Mistakes in…

Mistakes in the management of carbohydrate

intolerance and how to avoid them
Heinz F. Hammer, Johann Hammer and Mark Fox

C
arbohydrates not absorbed in the small intestine are
fermented by colonic bacteria to organic acids and gases1
(e.g. carbon dioxide, hydrogen and methane), part of which
is absorbed in the colon, the other part remaining in the lumen.2,3
Large interindividual differences have been demonstrated for the
production of such acids and gas.4,5 Carbohydrate malabsorption
can be diagnosed by using the hydrogen breath test, because AGAVE
the gases produced after administration of a provocative dose
of carbohydrate are unique products of bacterial carbohydrate
fermentation.6,7
Fermentation products are thought to cause symptoms of
bloating, abdominal pain, diarrhoea and nausea;8 however, the © JR Shadwell.
role of the intestine in the pathogenesis of such symptoms is
unclear in both adults and children. Indeed, an important discrepancy between the degree of malabsorption and symptom
9–11

severity has been established.12,13

Here, we discuss mistakes that are made when managing patients who have bloating, abdominal pain, diarrhoea and nausea, in
whom carbohydrate malabsorption or intolerance have been diagnosed or are thought to contribute to the condition. The discussion
focuses on lactose malabsorption, because of its well-known pathophysiology and high prevalence; however, similar mechanisms
apply for intolerances to other poorly-absorbed fermentable, oligosaccharides, disaccharides, monosaccharides and polyols (sugar
alcohols) (FODMAPs) and related artificial sweeteners. As treatment focuses on symptom relief, evaluation of complaints that are
presumably related to carbohydrate ingestion has to place emphasis on symptom assessment.14

Mistake 1 Failing to distinguish food Food allergy is caused by an apparently Symptom development and severity in
intolerance from food allergy dose-independent reaction of the immune those with a food intolerance depends on the
Many patients report having a reaction to system that can affect many organs and amount of the food ingested, the digestion and
food and that may be ascribed to an allergy; systems, and in some cases can be life
however, especially in adults, most food threatening. By contrast, the symptoms and
reactions are caused by intolerance. For clinical consequences of food intolerance © UEG 2019 Hammer, Hammer and Fox.
practical purposes, patients have to be made are dose dependent, generally less Cite this article as: Hammer HF, Hammer J and
Fox M. Mistakes in the management of
aware of the difference between food allergy serious and are often limited to digestive carbohydrate intolerance and how to avoid them.
and food intolerance. problems.15,16 UEG Education 2019; 19: 9–14.
Heinz F. Hammer is Associate Professor at the
Medical University Graz, Department of
Mechanism Example
Gastroenterology and Hepatology, Graz, Austria.
Johann Hammer is Associate Professor at the
Maldigestion, malabsorption Absence of an enzyme needed for digestion Medical University Vienna, University of Internal
(e.g. lactase deficiency) Medicine III, Department of Gastroenterology and
Hepatology, Vienna, Austria. Mark Fox is Professor of
Physiologically incomplete absorption FODMAPs, magnesium Gastroenterology at the University of Zürich, Zürich,
Switzerland and lead physician at Digestive
Function: Basel, the Laboratory and Clinic for Motility
Dysregulated handling of bowel contents IBS Disorders and Functional GI Disease at Klinik
Arlesheim, Arlesheim, Basel-Land, Switzerland.
Reaction to the products of digestion Histamine, gas, short-chain fatty acids Correspondence to: heinz.hammer@medunigraz.at
Conflicts of interest: MF has received funding for
Sensitivity to food additives or contents Sorbitol, fructose, xylitol research and/or support of educational projects by
Given Imaging/Medtronic, Sandhill Scientific
Concurrent medical conditions Previous surgery, concurrent diseases Instruments and Medical Measurement Systems,
Mui Scientific, Reckitt Benckiser, Astra Zeneca and
Nestlé. HFH and JH declare no conflicts of interest
Concurrent psychological conditions Stress, psychological factors related to this article.
Published online: April 26, 2019.
Table 1 | Mechanisms involved in food intolerance.

