Journal of Parenteral and Enteral

Nutrition http://pen.sagepub.com/

Nutrition and Fluid Optimization for Patients With Short Bowel Syndrome
Laura E. Matarese
JPEN J Parenter Enteral Nutr 2013 37: 161 originally published online 21 December 2012
DOI: 10.1177/0148607112469818

The online version of this article can be found at:

http://pen.sagepub.com/content/37/2/161

Published by:

http://www.sagepublications.com

On behalf of:

The American Society for Parenteral & Enteral Nutrition

Additional services and information for Journal of Parenteral and Enteral Nutrition can be found at:

Email Alerts: http://pen.sagepub.com/cgi/alerts

Subscriptions: http://pen.sagepub.com/subscriptions

Reprints: http://www.sagepub.com/journalsReprints.nav

Permissions: http://www.sagepub.com/journalsPermissions.nav

>> Version of Record - Feb 8, 2013

OnlineFirst Version of Record - Dec 21, 2012

What is This?

Downloaded from pen.sagepub.com at UNIV OF VIRGINIA on November 16, 2013

469818 PENXXX10.1177/014860
7112469818Journal of Parenteral and Enteral Nutrition / Vol. XX, No. X, Month XXXXNutrition and
Fluid Optimization for SBS / Matarese
2013

Tutorial

Nutrition and Fluid Optimization for Patients Journal of Parenteral and Enteral
Nutrition
With Short Bowel Syndrome Volume 37 Number 2
March 2013 161-170
© 2012 American Society
for Parenteral and Enteral Nutrition
DOI: 10.1177/0148607112469818
jpen.sagepub.com
Laura E. Matarese, PhD, RD, LDN, FADA, CNSC hosted at
online.sagepub.com

Abstract
Short bowel syndrome (SBS) is characterized by nutrient malabsorption and occurs following surgical resection, congenital defect, or
disease of the bowel. The severity of SBS depends on the length and anatomy of the bowel resected and the health of the remaining tissue.
During the 2 years following resection, the remnant bowel undergoes an adaptation process that increases its absorptive capacity. Oral diet
and enteral nutrition (EN) enhance intestinal adaptation; although patients require parenteral nutrition (PN) and/or intravenous (IV) fluids
in the immediate postresection period, diet and EN should be reintroduced as soon as possible. The SBS diet should include complex
carbohydrates; simple sugars should be avoided. Optimal fat intake varies based on patient anatomy; patients with end-jejunostomies can
tolerate a higher proportion of calories from dietary fat than patients with a remnant colon. Patients with SBS are prone to deficiencies
in vitamins, minerals, and essential fatty acids; serum levels should be periodically monitored and supplements provided as needed.
Prebiotic or probiotic therapy may be beneficial for patients with SBS, although further research is needed to determine optimal protocols.
Patients with SBS, particularly those without a colon, are at high risk of dehydration; oral rehydration solutions sipped throughout the day
can help maintain hydration. One of the primary goals of SBS therapy is to reduce or eliminate dependence on PN/IV; optimization of
EN and hydration substantially increases the probability of successful PN/IV weaning. (JPEN J Parenter Enteral Nutr. 2013;37:161-170)

Keywords
enteral nutrition; parenteral nutrition; gastroenterology; fluids-electrolytes/acid base; fiber

Introduction to Intestinal Failure Relationship Between Remnant Bowel

Intestinal failure is a condition resulting from obstruction,
dysmotility, surgical resection, congenital defect, or disease-
associated loss of absorption characterized by the inability to
maintain protein-energy, fluid, electrolyte, or micronutrient
balance when on a conventional diet.1,2 Short bowel syndrome
(SBS) is one of the most common forms of intestinal failure.
Patients with SBS typically experience severe diarrhea, steat-
orrhea, nutrient deficiencies, electrolyte disturbances, dehy-
dration, malnutrition, and weight loss.3 Common conditions
resulting in SBS include surgical resection due to Crohn’s
disease, ulcerative colitis, malignancy, mesenteric vascular
disease, trauma, adhesions, or small bowel volvulus.3,4 Some
patients also experience malabsorption due to irradiation and
mucosal disease. The exact prevalence of SBS in the United
States is unknown but has been estimated at 10,000–15,000
patients.2,5 Many patients with intestinal failure, particularly
SBS, require long-term parenteral nutrition (PN) and/or intra-
venous (IV) fluids. However, long-term PN/IV use has been
associated with serious adverse events; large annual expense;
and, for many, reduced quality of life.6-9 Optimizing the hydra-
tion and enteral nutrition (EN) through individualized dietary
and pharmaceutical management of SBS can reduce or elimi-
nate the need for PN/IV and improve outcomes for this patient
population.
and Severity of SBS
In healthy adults, length of the small intestine varies from
about 300–1000 cm (mean, 635 cm), whereas the colon is
estimated at about 160 cm.10 Fortunately, the bowel is
equipped with a large functional reserve, and patients can usu-
ally compensate for resections of ≤50% of bowel length.11
However, bowel resections of >75% often require dietary
modification and, for more severe cases, partial or complete
support with PN/IV fluids.11,12
From East Carolina University, Greenville, North Carolina.
Financial disclosure: Writing support was provided by Heather Heerssen,
PhD, of Complete Healthcare Communications, Inc (Chadds Ford, PA)
and was funded by NPS Pharmaceuticals.
Dr Matarese is a member of NPS Pharmaceuticals publication advisory
board.
Received for publication October 16, 2012; accepted for publication
November 8, 2012.
This article originally appeared online on December 21, 2012.
Corresponding Author:
Laura E. Matarese, PhD, RD, LDN, FADA, CNSC, Associate Professor,
Gastroenterology, Hepatology and Nutrition, East Carolina University,
600 Moye Blvd, Vidant MA 338, Greenville, NC 27834, USA.
E mail: mataresel@ecu.edu.

