Best Practice & Research Clinical Gastroenterology 30 (2016) 213e224

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Best Practice & Research Clinical

Gastroenterology

Acquired causes of intestinal malabsorption

F. van der Heide, MD, PhD, Gastroenterologist and
Hepatologist *
Department of Gastroenterology and Hepatology, University of Groningen and University Medical Centre
Groningen, Groningen, The Netherlands

a b s t r a c t
Keywords:
Diarrhoea This review focuses on the acquired causes, diagnosis, and treat-
Enteropathies ment of intestinal malabsorption. Intestinal absorption is a com-
Intestinal failure plex process that depends on many variables, including the
Intestinal adaptation digestion of nutrients within the intestinal lumen, the absorptive
Intestinal absorption surface of the small intestine, the membrane transport systems,
Malabsorption
and the epithelial absorptive enzymes.
Micronutrients
Short bowel syndrome
Acquired causes of malabsorption are classified by focussing on the
Stool tests three phases of digestion and absorption: 1) luminal/digestive
phase, 2) mucosal/absorptive phase, and 3) transport phase. Most
acquired diseases affect the luminal/digestive phase. These include
short bowel syndrome, extensive small bowel inflammation,
motility disorders, and deficiencies of digestive enzymes or bile
salts. Diagnosis depends on symptoms, physical examination, and
blood and stool tests.
There is no gold standard for the diagnosis of malabsorption.
Further testing should be based on the specific clinical context and
the suspected underlying disease. Therapy is directed at nutri-
tional support by enteral or parenteral feeding and screening for
and supplementation of deficiencies in vitamins and minerals.
Early enteral feeding is important for intestinal adaptation in short
bowel syndrome. Medicinal treatment options for diarrhoea in
malabsorption include loperamide, codeine, cholestyramine, or
antibiotics.
© 2016 Elsevier Ltd. All rights reserved.

* Corresponding author. Hanzeplein 1, 9700 RB Groningen, The Netherlands. Tel.: þ31 050 3612620; fax: þ31 050 3619306.
E-mail address: f.van.der.heide@umcg.nl.

http://dx.doi.org/10.1016/j.bpg.2016.03.001
1521-6918/© 2016 Elsevier Ltd. All rights reserved.
214 F. van der Heide / Best Practice & Research Clinical Gastroenterology 30 (2016) 213e224

Introduction

The intestinal absorption of fluids, electrolytes, macronutrients (proteins, carbohydrates, and fats),
and micronutrients (vitamins, minerals, and trace elements) is a delicate and complex process. Mul-
tiple factors are involved in this process, including the digestion of nutrients within the intestinal
lumen, intestinal length and absorptive surface, the presence or absence of particular intestinal
components such as the colon and Bauhin's valve, and the functioning of the membrane transport
systems of the small intestinal epithelium involved in the absorption of specific micronutrients. A
disruption in the process of intestinal absorption may lead to malabsorption. In clinical practice,
malabsorption refers to impairments in both the absorption and digestion processes, for these are
interdependent. Intestinal malabsorption can result from congenital and acquired causes. Acquired
causes include maldigestion, loss of intestinal length due to resections, loss of absorptive surface due to
inflammatory diseases, motility disorders, defects in the membrane transport systems of the small
intestinal epithelium, and acquired defects in the epithelial absorptive surface [1]. The malabsorption
can be global or partial (isolated). Global malabsorption results from diseases associated with either
diffuse mucosal involvement or a reduced absorptive surface. Partial malabsorption results from dis-
eases that interfere with the absorption of specific nutrients.
Malabsorption can lead to a number of clinical conditions, which have several definitions,
depending on the severity and/or consequences of the malabsorption for the patient. Intestinal
insufficiency or deficiency is the definition used when discussing impaired intestinal absorption and
functioning. The European Society for Clinical Nutrition and Metabolism (ESPEN) defines intestinal
insufficiency or deficiency as “the reduction of gut absorptive function that does not require intrave-
nous supplementation to maintain health and/or growth”. When the reduction of absorptive function
does require intravenous supplementation, it is defined as intestinal failure [2].
This review specifically focuses on the acquired causes of intestinal malabsorption and discusses the
various diagnostic tools and treatment options.

Causes of acquired intestinal malabsorption

Acquired intestinal malabsorption can affect all age categories. Causes include gastrointestinal and
systemic diseases, benign and malignant diseases, acute and chronic enteropathies, infectious and
parasitic diseases, pancreatic and biliary diseases, and post-radiation/chemotherapy-induced enteritis
[3,4]. When discussing the numerous causes of acquired intestinal malabsorption, it is important to
focus on the following three phases of the process of digestion and nutrient absorption: 1) luminal and
brush border processing, 2) absorption into the intestinal mucosa, and 3) transport into the circulation
[5]. Malabsorption can result from defects occurring at each of these three phases, and one or more
defects may exist concurrently. In the following sections of this article, the acquired causes of
malabsorption are discussed in the context of the above-mentioned phases of the process of nutrient
absorption. Table 2 provides an overview of the causes of malabsorption.

