ORIGINAL ARTICLE
Lactose Malabsorption and Intolerance in the Elderly
M. Di Stefano, G. Veneto, S. Malservisi, A. Strocchi & G. R. Corazza
Gastroentrolog y Unit, IRCCS “S. Matteo” Hospital, University of Pavia, Pavia, Italy.
Di Stefano M, Veneto G, Malservisi S, Strocchi A, Corazza GR. Lactose malabsorptio n and intoleranc e
in the elderly. Scand J Gastroenterol 2001;36:1274 –1278.
Background: Lactase activity declines with age in rats, but it is not clear whether this model is also
shared by humans. Few studies have evaluated lactose intoleranc e and malabsorptio n in the elderly and
no deŽ nite conclusion s can be drawn. The aim of our study was therefore to verify the impact of age on
lactose intoleranc e and malabsorption . Methods: Eighty-four healthy subjects took part in the study.
Thirty-thre e were <65 years, 17 were between 65 and 74 years and 34 were >74 years. All the subjects
underwent a preliminary evaluation of intestina l gas productio n capacity and oro-cecal transit time by H2 /
CH4 breath test after lactulose. After a 3-day period, an H2 /CH4 breath test after lactose was performed .
The occurrenc e of intoleranc e symptoms during the test and in the 24 h after the test was recorded .
Results: Breath H2 and CH4 excretion parameters at fasting and after lactulose did not differ between the
three groups. Cumulative breath H2 excretion after lactose was higher in subjects >74 years than in
subjects <65 years and in subjects aged 65–74 years, while no differenc e was found between the latter
two groups. In subjects >74 years, the prevalenc e of lactose malabsorption was higher than in the other
two groups, while no signiŽ cant difference was observed between subjects <65 years and subjects aged
65–74 years. Within the malabsorbe r subjects, the prevalence of lactose intolerance was higher in
subjects <65 years than in those aged 65–74 years and in those aged >74 years. No signiŽ cant differenc e
was found between the latter two groups. No difference was found between the three groups in terms of
daily calcium intake and a signiŽ cant negative correlation between symptom score and daily calcium
intake was only found in the group of subjects aged <65 years. Conclusions: As age increases , the
prevalence of lactose malabsorptio n shows an increase while the prevalence of intoleranc e symptoms
among malabsorber s shows a decrease . Accordingly, daily calcium intake was similar among the adults
and elderly studied.
Key words: Elderly; H2 -breath test; intestina l gas production ; lactose intolerance ; lactose malabsorption ;
methane production
G. R. Corazza, Gastroenterolog y Unit, IRCCS “S. Matteo” Hospital, Viale Golgi 19, 27100, Pavia, Italy
(fax. ‡39 0382 502618, e-mail. m.distefano@smatteo.pv.it )
H
Ó
uman adult-type hypolactasia is widespread throughout the world due to a genetically determined
decline of lactase activity inherited through an
autosomal recessive gene (1). Its prevalence is highly
variable, ranging from 5% in north-west Europe to almost
100% in some Asian populations (2). On clinical grounds,
hypolactasia is responsible for lactose malabsorption, which
may cause symptoms such as abdominal pain, bloating,
 atulence and diarrhea, evoked by milk consumption (3).
In human beings, the lactase decline pattern is similar to
that observed in mammals such as rats (4). However, although
in rats lactase activity declines further in old age (5–7), it is
not very clear whether this model is also shared by humans.
The measurement of lactase activity, in fact, gave con icting
results (8, 9) probably because of the marked effect of small
differences in the biopsy site (10). Only a few studies have
evaluated lactose intolerance and malabsorption in the elderly
by means of the hydrogen (H2 ) breath test (11–14), but, again,
no deŽ nite conclusions could be drawn owing to differences
2001 Taylor & Francis
in the methods used and in the ethnic background of the
subjects.
Accordingly, the aim of this study was to verify the impact
of age on lactose intolerance and malabsorption assessed by
the H2 breath test. Unlike previous studies, breath H2 and
methane (CH4) excretion after lactulose administration were
Ž rst evaluated in all subjects to exclude the possible
interference of unrelated factors such as differences in (a)
H2 production capacity (15), (b) small intestine transit time
(16), (c) occurrence of bacterial overgrowth (17) and (d)
colonic H2 consumption (18).
Subjects and Methods
Patients
Eighty-four healthy subjects (60 women, 24 men; age range
23–94 years) took part in the study. Thirty-three subjects were
<65 years (23 women, 10 men; mean age 45 § 15 years).