Downloaded from pen.sagepub.com at UNIV OF VIRGINIA on November 16, 2013

162 Journal of Parenteral and Enteral Nutrition 37(2)
From a functional standpoint, the bowel is not uniform; thus,
the region of bowel resected has a large impact on the degree of
nutritional support required. Resections of the proximal bowel,
including the duodenum and proximal jejunum, are generally
better tolerated because of ileal compensation and adaptation.13
There is also evidence that fat in the proximal small intestine
inhibits intestinal transit as the jejunal brake.14
However, a relative lactose intolerance may occur follow-
ing jejunal resection because most lactase is synthesized in the
jejunum and proximal ileum.15 Ileal resections are generally
more poorly tolerated than jejunal resections because adaptive
hyperplasia in the remaining jejunum is limited. Loss of ileal
tissue has a greater impact on absorption than more proximal
resections in part because entry of nutrients into the ileum
increases intestinal transit time (the “ileal brake”).16,17 The dis-
tal ileum also has important roles in bile salt and vitamin B12
absorption.18-20 Ileal resections of >100 cm result in a net loss
of bile salts, compromising fat digestion and potentially wors-
ening steatorrhea.21 In addition, patients with resection of more
than 60 cm of the distal ileum generally require B12 supple-
mentation.22 There is evidence that in short bowel patients with
a retained colon, high values of peptide YY may slow gastric
emptying of liquid and contribute to the “colonic brake.”23
The ileocecal valve connecting the ileum and the colon is
thought to increase intestinal transit time and prevent move-
ment of colonic bacteria into the small intestines.24 However,
in a study of 16 patients with normal bowel length, those with
ileocecal valve resection showed similar small bowel transit
times as patients with intact valves; furthermore, no episodes
of ileocecal reflux were observed in either group.25 Nonetheless,
all attempts are made to preserve the ileocecal valve during
surgical resection.
The colon has critical roles in fluid and nutrient absorption.
Under normal conditions, the colon absorbs up to 1.9 L of
fluid per day; when fluid is slowly infused directly into the
cecum, the colon has the capacity to absorb more than 5 L of
fluid per day.26 Therefore, patients lacking a colon are at
greater risk of dehydration. Furthermore, an intact colon
delays gastric emptying and increases intestinal transit time
due to higher postprandial peptide YY levels.23,27 Finally, the
colon is capable of salvaging calories through anaerobic bacte-
rial fermentation of undigested carbohydrates into absorbable
short-chain fatty acids (SCFAs); this can provide an important
additional source of nutrition for patients with SBS.28-30
The severity of SBS depends on the both the length and
location of the resection, as well as the functional capacity of
the remaining bowel. Patients with SBS-associated intestinal
failure (ie, patients who require PN/IV) can be classified into
6 groups (Figure 1). Because of the fluid-absorbing functions
of the colon, patients with an end-jejunostomy generally
require more IV fluids than patients with the colon in continu-
ity. This may be in the form of standard IV fluids or IV solu-
tions with customized electrolytes. In contrast, patients with a
colon in continuity are more likely to have higher caloric needs
and require more energy than fluids. As the severity of disease
Downloaded from pen.sagepub.com at UNIV OF VIRGINIA on November 16, 2013
Figure 1. Characteristics of fluid/nutrient requirements of patients
with short bowel syndrome based on remnant bowel anatomy.
IV, intravenous fluid; PN, parenteral nutrition. Figure based on
unpublished discussions with P. Jeppesen (April 2012) and Efsen
E, Jeppesen PB. Modern treatment of adult short bowel syndrome
patients. Minerva Gastroenterol Dietol. 2011;57:405-417.
increases, a greater proportion of energy and fluid must be
delivered by PN/IV. This is illustrated by the volume needs of
the patient. Once the patient reaches the point where more than
21 L per week are required, PN will be necessary.
Intestinal Adaptation
In the 2 years following resection, the absorptive capacity of
the remaining mucosa increases.6,31 Mechanisms underlying
enhancements in absorption include crypt cell hyperplasia,
increased villus height and crypt depth, and upregulation of
epithelial transporter proteins.32-34
Proper dietary management of SBS can augment intestinal
adaptation. Compared with PN/IV, EN results in greater
adaptation and should be instituted to the extent possible.35-38
The type of nutrition consumed has important effects. In pre-
clinical studies, complex luminal nutrients in the form of
whole foods were potent stimuli to intestinal adaptation.39
For example, following small bowel resection, piglets main-
tained on pig chow gained significantly more weight than
similar animals fed an isocaloric diet consisting only of
elemental formula. In addition, villus height was consistently
greater in the chow-fed piglets.40 Similarly, rats fed a poly-
meric diet demonstrated significantly increased intestinal
weight, mucosal weight, and sucrase activity of the distal
intestines compared with rats fed an equal number of calories
via an elemental diet.41
PN and IV Fluid Optimization
All patients with SBS require PN in the initial postresection
period. Some patients are able to wean off PN during the adap-
tive and postadaptive phases, whereas others may require par-
tial or total PN for the long term to maintain appropriate
nutrition and hydration status. The American Society for
Parenteral and Enteral Nutrition (A.S.P.E.N.) has published
general guidelines for the use of EN and PN.42 EN is preferable
to PN when possible. PN should provide energy sufficient for
healthy adults, approximately 20–35 kcal/kg (85–145 kJ/kg)
per day. To avoid adverse metabolic events, carbohydrates and
lipids should be limited to ≤7 and 1.0 g/kg/d, respectively.
Matarese 163
To prevent essential fatty acid deficiency, approximately 1%–
2% of total calories should come from linoleic acid and 0.5%
from α-linolenic acid. Finally, PN should provide 186 mg/kg/d
of essential amino acids or 25%–30% of total protein intake.
The A.S.P.E.N. PN guidelines are not specific to the SBS
population. Because of the severe malabsorption experienced
by these patients, caloric and nutrition requirements may be
greater than for other patients requiring PN. Recommended
total caloric delivery to patients with SBS is estimated at
32 kcal/kg/d but should be individualized for each patient.43,44
Lipids should make up 20%–40% of total calories but should
not exceed 1 g/kg/d.43,45 Carbohydrates are provided in the
form of dextrose. In general, patients will need at least 100–
120 g/d of dextrose to support minimal body functions. Patients
with SBS may require 2.5–6 g/kg/d dextrose depending on
the level of repletion required. One to 1.5 g/kg/d of protein
is recommended.43,45 Frequent monitoring of blood chemistry
is required to ensure that electrolytes, vitamins, and minerals
are maintained at proper levels and balance, through specific
supplementation as needed.
Some patients will require IV fluids in addition to PN to
maintain proper hydration. Patients with end-jejunostomy in
particular can experience high stomal outputs, increasing their
fluid needs to >3 L/d. 46 For patients receiving nocturnal PN,
the infusion of additional IV fluids such as normal saline dur-
ing the day may be helpful to prevent intermittent dehydration
and reduce injury to the kidney.
EN Optimization
Enteral stimulation, via oral diet if possible and tube feeding
as necessary, is recommended as soon as feasible after resec-
tion to promote intestinal adaptation.35-38 In general, the
introduction of EN can be considered when diarrhea is lim-
ited to <2 L/d, hydration and electrolytes are stable, and
bowel activity has resumed.43 When there is more than 2 L of
output per day, the use of EN would likely be contraindicated
as tolerance would be limited.
Tube Feeding
Following resection, patients are typically advanced from
complete PN/IV to tube feeding or an oral diet as tolerated.
A recent study suggests that continuous tube feeding, alone
or in combination with oral feeding, increases intestinal mac-
ronutrient nutrient absorption compared with oral feeding
alone in the postoperative period. There was a significant
increase in total calories, lipids, and protein in patients who
received enteral tube feeding and oral combined with tube
feeding compared with oral feedings alone. The benefit asso-
ciated with tube feeding in this study may be derived from
the continuous mode of administration and the resulting
persistent luminal stimulation.47
For patients with SBS who require tube feeding, studies
suggest that elemental and polymeric diets are similar in terms
Downloaded from pen.sagepub.com at UNIV OF VIRGINIA on November 16, 2013
of nutrient absorption and fluid and electrolyte loss.48,49
However, polymeric diets are less costly and less hyperos-
motic than elemental diets and generally well tolerated. In
addition, polymeric diets may better enhance intestinal adapta-
tion when compared with elemental diets.50 Given these advan-
tages, polymeric diets are more commonly administered to
patients with SBS unless severe malabsorption is present.43
Dietary Management of SBS
Because of the heterogeneous nature of the patient population
and the complexities associated with performing these exper-
iments, few comparative studies of the effects of diet compo-
sition on absorption have been conducted in patients with
SBS (Table 1). Furthermore, those studies that have been
performed are limited by small sample sizes and diverse
patient populations with varying lengths of bowel and varying
degrees of healthy functional mucosa. Therefore, many of the
recommendations for dietary management of patients with
SBS come from observational studies and extensive clinical
experience. It is well recognized that nutrition therapy plays a
critical role in maximizing the rehabilitation of patients with
SBS, regardless of whether they have received reconstructive
surgery to restore the gastrointestinal (GI) anatomy or to
lengthen or taper the bowel (Figure 2).
Diets should be individualized based on remnant anatomy
and mucosal health. However, a few principles are applicable
to the SBS population as a whole. Most patients with SBS
can benefit from adaptive hyperphagia, the process of con-
suming multiple small meals per day, to increase net nutrient
absorption.51 In general, caloric intake should be increased by
at least 50% over a typical diet to compensate for malabsorp-
tion associated with SBS.52 The SBS diet should be rich in
complex carbohydrates.22 This diet avoids the high osmotic
load generated by disaccharides that can aggravate diarrhea or
increase ostomy output.53 Although the optimal amount of fats
to be consumed varies based on remnant anatomy (Table 2
and below), all patients should be encouraged to consume fats
high in essential fatty acids (EFAs) to prevent EFA deficien-
cies.54 Proteins should make up 20% of dietary intake.22
Because more than 80% of ingested protein is absorbed by
patients with SBS, protein supplementation is generally not
necessary in the absence of bacterial overgrowth or active dis-
ease that may be observed in Crohn’s flare-ups.55
Dietary Management for Patients With
SBS and Colon in Continuity
Patients with colon in continuity can salvage up to 1000 addi-
tional calories per day through colonic bacterial fermentation
of unabsorbed carbohydrates into absorbable SCFAs.28-30
Therefore, these patients derive added benefit from a diet that
is high in complex carbohydrates (Table 2). In contrast, dietary
fat content should be minimized for patients with a remnant
colon. Three clinical studies have demonstrated superior out-
164 Journal of Parenteral and Enteral Nutrition 37(2)