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 Mistakes in…
assimilation of the food, and whether or not backgrounds, the clinical consequences of interplay between products of bacterial
this process is tolerated. Different mechanisms which range from being harmless nuisances carbohydrate metabolism and the structures
that may be involved in food intolerance are to diseases requiring medical evaluation and and functions of the gastrointestinal tract results
shown in Table 1. treatment.15,16 in marked interindividual differences in the
In the case of food allergy, the responsible sensitivity to incompletely absorbed
allergen has to be completely avoided. carbohydrates and symptom development.
By contrast, in the case of intolerance the Mistake 3 Assuming that the mechanisms
focus is on reducing the intake of the underlying intolerance are completely
offending food. In addition, drugs that understood Mistake 4 Not considering the role
assist the digestion of certain foods or treat The typical symptoms of lactose malabsorption of all poorly absorbed, fermentable
underlying conditions can be administered as (i.e. abdominal pain, bloating, flatulence and carbohydrates in patients with suspected
part of the medical treatment for those with a diarrhoea) are generally attributed to bacterial carbohydrate intolerance
food intolerance. fermentation of lactose in the large intestine. In addition to the commonly considered
Fermentation products increase the osmotic simple carbohydrates lactose or fructose, many
gradient, causing water to shift into the other incompletely absorbed carbohydrates
Mistake 2 Not considering the lumen to restore an isotonic milieu19 that may may reach the colon and be fermented by
mechanisms underlying the relationship contribute to abdominal pain sensation and bacteria.24,25 Indeed, the mechanisms by which
between food ingestion and symptom diarrhoea.4 The gases released by colonic lactose or fructose malabsorption lead to
development fermentation contribute to the sensation of intolerance are shared by many other types of
Patients who notice abdominal symptoms after bloating and to flatulence.5 carbohydrate, including starch and nonstarch
eating a particular food frequently consider Although colonic events have a major role in polysaccharides and FODMAPs.20,25,26
that food to be the direct cause of symptoms, symptom generation, some symptoms develop Reducing dietary FODMAPs in general
and may rely on its avoidance to treat their rapidly, before intestinal contents have reached can be recommended to patients who have a
symptoms. However, in clinical practice, the colon. This may be a consequence of an documented lactose or fructose intolerance but
the association between food intake and overactive gastro-colic reflex or it may indicate do not gain adequate relief on a diet free from
symptom development may have different that distension of the small intestine by fluids20,21 lactose or fructose. Subsequently, individual
causal relationships (Table 2).17,18 These can also contribute to some symptoms after foods are slowly reintroduced into the
relationships must be considered so that a carbohydrate load. The latter mechanism is diet. Documenting individual intolerances
diagnostic evaluation and treatment of any marked in the presence of small intestinal can provide a focus on specific dietary
underlying disease is not delayed. bacterial overgrowth (SIBO), in which components—thereby reducing the complexity
In patients who are lactose intolerant, fermentation and gas production occur already of the diet and its potentially restrictive effect
it may be unclear whether acquired primary in the mid-gut.22 Notwithstanding the above, the on costs, quality of life, long-term safety,
lactase deficiency or another small intestinal perception of bloating is not determined only nutritional adequacy and faecal microbiota.18
disorder (e.g. chronic infection, coeliac disease by the amount of gas in the intestine.5 Increased
or inflammatory bowel disease (IBD)) is visceral sensitivity to the presence of gas is a
responsible. Therefore, it may be necessary to very frequent finding in patients who have Mistake 5 Ignoring the possibility that
exclude other malabsorptive disorders, functional gastrointestinal disorders and comorbidities influence symptoms
especially if the patient’s ethnic background is complain of bloating.23 in patients with carbohydrate
associated with a low prevalence of acquired Practically speaking, it is important to malabsorption
primary lactase deficiency. remember that different factors are responsible Abdominal pain, bloating and a variable bowel
For practical purposes, food intolerances for the development of symptoms in patients habit are nonspecific symptoms that can occur
may have different functional or organic with carbohydrate malabsorption. The complex with various functional or organic diseases,

