrease in infection rates without affect-
ing mortality.
In conclusion, there is now clear evidence supporting the idea that con-
trolled short periods of starvation are not indicated in most surgical patients.
In addition, the accumulating data demonstrate that the gastrointestinal
tract can be used successfully in most surgical/critically ill patients.

Permissive underfeeding
An interesting observation of virtually all studies on EEN is the realiza-
tion that in most, there is a failure to meet intake of planned caloric goals. In
general, most patients on EEN meet between 50% and 70% of caloric goals
[11]. Yet, there appears to be a benefit from lower caloric intake, which has
1486 OCHOA & CABA

raised considerable interest in the concept of ‘‘permissive underfeeding.’’

This observation raises several interesting possibilities.
The first is that caloric intake has been set at inappropriately high levels.
Historically, caloric goals (CGs) were decided on in an attempt to curtail the
catabolic response and loss of muscle and visceral mass that invariably oc-
curs after surgery/trauma and critical illness. In the absence of stress, provi-
sion of small amounts of carbohydrate (400 calories/d) leads to sparing of
muscle breakdowndthe so called ‘‘protein-sparing’’ effect of glucose. In
the presence of traumatic or septic stress, however, the provision of carbo-
hydrates, even at caloric goals, fails to protect muscle mass, thus making CG
unnecessary.
Guidelines to determine CGs have been written by several organizations.
In 1997 the American College of Chest Physicians (ACCP) published guide-
lines based on expert opinion [12]. Similar, though more modest guidelines
have been published by the American Society of Parenteral and Enteral Nu-
trition (ASPEN) [13]. Finally, the Canadian Critical Care Task force has de-
termined that there are insufficient data to suggest what number of calories
should be given to critically ill patients [10]. Thus, all the hospital nutrition
authoritative organizations agree that CGs in surgical/trauma critically ill
patients have never been successfully determined.
The second possibility is that EEN produces benefits through mecha-
nisms that are independent of CGs. Starvation is associated with significant
abnormalities in gastrointestinal function, including mucosal atrophy and
loss of gastrointestinal associated lymphoid tissue (GALT). EEN maintains
normal gastrointestinal function even when CGs are not met. Thus, it is sug-
gested that a small amount of nutrients, which ‘‘bathe’’ the gut mucosa, is all
that is necessary or desirable. It appears to be important to provide at least
some protein, though again how much should be provided initially is still
undetermined.
Another possibility is that meeting CGs is associated with complications,
including overfeeding. Provision of EN is associated with an increased num-
ber of side effects as the dietary volume delivered is increased in an attempt
to meet caloric goals. In addition, calorically dense formulas with high con-
centrations of fat can overwhelm the digestive and absorptive capacity of
the gastrointestinal tract. Thus, investigators have noticed increased gastric
residuals, bloating, and diarrhea when high volumes are delivered or when
high fat formulas are provided to critically ill surgical/trauma patients. Fur-
thermore, overfeeding is associated with a large number of complications,
and may indeed increase mortality. Overfeeding negatively affects function
of every organ (Fig. 2) [14]. Overfeeding causes encephalopathy, increases
cardiac and respiratory demands, prolongs ventilator dependency, and
causes immune dysfunction. Thus, the dangers of overfeeding cannot be
overemphasized.
It would be simple to avoid overfeeding if clinicians used a reliable of way
of determining the caloric needs of a given patient. Most clinicians
 ADVANCES IN SURGICAL NUTRITION 1487

Fig. 2. Negative Effects of overfeeding. (From Klein CJ, Stanek GS, Wiles III CE. Overfeeding
macronutrients to critically ill adults: metabolic complications. J Am Diet Assoc 1998;98:796;
with permission.)

(including nutritionists) rely on population-based calculated formulas such

as the Harris-Benedict formulas. These formulas were generated far before
the availability of intensive care units, and thus it is unclear as to whether
they are applicable to that setting. Unfortunately, the use of these formulas
may lead to overfeeding in up to 30% of patients, and thus may cause harm.
The use of indirect calorimetry may provide a more reliable mechanism of
determining the appropriate calories needed by a given patient [15]. Unfor-
tunately, indirect calorimetry is labor intensive and difficult to do, and is not
available in many institutions. Furthermore, there is no significant evidence
that performing indirect calorimetry is cost-effective.