Table 1. Published Clinical Studies of Nutrition Management for Patients With Short Bowel Syndrome.
Author Number and Subject Type Small Bowel Length Diet Composition Outcomes
Andersson et al56 10 ileal resection with Mean 92-cm small intestine 100 g fat vs 40 g fat Reduced water and
intact colon resected (range, 35–150 cm) sodium excretion
1 ileostomy with low-fat diet
2 active Crohn’s without
resection
Hessov et al57,a 6 ileal resection with intact Mean 145-cm ileum resected 100 g fat vs 40 g fat High-fat diet
colon (range, 35–195 cm) increased divalent
1 ileostomy cation loss
2 active Crohn’s without
resection
Jeppesen and 6 jejunostomy Mean 203 cm for patients without 56% LCT vs 28% MCT + Improved fat
Mortensen60 3 ileostomy colon; mean 143 cm for patients 28% LCT absorption with
2 jejunum-colon with colon MCT when colon
8 jejunum-ileum-colon present
McIntyre et al49 7 jejunostomy Mean 101 cm Chemically defined vs No difference
(range, 60–150 cm) polymeric formula and 3
diets of variable fat/fiber
Nordgaard et al58 6 jejunostomy Mean 168 cm High-carbohydrate diet Increased energy
8 with colon in continuity (range, 100–250 cm) (60% carbohydrates + absorption with low-
Mean 114 cm 20% fat) vs high-fat diet fat diet with colon
(range, 50–245 cm) (20% carbohydrates +
60% fat)
Ovesen et al71 5 jejunostomy Mean 83 cm (range, 35–125 cm) 30% fat vs 60% fat High-fat diet
(PUFA:SFA 1:1) vs 60% increased mineral
fat (PUFA:SFA 1:4) losses
Woolf et al59 5 jejunostomy 30 cm to ½ small bowel 60% vs 20% fat No difference in
3 remnant colon fecal output, energy
absorption, or zinc-
calcium-magnesium
balance
LCT, long-chain triglyceride; MCT, medium-chain triglyceride; PUFA, polyunsaturated fatty acid; SFA, saturated fatty acid. Adapted with permission
from Matarese LE. Short bowel syndrome. In: Mullin GE, Matarese LE, Palmer M, eds. The Gastrointestinal and Liver Disease Nutrition Desk Refer-
ence. Boca Raton, FL: CRC Press; 2012:35-49.
a
Follow-up study on patient population in Andersson H. Fat-reduced diet in the symptomatic treatment of patients with ileopathy. Nutr Metab.
1974;17(2):102-111.

comes with a lower fat diet compared with a higher fat diet in
this group, including reduced fluid and sodium losses and
increased nutrient and mineral absorption (Table 1).56-58 In
addition, malabsorbed fats can contribute to steatorrhea. One
small clinical study reported no difference in energy absorp-
tion, fluid loss, or mineral absorption with a low-fat vs high-
fat diet, but only 3 of the 8 enrolled patients had a remnant
colon.59 The type of fat consumed also has important effects
on nutrition outcomes. For patients with a remnant colon, a
diet that includes medium-chain triglycerides (MCTs) has
been shown to improve overall fat absorption compared with
a similar diet that incorporated only long-chain triglycerides.60
Patients with ileal resection >100 cm and remnant colon are
at increased risk of oxalate kidney stone formation.61 The defi-
cit of bile salts leads to an excess of malabsorbed fats in the
colon. These fats bind to calcium, which would otherwise bind
oxalates. The free oxalates pass into the bloodstream and can
then precipitate in the kidney.62 Therefore, the diets of patients
with SBS with remnant colon should be low in oxalates and
high in calcium to lower the probability of nephrolithiasis.63
Diets that include soluble fiber (eg, pectin) are helpful for
patients with SBS. Soluble fiber can solidify stool, increase
colonic transit time, and act as a substrate for colonic fermen-
tation into SCFAs.64-66 In contrast to soluble fibers, insoluble
fibers such as wheat bran decrease gastrointestinal transit time
and therefore have less benefit for patients with SBS.67
Furthermore, diets that are very high in either type of fiber
should be restricted to patients with >3 L/d diarrhea because
fiber has the potential to impede fat and mineral
absorption.68-70
Dietary Management for Patients With
SBS and Jejunostomy or Ileostomy
For patients with SBS and an ostomy, a significant propor-
tion of calories (40%–50%) should originate from complex

Downloaded from pen.sagepub.com at UNIV OF VIRGINIA on November 16, 2013

Matarese 165

Table 2. Diet for Short Bowel Syndrome Based on

Remnant Anatomy.68
Colon Present Colon Absent
Carbohydrate 50%–60% of energy 40%–50% of energy
intake intake
Complex carbohydrates Complex carbohydrates
Fat 20%–30% of energy 30%–40% of energy
intake intake
Ensure adequate intake Ensure adequate intake
of EFAs, MCTs/LCTs of EFAs and LCTs
Protein 20% of energy intake 20% of energy intake
High biological value High biological value
Fiber Soluble fiber for net Soluble fiber for net
secretors secretors
Oxalate Restrict No restriction necessary
Fluids ORS and/or hypotonic ORS
EFA, essential fatty acid; LCT, long-chain triglyceride; MCT, medium-
chain triglyceride; ORS, oral rehydration solution. Reproduced with
permission from Matarese LE. Síndrome de intestino corto: principios
actuales de tratamiento. In: Prado RA, Márquez HA, Moya DA, eds.
Nutricion Enteral y Parenteral. 2nd ed. New York, NY: McGraw-Hill;
2012:484-496.