Seventeen subjects were between 65 and 74 years (12 women,
Lactose and Elderly
Table I. Mean body mass index (BMI), triceps skin fold (TSF) and
middle arm circumferenc e (MAC) in 84 healthy subjects accordin g
to age
BMI (kg/m 2 )
TSF (mm)
MAC (cm)
<65 years
65–74 years
>74 years
22 § 3
22 § 1
24 § 4
21 § 4
21 § 3
23 § 1
20 § 5
20 § 1
22 § 1
5 men; mean age 69 § 3 years) and 34 subjects were >74
years (25 women, 9 men; mean age 81 § 4 years). Thirtythree subjects (all <65 years) were members of medical or
paramedical staff of our hospital, while 51 were members of
the ‘Third Age University’, an association organizing cultural
and recreational events for elderly people. All were compliant
and gave their informed consent to the study. Subjects with
intestinal, liver, renal, chest, cardiac, metabolic or neurologic
disease or who were taking antibiotics, prokinetics, laxatives
or any other drug known to in uence colonic  ora in the
month preceding the study were excluded.
In all subjects nutritional status was assessed by anthropometric criteria. As given in Table I, there was no signiŽ cant
difference between the three groups of subjects in terms of
body mass index, thickness of tricipital skin fold and middle
arm circumference.
Daily calcium intake was assessed in each subject by
completing a dietary diary for three non-consecutive days
(two non-consecutive weekdays and one weekend day) listing
all the food eaten and the respective quantities, evaluated on
the basis of usual portion sizes (19). The diaries were then
checked by one of the authors, who was unaware of the
clinical details of the subjects and analyzed on the basis of
food-composition tables provided by the Italian National
Institute of Nutrition (20). Moreover, each subject was asked
whether milk and dairy product consumption led to appreciable abdominal symptoms.
Breath testing
In order to avoid prolonged intestinal gas production,
because of the presence of non-absorbable or slowly
fermentable material in the colonic lumen, the breath test
was preceded by a preparation procedure based on the
consumption, the evening before the test day, of a meal
consisting of only rice, meat and olive oil (21). This meal was
then followed by a 12-h fasting period. Breath testing started
between 0830 h and 0930 h, after thorough mouthwashing
with 40 mL of 1% chlorhexidine solution. Smoking and
physical exercise were not allowed for 1 h prior to and
throughout the test.
Sampling of alveolar air was performed by means of a
commercial device (Gasampler Quintron, Milwaukee, Wis.,
USA), which allows the Ž rst 500 mL of dead space air to be
separated and discarded while the remaining 700 mL of endalveolar air are collected in a gas-tight bag. Subjects were
instructed to avoid deep inspiration and not to hyperventilate
1275
before exhalation. A gas chromatograph dedicated to the
detection of H2 and CH4 in air samples was used for breath
samples analysis (Model DP12, Quintron Instrument, Milwaukee, Wis., USA). The accuracy of the detector was §2
ppm with a linear response range between 2 and 150 ppm of
H2 and between 2 and 50 ppm of CH4.
All the subjects underwent a preliminary evaluation of
intestinal gas production capacity and oro-cecal transit time
by H2 breath test after the ingestion of 400 mL of an isoosmotic solution containing 20 g of lactulose, a nonabsorbable disaccharide, which is fermented by colonic  ora.
Breath samples were taken at fasting and every 10 min for a 4h period. Subjects were considered low H2 excretors if no
breath sample contained an H2 concentration exceeding 20
ppm (15) and the test was considered a false-negative if an
increase of breath H2 excretion greater than 20 ppm over the
baseline was not evident (22). A 67-old-woman and a 75-oldwoman fulŽ lled these criteria and were excluded from the
subsequent stages of the study. For each subject fasting, peak
– that is the maximum increase over the baseline – and total
excretion – evaluated by means of area under the timeconcentration curve calculation (23) – of H2 were recorded.
Oro-cecal transit time was indicated by the presence of three
sustained increments of H2 breath excretion of at least 10 ppm
over the baseline (24).
Breath methane (CH4 ) excretion, the most important
metabolic pathway of H2 consumption (25), was also
measured and the prevalence of CH4 producers, i.e. subjects
with mean breath CH4 excretion higher than 5 ppm, and the
maximum peak, the time of appearance of the maximum peak
and total breath CH4 excretion, were calculated.
After at least a 3-day period, the H2 /CH4 breath test after
lactose ingestion was performed. The test solution consisted
of 400 mL of semi-skimmed milk, containing 20 g of lactose.
Breath samples were taken at fasting and every 30 min for a
4-h period. The test was considered as indicative of the
presence of lactose malabsorption when the peak of H2 breath
excretion over the baseline was ¶20 ppm (26, 27).