Luminal and brush border processing phase

Diseases affecting the luminal phase of the intestinal absorption process are responsible for the
majority of acquired causes of malabsorption. These can be divided into diseases affecting the

Table 1
Risk factors for developing short bowel disease.

Children Adults

Resection of 70% of total length of small bowel or Duodenostomy

remaining length starting at the ligament of Treitz:
<50 cm with preterm birth (36 weeks)
<75 cm with term birth (37e41 weeks)
<100 cm with child >1 year old
Jejunoileal anastomosis and <35 cm residual small intestine
Jejunocolic or ileocolic anastomosis and <60 cm
residual small intestine
End jejunostomy and <115 cm residual small intestine
 F. van der Heide / Best Practice & Research Clinical Gastroenterology 30 (2016) 213e224 215

Table 2
Causes of malabsorption.

Causes of malabsorption Entity Specific diseases

Luminal phase
Affecting absorptive surface
Deficiency of digestive
enzymes/substrates
Mucosal (absorptive) phase
Transport phase
Short bowel syndrome
Intestinal mechanical obstruction
Intestinal fistula
Intestinal dysmotility
Small bowel mucosal disease Crohn's disease
Coeliac disease
Radiation enteritis
Autoimmune enteropathy
Amyloidosis
Giardiasis
Tropical sprue
Whipple's disease
Bariatric surgery
Digestive enzyme deficiency Chronic pancreatitis
Cystic fibrosis
Gastrinoma (acid inactivation of lipase)
Orlistat (inactivation of lipase)
Decreased bile salts Cirrhosis (decreased synthesis)
Chronic cholestasis (impaired secretion)
Bacterial overgrowth (bile salt deconjugation)
Ileal disease or resection (increased losses)
Specific nutrients Pernicious anaemia (cobalamine/vitamin B 12)
Brush border enzyme deficiency Lactase deficiency
Enterocyte defect Crohn's disease
Coeliac disease
Lymphatic obstruction Intestinal lymphangiectasia
Tumour
Infection
Surgery

absorptive surface and diseases causing deficiencies of digestive enzymes or substrates. An important
clinical cause of malabsorption is a reduced absorptive surface as a result of inadequate intestinal
length caused by, for the most part, surgical resections. The main reasons for extensive intestinal
surgery in children in developed countries are gastroschisis, volvulus, necrotizing enterocolitis, in-
testinal atresia, and extensive aganglionosis in Hirschsprung's disease [6e8]. For adults, the main
reasons for intestinal resections are mesenteric infarction (arterial or venous thrombosis), Crohn's
disease, radiation enteritis, surgical complications, intestinal volvulus, familial polyposis, abdominal
trauma, intestinal angiomatosis, and complicated intussusception [2].
Intestinal resections can lead to short bowel syndrome. Short bowel syndrome is characterized by
suboptimal absorption of nutrients due to inadequate small intestinal length [9]. In general, in adults
nutritional/fluid supplements are likely to be needed if less than 200 cm of small bowel remains. Table
1 lists the risk factors for developing short bowel syndrome in children [10] and adults [11,12]. Con-
tinuity with a remaining colon after resection is important. The primary functions of the colon are the
absorption of fluids and electrolytes and the uptake of short-chain fatty acids. These acids play an
important role in the intestinal energy metabolism and are produced when dietary fibres are fer-
mented by intestinal microbiota [13]. Another important factor in the development of short bowel
syndrome is the absence of Bauhin's valve. Resection of the ileocaecal valve may allow colonic bacteria
to populate the small intestine, resulting in bacterial overgrowth. Because bacteria compete for nu-
trients with enterocytes [11], bacterial overgrowth may negatively impact on both digestion and
nutrient assimilation.
Data on the epidemiology of short bowel syndrome are scarce, which can partly be explained by a
lack of well-defined patient cohorts and use of different definitions. A study in Canadian children
216 F. van der Heide / Best Practice & Research Clinical Gastroenterology 30 (2016) 213e224