and supplemented as needed. Supplemental calcium should be

Figure 2. Algorithm for the management of patients with SBS.
GI, gastrointestinal; H2, histamine H2 receptor antagonists; ORS,
oral rehydration solution; SBS, short bowel syndrome.
carbohydrates; simple carbohydrates should be avoided to
reduce ostomy output (Table 2).7,22 Clinical studies suggest
that these patients can tolerate a higher fat diet (30%–40% of
calories) than patients with a colon in continuity (Table 1).
No differences in energy absorption, ostomy output, fat
absorption, or sodium and potassium excretion were observed
between higher fat and lower fat diets for patients with end-
jejunostomies.58,71 However, one of the studies reported less
divalent cation absorption with the higher fat diet.71 In addi-
tion, MCT supplementation decreases carbohydrate and
protein absorption in this population and should be avoided.60
Soluble fiber (dietary or supplements) can be administered as
needed to thicken ostomy effluent.22
Nutrition Supplements
Because of malabsorption, patients with SBS typically require
oral supplementation of vitamins and micronutrients at dos-
ages higher than the dietary reference intakes for healthy
individuals (Table 3).22 Minerals and trace elements such as
magnesium and zinc can be easily depleted with diarrhea or
excessive ostomy output72,73; serum levels should be evaluated
provided to reduce the risk of oxalate kidney stone forma-
tion.74,75 Calcium citrate is preferred over calcium carbonate
because of its greater solubility and better absorption.76
Patients with SBS have poor absorption of fat-soluble vita-
mins (eg, vitamins A, D, and E), which likely need to be sup-
plemented.54,77 Patients with large ileal resections usually
require vitamin B12 supplementation because B12 carrier pro-
teins are localized to the distal ileum.18,20 Vitamin B12 is typi-
cally administered as a 1000-µg monthly injection;
supplementation for other vitamins and minerals may need to
be provided as liquid rather than pill formulations to increase
bioavailability.43,44
Adjunctive Medications
Patients with SBS usually require adequate pharmacologic
interventions to mitigate disease symptoms (Figure 2).
Among the most commonly prescribed adjunctive medica-
tions are antidiarrheals that slow gut motility, including
diphenoxylate-atropine, loperamide, codeine, and opium.78-80
Because of the gastrocolic response, antidiarrheals are most
effective when administered 30–60 minutes before a meal.63
The effect of antidiarrheals may diminish with use, so dos-
ages should be monitored and adjusted as needed.81 For
patients with choleretic diarrhea, bile salt–binding resins (eg,
cholestyramine and colestipol) can be of benefit.21 However,
bile salt–binding resins may worsen steatorrhea or decrease
absorption of fat-soluble vitamins, so careful patient moni-
toring is required.21,82