Causal relationship Example Clinical consequence

Food content is the cause of a disease Food allergy, coeliac disease, alcoholic pancreatitis Remove the offending food

Symptoms after food ingestion are a Biliary disease, irritable bowel syndrome (IBS), Detect and treat the underlying
clinical manifestation of an underlying functional dyspepsia, small bowel obstruction, disease, reduce the offending food
gastrointestinal, biliopancreatic or hepatic lactase deficiency
disease or abnormality

Food contents stimulate or alter normal Caffeine, fat, capsaicin (chilli), glutamate, Symptoms unrelated to a disease,
functions, possibly with the prerequisite histamine reduce the offending food
of perturbed gastrointestinal function

Excessive ingestion of certain foods FODMAPs, magnesium Symptoms unrelated to a disease,

overwhelm normal physiologic absorptive reduce the offending food component
capacities

Table 2 | Causal relationships between food intake and the gastrointestinal tract in the pathogenesis of food-associated symptoms.

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 Mistakes in…
with or without carbohydrate malabsorption. has been shown to reduce symptoms in patients are likely to have functional dyspepsia
In particular, intolerance of numerous foods is with IBS.35,36 triggered by gastric distention rather than a
a hallmark of irritable bowel syndrome (IBS).27 specific food intolerance.
Potential comorbidities must be considered to
better understand the treatment options for Mistake 6 Putting too much trust in
patients who have these symptoms. breath testing Mistake 7 Misinterpreting lactase
Patient history may provide a clue towards HBTs are the most commonly used tests for deficiency or lactose malabsorption as
understanding the pathogenesis of their evaluating lactose malabsorption.6 Diagnostic lactose intolerance
symptoms. Those who have food intolerances evaluation with the HBT and symptom Various methods are available to assess the
with a defined aetiology, such as primary assessment by questionnaire can be performed different parts of the process that leads from
lactase deficiency, tend to have discrete independent of the carbohydrate source or its lactose maldigestion to the generation of
symptoms that occur only after ingestion chemical constitution, which makes it possible symptoms (figure 1). These methods include
of the respective food. By contrast, those who to also test for incomplete absorption of genetic testing for lactase deficiency,
have a functional aetiology, such as IBS, carbohydrates other than lactose. determining lactase activity in biopsy samples
often complain of multiple gastrointestinal A false-positive HBT, often characterized by a taken from the small intestine, the HBT and
and other symptoms that change over time rapid increase in the concentration of hydrogen symptom assessment.
(e.g. dyspepsia, chronic headache and in the breath, can result from poor oral hygiene, A major limitation of the HBT is that after
fibromyalgia).28,29 SIBO or rapid intestinal transit.6,37,38 Conversely, a a provocative dose of a carbohydrate has
There is a large overlap between the false-negative HBT result occurs in at least 10% been given symptom assessment is often
occurrence of lactose malabsorption and IBS, of patients because their colonic microbiome inadequate. This means that the relationship
both of which are common conditions world- does not produce sufficient hydrogen to be between ingestion of the carbohydrate and
wide. Altering dietary intake of fermentable detected by current technology.6,39 If suspected, symptom development is not established. The
carbohydrates, including lactose in patients this can be confirmed by a lack of increase in same is true for the other blood and biopsy
with lactase deficiency, is known to alter breath hydrogen excretion in a lactulose HBT tests listed above. These tests, therefore,
symptoms in IBS.30 In this condition, the risk (lactulose being a disaccharide not digested establish lactose malabsorption, lactase
of developing symptoms after lactose by the small bowel).39 In clinical trials, the deficiency or the genetic predisposition to
ingestion is related not only to the dose of measurement of methane in addition to lactase deficiency,42 but they do not
lactose ingested but also to patient factors.31 hydrogen improves test sensitivity in hydrogen establish lactose intolerance, which is the
These factors include a history of abdominal nonexcretors;40,41 however, in practice, main focus of clinical evaluation and treatment