demonstrated an overall incidence of short bowel syndrome of 22.1 per 1,000 neonatal intensive care
unit admissions and 24.5 per 100,000 live births [14]. Data on adults are mostly based on studies on
cohorts of patients requiring long-term home parenteral nutrition for short bowel syndrome. Data
from the United Kingdom and Spain showed an incidence of 2 and 1.8 patients per one million pop-
ulation, respectively [15,16]. In addition, data from the United States showed that approximately
10,000e20,000 patients received home parenteral nutrition for short bowel syndrome [17]. A recent
report on 37 Dutch children dependent on home parenteral nutrition found that approximately 45% of
these children required parenteral nutrition for short bowel syndrome [18].
Next to short bowel syndrome, intestinal mechanical obstruction and intestinal fistulas can also
cause inadequate intestinal length. Mechanical obstruction can result from intraluminal conditions
such as strictures due to Crohn's disease, extra-luminal conditions such as extensive adhesions (“frozen
abdomen”), and acute or chronic events such as peritoneal carcinomatosis [2]. Obstruction can lead to
malabsorption due to decreased nutrition, increased intestinal secretion of fluids and electrolytes in
the obstructed segment, and increased intestinal losses of fluids and electrolytes due to vomiting or
nasogastric drainage. The numerous causes of intestinal fistulas include Crohn's disease, diverticular
disease, pancreatic disease, radiation enteritis, iatrogenic causes such as surgery or percutaneous
drainage, infectious diseases such as tuberculosis or actinomycosis, trauma, foreign bodies and ma-
lignancies such as colon cancer, ovarian cancer, or small bowel malignancy [2]. Fistulas can lead to
malabsorption because large areas of absorptive mucosal surface are bypassed. This results in pre-
mature loss of intestinal contents and thus loss of nutrients and energy.
The luminal process of absorption can be dysregulated by intestinal dysmotility disorders, resulting
in disordered propulsion of the intestinal contents, while luminal lesions that might cause fixed ob-
structions are absent. Hence, while the length of the intestine is adequate, it is rendered dysfunctional
by the disorder. Dysmotility disorders involving more than one part of the intestine may lead to
malabsorption, especially when the small bowel is involved. An example of an acute intestinal dys-
motility disorder is postoperative or acute critical illness-related ileus, which results from impaired
gastrointestinal motility associated with systemic or intra-abdominal inflammation. Chronic intestinal
pseudo-obstruction is associated with permanent intestinal dysmotility [19,20] and can result from
several diseases, including infections, autoimmune processes, mitochondrial dysfunction, and side
effects of medication [2]. Specific acquired causes of chronic intestinal pseudo-obstruction are diabetes,
systemic scleroderma, amyloidosis, or intestinal pseudo obstruction. In most cases, however, the cause
is unknown. Chronic intestinal pseudo-obstruction can be subdivided histologically into three cate-
gories: neuropathies, myopathies, or mesenchymopathies (involving the interstitial cells of Cajal)
[19,20]. These disorders cause malabsorption because of feeding-related exacerbation of digestive
symptoms, which in turn leads to restrictions in oral/enteral nutrition, or because of episodes of non-
mechanical intestinal obstruction. In addition, malabsorption can be the result of small bowel bacterial
overgrowth, increased intestinal secretion and/or losses of fluids and electrolytes from the dilated
bowel segments, or intestinal resections performed to relieve symptoms. In adults, approximately 20%
of cases involving home parenteral nutrition for chronic intestinal failure are due to chronic intestinal
pseudo-obstruction [21]. The aforementioned report on 37 Dutch children dependent on home
parenteral nutrition found that approximately 40% of these children were on parenteral nutrition due
to a motility disorder [18].
Other causes of malabsorption due to reduced absorptive surface are small bowel mucosal diseases
such as Crohn's disease, coeliac disease, radiation enteritis, chemotherapy-induced enteritis, autoim-
mune enteropathy, and amyloidosis. Infectious causes of malabsorption include giardiasis, tropical
sprue, and Whipple's disease. Tropical sprue is most common in Southeast Asia, the Caribbean, and
India. The aetiology of tropical sprue is unknown, but it is assumed to result from exposure to enteric
bacteria [22]. Whipple's disease is a rare disease that usually affects middle-aged men. It is caused by
Tropheryma whipplei, a fastidious intracellular organism [22].
The possible development of malabsorption due to small bowel mucosal diseases depends on the
location, severity, and extension of the disease. Diffuse and/or extensive small bowel mucosal disease
leads to loss of absorptive mucosal surface, and, consequently, to impaired absorption of almost all
nutrients. The impaired absorption, in turn, can lead to protein-losing enteropathies. If the disease is
limited to a specific intestinal region, specific nutrient deficiencies may be found in patients. An
 F. van der Heide / Best Practice & Research Clinical Gastroenterology 30 (2016) 213e224 217