Downloaded from pen.sagepub.com at UNIV OF VIRGINIA on November 16, 2013

166 Journal of Parenteral and Enteral Nutrition 37(2)
Table 3. Vitamin and Mineral Supplementation for Patients With Short Bowel Syndrome Weaning From Parenteral
Nutrition.
Nutrient Strength
Vitamin B12 1000 µg
Vitamin A 25,000 IU
Vitamin D 1000 IU
Vitamin E 400 IU
Calcium 500- to 600-mg tablet
Magnesium lactate 8-mg tablet
Magnesium gluconate 1000-mg tablet (or liquid)
Potassium chloride 20-mg tablet
Phosphate (NeutraPhos) 250-mg package
Sodium bicarbonate 650-mg tablet
Chromium 100-µg tablet
Copper 3-mg tablet
Selenium 200-µg tablets
Zinc sulfate 220-mg tablet
IU, International Unit; PO, by mouth; tid, 3 times daily. Adapted with permission from Matarese LE. Síndrome de intestino corto: principios actuales de
tratamiento. In: Prado RA, Márquez HA, Moya DA, eds. Nutricion Enteral y Parenteral. 2nd ed. New York, NY: McGraw-Hill; 2012:484-496.
Gastric acid hypersecretion promotes both diarrhea,
because of excess luminal fluid, and malabsorption, because of
pancreatic enzyme and bile salt denaturation.83-85 Antisecretory
agents, such as histamine receptor antagonists and proton-
pump inhibitors, can alleviate symptoms of gastric hypersecre-
tion.86,87 α2-Adrenergic receptor agonists have been shown to
reduce fecal volume,88 whereas somatostatin analogues
(octreotide) are effective in controlling hypersecretory states
and severe diarrhea.89 However, caution should be exercised
when administering octreotide, which has been shown to
inhibit intestinal adaptation in some, but not all, animal mod-
els.90-93 The combination of an antisecretory agent with supple-
mentary pancreatic enzyme or bile salt may improve
hypersecretion-associated malabsorption.63,83
Antibiotic therapy should be administered as necessary to
combat bacterial overgrowth. Broad-spectrum oral antibiotics
should be rotated over the first 7–10 days of each month to
avoid resistance.63 In addition, recent studies suggest that pre-
biotics and probiotics may be of benefit to patients with SBS.
In preclinical experiments, prebiotics or probiotics increased
intestinal adaptation, reduced bacterial translocation from the
gastrointestinal lumen, and restored normal bacterial flora.94-96
Although no clinical trials on the efficacy of prebiotics or pro-
biotics have been conducted in adults with SBS, 2 studies
evaluating pediatric patients with SBS receiving synbiotics
(both prebiotics and probiotics) have been reported.97,98
Synbiotic protocols improved bacterial profiles, increased
colonic carbohydrate fermentation, and accelerated weight and
height gains in treated patients. However, because these stud-
ies were small, including only 11 patients, the significance of
these changes could not be established.97,98
Finally, growth factor therapy may facilitate intestinal
adaptation in patients with SBS. Human growth hormone and
Downloaded from pen.sagepub.com at UNIV OF VIRGINIA on November 16, 2013
Dose
Injection once monthly
1 tablet PO daily
1 tablet PO daily
1 tablet PO daily
1–2 tablets PO tid
1–2 tablets PO tid
1–3 tablets PO tid
1–2 tablets PO daily
1 package PO tid
1 tablet PO tid
1–2 tablets PO tid
1–2 tablets PO daily
1 tablet PO daily
1–3 tablets PO daily
glucagon-like peptide 2 (GLP-2) have each been shown to
enhance intestinal adaptation and nutrient absorption in pre-
clinical and clinical studies.99-104 In a phase III trial conducted
in PN/IV-dependent patients with SBS, administration of
recombinant human growth hormone (Zorbtive; EMD Serono,
Rockland, MD) with modified diet resulted in a significant
decrease in PN/IV volume, calories, and infusion frequency
compared with glutamine treatment with modified diet.
However, reductions in PN/IV requirements were even greater
and longer lasting in a third group, which received a modified
diet with both growth hormone and glutamine.105 In another
recently published phase III trial, patients with intestinal fail-
ure associated with SBS who received teduglutide (GATTEX;
NPS Pharmaceuticals, Bedminster, NJ), a degradation-
resistant analogue of GLP-2, showed significant reductions in
PN/IV volume and number of infusion days compared with
patients who received placebo.106 Currently, Zorbtive is
approved in the United States and teduglutide is approved in
Europe (Revestive; Takeda, Osaka, Japan), both for the treat-
ment of patients with SBS.
Optimization of Oral Fluids
Approximately 8 L of fluid, derived from oral ingestion and
internal secretions, enters the small bowel each day; most of
this volume is recovered by the distal small bowel and
colon.26,43 Patients with resections of the ileum or colon are at
high risk of diarrhea and dehydration, so proper fluid manage-
ment is critical. For patients with end-jejunostomy or ileos-
tomy, oral consumption of fluids should be greater than
ostomy output (generally 1.5–2 L/d).61 Oral rehydration solu-
tions (ORS) take advantage of the sodium-glucose co-trans-
port system; they are optimally formulated with glucose and
Matarese 167
electrolytes to maintain hydration and are typically necessary
for these patients.107,108 Patients who retain at least half of their
colon may be able to maintain proper hydration and sodium
absorption without ORS.53 All patients with SBS should avoid
hypertonic fluids (eg, fruit juices) because beverages contain-
ing high sugar concentrations unbalanced by salt promote
influx of sodium and water into the gut lumen.43,109 Hypotonic
fluids (eg, tap water) promote sodium loss and should also be
avoided, as should diuretics such as caffeinated beverages and
alcohol.43,53,108 Liquids should be consumed slowly and con-
tinuously throughout the day to avoid gastric dumping.22
Rationale and Considerations for
PN/IV Fluid Weaning
Up to 55% of adults with SBS can be weaned off PN/IV within
5 years.110 Factors associated with successful PN/IV weaning
include greater length of remaining bowel, presence of a colon
in continuity, and higher fasting plasma citrulline levels.110,111
The health of the remaining mucosal tissue is another impor-
tant variable in successful weaning; patients with mucosal
inflammation remain dependent on PN/IV longer than patients
without mucosal inflammation.112
To increase the probability of successful weaning, nutrition
and fluid intake must be optimized before initiating the wean-
ing program.113 The patient should be able to obtain approxi-
mately 80% of daily energy requirements through oral nutrition
while maintaining body weight, and electrolyte levels must be
stable. Urine production should be >1 L/d and ≥0.5 mL/kg/h
on PN/IV-free nights, and enteral balance (oral fluid intake
minus stool output) should be between 500 and 1000 mL/d.
Proper patient education is another critical component of
weaning.113 Patients should be familiar with their anatomy and
have a basic understanding of the disease, prescribed medica-
tions, and nutrition and hydration guidelines. Finally, clearly
defined goals should be established with the patient before
attempting weaning, including a target body weight and a
desired outcome for the weaning program, either reduction or
complete elimination of PN/IV.113
Two methods for weaning have been established.113 In both
methods, a gradual reduction of PN/IV is necessary. In the first
method, the number of PN/IV days is slowly decreased.113
Patients tend to prefer eliminating PN/IV sessions if possible,
but this method raises the risk of dehydration on days without
PN/IV. In the second method, the volume of PN/IV delivered
during each session is reduced.113 Dehydration is less problem-
atic with this method, but the patient loses the advantage of
decreasing the number of PN/IV sessions. With either method,
nutrition and hydration status, as well as blood levels of elec-
trolytes and minerals, should be assessed weekly.113 Vitamin
and trace element status should be evaluated every 1–3 months
during the weaning process. Vitamin and mineral supplemen-
tation may need to be increased as weaning proceeds. In
Downloaded from pen.sagepub.com at UNIV OF VIRGINIA on November 16, 2013
addition, supplemental IV fluids, tube feeding, or infusion with
ORS may be required during the weaning process.114
It is important to note that in the process of weaning, fluid