surgery or recent gastrointestinal disease,32 measurement of methane increases the cost of symptomatic patients referred for testing.
evidence of an activated mucosal immune and complexity of the test. False negatives may Furthermore, the HBT is usually performed
system (e.g. increased mast cells in biopsy also occur if orocoecal transit time is prolonged with very high doses of the test carbohydrate
samples from the small intestine and colon),33 and lactose enters the large bowel after the and is not repeated with low doses that may be
the presence of SIBO22 and colonic dysbiosis test is completed, usually after 3 hours.39 more relevant.
(as determined by excessive hydrogen Interpreting the findings of breath studies is Given that genetic tests, enzyme activity
production during a lactose hydrogen breath challenging in patients who report abdominal testing of biopsy samples and breath tests only
test [HBT]).31,34 Psychosocial factors, such symptoms after carbohydrate ingestion without demonstrate enzyme deficiency, maldigestion or
as the presence of psychological disease evidence of malabsorption (i.e. no increase malabsorption, validated symptom assessment
and/or high levels of 'life event stress', are in breath hydrogen). A study of fructose and is required for assessment of clinically relevant
also important.32 Many of these factors, fructose oligomers showed short-chain and intolerance. Suggestions for adhering to diets
especially inflammation and anxiety, are long-chain carbohydrates had different effects or using enzyme supplements (e.g. containing
associated with visceral hypersensitivity in in the small intestine and colon,20 raising the lactase or xylose isomerase43) should be limited
patients with IBS. possibility that symptoms after carbohydrate to cases of documented intolerance, for which
In individuals with lactose malabsorption ingestion may occur without carbohydrates the relationship between ingestion of a
various somatic and psychosocial factors impact having to reach the colon (malabsorption). carbohydrate and development of symptoms
on the risk of symptom development after Considering the pretest probability of lactase is validated.
ingestion of small to moderate amounts deficiency (according to ethnic background)
of lactose (i.e. clinically relevant lactose is helpful. If the pretest probability of lactase
intolerance). The shared aetiology of these deficiency is high, then the occurrence of typical Mistake 8 Relying on unvalidated
conditions suggests that lactose intolerance symptoms 30–90 minutes after lactose ingestion symptom assessment
is a form of functional bowel disease and, may be sufficient to establish the diagnosis, and Documentation of intolerance is the main
indeed, food intolerance is recognized as an breath hydrogen may not need to be measured. indication for dietary or drug treatment
important cause of symptoms in many IBS Conversely, if the pretest probability of lactase and symptom assessments during HBT
patients.31 deficiency is low, then it is probable that the measurements should be standardized to avoid
In lactose or fructose intolerant patients symptoms represent a nocebo effect (i.e. an bias.8,12 Test-specific symptom questionnaires for
whose symptoms persist while on an exclusion adverse response to a nonharmful stimulus) the assessment of symptoms during breath tests
diet, other factors and diseases contributing or that the symptoms are elicited in the small have been developed and validated for both
to the pathogenesis of symptoms have to be bowel without malabsorption being present. the paediatric and the adult populations.11,44–46
considered and treated accordingly, typically the It should also be noted that patients These should be preferred to the use of
functional bowel disorders IBS and functional who report symptoms within a few minutes unvalidated,19 self-made symptom assessment13
dyspepsia. A reduction of FODMAPs in the diet (<10 min) after ingestion of a test carbohydrate or generic gastrointestinal questionnaires that

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 Mistakes in…
Clinical tests Genetic test Serum glucose Breath test Symptoms
Enzyme activity questionnaire

Lactase H2

+ SCFAs Gastrointestinal
Digestion + Colonic
symptoms
bacteria H2 H2
Lactose H2O Glucose Galactose ∙ Bloating
∙ Abdominal pain
CH4
Maldigestion +/– ∙ Nausea
∙ Diarrhoea
CO2 ∙ Gas

Concurrent disease
IBS IBS
Small intestine Colon

Symptoms due to distension?