Early enteral nutrition

Enteral nutrition has shown its greatest effectiveness when started early.
Even though there is significant heterogeneity between the different studies,
EEN is defined as that nutrition started within 24 to 48 hours of admission
to the ICU. Across all critically ill patient populations, patients receiving
EEN exhibit a clear trend toward a decrease in mortality (P ¼ 0.08) and in-
fection rates [10,16]. In practical terms, EEN is started as soon as the pa-
tient’s hemodynamic status is stabilized. Ideally, a small-bore feeding tube
is placed and diet is started at low volumes. Low volumes are associated
1488 OCHOA & CABA

with decreased complications such as abdominal distention, increased gastric

residuals, and vomiting. The authors routinely supplement these patients
with additional protein to meet goals of 1.5 to 2 g/kg/d. Consideration to
providing additional early micronutrients should also be given.
In conclusion, CS is not necessary or desirable in most patients. Oral or
enteral nutrition can be achieved in most surgical/trauma and in critically ill
patients. Enteral nutrition should be started as early as possible, ideally
within the first 24 hours of arrival. Meeting caloric goals is not necessary
or desirable, though the degree of underfeeding that is beneficial remains
undetermined.

Total parenteral nutrition

Compared with EN, TPN appears to offer distinct advantages. Establish-
ing delivery access is far simpler and more reliable for TPN. In addition,
TPN delivery does not have to be stopped for surgical procedures or trips
outside of the ICU. Not surprisingly, patients on TPN consistently meet
caloric goals more often than those given EN. These observations led
clinicians to advocate the use of TPN, implying that its use would be
of benefit. This, however, is not the case.
Multiple studies have demonstrated that in surgical patients, trauma vic-
tims, and critically ill patients, TPN is inferior to EN. In the ICU, for example,
13 different studies have demonstrated that EN is associated with decreased
rates of infections when compared with TPN, though there is no evidence
of an effect on mortality [10,16]. In critically ill trauma patients also, the
use of TPN is associated with increased morbidity, including infections, a
longer length of stay in the ICU, and prolonged ventilator dependency [17].
In 1993, a carefully performed prospective randomized study compared
the use of postoperative TPN with simple starvation [18]. Three hundred pa-
tients divided equally into two groups scheduled to undergo elective gastro-
intestinal or urologic surgery received TPN or D10W plus electrolytes
starting on the first postoperative day. This regimen was maintained until
the patient started eating, or for up to 2 weeks if the patient failed to take
adequate oral intake. Although most patients in both groups were able to
initiate oral intake, a small number of patients (24/150 in the TPN group,
28/150 in the D10W controls) failed to eat. One would have predicted
that those patients that received D10W for 2 weeks would have had a signif-
icantly poorer outcome when compared with those receiving TPN, because
of the previous knowledge of a protective role of TPN from the progression
toward malnutrition. Contrary to the predicted outcome, however, those
patients placed on TPN exhibited increased morbidity and mortality
(Fig. 3) [18]. Thus this well-performed study demonstrated that there is no
role for prophylactic TPN in surgical patients. Similarly, TPN used only
as a means of achieving caloric goals has failed to demonstrate clear benefits
in other patient populations such as trauma and surgical critically ill. The
 ADVANCES IN SURGICAL NUTRITION 1489

40 **
35
30
25
20
15
10 *
5
0
TPN + PO D10W + PO D10W + NPO TPN + NPO

Fig. 3. Mortality in the use of TPN. (Data from Sandstrom R, Drott C, Hyltander A, et al. The
effect of postoperative intravenous feeding (TPN) on outcome following major surgery evalu-
ated in a randomized study. Ann Surg 1993;217:192–5.)

role of TPN has therefore been progressively reduced. Nevertheless it re-

mains invaluable in several situations:
Nonstressed patient who has severe protein-calorie malnutrition, who is
scheduled to undergo surgery. A perfect example is the patient sched-
uled to undergo esophageal surgery because of obstruction. In the mal-
nourished patient, TPN given 7 days before surgery is associated with
a significant decrease in infection rates [19].
The patient who has short gut. Indefinite survival of patients who have
short gut is now possible thanks to the use of TPN. TPN can be
used for long-term management or as a bridge to intestinal transplant.
Patients who fail oral/enteral nutrition. A frequent consult to any nutri-
tion intervention team is that of failure to achieve adequate enteral nu-
trition support in a given patient. This is often used as an excuse to
start TPN. More often, however, adequate evaluation of the patient
and implementation of simple measures lead to successfully achieving
adequate EN. It is only after an adequate attempt at enteral nutrition
that TPN should be implemented. There are currently no clear guide-
lines as to what constitutes a failed attempt at EN. It is clear though,
that it is not necessary, at least early on, to meet caloric goals through
the enteral route to see its benefits. There is no role for the use of com-
bined TPN and EN [10].