overload is a potential risk as the bowel adapts and begins to
absorb more. Thus, careful and periodic monitoring will be
required until the patient is fully autonomous or has achieved
the maximum goal.
Conclusions
Management of patients with SBS is complex. The patient
population is heterogeneous, and treatment must be individu-
alized based on the GI anatomy, length, and health of the
remnant bowel. Along with maximal pharmaceutical manage-
ment, optimization of nutrition and fluid status is a critical
factor in improving patient outcomes. Long-term PN/IV has
been associated with complications such as catheter sepsis,
vascular thrombosis, cholelithiasis, and metabolic bone dis-
ease. In addition, it is associated with high costs and dimin-
ished quality of life.6-9 The goal of SBS therapy should be to
decrease PN/IV dependence to the extent possible. Even in the
absence of complete weaning, reductions in the number of
PN/IV days or session volumes can be beneficial to patients.
Introducing appropriate EN and hydration as soon as possible
following resection will facilitate intestinal adaptation and
may promote eventual full weaning. Throughout the adaptive
and postadaptive phases of recovery, the patient should be
periodically reevaluated to determine whether further reduc-
tions in PN/IV are possible.
Glossary
Colon in continuity: Surgical resection of the small intestines in
which some or all of the colon is retained.
End-jejunostomy: Surgical creation of an opening between
the jejunum, the middle portion of the small bowel, and the
abdominal wall, accompanied by the surgical removal of the
ileum, colon, and some of the jejunum.
Ileostomy: Surgical creation of an opening between the ileum,
the distal portion of the small bowel, and the abdominal wall,
accompanied by the surgical removal of the colon and part of the
ileum.
Intestinal adaptation: An increase in the absorptive capacity
of the intestines that typically occurs within the first 2 years fol-
lowing surgical resection via hyperplasia of intestinal cells and
upregulation of transporter proteins.
Intestinal failure: The inability to maintain protein-energy,
fluid, electrolyte, or micronutrient balance when on a conven-
tional diet, because of obstruction, dysmotility, surgical resection,
or disease of the intestines.
Oral rehydration solution (ORS): Liquids that are optimally
formulated with glucose and electrolytes to maintain hydration
and prevent diarrhea.
168 Journal of Parenteral and Enteral Nutrition 37(2)
Prebiotics: Nondigestible foods that stimulate the growth
or activity of beneficial bacteria in the gut.
Probiotics: Nonpathogenic, living bacteria or yeast intro-
duced into the gut for health benefits.
Short bowel syndrome (SBS): A decrease in the length
and functional capacity of the intestines due to resection or
disease.
Further Reading
Compher C, Gilroy R, Pertkiewicz M, et al. Maintenance of parenteral nutri-
tion volume reduction, without weight loss, after stopping teduglutide in
a subset of patients with short bowel syndrome. JPEN J Parenter Enteral
Nutr. 2011;35:603-609.
Jeppesen PB. Teduglutide, a novel glucagon-like peptide 2 analog, in the treat-
ment of patients with short bowel syndrome. Therap Adv Gastroenterol.
2012;5:159-171.
Jeppesen PB, Lund P, Gottschalck IB, et al. Short bowel patients treated for
two years with glucagon-like peptide 2 (GLP-2): compliance, safety, and
effects on quality of life. Gastroenterol Res Pract. 2009;2009:425759.
Jeppesen PB, Lund P, Gottschalck IB, et al. Short bowel patients treated for two
years with glucagon-like peptide 2: effects on intestinal morphology and
absorption, renal function, bone and body composition, and muscle func-
tion. Gastroenterol Res Pract. 2009;2009:616054.
Norholk LM, Holst JJ, Jeppesen PB. Treatment of adult short bowel syndrome
patients with teduglutide. Expert Opin Pharmacother. 2012;13:235-243.
Tappenden KA. Emerging therapies for intestinal failure. Arch Surg.
2010;145:528-532.
Thompson JS, Rochling FA, Weseman RA, Mercer DF. Current management of
short bowel syndrome. Curr Probl Surg. 2012;49:52-115.
Vipperla K, O’Keefe SJ. Teduglutide for the treatment of short bowel syn-
drome. Expert Rev Gastroenterol Hepatol. 2011;5:665-678.
References
1. Hollwarth ME. Short bowel syndrome: pathophysiological and clinical
aspects. Pathophysiology. 1999;6:1-19.
2. O’Keefe SJ, Buchman AL, Fishbein TM, Jeejeebhoy KN, Jeppesen PB,
Shaffer J. Short bowel syndrome and intestinal failure: consensus defini-
tions and overview. Clin Gastroenterol Hepatol. 2006;4:6-10.
3. Thompson JS, Weseman R, Rochling FA, Mercer DF. Current management
of the short bowel syndrome. Surg Clin North Am. 2011;91:493-510.
4. Nightingale J, Woodward JM; Small Bowel Nutrition Committee of
the British Society of Gastroenterology. Guidelines for management of
patients with a short bowel. Gut. 2006;55(suppl 4):iv1-12.
5. Weireiter L. Nutritional hope or hype for short bowel syndrome? Am J
Gastroenterol. 1996;91:2246-2247.
6. Buchman AL, Scolapio J, Fryer J. AGA technical review on short bowel
syndrome and intestinal transplantation. Gastroenterology. 2003;124:1111-
1134.
7. Compher C, Winkler M, Boullata JI. Nutritional management of short
bowel syndrome. In: Marian M, Russell MK, Shikora SA, eds. Clinical
Nutrition for Surgical Patients. Sudbury, MA: Jones and Bartlett; 2008.
8. DiBaise JK. Home parenteral nutrition: complications, survival, costs and
quality of life. In: Langnas A, Goulet O, Quigley EM, Tappenden KA, eds.
Intestinal Failure: Diagnosis, Management and Transplantation. Oxford,
England: Blackwell; 2008.
9. Winkler MF. Quality of life in adult home parenteral nutrition patients.
JPEN J Parenter Enteral Nutr. 2005;29:162-170.
10. Hounnou G, Destrieux C, Desme J, Bertrand P, Velut S. Anatomical study
of the length of the human intestine. Surg Radiol Anat. 2002;24:290-294.
11. Jeejeebhoy KN. Short bowel syndrome: a nutritional and medical
approach. CMAJ. 2002;166:1297-1302.
Downloaded from pen.sagepub.com at UNIV OF VIRGINIA on November 16, 2013
12. Haymond HE. Massive resection of the small intestine: an analysis of 257
cases. Surg Gynecol Obstet. 1935;51:693-705.
13. Dowling RH, Booth CC. Structural and functional changes following
small intestinal resection in the rat. Clin Sci. 1967;32:139-149.
14. Lin HC, Zhao XT, Wang L. Jejunal brake: inhibition of intestinal transit by
fat in the proximal small intestine. Dig Dis Sci. 1996;41:326-329.
15. Torp N, Rossi M, Troelsen JT, Olsen J, Danielsen EM. Lactase-phlorizin
hydrolase and aminopeptidase N are differentially regulated in the small
intestine of the pig. Biochem J. 1993;295(pt 1):177-182.
16. Spiller RC, Trotman IF, Adrian TE, Bloom SR, Misiewicz JJ, Silk DB.
Further characterisation of the ‘ileal brake’ reflex in man—effect of ileal
infusion of partial digests of fat, protein, and starch on jejunal motil-
ity and release of neurotensin, enteroglucagon, and peptide YY. Gut.
1988;29:1042-1051.
17. Spiller RC, Trotman IF, Higgins BE, et al. The ileal brake—inhibition of
jejunal motility after ileal fat perfusion in man. Gut. 1984;25:365-374.
18. Booth CC, Mollin DL. The site of absorption of vitamin B12 in man. Lan-
cet. 1959;1:18-21.
19. Meihoff WE, Kern F, Jr. Bile salt malabsorption in regional ileitis, ileal
resection and mannitol-induced diarrhea. J Clin Invest. 1968;47:261-267.
20. Okuda K. Discovery of vitamin B12 in the liver and its absorption factor
in the stomach: a historical review. J Gastroenterol Hepatol. 1999;14:301-
308.
21. Hofmann AF, Poley JR. Role of bile acid malabsorption in pathogenesis of
diarrhea and steatorrhea in patients with ileal resection, I: response to cho-
lestyramine or replacement of dietary long chain triglyceride by medium
chain triglyceride. Gastroenterology. 1972;62:918-934.
22. Matarese LE. Síndrome de intestino corto: principios actuales de trata-
miento. In: Prado RA, Márquez HA, Moya DA, eds. Nutricion Enteral y
Parenteral. 2nd ed. New York, NY: McGraw-Hill; 2012:484-496.
23. Nightingale JM, Kamm MA, van der Sijp JR, Ghatei MA, Bloom SR, Len-
nard-Jones JE. Gastrointestinal hormones in short bowel syndrome: peptide
YY may be the ‘colonic brake’ to gastric emptying. Gut. 1996;39:267-272.
24. Ricotta J, Zuidema GD, Gadacz TR, Sadri D. Construction of an ileocecal