example is vitamin B deficiency in patients in whom Crohn's disease has affected the terminal ileum.
Extensive small bowel mucosal disease has been reported to be the cause of chronic intestinal failure in
approximately 25% of children and 5% of adult patients on long-term home parenteral nutrition [2].
Small intestinal injury has been reported in association with the chronic use of several medications.
Medications that can cause this so-called drug-induced enteropathy include mycophenolate mofetil,
azathioprine, nonsteroidal anti-inflammatory drugs (NSAIDs) and olmesartan [22].
A relatively ‘new’ cause of acquired intestinal malabsorption is bariatric surgery for morbid obesity.
Bariatric surgery works as follows: 1) restriction of food intake by reducing the size of the stomach, 2)
malabsorption by bypassing a part of the small intestine to varying degrees, and 3) a combination of
restriction and malabsorption. Malabsorptive methods, for example, the Roux-en-Y gastric bypass, can
lead to deficiencies of iron, calcium, magnesium, and folic acid through bypassing the duodenum;
deficiencies of vitamin B12 due to decreased production of intrinsic factor by the reduced stomach; and
to steatorrhoea and subsequent deficiencies of fat-soluble vitamins, including vitamins D and E. After
bariatric surgery, vitamin and mineral deficiencies should be monitored and lifelong vitamin and
mineral supplementation is recommended [23].
The following paragraphs focus on acquired diseases that cause deficiencies of digestive en-
zymes or substrates. These deficiencies affect the luminal phase of the intestinal absorption pro-
cess. Chronic pancreatitis can lead to insufficiency of digestive enzymes, especially lipase, followed
by fat malabsorption. Cystic fibrosis can lead to chronic pancreatitis and, subsequently, to fat
malabsorption. A gastrinoma (ZollingereEllison syndrome) can cause steatorrhoea due to inacti-
vation of lipase by overproduction of gastric acid. Finally, fat malabsorption has also been associ-
ated with drug-related lipase inhibition, which may occur when orlistat is used in the treatment of
obesity [24e26].
Bile salts serve as an important substrate for the absorption process. Bile salts play a key role in the
internal digestion and absorption of dietary lipids by forming mixed micelles in the proximal intestine.
In the so-called enterohepatic circulation process, bile salts are synthesized by the liver and re-
absorbed by the distal ileum. Decreased levels of intestinal bile salts can lead to steatorrhoea, fol-
lowed by fat malabsorption. Possible causes of decreased bile salts include decreased synthesis due to
cirrhosis, impaired secretion due to biliary disorders with cholestasis, increased losses due to ileal
disease or resection, or deconjugation of bile salts due to small bowel bacterial overgrowth. Small
bowel bacterial overgrowth can also lead to malabsorption when the colonic-type bacteria produce
bacterial enterotoxins that cause fluid secretion and diarrhoea. Small bowel bacterial overgrowth is not
a disease in its own right; rather, it is a consequence of a disease that causes intestinal stasis. Intestinal
stasis can be caused by changes in intestinal anatomy after surgery, for example, afferent loops or blind
loops, but also by strictures or fistulas, diverticula, or dysmotility disorders.
Finally, diseases affecting the luminal phase of digestion can lead to partial malabsorption of specific
micronutrients. Pernicious anaemia is an example of such a disease. In pernicious anaemia, the gastric
parietal cells have stopped producing the intrinsic factor required for the intestinal vitamin B12 ab-
sorption, leading to decreased levels of vitamin B12.

Mucosal (absorptive) phase

Acquired causes of malabsorption in the mucosal absorptive phase of the intestinal absorption
process are discussed in the following section. The mucosal defect can be a brush border enzyme
deficiency, a brush border transport deficiency, or an enterocyte defect. The only clinically relevant
examples of acquired enzyme deficiencies are lactase deficiencies. Lactase is required for digestion of
lactose, a carbohydrate present in dairy products. There are three types of lactase deficiency: primary
lactase deficiency, developmental lactase deficiency, and secondary lactase deficiency. Primary lactase
deficiency is a genetically determined reduction or absence of lactase enzyme activity, which is
common in people of African or Asian descent and which manifests itself in adulthood. In contrast, the
majority of Caucasians, particularly those of northern European descent, maintain elevated lactase
enzyme activity throughout adult life. Developmental lactase deficiency occurs in premature infants.
Foetal lactase activity increases late in gestation, and premature infants born at 28e32 weeks of
gestation have reduced lactase activity [27]. Secondary lactase deficiency can be induced by underlying
218 F. van der Heide / Best Practice & Research Clinical Gastroenterology 30 (2016) 213e224

intestinal infections or diseases, for instance, coeliac disease or Crohn's disease, which cause villous
blunting or damage to the intestinal epithelium [28,29]. The lactase enzyme is usually the first of the
disaccharidases to be affected, presumably because of its distal location on the villus.
Acquired defects in brush border protein transporters and enterocyte function are caused by diffuse
small intestinal disease. In coeliac disease, inflammation causes mucosal dysfunction, which may lead
to abnormal uptake and re-esterification of lipids [30]. Crohn's disease can also lead to enterocyte
dysfunction.

Transport phase

The final phase of the absorption process concerns the transport of the absorbed nutrients into the
general circulation. The transport of lipids is particularly dependent on a well-functioning lymphatic
system. Lymphatic obstruction can impair the absorption of chylomicrons and lipoproteins and lead to
fat malabsorption, steatorrhoea, chylous ascites and/or a protein-losing enteropathy. The main causes
of lymphatic obstruction are primary intestinal lymphangiectasia (Waldmann's disease) [31] and
secondary obstruction due to neoplasia such as lymphoma or infections such as Whipple's disease,
tuberculous enteritis, or filariasis [32]. Furthermore, there are several surgical procedures that can lead
to obstructions in the intestinal lymphatic system and, subsequently, cause chylous ascites. Surgical
procedures most frequently associated with chylous ascites are resection of abdominal aortic aneurysm
and retroperitoneal lymph node dissection.