Figure 1 | Processes involved in lactose digestion, malabsorption and In individuals with lactase deficiency, lactose enters lower parts of the small
intolerance. In individuals with lactase persistence, lactose is digested by and the large intestine along with water. Colonic bacteria then ferment lactose
lactase to glucose and galactose, which are absorbed from the small intestine. to generate gas and short-chain fatty acids (SCFAs). Absorbed hydrogen can
Lactase activity can be measured in biopsy samples and genetic testing can be measured in the breath via the hydrogen breath test (HBT). The interplay
detect mutations associated with lactase persistence. Glucose absorption with concurrent diseases, such as irritable bowel syndrome (IBS), leads to the
can be demonstrated by a rise in serum glucose concentration. development of gastrointestinal symptoms.

are not specifically targeted to the population lactose, which approximates the dose most daily doses may be tolerated.50 However,
to be studied and the topic of carbohydrate often applied in clinical studies (35–50g). the consumed amount of different poorly
intolerance.47,48 It should also be noted that when lactose absorbable carbohydrates from different
Unvalidated symptom questionnaires malabsorbers ingest lactose with other sources, like dietary fibres or FODMAPs, may
should be avoided, as it is not known if these nutrients, they usually tolerate the consumption be enough to cause symptoms.
methods really measure what is intended of higher doses of lactose.49
and if the data are obtained in a consistent, Of the symptoms related to carbohydrate
uniform manner that can be compared to malabsorption, the pathophysiology of Mistake 10 Omitting professional dietary
other centres. Limited confidence in the results carbohydrate-induced diarrhoea is probably counselling and follow up
impacts both the clinical interpretation of the best studied. Diarrhoeal response to a Patients for whom there is a clear
individual lactose breath test results—in terms disaccharide load depends on the amount of association between symptoms and lactose
of intolerance testing—and reliance on the malabsorbed carbohydrate.4 The colon has a ingestion should be educated about
results of scientific reports. large capacity to absorb fermentation products appropriate dietary restrictions. Individuals
and thus to avoid faecal excretion of osmotic who develop symptoms only after ingestion of
loads.19 This colonic salvage becomes saturated dairy products require only a lactose-reduced
Mistake 9 Overlooking the dose as the quantity of carbohydrates reaching diet. However, as many carbohydrates other
dependency of symptom development the colon increases. For instance, in healthy than lactose are incompletely absorbed by the
Patients sometimes assume that small individuals, ingestion of 45g of nonabsorbable normal small intestine,24 and because dietary
amounts of lactose, for example those disaccharide lactulose increased faecal water fibre is also metabolized by colonic bacteria,
present as additives in drugs, cause symptoms excretion only minimally. Only when greater symptom persistence while on a lactose-
of intolerance. Some pharmaceutical than 80g lactulose was ingested, did significant reduced diet is not uncommon. Extending
companies have recognised this as a potential diarrhoea develop.3,19 The equivalent amount the diet to include global reduction of other
market and advertise their drugs as being of lactose (45g) can be expected to be partially poorly fermentable carbohydrates may be
lactose free. As such, it is clinically relevant digested and absorbed in the small intestine helpful for such patients.35,51 In particular many
to understand the dose of lactose required to even in lactose malabsorbers,12 making it patients with IBS and lactose intolerance require
induce notable symptoms (i.e. intolerance). unlikely that this amount alone is responsible advice on a FODMAP-reduced diet rather than
Increasing the dose of lactose during for severe diarrhoea. 'only' a lactose-reduced diet. Depending on
a lactose challenge increases the number Symptom development attributable to local care provisions, this may be best served by
of individuals who report abdominal carbohydrate malabsorption depends on the well-trained dietitians, who can provide dietary
symptoms.14 In one double blind study, amount of carbohydrate reaching the colon. counselling and follow up. Ideally, clinical
ingestion of less than 10g lactose rarely induced Usually more than 10g of lactose has to be decisions regarding dietary treatment should
abdominal symptoms in healthy controls, but ingested to cause symptoms. When lactose is be supported by carbohydrate intolerance
73% reported symptoms after ingestion of 40g consumed in divided doses, even higher documented by the results of a structured

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 Mistakes in…
and validated assessment of symptoms after 4. Hammer HF, et al. Carbohydrate malabsorption. Its 25. Wilder-Smith CH, et al. Fermentable sugar
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