valve and its role in massive resection of the small intestine. Surg Gynecol
Obstet. 1981;152:310-314.
25. Fich A, Steadman CJ, Phillips SF, et al. Ileocolonic transit does not change
after right hemicolectomy. Gastroenterology. 1992;103:794-799.
26. Debongnie JC, Phillips SF. Capacity of the human colon to absorb fluid.
Gastroenterology. 1978;74:698-703.
27. Nightingale JM, Kamm MA, van der Sijp JR, et al. Disturbed gastric emp-
tying in the short bowel syndrome: evidence for a ‘colonic brake’. Gut.
1993;34:1171-1176.
28. Royall D, Wolever TM, Jeejeebhoy KN. Evidence for colonic conservation
of malabsorbed carbohydrate in short bowel syndrome. Am J Gastroen-
terol. 1992;87:751-756.
29. Bond JH, Currier BE, Buchwald H, Levitt MD. Colonic conservation of
malabsorbed carbohydrate. Gastroenterology. 1980;78:444-447.
30. Nordgaard I, Hansen BS, Mortensen PB. Importance of colonic support
for energy absorption as small-bowel failure proceeds. Am J Clin Nutr.
1996;64:222-231.
31. Gouttebel MC, Saint Aubert B, Colette C, Astre C, Monnier LH, Joyeux H.
Intestinal adaptation in patients with short bowel syndrome: measurement
by calcium absorption. Dig Dis Sci. 1989;34:709-715.
32. Doldi SB. Intestinal adaptation following jejuno-ileal bypass. Clin Nutr.
1991;10:138-145.
33. Hines OJ, Bilchik AJ, McFadden DW, et al. Up-regulation of Na+,K+
adenosine triphosphatase after massive intestinal resection. Surgery.
1994;116:401-407, discussion 408.
34. Hines OJ, Bilchik AJ, Zinner MJ, et al. Adaptation of the Na+/glucose
cotransporter following intestinal resection. J Surg Res. 1994;57:22-27.
35. Feldman EJ, Dowling RH, McNaughton J, Peters TJ. Effects of oral versus
intravenous nutrition on intestinal adaptation after small bowel resection in
the dog. Gastroenterology. 1976;70:712-719.
Matarese 169
36. Ford WD, Boelhouwer RU, King WW, de Vries JE, Ross JS, Malt RA.
Total parenteral nutrition inhibits intestinal adaptive hyperplasia in young
rats: reversal by feeding. Surgery. 1984;96:527-534.
37. Johnson LR, Copeland EM, Dudrick SJ, Lichtenberger LM, Castro GA.
Structural and hormonal alterations in the gastrointestinal tract of parenter-
ally fed rats. Gastroenterology. 1975;68:1177-1183.
38. Morin CL, Ling V, Van Caillie M. Role of oral intake on intestinal adap-
tation after small bowel resection in growing rats. Pediatr Res. 1978;12:
268-271.
39. Tappenden KA. Mechanisms of enteral nutrient-enhanced intestinal adap-
tation. Gastroenterology. 2006;130:S93-S99.
40. Bines JE, Taylor RG, Justice F, et al. Influence of diet complexity on intes-
tinal adaptation following massive small bowel resection in a preclinical
model. J Gastroenterol Hepatol. 2002;17:1170-1179.
41. Buts JP, Morin CL, Ling V. Influence of dietary components on intes-
tinal adaptation after small bowel resection in rats. Clin Invest Med.
1979;2:59-66.
42. American Society for Parenteral and Enteral Nutrition Board of Direc-
tors. Guidelines for the use of parenteral and enteral nutrition in adult
and pediatric patients. JPEN J Parenter Enteral Nutr. 2002;26:1SA-
138SA.
43. Sundaram A, Koutkia P, Apovian CM. Nutritional management of short
bowel syndrome in adults. J Clin Gastroenterol. 2002;34:207-220.
44. Jeejeebhoy KN. Management of short bowel syndrome: avoidance of total
parenteral nutrition. Gastroenterology. 2006;130:S60-S66.
45. Vanderhoof JA, Young RJ. Enteral and parenteral nutrition in the care of
patients with short-bowel syndrome. Best Pract Res Clin Gastroenterol.
2003;17:997-1015.
46. O’Keefe SJ, Peterson ME, Fleming CR. Octreotide as an adjunct to home
parenteral nutrition in the management of permanent end-jejunostomy syn-
drome. JPEN J Parenter Enteral Nutr. 1994;18:26-34.
47. Joly F, Dray X, Corcos O, Barbot L, Kapel N, Messing B. Tube feeding
improves intestinal absorption in short bowel syndrome patients. Gastro-
enterology. 2009;136:824-831.
48. Levy E, Frileux P, Sandrucci S, et al. Continuous enteral nutrition dur-
ing the early adaptive stage of the short bowel syndrome. Br J Surg.
1988;75:549-553.
49. McIntyre PB, Fitchew M, Lennard-Jones JE. Patients with a high jejunos-
tomy do not need a special diet. Gastroenterology. 1986;91:25-33.
50. Healey KL, Bines JE, Thomas SL, et al. Morphological and functional
changes in the colon after massive small bowel resection. J Pediatr Surg.
2010;45:1581-1590.
51. Crenn P, Morin MC, Joly F, Penven S, Thuillier F, Messing B. Net diges-
tive absorption and adaptive hyperphagia in adult short bowel patients.
Gut. 2004;53:1279-1286.
52. DiBaise JK, Young RJ, Vanderhoof JA. Intestinal rehabilitation and
the short bowel syndrome: part 2. Am J Gastroenterol. 2004;99:1823-
1832.
53. Matarese LE, O’Keefe SJ, Kandil HM, Bond G, Costa G, Abu-Elmagd K.
Short bowel syndrome: clinical guidelines for nutrition management. Nutr
Clin Pract. 2005;20:493-502.
54. Jeppesen PB, Hoy CE, Mortensen PB. Deficiencies of essential fatty
acids, vitamin A and E and changes in plasma lipoproteins in patients
with reduced fat absorption or intestinal failure. Eur J Clin Nutr. 2000;54:
632-642.
55. Woolf GM, Miller C, Kurian R, Jeejeebhoy KN. Nutritional absorption
in short bowel syndrome: evaluation of fluid, calorie, and divalent cation
requirements. Dig Dis Sci. 1987;32:8-15.
56. Andersson H. Fat-reduced diet in the symptomatic treatment of patients
with ileopathy. Nutr Metab. 1974;17:102-111.
57. Hessov I, Andersson H, Isaksson B. Effects of a low-fat diet on min-
eral absorption in small-bowel disease. Scand J Gastroenterol. 1983;18:
551-554.
58. Nordgaard I, Hansen BS, Mortensen PB. Colon as a digestive organ in
patients with short bowel. Lancet. 1994;343:373-376.
Downloaded from pen.sagepub.com at UNIV OF VIRGINIA on November 16, 2013
59. Woolf GM, Miller C, Kurian R, Jeejeebhoy KN. Diet for patients with a
short bowel: high fat or high carbohydrate? Gastroenterology. 1983;84:823-
828.
60. Jeppesen PB, Mortensen PB. The influence of a preserved colon on the
absorption of medium chain fat in patients with small bowel resection. Gut.
1998;43:478-483.
61. Matarese LE, Steiger E. Dietary and medical management of short bowel
syndrome in adult patients. J Clin Gastroenterol. 2006;40:S85-S93.
62. Nightingale JM, Lennard-Jones JE, Gertner DJ, Wood SR, Bartram CI.
Colonic preservation reduces need for parenteral therapy, increases inci-
dence of renal stones, but does not change high prevalence of gall stones in
patients with a short bowel. Gut. 1992;33:1493-1497.
63. Matarese LE. Short bowel syndrome. In: Mullin GE, Matarese LE, Palmer
M, eds. The Gastrointestinal and Liver Disease Nutrition Desk Reference.
Boca Raton, FL: CRC Press; 2012:35-49.
64. Meier R, Beglinger C, Schneider H, Rowedder A, Gyr K. Effect of a liquid
diet with and without soluble fiber supplementation on intestinal transit
and cholecystokinin release in volunteers. JPEN J Parenter Enteral Nutr.
1993;17:231-235.
65. Cummings JH, Southgate DA, Branch WJ, et al. The digestion of pectin in
the human gut and its effect on calcium absorption and large bowel func-
tion. Br J Nutr. 1979;41:477-485.
66. Atia A, Girard-Pipau F, Hebuterne X, et al. Macronutrient absorption char-
acteristics in humans with short bowel syndrome and jejunocolonic anasto-
mosis: starch is the most important carbohydrate substrate, although pectin
supplementation may modestly enhance short chain fatty acid production
and fluid absorption. JPEN J Parenter Enteral Nutr. 2011;35:229-240.
67. Otsuka M, Satchithanandam S, Calvert RJ. Influence of meal distribution
of wheat bran on fecal bulk, gastrointestinal transit time and colonic thy-
midine kinase activity in the rat. J Nutr. 1989;119:566-572.
68. Byrne TA, Veglia L, Camelio M, et al. Beyond the prescription: opti-
mizing the diet of patients with short bowel syndrome. Nutr Clin Pract.
2000;15:306-311.
69. Byrne TA, Morrissey TB, Nattakom TV, Ziegler TR, Wilmore DW. Growth
hormone, glutamine, and a modified diet enhance nutrient absorption in
patients with severe short bowel syndrome. JPEN J Parenter Enteral Nutr.
1995;19:296-302.
70. Gralak MA, Leontowicz M, Morawiec M, Bartnikowska E, Kulasek GW.
Comparison of the influence of dietary fibre sources with different propor-
tions of soluble and insoluble fibre on Ca, Mg, Fe, Zn, Mn and Cu apparent
absorption in rats. Arch Tierernahr. 1996;49:293-299.