Diagnosis

The diagnostic process starts with recognizing the symptoms of intestinal malabsorption. Although
the underlying pathophysiology of diseases affecting the absorptive surface varies, the clinical con-
sequences may be similar. Symptoms include chronic diarrhoea, weight loss, steatorrhoea, malnutri-
tion with muscle wasting, anaemia, and/or deficiencies. Symptoms are more specific in diseases that
affect either specific digestive enzymes or the mucosal or transport phase. In case of fat malabsorption,
patients may present with steatorrhoea, pale and voluminous stools, and diarrhoea without flatulence.
Symptoms of patients suffering from carbohydrate malabsorption include watery diarrhoea, flatulence,
and abdominal distension occurring within 90 min after ingestion of carbohydrates. Finally, neuro-
logical symptoms and anaemia are prevalent in patients with pernicious anaemia. Symptoms may be
absent or subtle. Fatty stools, for example, may appear normal to the patient, and anaemia or osteo-
penia may sometimes be the only indication for a malabsorptive disease [33]. The anamnesis should
include a patient's history, use of alcohol, and previous surgery. The physical examination may identify
malnutrition, muscle wasting, oedema, and specific symptoms such as glossitis and cheilosis.
After identifying relevant symptoms, the next step is to conduct laboratory tests (see Table 3). The
various diagnostic tools for specific diseases causing malabsorption will not be discussed in detail here.
The sequence, number, and use of specific tests need to be individually tailored to the clinical context
and local expertise. Blood tests can reveal anaemia and nutrient deficiencies. Normal levels may
suggest that malabsorption is not the problem. On the other hand, a deficiency of one of these vitamins
may not necessarily mean that malabsorption is present. Several tests are available for the assessment
of protein malnutrition, including albumin, transferrin, prealbumin, and retinol-binding protein. All of
these tests, however, have certain limitations [34]. Altogether, there is no ‘gold standard’ for the
diagnosis of malabsorption syndrome.
Further testing often starts with a faecal fat test, which measures the amount of fat in the patient's
faeces. There are two reasons why malabsorption of fat is the most often used indicator of intestinal
malabsorption. First, fat is most susceptible to be affected by malabsorptive diseases. Second, fat is a
critical factor in weight loss because it is the most calorically dense macronutrient. In healthy children
and adults, more than 94% of dietary fat is absorbed. In persons who are on a diet containing 100 g of fat
per day, the presence of >6 g of fat in their 24-hour faeces collection indicates fat malabsorption. It is
also possible to look at the fractional fat excretion (percentage of dietary fat not absorbed). A value of
>6% is suggestive of fat malabsorption. A qualitative assessment of faecal fat will suffice and is much
easier and cheaper to perform than a 72-hour faecal fat test. Faeces can also be tested for volume,
 F. van der Heide / Best Practice & Research Clinical Gastroenterology 30 (2016) 213e224 219

Table 3
Diagnostic tools for the evaluation of intestinal malabsorption.

Test Target Aim

Blood Tests Haemoglobin Nutrient deficiencies

MCV
Iron
Ferritin
Total iron binding capacity
Folate
Vitamin B12
25-hydroxyvitamin D
Calcium
Phosphorus
Magnesium
Cholesterol
Albumin
Pre-albumin
Prothrombin time
Stool Tests Fat excretion 24-hour sample Fat malabsorption
Elastase Pancreatic insufficiency
Cultures Exclude infectious causes
Urine D-xylose test Malabsorption proximal small intestine
Breath Tests Breath hydrogen with lactose Lactose intolerance
Breath hydrogen with glucose Bacterial overgrowth in small intestine
Small bowel biopsy Histology Evaluation of small bowel disease (Crohn's disease,
coeliac disease, or autoimmune enteropathy)
Enzyme activity Disaccharidase activity
Imaging Radiography using barium Small bowel imaging
MRI/CT Small bowel imaging
Endoscopy Gastrointestinal tract imaging
EUS Chronic pancreatitis