During the test, all the subjects were asked to record the
occurrence of intolerance symptoms experienced during the
24-h period after the test. Bloating, abdominal pain or cramps,
diarrhoea and  atulence were ranked as follows: 0 = absence
of the symptoms, 1 = trivial symptoms, 2 = mild symptoms,
3 = moderate symptoms, 4 = strong symptoms, 5 = severe
symptoms (28). The individual scores were then added
together and a mean of the individual values was given.
The individual maximum score was 5.
Data analysis
All variables were expressed as mean § standard deviation
(s). All continuous variables showed a normal distribution
with the Kolmogorov-Smirnov normality test. The unpaired t
test was computed for the comparison between two groups
and parametric one-way analysis of variance and Duncan’s
test were used for the comparison of the means of more than
Scand J Gastroenterol 2001 (12)
1276
M. Di Stefano et al.
Table II. Breath hydrogen and methane excretion parameters after lactulose in the three groups of subjects
Hydrogen
Fasting breath Peak of breath
excretion
excretion
(ppm)
(ppm)
<65
65–74
>74
3.7 § 1.8
4.2 § 5.3
3.1 § 2.3
54.3 § 33.2
58.2 § 32.9
62.2 § 48.7
Methane
Total breath
excretion
(ppm/min)
Oro-cecal
transit time
(min)
610 § 73
684 § 70
658 § 101
128 § 20
135 § 22
133 § 18
two groups and for the multiple comparisons of the means
between the pairs of groups, respectively. Differences
between proportions were assessed by the chi-squared test.
Pearson’s correlation coefŽ cient was computed for the
parametric estimates of the level of association between two
variables. A P value <0.05 was considered signiŽ cant.
Results
Table II indicates that subjects <65 years, between 65 and 74
years and >74 years did not signiŽ cantly differ as regards a
series of breath H2 and CH4 excretion parameters at fasting
and after 20 g of lactulose.
Fasting breath H2 concentrations (21) and the analysis of
the breath H2 excretion after lactulose administration (29) did
not suggest the presence of small intestine bacterial overgrowth in any subject.
Mean cumulative breath H2 excretion after lactose administration was signiŽ cantly higher in subjects >74 years
(236 § 35 ppm £ min) than in subjects <65 years (123 §
17 ppm £ min; P < 0.005) and in subjects aged 65–74 years
(159 § 36 ppm £ min; P < 0.01), while no signiŽ cant difference was found between the latter two groups (Fig. 1). The
prevalence of lactose malabsorption is shown in Fig. 2. In
subjects >74 years, this prevalence (83%) was signiŽ cantly
higher than in the other two groups. Again, no signiŽ cant
Fig. 1. Mean cumulative breath H2 excretion after lactose
administratio n in the three groups of subjects studied.
Scand J Gastroenterol 2001 (12)
Prevalence of Peak of breath
Time of
producers
excretion
appearance
(%)
(ppm)
of peak (min)
35
33
41
50.3 § 22.2
51.2 § 29.9
48.2 § 25.3
89 § 78
81 § 59
89 § 79
Total breath
excretion
(ppm/min)
335 § 99
367 § 115
325 § 151
difference was observed between subjects <65 years (58%)
and subjects aged 65–74 years (65%).
As regards lactose intolerance, all subjects but two (aged 36
and 44 years) who complained of appreciable abdominal
symptoms after milk and dairy product consumption turned
out to be malabsorbers at the H2 breath test. Fig. 2 also shows
that within the subjects with documented lactose malabsorption the prevalence of lactose intolerance was signiŽ cantly
higher in subjects <65 years (80%) than in those aged 65–74
years (50%) and in those aged >74 years (48%). No
signiŽ cant difference was found between the latter two
groups.
As regards severity of intolerance, mean symptom scores
showed no signiŽ cant differences between the three groups of
subjects studied (2.7 § 2.5 for subjects <65 years, 2.4 § 2.2
for subjects aged 65–74 years and 2.5 § 2.2 for subjects >74
years). No difference was found between the three groups in
terms of daily calcium intake (695 § 85 mg/day for subjects
<65 years, 785 § 92 mg/day for subjects aged 65–74 years
and 810 § 110 for subjects >74 years).
A signiŽ cant correlation (r = ¡0.73, P < 0.001) between
symptom score and daily calcium intake was only found in the
group of subjects aged <65 years (r = ¡0.08, for the group of
subjects aged 65–74 years, and r = ¡0.22, for the group of
subjects aged >74 years).