71. Ovesen L, Chu R, Howard L. The influence of dietary fat on jejunostomy
output in patients with severe short bowel syndrome. Am J Clin Nutr.
1983;38:270-277.
72. Arora R, Kulshreshtha S, Mohan G, Singh M, Sharma P. Estimation of
serum zinc and copper in children with acute diarrhea. Biol Trace Elem
Res. 2006;114:121-126.
73. Lim P, Jacob E. Tissue magnesium level in chronic diarrhea. J Lab Clin
Med. 1972;80:313-321.
74. Liebman M, Chai W. Effect of dietary calcium on urinary oxalate excretion
after oxalate loads. Am J Clin Nutr. 1997;65:1453-1459.
75. Curhan GC, Willett WC, Rimm EB, Stampfer MJ. A prospective study of
dietary calcium and other nutrients and the risk of symptomatic kidney
stones. N Engl J Med. 1993;328:833-838.
76. Hanzlik RP, Fowler SC, Fisher DH. Relative bioavailability of calcium
from calcium formate, calcium citrate, and calcium carbonate. J Pharma-
col Exp Ther. 2005;313:1217-1222.
77. Burnes JU, O’Keefe SJ, Fleming CR, Devine RM, Berkner S, Herrick L.
Home parenteral nutrition—a 3-year analysis of clinical and laboratory
monitoring. JPEN J Parenter Enteral Nutr. 1992;16:327-332.
78. Kramer P. Effect of antidiarrheal and antimotility drugs on ileal excreta.
Am J Dig Dis. 1977;22:327-332.
79. King RF, Norton T, Hill GL. A double-blind crossover study of the effect
of loperamide hydrochloride and codeine phosphate on ileostomy output.
Aust N Z J Surg. 1982;52:121-124.
170 Journal of Parenteral and Enteral Nutrition 37(2)
80. Newton CR. Effect of codeine phosphate, Lomotil, and Isogel on ileos-
tomy function. Gut. 1978;19:377-383.
81. Tan-No K, Niijima F, Nakagawasai O, Sato T, Satoh S, Tadano T. Devel-
opment of tolerance to the inhibitory effect of loperamide on gastrointes-
tinal transit in mice. Eur J Pharm Sci. 2003;20:357-363.
82. Thompson WG, Thompson GR. Effect of cholestyramine on the absorp-
tion of vitamin D3 and calcium. Gut. 1969;10:717-722.
83. Parrish CR. The clinician’s guide to short bowel syndrome. Pract Gastro-
enterol. 2005;29:67-106.
84. Go VL, Poley JR, Hofmann AF, Summerskill WH. Disturbances in fat
digestion induced by acidic jejunal pH due to gastric hypersecretion in
man. Gastroenterology. 1970;58:638-646.
85. Wilson SD, Soergel K, Go VL. Diarrhoea, gastric hypersecretion, and
“cholecystokinin-like” hormone. Lancet. 1973;1:1515-1516.
86. Saunders DR, Saunders MD, Sillery JK. Beneficial effects of glucose
polymer and an H2-receptor blocker in a patient with a proximal ileos-
tomy. Am J Gastroenterol. 1989;84:192-194.
87. Jeppesen PB, Staun M, Tjellesen L, Mortensen PB. Effect of intravenous
ranitidine and omeprazole on intestinal absorption of water, sodium, and
macronutrients in patients with intestinal resection. Gut. 1998;43:763-769.
88. Buchman AL, Fryer J, Wallin A, Ahn CW, Polensky S, Zaremba K.
Clonidine reduces diarrhea and sodium loss in patients with proxi-
mal jejunostomy: a controlled study. JPEN J Parenter Enteral Nutr.
2006;30:487-491.
89. O’Keefe SJ, Haymond MW, Bennet WM, Oswald B, Nelson DK, Shorter
RG. Long-acting somatostatin analogue therapy and protein metabolism
in patients with jejunostomies. Gastroenterology. 1994;107:379-388.
90. Vanderhoof JA, Kollman KA. Lack of inhibitory effect of octreotide on
intestinal adaptation in short bowel syndrome in the rat. J Pediatr Gastro-
enterol Nutr. 1998;26:241-244.
91. Seydel AS, Miller JH, Sarac TP, Ryan CK, Chey WY, Sax HC. Octreotide
diminishes luminal nutrient transport activity, which is reversed by epi-
dermal growth factor. Am J Surg. 1996;172:267-271.
92. Bass BL, Fischer BA, Richardson C, Harmon JW. Somatostatin analogue
treatment inhibits post-resectional adaptation of the small bowel in rats.
Am J Surg. 1991;161:107-111, discussion 111-112.
93. Sagor GR, Ghatei MA, O’Shaughnessy DJ, Al-Mukhtar MY, Wright NA,
Bloom SR. Influence of somatostatin and bombesin on plasma entero-
glucagon and cell proliferation after intestinal resection in the rat. Gut.
1985;26:89-94.
94. Eizaguirre I, Urkia NG, Asensio AB, et al. Probiotic supplementation
reduces the risk of bacterial translocation in experimental short bowel
syndrome. J Pediatr Surg. 2002;37:699-702.
95. Mogilner JG, Srugo I, Lurie M, et al. Effect of probiotics on intestinal
regrowth and bacterial translocation after massive small bowel resection
in a rat. J Pediatr Surg. 2007;42:1365-1371.
96. Tolga Muftuoglu MA, Civak T, Cetin S, Civak L, Gungor O, Saglam A.
Effects of probiotics on experimental short-bowel syndrome. Am J Surg.
2011;202:461-468.
97. Uchida K, Takahashi T, Inoue M, et al. Immunonutritional effects dur-
ing synbiotics therapy in pediatric patients with short bowel syndrome.
Pediatr Surg Int. 2007;23:243-248.
98. Kanamori Y, Sugiyama M, Hashizume K, Yuki N, Morotomi M, Tanaka
R. Experience of long-term synbiotic therapy in seven short bowel
patients with refractory enterocolitis. J Pediatr Surg. 2004;39:1686-1692.
Downloaded from pen.sagepub.com at UNIV OF VIRGINIA on November 16, 2013
99. Drucker DJ, Erlich P, Asa SL, Brubaker PL. Induction of intestinal epi-
thelial proliferation by glucagon-like peptide 2. Proc Natl Acad Sci U S
A. 1996;93:7911-7916.
100. Tsai CH, Hill M, Asa SL, Brubaker PL, Drucker DJ. Intestinal growth-
promoting properties of glucagon-like peptide-2 in mice. Am J Physiol
Endocrinol Metab. 1997;273:E77-E84.
101. Jeppesen PB, Hartmann B, Thulesen J, et al. Glucagon-like peptide
2 improves nutrient absorption and nutritional status in short-bowel
patients with no colon. Gastroenterology. 2001;120:806-815.
102. Washizawa N, Gu LH, Gu L, Openo KP, Jones DP, Ziegler TR. Compara-
tive effects of glucagon-like peptide-2 (GLP-2), growth hormone (GH),
and keratinocyte growth factor (KGF) on markers of gut adaptation after
massive small bowel resection in rats. JPEN J Parenter Enteral Nutr.
2004;28:399-409.
103. Gomez de Segura IA, Aguilera MJ, Codesal J, Codoceo R, De-Miguel E.
Comparative effects of growth hormone in large and small bowel resec-
tion in the rat. J Surg Res. 1996;62:5-10.
104. Seguy D, Vahedi K, Kapel N, Souberbielle JC, Messing B. Low-dose
growth hormone in adult home parenteral nutrition-dependent short bowel
syndrome patients: a positive study. Gastroenterology. 2003;124:293-
302.
105. Byrne TA, Wilmore DW, Iyer K, et al. Growth hormone, glutamine, and
an optimal diet reduces parenteral nutrition in patients with short bowel
syndrome: a prospective, randomized, placebo-controlled, double-blind
clinical trial. Ann Surg. 2005;242:655-661.
106. Jeppesen PB, Pertkiewicz M, Messing B, et al. Teduglutide reduces need
for parenteral support among patients with short bowel syndrome with
intestinal failure [published online September 11, 2012]. Gastroenterol-
ogy. doi:10.1053/j.gastro.2012.09.007.
107. MacMahon RA. The use of the World Health Organization’s oral rehydra-
tion solution in patients on home parenteral nutrition. JPEN J Parenter
Enteral Nutr. 1984;8:720-721.
108. Griffin GE, Fagan EF, Hodgson HJ, Chadwick VS. Enteral therapy in the
management of massive gut resection complicated by chronic fluid and
electrolyte depletion. Dig Dis Sci. 1982;27:902-908.
109. Spiller RC, Jones BJ, Silk DB. Jejunal water and electrolyte absorption
from two proprietary enteral feeds in man: importance of sodium content.
Gut. 1987;28:681-687.
110. Messing B, Crenn P, Beau P, Boutron-Ruault MC, Rambaud JC,
Matuchansky C. Long-term survival and parenteral nutrition depen-
dence in adult patients with the short bowel syndrome. Gastroenterology.
1999;117:1043-1050.
111. Crenn P, Coudray-Lucas C, Thuillier F, Cynober L, Messing B. Posta-
bsorptive plasma citrulline concentration is a marker of absorptive
enterocyte mass and intestinal failure in humans. Gastroenterology.
2000;119:1496-1505.
112. Kaufman SS, Loseke CA, Lupo JV, et al. Influence of bacterial over-
growth and intestinal inflammation on duration of parenteral nutrition in
children with short bowel syndrome. J Pediatr. 1997;131:356-361.
113. DiBaise JK, Matarese LE, Messing B, Steiger E. Strategies for parenteral
nutrition weaning in adult patients with short bowel syndrome. J Clin
Gastroenterol. 2006;40:S94-S98.
114. Matarese LE. Rehabilitation in intestinal failure. In: Waitzberg D, ed.
Nutrição Oral e Parenteral na Prática Clínica. 4th ed. São Paulo, Brazil;
Atheneu; 2009:1625-1640.