elastase (pancreatic insufficiency), bile acids, and infectious diseases. Finally, faeces can be tested for
alpha-1 antitrypsin clearance for analysis of protein losing enteropathy. Alpha-1 antitrypsin is resistant
to proteolysis and degradation in the intestinal lumen and is therefore excreted intact in faeces [35]. By
measuring the alpha-1 antitrypsin concentration in faeces and a simultaneous plasma sample, a
reliable estimate of intestinal protein loss can be obtained. A 24-hour faecal sample combined with
plasma is preferred, but a faeces portion to measure the alpha-1 antitrypsin concentration is also
reliable. An important drawback, however, is that diarrhoea itself can lead to increased plasma
clearance of alpha-1 antitrypsin [36].
Breath tests can be used to test for malabsorption of carbohydrates, including lactose, fructose, and
sucrose. Hydrogen and methane gases are produced by fermentation of unabsorbed carbohydrates, for
instance, lactose, by intestinal bacteria. Hydrogen is excreted through the lungs and measured. The
presence of hydrogen gas in the breath after ingesting a product containing lactose may indicate lactase
deficiency. In addition to testing for carbohydrate malabsorption, breath tests can also be used when
small intestinal bacterial overgrowth is suspected. Small intestinal bacterial overgrowth may be
associated with increased fermentation of dietary carbohydrates, which is caused by bacteria in the
small bowel and can lead to symptoms of lactose intolerance. A very early peak of hydrogen in the
breath after the ingestion of lactulose or glucose may indicate bacterial overgrowth [37]. This peak
generally occurs 15e30 min after ingestion and is often accompanied by symptoms such as abdominal
cramps, flatulence, and abdominal distension. Carbohydrate malabsorption can also be determined by
enzymatic activity measured in small bowel biopsies. A jejunal biopsy allows for assessment of the
enzymatic activity of lactase and other disaccharidases such as maltase and saccharase. These biopsies,
however, are rarely performed due to the availability of non-invasive diagnostic tests. Biopsies in the
context of malabsorption syndrome are most often used to evaluate for underlying small bowel
pathology.
A classic test for diagnosing malabsorption is the D-xylose (a pentose monosaccharide) absorption
test. This test measures the absorptive capacity of the proximal small intestine [38] and is performed by
220 F. van der Heide / Best Practice & Research Clinical Gastroenterology 30 (2016) 213e224

collecting urine for 5 h after ingestion of 25 g D-xylose. Excretion of less than 3.5e6 g of D-xylose
suggests abnormal absorption. This test, however, has a high false-negative rate, and several conditions
may lead to false positive results, including renal dysfunction, impaired gastric emptying, ascites,
bacterial overgrowth, or drug use. The so-called Schilling test can be used to determine the cause of
vitamin B12 malabsorption. The test is performed by administering radiolabelled vitamin B12, followed
by a 24-hour urine collection to measure vitamin B12 excretion. However, the test has become obsolete
due to the availability of serum B12 and methylmalonic acid tests.
The final category of diagnostic tools concerns imaging. Radiographic examination of the small
bowel with barium contrast is used for evaluating anatomic abnormalities such as strictures and fis-
tulas in Crohn's disease and for defining the extent of previous intestinal surgery. In the last decades,
MRI and/or CT scans are increasingly used for this purpose. Endoscopy of the upper and lower
gastrointestinal tract can identify macroscopic abnormalities such as Crohn's disease and coeliac dis-
ease, while at the same time histological samples can be taken for microscopic examination. The small
bowel is difficult to reach by standard duodenoscopy and/or colonoscopy, but can be examined by
using balloon-assisted enteroscopy or video capsule endoscopy. Furthermore, endoscopic ultrasound
can be used for evaluating suspected chronic pancreatitis.

Treatment options

Treatment is of course dependent on the underlying disease and can encompass, for instance, a
gluten free diet for coeliac disease, immunomodulators for Crohn's disease, or alcohol abstinence with
enzyme replacement therapy for chronic pancreatitis. The specific details of each of these treatment
options will not be discussed here. Instead, the focus will be on the general therapeutic options. First,
therapeutic options for short bowel syndrome are discussed. This syndrome is a major cause of in-
testinal absorption because it leads to reduced absorptive surface. Next, the treatment of diarrhoea and
the options for specific nutritional support, including correction of nutritional deficiencies, are
discussed.
Short bowel syndrome is often caused by extensive surgical resection. After resection, resolution of
short bowel syndrome can occur spontaneously by means of the process of intestinal adaptation. This
process can take years and is caused by an increase in intestinal villi length leading to an increase in
absorptive surface [39]. The extent of the adaptation depends on the underlying disease, the small
bowel remnant length, and the presence of the ileocaecal valve [40]. Furthermore, it is important to
note that while the ileum can take over specific functions of the jejunum in the process of intestinal
adaptation, the same does not hold for the jejunum [40,41]. Also, as mentioned before, continuity of the
remaining colon is important for the absorption of fluids and electrolytes and for the intestinal energy
metabolism by means of the production of short-chain fatty acids by colonic microbiota.
Medical treatment of chronic intestinal failure relies on intestinal rehabilitation programs that aim
to restore bowel function through enteral nutrition, pharmacological therapy, and/or surgical therapy
[42]. A Dutch intestinal rehabilitation program led to intestinal autonomy in 84% of the 19 children with
short bowel syndrome [43]. Early enteral feeding after surgery is essential because deprivation of
enteral calories causes atrophy of the intestinal mucosa, even when adequate parenteral nutrition
support is present [44]. Early enteral feeding triggers the shortened intestine to make structural and
functional adaptations, which will lead to the absorption of luminal nutrients [45]. Surgical treatment
of short bowel syndrome includes lengthening procedures such as longitudinal intestinal lengthening
and tailoring (LILT), Bianchi-procedure, and serial transverse enteroplasty (STEP) [46]. Gut hormones
can promote intestinal adaptation and may decrease of even eliminate the need for parenteral support
[47]. Teduglutide, for example, is a recombinant analogue of human glucagon-like peptide. When all of
the above-mentioned treatments fail, patients with chronic intestinal failure are destined to perma-
nent home parenteral nutrition [48]. An intestinal transplant is an accepted alternative for those pa-
tients on permanent home parenteral nutrition who face severe and life-threatening complications
such as central line-associated infections and/or thrombosis [48,49].
Diarrhoea is often an important symptom of malabsorption syndrome. Diarrhoea not only has a
severe impact on patients' quality of life, it also leads to loss of fluids and energy. Especially in those
patients whose disease is not treatable, managing diarrhoea becomes the cornerstone of treatment.
 F. van der Heide / Best Practice & Research Clinical Gastroenterology 30 (2016) 213e224 221