Fig. 2. Prevalence of lactose malabsorptio n in the three groups of
subjects studied (a) and prevalence of lactose intolerance among
malabsorbers (b).
Lactose and Elderly
Discussion
Our study, performed on a cohort of healthy, well-nourished
subjects aged 23–94 years, shows that there is an agedependent increase of breath H2 excretion after the ingestion
of 400 mL of semi-skimmed milk. This increase can only be
ascribed to lactose malabsorption, since elderly and younger
adult subjects do not differ in terms of H2 production capacity
by colonic  ora (15), small intestine transit time (16),
occurrence of bacterial overgrowth (17), and colonic H2
consumption via CH4 production (18). The observation that
adults and elderly subjects show the same pattern of intestinal
gas production and consumption permits us to make at least
two general observations: Ž rst, no particular interpretation of
the results of H2-breath tests is necessary for elderly subjects;
second, age alone does not represent a factor predisposing to
alterations of intestinal gas metabolism and should not
condition the clinical-diagnostic classiŽ cation of elderly
patients.
Our study also demonstrates that the prevalence of lactose
malabsorption increases signiŽ cantly after the age of 74 years.
In a recent study (14) performed in a cohort of 80 healthy
Caucasian women aged 40–79, the prevalence of lactose
malabsorption was signiŽ cantly higher in subjects aged 60–79
(50%) than in subjects aged 40–59 (15%). In this study the
prevalence of lactose malabsorption in subjects aged 60–79
years was similar to that found in our healthy subjects aged
65–74 years. So, showing a further increase in subjects older
than 74 years, our data complete these results, suggesting a
more extended age-related decline of lactase activity during
the life span. Lactose malabsorption is therefore one of the
components of the broad spectrum of the aging gut and its
mechanism is not easy to explain. It has been suggested that
the increased enterocyte turnover shown both in aged animals
(30) and humans (31) means that an increased proportion of
relatively undifferentiated epithelial cells line the villi in the
elderly with a consequent functional immaturity and delayed
enzyme expression (5).
As far as the occurrence of symptoms after lactose administration is concerned, the prevalence of lactose intolerance
among malabsorbers was signiŽ cantly lower in subjects aged
>65 years than in younger adults and advancing age did not
determine a further decline in lactose intolerance. Our results
do not agree with a previous study (14) showing no difference
in prevalence of lactose intolerance between adults and
elderly malabsorbers. However, such a discrepancy may be
explained on the basis of a higher carbohydrate load used by
those authors.
In our elderly subjects, a higher lactose malabsorption and
a higher colonic H2 production after lactose administration
were associated with a lower rate of lactose intolerance.
Therefore, it can more reasonably be suggested that differences of viscerosensitivity between the age groups studied
may be responsible for our results. Recent papers have shown
that intra-esophageal balloon distension may cause a dramatic
1277
decrease in pain perception in elderly volunteers (32) and an
age-related abolishment or reduction of secondary esophageal
peristaltic activity (33) suggesting a possible role of abnormalities of afferent pathways and/or esophageal mechanoreceptors. It is therefore possible that similar alterations can
involve the gastrointestinal tract at different levels and further
studies are needed to clarify this issue.
Daily calcium intake did not differ between the three
groups and a signiŽ cant inverse correlation between severity
of symptoms and calcium intake was evident in adult subjects
only. Intolerant patients avoid milk and other dairy products,
drastically reducing their daily calcium intake and exposing
them to the risk of detrimental effects on bone and mineral
metabolism (34). Therefore, in the light of our results, the
lower prevalence of lactose intolerance may exert a protective
effect in the elderly against consequent nutritional deŽ cits.
The symptom score in our malabsorbers was in any case
limited and, considering differences in methods, was substantially similar to that reported in previous studies (28, 35).
It can therefore be stated that malabsorbers may be allowed to
follow a diet containing dairy products; a very recent paper
(36) has even shown that lactose malabsorption is not an
impediment to the ingestion of a dairy-rich diet supplying
around 1500 mg of calcium, the dose recommended by an
NIH Consensus Statement for the prevention of osteoporosis.
Our results do not agree with a recent study (14) which
showed a reduction of calcium intake in malabsorbers aged
>70 years compared to absorbers with similar age. However,
this Ž nding was based on a small number of subjects and,
moreover, data on the prevalence of lactose intolerance are
also lacking. In conclusion, on the basis of our results, the
ingestion of dairy products should be encouraged in the
elderly, also because of the known reduced intestinal capacity
to absorb calcium (37) and to adapt to a diet with low calcium
concentration (38).
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