Oral nutritional supplements

ONS are a frequent addition to the therapy of many patients in the hos-
pital. ONS are often concentrates of high amounts of calories with proteins
and micronutrients, including vitamins, and are heavily commercially adver-
tised. There is little evidence, however, that ONS indiscriminately adminis-
tered to hospitalized patients will benefit outcome.
1490 OCHOA & CABA

In a prospective randomized trial [20] conducted in patients undergoing

elective gastrointestinal surgery, for example, ONS demonstrated no differ-
ence in outcome when compared with controls. There was also no demon-
strable effect on prevention of weight loss. Similarly, ONS failed to show
any benefit at all in stroke patients admitted to a prospective randomized
multi-center trial [21]. Several studies have been performed in patients un-
dergoing hip replacements [22,23]. In this patient population, high protein
supplementation may be associated with a modest improvement in survival,
though the quality of the studies does not permit a definitive demonstration
of benefit.
Thus one cannot advocate the routine use of ONS.

Nutrients with pharmacologic properties

Surgery and trauma are associated with depression of adaptive T-cell
function, including decreased T-cell numbers, abnormally low circulating
CD4 counts, decreased T-cell proliferation, involution of the thymus, and
depressed delayed type hypersensitivity (DTH) [24,25]. In the late 1970s Bar-
bul and colleagues [26,27] demonstrated that arginine supplementation in
a rodent model of surgical trauma prevented thymic involution. These
changes in T-cell function have been considered pathologic and thought
to increase the susceptibility to infections that accompany any major surgery
or severe trauma. This hypothesis, though logical, has never been thor-
oughly tested or proven. Nevertheless, therapy to ‘‘normalize’’ T-cell func-
tion was deemed necessary and desirable. Arginine supplementation was
thus a potentially effective therapy for surgery/trauma-induced T-cell
suppression.
Independent of the arginine work, other investigators demonstrated that
a host of nutrients, including omega-3 fatty acids (u-FA), nucleic acids, and
glutamine, also affected immune function. These nutrients, along with argi-
nine, were eventually incorporated and commercialized as ‘‘immune enhanc-
ing diets’’ (IEDs) [28]. At least seven of these different diets exist in the
market, each one with its own proprietary mix of nutrients. Blending was
done despite incomplete knowledge of their mechanisms of action, possible
side effects, and unknown interactions between the different substances.
Nevertheless, multiple trials in different patient populations have tested
the use of IEDs and attempted to prove (or disprove) a beneficial effect
on outcome.
It is therefore not surprising that the results of these multiple studies are
conflicting, difficult to interpret, and even more difficult to incorporate into
practical clinical practices. Nevertheless, and acknowledging the multiple
shortcomings of this area of research, the ‘‘dust has begun to settle,’’ allow-
ing us to suggest some practical guidelines.
Arginine deficiency develops in several disease processes, including sur-
gery and trauma, hemorrhagic shock, ischemia reperfusion of the liver, in
 ADVANCES IN SURGICAL NUTRITION 1491

hemoytic diseases, and in certain forms of cancer. Arginine deficiency in

these diseases is the result of the abnormal expression of arginase, an
enzyme that metabolizes arginine to ornithine and urea.
Arginine deficiency affects key biological functions, including the gener-
ation of nitric oxide and T lymphocyte function. T lymphocyte changes
caused by arginine deficiency are characteristic, and include a decrease in
T-cell proliferation and the loss of the z chain, an essential component of
the T-cell receptor complex. Arginine supplementation at supraphysiologic
doses designed to overcome arginine deficiency restores nitric oxide produc-
tion and T-cell function.
In the immune system, arginase expression is upregulated by surgery/
trauma, and in cancer in a group of specialized myeloid cells, now called my-
eloid suppressor cells (MSC) [29]. Granulocytes appear to play a role as
MSC in humans. MSC deplete arginine necessary for normal T0-cell func-
tion, including that of T-cell receptor expression. It is hypothesized, but
only partially tested, that arginine supplementation may overcome the
effects of MSC.
A combination of arginine, u-3 FA, and nucleotides, given as a dietary
supplement perioperatively, decreases infection rates around 40% in pa-
tients undergoing high-risk surgery. The benefits of this dietary combination
are well-demonstrated in all meta-analyses, and currently considered Level I
evidence of benefit [30]. Thus the use of an IED should be standard of care
in all major surgical interventions, including cardiac and gastrointestinal
surgery.
The use of arginine-containing IEDs is highly controversial in septic, crit-
ically ill patients, with contradictory studies showing either increased or
decreased mortality. Glutamine, a neutral amino acid, which is also a precur-
sor of arginine, may benefit patients who have sepsis.
Diets containing u-3 FA may be of benefit in patients who have respira-
tory failure.

Summary
Nutrition interventions in surgical/trauma and critically ill patients have
evolved dramatically during the last 20 years, evolving from a supportive
therapy to a clear therapeutic role. Like any other form of therapy, NI
will benefit patients when adequately indicated and prescribed. NI, however,
may cause significant side effects and harm when poorly ordered.

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