Close attention should be paid to the underlying causes of diarrhoea, which include reduced intestinal
absorptive surface, excessive secretion of bile salts into the colon (known as cholorrhoea), small in-
testinal bacterial overgrowth, or dietary mistakes. In case of reduced absorptive surface, nonspecific
antidiarrhoeal agents are used. Loperamide is an opioid-receptor agonist that acts on the m-opioid
receptors in the myenteric plexus of the intestine. It has the same effect as morphine, but it does not
cross the bloodebrain barrier and its effects on the central nervous system are therefore minimal [50].
The low costs are an added advantage. Other options are codeine and opium tincture [12], which are
used in combination with loperamide. In case of very rapid intestinal transit, loperamide in liquid form
is preferred over tablets.
Cholestyramine is used in patients with cholorrhoea, which may occur after ileal resection. Chole-
styramine binds to bile salts in the small bowel by forming an insoluble complex, and, consequently,
interrupts the enterohepatic circulation. It is only useful when there is continuity with the colon, for this
type of diarrhoea is caused by an irritating effect of bile salts on the colonic mucosa. Cholestyramine can,
however, lead to deficiencies of fat soluble vitamins and is known to interact with other medications.
Steatorrhoea may also cause diarrhoea after intestinal resection. Therefore, it is important to distinguish
between steatorrhoea and cholorrhoea. The length of the resected ileum has a predictive value in this
respect: in adults less than 100 cm generally leads to cholorrhoea and more than 100 cm to steator-
rhoea. Stool tests can be used to distinguish between the two conditions. Finally, diarrhoea due to small
intestinal bacterial overgrowth can be treated by cyclic use of broad-spectrum antibiotics such as
rifaximin, metronidazole, ciprofloxacin, amoxicillin/clavulanic acid, neomycin, norfloxacin and doxy-
cycline [51,52]. There is no consensus on the most effective dose or duration of treatment.
Next, specific nutritional support for patients with intestinal malabsorption is discussed. It is
important to include a dedicated dietician or physician interested in nutritional support in the treat-
ment team. The first step of treatment should focus on weight loss and malnutrition. In general, un-
intended weight loss associated with illness of more than 10% of normal body weight is a clear sign of
malnutrition and linked to increased morbidity and mortality. Such a degree of weight loss should lead
to an aggressive nutrition plan. This starts with increasing the intake, which is best achieved by eating
small, frequent meals or by providing oral nutritional supplements. Small, frequent meals are also
helpful for short bowel syndrome, especially the less severe forms [53]. The second step of treatment
concerns enteral tube feeding. Polymeric formulae are better than elemental formulae because the
latter have a high osmotic value and can lead to diarrhoea. In patients with intestinal diseases,
including short bowel syndrome, continuous enteral feeding has been shown to improve intestinal
nutrient absorption and weight gain [54,55] and may therefore be better tolerated than bolus feeding
[56]. If the colon is present, dietary fibres can provide extra energy as a result of the short-chain fatty
acids produced by colonic fermentation of fibres. If these options prove to be insufficient, or if the
gastrointestinal tract is not accessible to enteral feeding, parenteral feeding is indicated. This should be
combined with enteral feeding whenever possible, given the beneficial effect of enteral feeding on
parenteral nutrition-associated liver disease.
Besides weight loss, malabsorption may lead to an imbalance in fluid and electrolyte absorption.
Malabsorption-induced diarrhoea often leads to loss of fluids and electrolytes, and patients risk
dehydration. This is particularly a problem in the absence of a colon. Dietary advice is the first step in
treating this type of diarrhoea. Patients should drink isotonic fluids and avoid hyperosmolar beverages
such as caffeine-containing beverages and sugared beverages (soft drinks and fruit juices). This holds
especially true for patients with short bowel syndrome. The well-known oral rehydration solution
(ORS) is important for rehydration. Its composition is based on the fact that the intestine remains able
to absorb water if glucose and salt are also present to assist in the transport of water from the intestinal
lumen. The sodium concentration of the small bowel luminal content is about 90 mmol/L, and this
should be the minimum concentration of sodium in ORS [57]. The composition of the ORS recom-
mended by the World Health Organization consists of 2.6 g sodium chloride, 2.9 g trisodium citrate,
1.5 g potassium chloride, and 13.5 g glucose per litre of water [58]. Unfortunately, many patients do not
tolerate ORS because of its bad taste. An alternative option is to dilute soft drinks and fruit juices with
water in a 1:1 ratio. Sport drinks often have a high sugar and low sodium content, which makes them
ineffective and which may even lead to further losses [59]. There are, however, some useful isotonic
sports drinks available.
222 F. van der Heide / Best Practice & Research Clinical Gastroenterology 30 (2016) 213e224

Table 4
Specific absorptive functions of different intestinal parts.

Intestinal part Specific nutrient

Duodenum Calcium, folic acid, magnesium, iron

Jejunum Most nutrients, calcium, zinc
Ileum Fluids, electrolytes, vitamins
Distal ileum Vitamin B12, bile salts
Colon Fluids, electrolytes, short-chain fatty acids

Finally, deficiencies of specific vitamins and minerals should be recognized. To this end, it is
important to know that nutrients are differentially absorbed in different locations throughout the small
bowel. Table 4 shows the specific absorptive functions of the different intestinal parts [45,60]. Hence,
specific deficiencies can be linked to the type of resection performed. Minerals and vitamins can often
be supplemented orally, except for vitamin B12 in pernicious anaemia. Oral magnesium supplemen-
tation is notoriously difficult because it may induce diarrhoea. In our experience, the best results are
achieved with magnesium gluconate and citrate. Loss of significant intestinal length results in need for
intravenous supplementation of fluids, salts, magnesium, and bicarbonate.

Summary

Intestinal absorption is a complex process that involves the digestion of nutrients within the in-
testinal lumen, the intestinal length and absorptive surface, and the membrane transport systems and
absorptive enzymes of the small intestinal epithelium. Malabsorption can lead to several clinical
conditions. Intestinal insufficiency is defined as a reduction of gut absorptive function that does not
require intravenous supplementation. When intravenous supplementation is required, the definition
intestinal failure is used. Malabsorption can be caused by maldigestion, loss of intestinal length, loss of
absorptive surface due to extensive inflammatory diseases, motility disorders, and defects in the
membrane transport systems or absorptive enzymes of the small intestinal epithelium. Causes of ac-
quired intestinal malabsorption include gastrointestinal and systemic diseases, which can be benign or
malignant, or infectious. The various causes can be classified by focussing on the three phases of
digestion and absorption: 1) the luminal/digestive phase, 2) the mucosal/absorptive phase, and 3) the
transport phase. The main group of acquired diseases affects the luminal/digestive phase and include,
for instance, short bowel syndrome, extensive small bowel inflammation, dysmotility disorders, and
deficiencies of digestive enzymes or bile salts. Table 2 lists all the causes of malabsorption.
Diagnosis of malabsorption depends on the combination of symptoms, physical examination, and
blood and stool tests. There is no gold standard for diagnosing malabsorption. Further testing should be
based on the specific clinical context and the suspected underlying mechanism and disease. Therapy is
generally supportive in the acute phase. Early enteral feeding plays an important role in stimulating the
intestinal adaptation process in short bowel syndrome. Therapy in the chronic phase involves nutri-
tional support by enteral or parenteral feeding, screening for deficiencies of vitamins and minerals, and
supplementation if necessary. Diarrhoea is an important symptom of malabsorption. Treatment op-
tions depend on the underlying cause of the diarrhoea and will often include loperamide, codeine,
cholestyramine, or antibiotics.

Practice Points

 Intestinal absorption is a complex process involving digestion, intestinal surface, enzymes,

and an intact epithelium.
 There is no gold standard for the diagnosis of malabsorption
 Treatment in general includes providing sufficient nutrition, either enteral and/or parenteral,
and supplementation of deficient nutrients
 F. van der Heide / Best Practice & Research Clinical Gastroenterology 30 (2016) 213e224 223

Research Agenda

 More specific diagnostic tools for intestinal malabsorption are necessary

 More studies on specific therapies in intestinal malabsorption and short bowel syndrome are
needed
 We need well-defined and widely accepted definitions of intestinal malabsorption and short
bowel syndrome

Conflict of interest

None.

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